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The relevance of time series in molecular ecology and conservation biology

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Abstract

The genetic structure of a species is shaped by the interaction of contemporary and historical factors. Analyses of individuals from the same population sampled at different points in time can help to disentangle the effects of current and historical forces and facilitate the understanding of the forces driving the differentiation of populations. The use of such time series allows for the exploration of changes at the population and intraspecific levels over time. Material from museum collections plays a key role in understanding and evaluating observed population structures, especially if large numbers of individuals have been sampled from the same locations at multiple time points. In these cases, changes in population structure can be assessed empirically. The development of new molecular markers relying on short DNA fragments (such as microsatellites or single nucleotide polymorphisms) allows for the analysis of long-preserved and partially degraded samples. Recently developed techniques to construct genome libraries with a reduced complexity and next generation sequencing and their associated analysis pipelines have the potential to facilitate marker development and genotyping in non-model species. In this review, we discuss the problems with sampling and available marker systems for historical specimens and demonstrate that temporal comparative studies are crucial for the estimation of important population genetic parameters and to measure empirically the effects of recent habitat alteration. While many of these analyses can be performed with samples taken at a single point in time, the measurements are more robust if multiple points in time are studied. Furthermore, examining the effects of habitat alteration, population declines, and population bottlenecks is only possible if samples before and after the respective events are included.

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... The amount of genetic diversity present within a species' populations is a critical component for species survival, as low levels of intraspecific genetic diversity will limit a species' capacity to adapt to present and future environmental changes [13][14][15][16]. ...
... However, the loss of allelic richness owing to drift can be made up for by high levels of gene flow and better dispersion abilities. Gene flow may be more restricted in smaller, lessconnected populations, which reduces its buffering effect and raises the likelihood of brother-sister mating, which increases the likelihood of inbreeding and inbreeding depression [13][14][15]. The latter dynamics have the potential to further reduce genetic within small populations, potentially resulting in the extinction vortex, a vicious cycle that could eventually result in extinction [13][14][15]. ...
... Gene flow may be more restricted in smaller, lessconnected populations, which reduces its buffering effect and raises the likelihood of brother-sister mating, which increases the likelihood of inbreeding and inbreeding depression [13][14][15]. The latter dynamics have the potential to further reduce genetic within small populations, potentially resulting in the extinction vortex, a vicious cycle that could eventually result in extinction [13][14][15]. ...
... Genetic structure of species and populations is shaped by the interaction of current and historical forces (Habel et al. 2014). Individual dispersal that maintains gene flow Electronic supplementary material The online version of this article (https ://doi.org/10.1007/s1059 ...
... Temporal data are extremely valuable to improve our understanding of long-term processes and their effects on the survival and maintenance of wildlife populations. However, the effect of habitat alteration, population declines, and bottlenecks on spatial genetic structure during different time periods has rarely been assessed at large spatial scales (Wandeler et al. 2007;Habel et al. 2014;Draheim et al. 2018). ...
... Recent gradual loss and fragmentation of capercaillie habitats suggests that information about connectivity among populations and effective population size is critical to conservation planning (van Strien et al. 2014;Mikoláš et al. 2017b;Klinga et al. 2019). There is thus a need to analyse population genetic data from different time periods (i.e., before and after important demographic events) to evaluate the effects of recent landscape dynamics and estimate the level of relative populations' fragmentation as a consequence of decreased habitat connectivity in the future (Habel et al. 2014). In the case of capercaillie of the Carpathian Mountains, the second half of twentieth century might be characterised by a stable, well-connected meta-population (Mikoláš et al. 2017b). ...
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A major concern in conservation biology today is the loss of genetic diversity in structured populations, which is often a consequence of habitat contraction and restricted gene flow over time. These dynamic biological processes require monitoring with temporal environmental and landscape genetic data. We compared the spatial genetic variation of a relict, umbrella species, the capercaillie (Tetrao urogallus), in two different demographic periods, as represented by older museum specimens (1960–1990) and recent non-invasive samples (2011–2015) collected from the Carpathian Mountains, where habitat connectivity has dramatically decreased in the past decade. Using a combination of species distribution modelling and spatial genetic inference, we analysed how climatic and environmental constraints shaped population structures of the species. Environmental and climate niche models confirmed that relict Carpathian capercaillie populations are temperature sensitive, and they occur in a narrow range of mountain forest habitats at the highest altitudes. We found that the environmental and climatic constraints led to genetically isolated populations, but we also detected clusters that did not match relatively interrupted areas of niche habitats. We observed a similar disruption of gene flow in both periods; however, a stronger signal of genetic structuring in recent samples indicated that the processes negatively affecting connectivity are ongoing. The effective population size of the Carpathian population has declined in recent years, but it has been low for at least the last five decades in the Western Carpathians. This study demonstrates the importance of temporal ecological and genetic data as an effective warning tool for the conservation and management of wildlife species.
... An essential factor for species survival is the level of genetic diversity present within its populations. Species which have a low level of intraspecific genetic diversity will have more limited potential to adapt to current and future changes in the environment (Frankham, 2005;Zayed, 2009;Habel et al., 2014;Koch et al., 2017). Small populations are more likely to have lower genetic diversity levels than large populations due to the impact of genetic drift, the random loss of genetic diversity over time (Reed and Frankham, 2003;Frankham, 2005;Zayed, 2009). ...
... However, high levels of gene flow and improved dispersal capacities can compensate for loss of allelic richness due to drift. In smaller less-connected populations, gene flow may be more limited, decreasing its buffering effect, which leads to lower genetic diversity and increase brother-sister mating chances, and in turn to inbreeding and inbreeding depression (Frankham, 2005;Zayed, 2009;Habel et al., 2014). The latter dynamics can further diminish genetic variability within small populations, potentially creating a vicious circle, known as the extinction vortex, which could ultimately lead to extinction (Frankham, 2005;Zayed, 2009;Habel et al., 2014). ...
... In smaller less-connected populations, gene flow may be more limited, decreasing its buffering effect, which leads to lower genetic diversity and increase brother-sister mating chances, and in turn to inbreeding and inbreeding depression (Frankham, 2005;Zayed, 2009;Habel et al., 2014). The latter dynamics can further diminish genetic variability within small populations, potentially creating a vicious circle, known as the extinction vortex, which could ultimately lead to extinction (Frankham, 2005;Zayed, 2009;Habel et al., 2014). ...
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Bumblebee species with declining population trends tend to show lower genetic diversity levels than stable species. The observed difference might be explained by abundance differences, with declining bumblebee species having lower genetic diversity levels simply due to their lower local species abundances. However, whether this holds true is not known. Here, we investigated whether bumblebee local abundances determines population genetic diversity levels. Therefore, local species abundances were measured for bumblebee species at four locations in Belgium and two locations in Estonia during bumblebee foraging years 2013–2017. These locations and countries were chosen to ensure the greatest possible variance in both local abundances and population trends for these species. Hence, genetic diversity levels were obtained for seven species by genotyping collected specimens with 16 microsatellites. Our results showed that the observed patterns in genetic diversity did not depend on local species abundance. So, although declining bumblebee species can become locally abundant, they will still show lower genetic diversity levels than stable species. This result implies that measuring bumblebees’ local abundance cannot be used to directly determine the health status of a population. Furthermore, this result has also major impact on future conservation strategies as increasing the genetic diversity levels of declining species will be very difficult, and habitat quality should be high to maintain their populations, otherwise these species are doomed to disappear first.
... Changes in population size over time (the demographic history of a species) can instead be reconstructed using genomic data because information on ancestral genomes and the evolutionary forces that shaped them is found within an individual's genome (Beichman et al., 2018). Time series genomic data can improve estimations of genetic changes in populations over time, but these analyses can also be performed with contemporary samples (Habel et al., 2014) when combined with modelling approaches to infer effective population sizes across time points . The advent of high-throughput sequencing technologies over the past 20 years means that genome sequence data are now widely available for nonmodel organisms, including species of conservation concern, and therefore can be used to inform their conservation management (Hohenlohe et al., 2021). ...
... Although more work is needed to assess when approaches to estimate effective population size are reliable (Hoban et al., 2014), genetic estimates can accurately reflect declines in population size (Pierson et al., 2018), even when declines are not as severe as those identified in this study (Razgour et al., 2021). A comparison of museum specimens to contemporary samples can improve the estimation of historic population sizes and genetic changes in populations over time (Habel et al., 2014) for species with adequate collections and when sufficient funding is available. ...
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Anthropogenically driven environmental changes over recent centuries have led to severe declines of wildlife populations. Better tools are needed to assess the magnitude and consequences of these declines. Anecdotal evidence suggests European bat populations have suffered substantial declines in the past centuries. However, there is little empirical evidence of these declines that can be used to put more recent population trends into historic context. This study is a collaboration between academics and conservation practitioners to develop molecular approaches capable of providing evidence of historic population changes that can inform conservation status assessments and management. We generated a genomic dataset of 46,872 SNPs for the Western barbastelle, Barbastella barbastellus , a regionally Vulnerable bat species, including colonies from across the species' British and Iberian ranges. We used a combination of landscape genetics and model‐based inference of demographic history to identify both evidence of population size changes and possible drivers of these changes. Levels of genetic diversity increased and inbreeding decreased with increasing broadleaf woodland cover around the colony. Genetic connectivity was impeded by artificial lights and facilitated by rivers and broadleaf woodland cover. The demographic history analysis showed that both the northern and southern British barbastelle populations have declined by 99% over the past 330–548 years. These declines may be linked to the loss of large oak trees and native woodlands due to shipbuilding during the early colonial period. Synthesis and applications . Genomic approaches can provide a better understanding of the conservation status of threatened species, within historic and contemporary contexts, and inform their conservation management. Our findings of will directly influence the definition of the Favourable Conservation Status of the barbastelle, in turn influencing considerations of the conservation of the species in development plans. Knowledge gained will also help set species recovery targets. Policymakers are interested in using our approach for other species. This study shows how we can bridge the implementation gap between genomic research and direct conservation applications. There is an urgent need to carry out such collaborative studies for other priority species to enable informed species recovery interventions via policy mechanisms and project delivery.
... To assess the loss of genetic diversity over time, a comparison of historical and contemporary populations is needed (Habel, Husemann, et al., 2014a;Leigh et al., 2019;Wandeler et al., 2007). Such approaches show that patterns vary between species. ...
... Genetic diversity and differentiation remained stable in the postglacial relict species L. helle, which is endangered in Europe (Habel, Meyer, & Schmitt, 2014b;van Swaay & Warren, 1999). In contrast, we observed a reduction in genetic diversity and a rise in genetic differentiation in L. hippothoe, which may hamper the species long-term survival in times of global change (Bijlsma & Loeschcke, 2012;Habel, Husemann, et al., 2014a). We argue that the difference among species arises from (1) inhabiting different biotopes, namely peat bogs and fallows in L. helle and traditional hay meadows in L. hippothoe, and associated (2) differences in recent land use change, (3) differences in population structure and history (see above). ...
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Biodiversity is currently declining at the global scale. Apart from species declines and lowered abundances, the loss of genetic diversity is equally concerning as it may undermine fitness and the potential to adapt to future environmental change. We compared genetic diversity of historical and recent Alpine populations of two butterfly species, Lycaena helle and L. hippothoe, over a period of about 10 years. Using microsatellite markers, we found no changes over time in L. helle, while genetic diversity decreased, and differentiation increased in L. hippothoe. Lycaena helle inhabits peat bogs and wetland fallows with populations being strongly isolated, while L. hippothoe used to occur in population networks on hay meadows, with the latter being strongly exposed to agricultural intensification. We conclude that currently L. hippothoe populations are strongly declining due to changes in land use, resulting in genetic erosion potentially due to the collapse of population networks. Stable genetic diversity was found in the glacial relict species Lycaena helle. Decreased genetic diversity was found in the grassland butterfly Lycaena hippothoe. We conclude that land use intensification may reduce genetic diversity over a period of only 10 years.
... Instead, the magnitude of drift is described by the effective population size (N E ), both being negatively correlated with each other (Wang et al., 2016). N E represents a key parameter in conservation and evolutionary biology (Charlesworth, 2009;Habel et al., 2014;Husemann et al., 2016;Lanfear et al., 2014;Luikart et al., 2010) and a variety of methods have been developed to estimate different types of N E in natural populations (Barker, 2011;Luikart et al., 2010;Palstra & Ruzzante, 2008;Wang et al., 2016). In conservation biology, N E is used as a measure of the susceptibility of a population to stochastic processes and inbreeding and hence can estimate the viability of a population (Hare et al., 2011). ...
... Variance N E , and some of the coalescent N E methods, require sampling of the same population at least twice at different points in time, preferably several generations apart. This represents a main limitation, as such samples are rarely available in nonmodel taxa and organisms with long generation times(Habel et al., 2014). ...
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Population genetics is a field of research that predates the current generations of sequencing technology. Those approaches, that were established before massively parallel sequencing methods, have been adapted to these new marker systems (in some cases involving the development of new methods) that allow genome-wide estimates of the four major micro-evolutionary forces—mutation, gene flow, genetic drift, and selection. Nevertheless, classic population genetic markers are still commonly used and a plethora of analysis methods and programs is available for these and high-throughput sequencing (HTS) data. These methods employ various and diverse theoretical and statistical frameworks, to varying degrees of success, to estimate similar evolutionary parameters making it difficult to get a concise overview across the available approaches. Presently, reviews on this topic generally focus on a particular class of methods to estimate one or two evolutionary parameters. Here, we provide a brief history of methods and a comprehensive list of available programs for estimating micro-evolutionary forces. We furthermore analyzed their usage within the research community based on popularity (citation bias) and discuss the implications of this bias for the software community. We found that a few programs received the majority of citations, with program success being independent of both the parameters estimated and the computing platform. The only deviation from a model of exponential growth in the number of citations was found for the presence of a graphical user interface (GUI). Interestingly, no relationship was found for the impact factor of the journals, when the tools were published, suggesting accessibility might be more important than visibility.
... This would be consistent with suggestions that peripheral populations may contain individuals with more dispersive morphs than core populations (Thomas et al., 2001;Parmesan, 2006). Movement and gene flow among local populations counter the effects of drift and, if sufficiently high, could contribute to maintaining some genetic diversity despite demographic instability (Habel et al., 2014, Jangjoo et al., 2016. However, the high temporal variation in allele frequencies that characterise the populations make the interpretation of spatial genetic patterns extremely challenging and likely overwhelm any signals reflecting spatial patterns of gene flow. ...
... Such inferences should instead be based on more direct measures such as mark-recapture data. Furthermore, to test for longer-term temporal changes in genetic diversity or structure, the use of historical samples or sampling over several decades is necessary (Habel et al., 2014). ...
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• The persistence and adaptation of leading‐edge peripheral populations may be critical for allowing species to shift their range limits under climate change. However, peripheral populations are potentially vulnerable to genetic, demographic, and environmental stochasticity. • Here, we characterise genetic variation across space and among years in northern peripheral populations of the Behr's hairstreak butterfly in British Columbia, Canada. This butterfly is dependent on antelope‐brush ecosystems that are threatened in this part of the world and is federally listed as Endangered in Canada. • Using a large panel of amplified fragment length polymorphism (AFLP) genetic markers, we found low diversity in these populations. We also detected a high degree of year‐to‐year variation in allele frequencies, resulting in low effective population size estimates. • Our findings suggest that Canadian populations of the Behr's hairstreak experience high genetic drift and may be vulnerable to genetic stochasticity. • Unstable demography, low effective population size, and low genetic diversity in these populations could impede their adaptation to rapidly changing environmental conditions and contribute to a contraction of the species' range under climate change.
... Understanding how demographic and genetic changes occur over time is critical to resolve evolutionary and conservation issues. Joint changes in demographic and genetic parameters over time have often been investigated through snap-shot approaches that investigate genetic changes between two (or more) periods during which demographic parameters have changed in the surveyed population (Schwartz et al. 2007, Habel et al. 2014. Nonetheless, using continuous monitoring (i.e. ...
... This shows the usefulness of continuous real-time monitoring to quantify, at a fine time-scale, both the genetic and demographic changes occurring in declining populations, which has strong implications for the prediction and prevention of extinction vortices in the wild. Continuous real-time monitoring combining genetic and demographic indicators is still rarely used (Habel et al. 2014), but we demonstrate that these indicators can jointly vary over short time scales. Moreover, we demonstrate how the spatial arrangement and the specificity of local populations within a landscape can modulate both local extinction rates and local genetic diversity distributions, which may dampen the pervasive genetic effects of demographic declines at the metapopulation scale. ...
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Quels mécanismes écologiques et évolutifs rendent les interactions entre espèces possibles ? J'ai abordé cette question en considérant l'interaction entre un parasite de poisson d'eau douce (Tracheliastes polycolpus) et plusieurs de ses hôtes cyprinidés. J'ai d'abord mis en avant le rôle de l'environnement à une échelle spatiale très fine (quelques centaines de mètres) sur le taux de rencontre entre ce parasite et ses hôtes. A plus large échelle spatiale (la France) j'ai illustré le rôle limitant de la résistance des populations hôtes sur la distribution de T. polycolpus. Par ailleurs j'ai montré que T. polycolpus parvient à parasiter différentes espèces hôtes en s'appuyant sur une expression plastique de ses gènes. Enfin, j'ai montré que les communautés bactériennes associées à l'hôte changent consécutivement à l'infection parasitaire dans une dynamique de co-infection avec le parasite. Par le déploiement d'approches variées et complémentaires, il apparaît que des facteurs environnementaux, liés à l'hôte, au parasite ou encore à leur cortège de bactéries contribuent à la réalisation d'une interaction étroite et durable tel que le parasitisme.
... This approach, which combines the sampling of many individuals and the characterization of a huge number of markers, allows the development of temporal studies, where samples from the same population are taken at different times with the aim to observe temporal changes in allelic frequencies, offering insights about the species population dynamics and demography. Effective population size (N e ), an important demographic parameter usually difficult to accurately estimate, can be more robustly assessed with temporal sampling and population genomic data [13,14]. Most studies that aimed to infer demographic dynamics based on genetic data approached that based on historical timescales (i.e., thousands of generations) and not on an ecological timescale (i.e., tens of generations) [15]. ...
... Besides that, population structure analyses indicated differentiation between years. SNPs are bi-allelic and expected to be less variable than microsatellites [13]. Despite of this, many studies reported sufficient power for SNPs to detect population structure, even in cases where divergence between populations is very low (e.g., [70]). ...
Article
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The New World screwworm (NWS) fly, Cochliomyia hominivorax (Diptera: Calliphoridae), is an economically important ectoparasite currently distributed in South America and in the Caribbean basin. The successful eradication of this species in USA, Mexico and continental Central America was achieved by a control program based on the sterile insect technique (SIT). In order to implement a genetic control strategy over the NWS fly’s current area of occurrence, first, it is necessary to understand the species dynamics and population structure. In order to address this objective, the spatial genetic structure of the NWS fly was previously reported in South America based on different genetic markers; however, to date, no study has investigated temporal changes in the genetic composition of its populations. In the current study, the temporal genetic structure of a NWS fly population from Uruguay was investigated through two consecutive samplings from the same locality over an interval of approximately 18 generations. The genetic structure was accessed with neutral and under selection SNPs obtained with genotyping-by-sequencing. The results gathered with these data were compared to estimates achieved with mitochondrial DNA sequences and eight microsatellite markers. Temporal changes in the genetic composition were revealed by all three molecular markers, which may be attributed to seasonal changes in the NWS fly’s southern distribution. SNPs were employed for the first time for estimating the genetic structure in a NWS fly population; these results provide new clues and perspectives on its population genetic structure. This approach could have significant implications for the planning and implementation of management programs.
... with shorter generation times (Laurent et al., 2011;Rey et al., 2015) than the species studied here. The major issues are that colonization events of a few to hundreds of generations often yield similar genetic signatures (Habel et al., 2014;Launey et al., 2010), and as such, estimates of demographic parameters such as bottleneck timing show relatively large confidence intervals (McCoy et al., 2014;Nunziata et al., 2017). Regardless of the uncertainties in timing, our data indicate that colonization has had a lasting impact on the genetic population of populations across small spatial and temporal scales. ...
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Understanding the adaptability of small populations in the face of environmental change is a central problem in evolutionary biology. Solving this problem is challenging because neutral evolutionary processes that operate on historical and contemporary timescales can override the effects of selection in small populations. We assessed the effects of isolation by colonization (IBC), isolation by dispersal limitation (IBDL) as reflected by a pattern of isolation by distance (IBD), and isolation by adaptation (IBA) and the roles of genetic drift and gene flow on patterns of genetic differentiation among 19 cave‐dwelling populations of Icelandic Arctic charr (Salvelinus alpinus). We detected evidence of IBC based on the genetic affinity of nearby cave populations and the genetic relationships between the cave populations and the presumed ancestral population in the lake. A pattern of IBD was evident regardless of whether high‐level genetic structuring (IBC) was taken into account. Genetic signatures of bottlenecks and lower genetic diversity in smaller populations indicate the effect of drift. Estimates of gene flow and fish movement suggest that gene flow is limited to nearby populations. In contrast, we found little evidence of IBA as patterns of local ecological and phenotypic variation showed little association with genetic differentiation among populations. Thus, patterns of genetic variation in these small populations likely reflect localized gene flow and genetic drift superimposed onto a larger‐scale structure that is largely a result of colonization history. Our simultaneous assessment of the effects of neutral and adaptive processes in a tractable and replicated system has yielded novel insights into the evolution of small populations on both historical and contemporary timescales and over a smaller spatial scale than is typically studied.
... The caveat is that these temporally deep historical data are often full of gaps over space and time, but even so the depth of the time frame provides data that complement the advantage (continuous inventory assessment) and disadvantage (limited temporal coverage) of contemporary monitoring assessments. Habel et al. (2014a) underlined the value of museum collections for preserving time series of species, enabling assessment of population structure change, useful in both molecular ecology and conservation biology. Several recent studies have used museum specimen data to assess abundance or biomass change in various insect groups over time as indicators of the degree or rate of global change. ...
Chapter
ABSTRACT Museum collections are essential repositories of taxonomic reference specimens, underlying and substantiating data that inform conservation management decisions. From a taxonomic and education perspective, they are fundamentally important in the process of documenting life on earth, describing species and informing society about the value of biodiversity. Taxonomy is a discipline that is central to interpreting the global biodiversity crisis. Natural history museum collections contain historical biodiversity data spanning both space and time and hence play an essential reference role in long-term insect monitoring and conservation. They are requisite repositories for contemporary inventory survey samples, necessary for assessing rate and impact of global declines in insects, a process that is largely reliant on curation and taxonomic analyses of specimens preserved in museum collections. Often under-valued, biological collections are a key resource that demands funding for the preservation of existing heritage objects, and for ongoing development and expansion of their holdings as part of documenting the rich, but highly threatened, biodiversity on our planet. Escalated recognition of the importance of these largely government-funded museum collections is required to ensure the continued maintenance of a resource that is needed for providing baseline data inputs into effective long-term management and conservation of ecosystems.
... The dawn of museomics makes it possible to extract genome-scale data from these specimens 22 . In the present study, we expanded these data to infer historical nuclear genomic diversity, population differentiation, as well as signatures of local adaptation [32][33][34][35] . ...
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Understanding the factors that predispose species and populations to decline and extinction is a major challenge of biodiversity research. In the present study, we investigated the historical population genomics of an extinct oyster population from the Wadden Sea collected between 1868 and 1888, and compared it to French and British populations sampled at the same time. The Wadden Sea is a unique habitat on the northern edge of the European oyster distribution. Our museomic results indicate that the now-extinct population was genetically isolated and had a lower nuclear genomic diversity than the examined French and British populations. Furthermore, genome scans revealed signatures of local adaptation, and population-specific divergence in several loci linked to fitness-relevant traits. The Wadden Sea oysters may have been predisposed for extinction because they were not naturally replenished from other populations, and the small population size did not allow them to adapt to anthropogenically-driven environmental change. In addition, anthropogenic translocations could not successfully replenish or replace this population because these foreign oysters may have been unable to reproduce in the unique Wadden Sea habitat. In summary, the Wadden Sea oysters exhibited all intrinsic drivers expected in a population predisposed for extinction.
... While large populations may appear robust due to their sheer numbers, the demonstrated low genetic diversity in this study, if confirmed across the entire genome, renders the species highly vulnerable to future climate change. (Frankham, 2005;Zayed, 2009;Habel et al., 2014;Koch et al., 2017). In summary, climate change can disturb ecological processes and subject species to stress, particularly when they exhibit low genetic variation. ...
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The objective of this research was to assess the genetic diversity and phylogeography of Bombus terrestris and examine the historical events that shaped its contemporary genetic structures using the COI mitochondrial marker. Specimens of the species were collected from its distribution range alongside the Alborz Mountain range, and GenBank sequences from the Eurasian distribution range were incorporated into the dataset. The COI sequences were employed in Bayesian and Maximum Likelihood analyses to generate phylogenetic trees for the species populations and to investigate the evolutionary history of the species. Additionally, species occurrence points and climate data were utilized in Species Distribution Modeling (SDM) analyses to reconstruct the species range under past, present, and future climate conditions. The ML and BI trees yielded similar topologies, indicating extremely low genetic diversity and a homogeneous structure in the species population distribution range in Eurasia. Demographic analyses suggested that the species may have experienced a bottleneck during the last glacial maximum in Eurasia, followed by a recent expansion. The SDM analyses revealed significant fluctuations in the species range in the past and expansion under present conditions. Given the high dispersal ability of the species, the population expansion rate has surpassed the rate of developing new genetic diversity, and the estimated polymorphic sites for the species are likely relatively recent. This low level of genetic variation can also be attributed to the absence of geographical barriers and the excellent flying ability of the queen bee, leading to sustained gene flow throughout the entire continent. Despite the general correlation between larger populations and higher genetic diversity, bumblebees can expand their population size without increasing genetic diversity when residing in resourceful habitats.
... Museum specimens collected prior to cryogenic tissue storage have long been used as genetic resources to address questions in ecology, evolutionary biology, and conservation (Habel et al., 2014;Wandeler et al., 2007). Genetic studies using these specimens have increased with the advent of high-throughput sequencing methods, which in comparison to prior Sanger sequencing methods, drastically increase the proportion of degraded DNA that is sequenced (Burrell et al., 2015). ...
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Museum specimens collected prior to cryogenic tissue storage are increasingly being used as genetic resources, and though high‐throughput sequencing is becoming more cost‐efficient, whole genome sequencing (WGS) of historical DNA (hDNA) remains inefficient and costly due to its short fragment sizes and high loads of exogenous DNA, among other factors. It is also unclear how sequencing efficiency is influenced by DNA sources. We aimed to identify the most efficient method and DNA source for collecting WGS data from avian museum specimens. We analyzed low‐coverage WGS from 60 DNA libraries prepared from four American Robin ( Turdus migratorius ) and four Abyssinian Thrush ( Turdus abyssinicus ) specimens collected in the 1920s. We compared DNA source (toepad versus incision‐line skin clip) and three library preparation methods: (1) double‐stranded DNA (dsDNA), single tube (KAPA); (2) single‐stranded DNA (ssDNA), multi‐tube (IDT); and (3) ssDNA, single tube (Claret Bioscience). We found that the ssDNA, multi‐tube method resulted in significantly greater endogenous DNA content, average read length, and sequencing efficiency than the other tested methods. We also tested whether a predigestion step reduced exogenous DNA in libraries from one specimen per species and found promising results that warrant further study. The ~10% increase in average sequencing efficiency of the best‐performing method over a commonly implemented dsDNA library preparation method has the potential to significantly increase WGS coverage of hDNA from bird specimens. Future work should evaluate the threshold for specimen age at which these results hold and how the combination of library preparation method and DNA source influence WGS in other taxa.
... Most genetic studies at the population level aim to investigate patterns of genetic structure occurring within and between geographically isolated populations (i.e., spatial genetic differentiation), but information on how genetic structure and diversity differ through time is often lacking (i.e., temporal genetic differentiation). Investigating temporal variation and the degree of genetic differentiation within a population can provide insights into the demographic stability of a population and its microevolutionary processes (Alonso-Blanco et al. 2005, Ayllon et al. 2006, Schwartz et al. 2007, Habel et al. 2014. Temporal genetic differentiation is influenced by the same factors as those affecting spatial genetic differentiation such as dispersal distance, immigration, selection, and population size (Loveless and Hamrick 1984, Waples and Gaggiotti 2006, Espíndola et al. 2012, Wogan and Wang 2018. ...
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Most population genetic studies concern spatial genetic differentiation, but far fewer aim at analyzing the temporal genetic changes that occur within populations. Vector species, including mosquitoes and biting midges, are often characterized by oscillating adult population densities, which may affect their dispersal, selection, and genetic diversity over time. Here, we used a population of Culicoides sonorensis from a single site in California to investigate short-term (intra-annual) and long-term (inter-annual) temporal variation in genetic diversity over a 3 yr period. This biting midge species is the primary vector of several viruses affecting both wildlife and livestock, thus a better understanding of the population dynamics of this species can help inform epidemiological studies. We found no significant genetic differentiation between months or years, and no correlation between adult populations and the inbreeding coefficient (FIS). However, we show that repeated periods of low adult abundance during cooler winter months resulted in recurring bottleneck events. Interestingly, we also found a high number of private and rare alleles, which suggests both a large, stable population, as well as a constant influx of migrants from nearby populations. Overall, we showed that the high number of migrants maintains a high level of genetic diversity by introducing new alleles, while this increased diversity is counterbalanced by recurrent bottleneck events potentially purging unfit alleles each year. These results highlight the temporal influences on population structure and genetic diversity in C. sonorensis and provide insight into factors effecting genetic variation that may occur in other vector species with fluctuating populations.
... Failure to adapt could ultimately lead to extinction. Therefore, knowledge of genetic diversity and geographic relationships of B. ignitus is crucial for long-term conservation, artificial selection, and the development of effective conservation strategies (Lee et al. 2006;Goulson et al. 2008;Zayed 2009;Whitehorn et al. 2009;Goka 2010;Habel et al. 2014). ...
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The bumblebee, Bombus ignitus (Hymenoptera, Apidae), plays a vital role in pollination in Northeast Asia, including Korea, China, Japan, and Far East Russia. Understanding the genetic makeup of the population can aid in its conservation. This study explores the DNA barcode region of cytochrome C oxidase subunit I (COI) of B. ignitus in commercial populations from Korea and Japan. The results reveal low intraspecific genetic diversity among commercially reared populations, with a maximum sequence divergence of 0.3%. Analysis of a 458-bp region of the COI gene, including 384 previously reported sequences, identified 20 haplotypes with the highest sequence divergence of 2.01% in East Asia. Commercial populations show a genetic similarity primarily with the Japanese population. Cross-mating with native populations could result in competition and genetic contamination, leading to reduced fitness and sensitivity to future environmental conditions. Morphological similarities make monitoring of such effects challenging. This study provides a basis for further research on population studies, conservation, and commercialization of local populations of B. ignitus for better pollination services while minimizing risks of reducing genetic diversity and increasing competition between native and introduced populations.
... Museum specimens represent a valuable and vast source of historical DNA (hDNA) for studying the evolutionary history of organisms (Buerki and Baker, 2016;Habel et al., 2014;Holmes et al., 2016). hDNA is derived from traditional voucher specimens archived in museum collections that are <200 years old (Card et al., 2021;Raxworthy and Smith, 2021), and has been successfully recovered from different parts of dried animal mounts, such as skin, bones, muscle, feathers, and toepads (Card et al., 2021). ...
Article
Natural history collections contain specimens that provide important insights into studies of ecology and evolution. With the advancement of high-throughput sequencing, historical DNA (hDNA) from museum specimens has become a valuable source of genomic data to study the evolutionary history of organisms. Low-coverage whole genome sequencing (WGS) has been increasingly applied to museum specimens for analyzing organelle genomes, but is still uncommon for genotyping the nuclear DNA fraction. In this study, we applied low-coverage WGS to phylogenomic analyses of parrots in the genus Agapornis by including both modern samples and historical specimens of ∼100-year-old. Agapornis are small-sized African and Malagasy parrots with diverse characters. Earlier phylogenetic studies failed to resolve the positions of some key lineages, prohibiting a robust interpretation of the biogeography and evolution of these African parrots. Here, we demonstrated the use of low-coverage WGS for generating both mitochondrial and nuclear genomic data, and evaluated data quality differences between modern and historical samples. Our resolved Agapornis phylogeny indicates the ancestor of Agapornis likely colonized Madagascar from Australasia by trans-oceanic dispersal events before dispersing to the African continent. Genome-wide SNPs also allowed us to identify the parental origins of hybrid Agapornis individuals. This study demonstrates the potential of applying low-coverage WGS to phylogenomics and population genomics analyses and illustrates how including historical museum specimens can address outstanding questions regarding the evolutionary history of contemporary lineages.
... Due to the valuable genetic information obtained, temporal genomics is increasing in popularity and demand (Habel et al., 2014), particularly because appropriate conservation measures are dependent on ongoing responses to climate change. For example, assisted gene flow may accelerate the dispersal or movement of pre-adapted genes, but can also counteract the process of adaptation by disrupting ongoing local beneficial allele frequency shifts (Aitken & Whitlock, 2013). ...
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Monitoring the evolutionary responses of species to ongoing global climate change is critical for informing conservation. Population genomic studies that use samples from multiple time points (“temporal genomics”) are uniquely able to make direct observations of change over time. Consequently, only temporal studies can show genetic erosion or spatiotemporal changes in population structure. Temporal genomic studies directly examining climate change effects are currently rare but will likely increase in the coming years due to their high conservation value. Here, we highlight four key genetic indicators that can be monitored using temporal genomics to understand how species are responding to climate change. All indicators crucially rely on having a suitable baseline that accurately represents the past condition of the population, and we discuss aspects of study design that must be considered to achieve this. Population genomic studies that use samples from multiple time points (“temporal genomics”) are uniquely able to make direct observations of change over time, and are critical to documenting how species are responding to climate change. Here, we highlight some key genetic indicators that can be monitored using temporal genomics to understand how species are responding to climate change: genetic erosion, spatiotemporal population structure, hybridization, and adaptation.
... One promising avenue for inferring recent changes in N e is by comparing genetic patterns in historical and modern samples. Advances in obtaining genetic material from museum specimens or other historical samples have made the acquisition of both baseline and contemporary genetic data (henceforth "temporal data") a possibility (Nielsen and Hansen 2008, Bi et al. 2013, Habel et al. 2014, Diez-del-Molino et al. 2018, Oosting et al. 2019. For example, temporal RADseq data from salamanders has been used to accurately reconstruct known recent declines and expansions (Nunziata et al. 2017). ...
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Synopsis Understanding recent population trends is critical to quantifying species vulnerability and implementing effective management strategies. To evaluate the accuracy of genomic methods for quantifying recent declines (beginning <120 generations ago), we simulated genomic data using forward-time methods (SLiM) coupled with coalescent simulations (msprime) under a number of demographic scenarios. We evaluated both site frequency spectrum (SFS)-based methods (momi2, Stairway Plot) and methods that employ linkage disequilibrium information (NeEstimator, GONE) with a range of sampling schemes (contemporary-only samples, sampling two time points, and serial sampling) and data types (RAD-like data and whole-genome sequencing). GONE and momi2 performed best overall, with >80% power to detect severe declines with large sample sizes. Two-sample and serial sampling schemes could accurately reconstruct changes in population size, and serial sampling was particularly valuable for making accurate inferences when genotyping errors or minor allele frequency cutoffs distort the SFS or under model mis-specification. However, sampling only contemporary individuals provided reliable inferences about contemporary size and size change using either site frequency or linkage-based methods, especially when large sample sizes or whole genomes from contemporary populations were available. These findings provide a guide for researchers designing genomics studies to evaluate recent demographic declines.
... The utility of time-series data in ecology and evolutionary research has long been recognized (Swetnam et al. 1999;Habel et al. 2014). Early genetic timeseries research was pioneered by experimental evolution studies with model species and few genetic markers (Dobzhansky and Pavlovsky 1957). ...
Article
Introduction The application of genomics to evolutionary biology has provided unprecedented power and resolution to investigate processes like mutation (Nachman and Crowell 2000; Rozhok and Degregori 2019), genetic drift (Whitney and Garland 2010; Funk et al. 2016), gene flow (Gallego-García et al. 2019; LaCava et al. 2021), and natural selection (Brauer et al. 2016; Martins et al. 2018). Evolutionary genomics has historically used contemporary or single-timepoint samples to study microevolutionary processes that most often depend on idealized model assumptions (e.g., Wright–Fisher model) (Butlin 2008; Hoban et al. 2016). For example, genome scanning methods aim to detect natural selection by assuming that the impact of selection can be discerned from the effects of neutral evolutionary processes on genetic differentiation (Hoban et al. 2016). However, different demographic scenarios can also produce signatures of selection, leading to false positives (Lotterhos and Whitlock 2015; Haasl and Payseur 2016). Similarly, when using measures of genetic differentiation to estimate gene flow, most models assume that population size is large enough that genetic drift is negligible—that is, not driving neutral divergence between populations (Whitlock and McCauley 1999; Ma et al. 2015).
... The utility of time-series data in ecology and evolutionary research has long been recognized (Swetnam et al. 1999;Habel et al. 2014). Early genetic timeseries research was pioneered by experimental evolution studies with model species and few genetic markers (Dobzhansky and Pavlovsky 1957). ...
Article
Sequencing data—genomics, transcriptomics, epigenomics, proteomics, and metabolomics—have revolutionized biological research, enabling a more detailed study of processes, ranging from subcellular to evolutionary, that drive biological organization. These processes, collectively, are responsible for generating patterns of phenotypic variation and can operate over dramatically different timescales (milliseconds to billions of years). While researchers often study phenotypic variation at specific levels of biological organization to isolate processes operating at that particular scale, the varying types of sequence data, or ‘omics, can also provide complementary inferences to link molecular and phenotypic variation to produce an integrated view of evolutionary biology, ranging from molecular pathways to speciation. We briefly describe how ‘omics has been used across biological levels and then demonstrate the utility of integrating different types of sequencing data across multiple biological levels within the same study to better understand biological phenomena. However, single time point studies cannot evaluate the temporal dynamics of these biological processes. Therefore, we put forward temporal ‘omics as a framework that can better enable researchers to study the temporal dynamics of target processes. Temporal ‘omics is not infallible, as the temporal sampling regime directly impacts inferential ability. Thus, we also discuss the role the temporal sampling regime plays in deriving inferences about the environmental conditions driving biological processes and provide examples that demonstrate the impact of the sampling regime on biological inference. Finally, we forecast the future of temporal ‘omics by highlighting current methodological advancements that will enable temporal ‘omics to be extended across species and timescales. We extend this discussion to using temporal multi-omics to integrate across the biological hierarchy to evaluate and link the temporal dynamics of processes that generate phenotypic variation.
... Altogether these results highlighted the importance of performing spatial replication in conservation genetics studies to accurately assess the effects of landscape characteristics on population structure, genetic diversity and persistence probability (Short-Bull et al. 2011;Habel et al. 2013). Additional spatial replications in other more or less anthropized ecological contexts (e.g. ...
Article
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Understanding landscape impacts on gene flow is necessary to plan comprehensive management and conservation strategies of both the species of interest and its habitat. Nevertheless, only a few studies have focused on the landscape genetic connectivity of the European wildcat, an umbrella species whose conservation allows the preservation of numerous other species and habitat types. We applied population and landscape genetics approaches, using genotypes at 30 microsatellites from 232 genetically-identified wildcats to determine if, and how, landscape impacted gene flow throughout France. Analyses were performed independently within two population patches: the historical north-eastern patch and the central patch considered as the colonization front. Our results showed that gene flow occurred at large spatial scales but also revealed significant spatial genetic structures within population patches. In both population patches, arable areas, pastures and permanent grasslands and lowly fragmented forested areas were permeable to gene flow, suggesting that shelters and dietary resources are among the most important parameters for French wildcat landscape connectivity, while distance to forest had no detectable effect. Anthropized areas appeared highly resistant in the north-eastern patch but highly permeable in the central patch, suggesting that different behaviours can be observed according to the demographic context in which populations are found. In line with this hypothesis, spatial distribution of genetic variability seemed uneven in the north-eastern patch and more clinal in the central patch. Overall, our results highlighted that European wildcat might be a habitat generalist species and also the importance of performing spatial replication in landscape genetics studies.
... Given that conserving genetic diversity and minimising inbreeding are important goals of most if not all captive breeding programmes 27,28 and reduced genetic diversity has been associated with increased extinction risk and reduced adaptive potential 29,30,31 , knowledge of the effects of captive breeding on genetic diversity is crucial. However, genetic time-series data are still uncommon for both captive and wild populations 32,33,34,35 . Temporal data can be especially informative about changes in key genetic characteristics of a population such as allelic richness, heterozygosity and the effective population size (N e ); measures that re ect a combination of the speed of allele frequency change through genetic drift, the e cacy of selection and expected genetic diversity levels for selectively neutral loci 36, 37 . ...
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Endangered species with small population sizes are susceptible to genetic erosion, which can be detrimental to long-term persistence. Consequently, monitoring and mitigating the loss of genetic diversity are key to successful conservation. The peninsular pronghorn ( Antilocapra americana peninsularis ) is an endangered pronghorn subspecies that is almost entirely held in captivity. Captive breeding has increased the number of pronghorns from 25 founders in 1997 to around 700 individuals today, but it is unclear how the genetic diversity of the captive herd may have changed over time. We therefore generated and analysed microsatellite data spanning 2009–2021. We found a decline in heterozygosity and an increase in the proportion of inbred individuals over time. However, these trends appear to have abated in response to a genetically informed selective breeding attempt undertaken in 2018. We also reconstructed the recent demographic history of the peninsular pronghorn, revealing two sequential population declines putatively linked to the desertification of the Baja California peninsula around 6,000 years ago, and hunting and habitat loss around 500 years ago. Our results provide insights into the genetic diversity of an endangered antelope and highlight the potential for selective breeding to have positive conservation outcomes.
... Even a large reintroduced population with effective recruitment may harbor low genetic diversity and high inbreeding (e.g., the Alpine ibex (Capra ibex): Grossen et al., 2018), reducing adaptive potential and increasing vulnerability to environmental change (Schwartz et al., 2007). Most genetic monitoring studies are still limited to snapshots in time and space (Schwartz et al., 2007;Habel et al., 2014), impacting on assessments of post reintroduction meta-population dynamics (Mathieu-Bégné et al., 2019) and the success of genetic rescue interventions (Frankham, 2015;White et al., 2018;Fitzpatrick et al., 2020). Where it has been implemented (e.g., Dowling et al., 2014;Osborne et al., 2012), long-term monitoring illustrates beneficial aspects of captive breeding programs, such as how rearing wild-caught larvae (as opposed to captive breeding) can help maintaining genetic diversity. ...
Article
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Restoration programs in the form of ex‐situ breeding combined with reintroductions are becoming critical to counteract demographic declines and species losses. Such programs are increasingly using genetic management to improve conservation outcomes. However, the lack of long‐term monitoring of genetic indicators following reintroduction prevents assessments of the trajectory and persistence of reintroduced populations. We carried out an extensive monitoring program in the wild for a threatened small‐bodied fish (southern pygmy perch, Nannoperca australis) to assess the long‐term genomic effects of its captive breeding and reintroduction. The species was rescued prior to its extirpation from the terminal lakes of Australia's Murray‐Darling Basin, and then used for genetically informed captive breeding and reintroductions. Subsequent annual or biannual monitoring of abundance, fitness, and occupancy over a period of 11 years, combined with postreintroduction genetic sampling, revealed survival and recruitment of reintroduced fish. Genomic analyses based on data from the original wild rescued, captive born, and reintroduced cohorts revealed low inbreeding and strong maintenance of neutral and candidate adaptive genomic diversity across multiple generations. An increasing trend in the effective population size of the reintroduced population was consistent with field monitoring data in demonstrating successful re‐establishment of the species. This provides a rare empirical example that the adaptive potential of a locally extinct population can be maintained during genetically informed ex‐situ conservation breeding and reintroduction into the wild. Strategies to improve biodiversity restoration via ex‐situ conservation should include genetic‐based captive breeding and longitudinal monitoring of standing genomic variation in reintroduced populations.
... (2) address redundancy by inferring metapopulation connectivity between warm-and cold-water subregions ; and (3) address representation and resilience by estimating N e and genetic signals of bottlenecks (1870s-2018) for the NW Atlantic Roseate Tern metapopulation. We apply a unique approach that combined extensive demographic data with recently developed microsatellite markers (Janowski et al. 2016, Schlesselmann andRobertson 2017), historical sampling of archival DNA (Habel et al. 2014), and forward genetic simulations (Strand and Niehaus 2018) to inform management strategies for this endangered species. ...
Article
Despite intensive management since the 1970s, recovery of the endangered northwestern Atlantic population of the Roseate Tern (Sterna dougallii dougallii) has not offset low productivity from a female-biased sex ratio, low adult survival, and habitat constriction. Now, >90% of individuals breed at three sites within 200 km from Long Island, NY, to Buzzards Bay, MA (warm-water subregion). To characterize the impact of historical bottlenecks, metapopulation structure, and demographic fluctuations on genetic variation, Roseate Terns from the warm-water (1870s, 1970s, 1997, 2016) and cold-water (Nova Scotia, Canada; 2018) subregions were genotyped at 8–16 microsatellites and 2–3 mitochondrial regions. Diversity declined in the warm-water subregion from the 1870s (expected heterozygosity [HE] = 0.44, allelic richness [AR] = 2.86) and 1970s (HE = 0.53, AR = 3.25) to 1997 (HE = 0.38, AR = 2.58). Genetic signatures of bottlenecks persisted in 1997 (P = <0.001–0.003) and 2016 (P = <0.001–0.005), but an increase in variation occurred by 2016 (HE = 0.50, AR = 2.85). Weak structure was detected between contemporary warm- and cold-water subregions (θ = 0.06) and within the warm-water subregion (θ = 0.04). Both demographic (3,439–3,821) and genetic (3,040) estimates suggested effective population size (Ne) stability over the last 100 years, despite large fluctuations in census size (4,000–8,662). Results suggest that 50 years of management (restoring habitat, preventing gull encroachment, controlling predators) at colony sites supported a small, stable Ne and maintained a hierarchical metapopulation that allowed gene flow to redistribute genetic variation throughout the northwest Atlantic. The metapopulation remains highly vulnerable to stochastic events but harbors resiliency and redundancy through gene flow and a stable Ne. For long-term persistence from a genetic perspective, managers must maintain the major source colonies, increase the availability of high-quality peripheral breeding sites, and protect concentrated nonbreeding sites that facilitate gene flow.
... The level of genetic diversity plays an important role in the successful adaptation of a population to adverse and uncertain environmental conditions such as a changing climate (Kawecki and Ebert 2004). Failure of adaptation due to low genetic diversity could lead to extinction; therefore, having some information on the genetic diversity and geographic relationships of a population is crucial for decisions on the conservation of a species, especially if we are dealing with an important pollinator (Goulson et al. 2008;Zayed 2009;Habel et al. 2014). ...
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The bumble bee Bombus polaris (Curtis 1835) is known from the northernmost region of Greenland. But how it can survive there, where in terms of geographic origin it came from, and which species in addition to B. pyrrhopygus (Friese 1902) genetically it is most closely related to are insufficiently answered questions that have motivated us to carry out this study. On the basis of a molecular analysis of the cytochrome oxidase I gene of a B. (Alpinobombus) polaris from North Greenland (82° 48′ N; 42° 14′ W), we conclude that the female specimen we analysed was most closely related to the Canadian populations of B. polaris . Geographic proximity, occurrence of B. polaris on Ellesmere Island and wind direction are likely factors that have aided B. polaris to establish itself in northern and eastern Greenland. The presence of five haplotypes in the studied sequences from Greenland indicates a moderately high level of genetic diversity of B. polaris in Greenland, reflecting the successful adaptation of B. polaris populations. In the broader context of entomological life in the high Arctic, our results on B. polaris allow us to conclude that the survival of pollinating species in the high Arctic under the changing climate scenario depends not only on the weather but also on an individual’s opportunity to continue to locate suitable food sources, i.e. pollen and nectar in the case of B. polaris . This aspect, briefly touched upon in this study, is of relevance not just to B. polaris , but the Arctic entomofauna generally.
... Gene flow among populations and the dispersal capacity of individuals are essential for the maintenance of genetic diversity over time, which is crucial for species survival (Maebe et al. 2019a). Indeed, low levels of intraspecific genetic diversity can restrict the potential of species to adapt to environmental change (Frankham 2005;Zayed 2009;Habel et al. 2014;Koch et al. 2017;Maebe et al. 2019aMaebe et al. , 2019b. Among the effects of limited dispersal capability, populations that were previously but are no longer well-connected can attain significant population structure (Frankham 2005;Kokko and López-Sepulcre 2006;Zayed 2009;Maebe et al. 2019b). ...
Article
In many organisms, habitat affects ecological and genetic diversity and, for certain species, it is expected that a large population should have higher genetic diversity than a smaller population. We analysed the genetics of males of the orchid bee, Eulaema nigrita (Hymenoptera: Apidae) and examined the links between local abundance and habitat with genetic diversity. We also investigated the impact of landscape features on genetic population structure, through microsatellite and mitochondrial DNA analysis, among populations found across 700 km of Brazilian Atlantic forest fragments. We found that genetic variation was not a function of local abundance, but it correlated significantly with habitat. There was significant but low genetic differentiation among populations. We found a single mitochondrial DNA haplotype in all sequenced specimens, which may be widespread throughout the Atlantic forest. Our results reinforce the idea that orchid bees can fly long distances. High-dispersal capacity, together with insufficient time in eventual isolation, can directly contribute to the high degree of similarity among populations for this species, despite their wide geographical distribution.
... Hence, they represent invaluable and irreplaceable assets for reconstructing patterns and processes of evolution across time and space (Habel, Husemann, Finger, Danley, & Zachos, 2014;Kemp, 2015;Peacock, Hekkala, Kirchoff, & Heki, 2017;Wandeler, Hoeck, & Keller, 2007;Yeates, Zwick & Mikheyev, 2016) and are unique archives for biodiversity (Rocha et al., 2014). These collections have played key roles in many scientific discoveries that changed our knowledge about the environment and our place in the natural world (Funk, 2018). ...
Article
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Millions of scientific specimens are housed in museum collections, a large part of which are fluid preserved. The use of formaldehyde as fixative and subsequent storage in ethanol is especially common in ichthyology and herpetology. This type of preservation damages DNA and reduces the chance of successful retrieval of genetic data. We applied ancient DNA extraction and single stranded library construction protocols to a variety of vertebrate samples obtained from wet collections and of different ages. Our results show that almost all samples tested yielded endogenous DNA. Archival DNA extraction was successful across different tissue types as well as using small amounts of tissue. Conversion of archival DNA fragments into single‐stranded libraries resulted in usable data even for samples with initially undetectable DNA amounts. Subsequent target capture approaches for mitochondrial DNA using home‐made baits on a subset of 30 samples resulted in almost complete mitochondrial genome sequences in several instances. Thus, application of ancient DNA methodology makes wet collection specimens, including type material as well as rare, old or extinct species, accessible for genetic and genomic analyses. Our results, accompanied by detailed step‐by‐step protocols, are a large step forward to open the DNA archive of museum wet collections for scientific studies.
... A different approach uses the preserved specimens itself in museum genomic analyses [73,74]. Both decline and expansion should leave population genetic signatures, i.e. changes in effective population size [75][76][77][78][79][80], which can be inferred from a few specimens [81]. This is certainly an exciting new route to explore the potential of natural history collections. ...
Article
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Changing species assemblages represent major challenges to ecosystems around the world. Retracing these changes is limited by our knowledge of past biodiversity. Natural history collections represent archives of biodiversity and are therefore an unparalleled source to study biodiversity changes. In the present study, we tested the value of natural history collections for reconstructing changes in the abundance and presence of species over time. In total, we scrutinized 17 080 quality-checked records for 242 epibenthic invertebrate species from the North and Baltic Seas collected throughout the last 200 years. Our approaches identified eight previously reported species introductions, 10 range expansions, six of which are new to science, as well as the long-term decline of 51 marine invertebrate species. The cross-validation of our results with published accounts of endangered species and neozoa of the area confirmed the results for two of the approaches for 49 to 55% of the identified species, and contradicted our results for 9 to 10%. The results based on relative record trends were less validated. We conclude that, with the proper approaches, natural history collections are an unmatched resource for recovering early species introductions and declines.
... While this research has produced important insights into how populations evolve in urban areas, ecologists recognize that results from analyses across space do not always replicate results from analyses through time (Johnson & Miyanishi, 2008;Wolkovich et al., 2012). This is also true for evolutionary biology, where temporal sampling can help disentangle the effects of multiple selective pressures, reveal signatures of selection obscured by demography, and facilitate clearer understandings of evolutionary processes (Habel, Husemann, Finger, Danley, & Zachos, 2013;Mathieson et al., 2015;Shultz, Baker, Hill, & Nolan, 2016). The specimens housed in natural history museums can provide this critical temporal study design. ...
... Natural history collections span from the seventeenth century on, making them invaluable representations of a record of anthropogenic change on a global scale (Nelson and Ellis, 2018). The value of these historic specimens lies in their ability to be used in time-series data, representing multiple collecting events of a locality or generations of a species over time (Lister and Climate Change Research Group, 2011;Habel et al., 2014;Holmes et al., 2016). Despite the nearly unlimited potential of natural history collections, they are under threat from lack of funding, cuts to stewardship positions (curators, collections managers, researchers), and lack of space. ...
Article
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Natural history collections are critical for modern scientific investigations, which are greatly expanding on the potential data applications of historic specimens. However, using these specimens outside their original intent introduces biases and potential misinterpretations. Anthropogenic biases can be introduced at any point during the life of museum specimens, from collection, preparation, and accession, to digitization. These biases can cause significant effects when the user is unaware of the collection context, as specific collection biases are often known anecdotally, but not ubiquitously. In this case study, the University of Kansas collection of Spence Shale Lagerstätte material was examined for anthropogenic biases using a collections inventory, interviews with stakeholders, and a literature review. Biases were found related to collector interest, locality preference, and researcher interest and specialization. These biases create a distorted view on the diversity and ecology of the Spence Shale, and need to be considered in future research.
... While this research has produced important insights into how populations evolve in urban areas, ecologists recognize that results from analyses across space do not always replicate results from analyses through time (Johnson & Miyanishi, 2008;Wolkovich et al., 2012). This is also true for evolutionary biology, where temporal sampling can help disentangle the effects of multiple selective pressures, reveal signatures of selection obscured by demography, and facilitate clearer understandings of evolutionary processes (Habel, Husemann, Finger, Danley, & Zachos, 2013;Mathieson et al., 2015;Shultz, Baker, Hill, & Nolan, 2016). The specimens housed in natural history museums can provide this critical temporal study design. ...
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Urban environments are among the fastest changing habitats on the planet, and this change has evolutionary implications for the organisms inhabiting them. Herein, we demonstrate that natural history collections are critical resources for urban evolution studies. The specimens housed in these collections provide great potential for diverse types of urban evolution research, and strategic deposition of specimens and other materials from contemporary studies will determine the resources and research questions available to future urban evolutionary biologists. As natural history collections are windows into the past, they provide a crucial historical timescale for urban evolution research. While the importance of museum collections for research is generally appreciated, their utility in the study of urban evolution has not been explicitly evaluated. Here, we: A) demonstrate that museum collections can greatly enhance urban evolution studies, B) review patterns of specimen use and deposition in the urban evolution literature, C) analyze how urban vs. rural and native vs. nonnative vertebrate species are being deposited in museum collections, and D) make recommendations to researchers, museum professionals, scientific journal editors, funding agencies, permitting agencies, and professional societies to improve archiving policies. Our analyses of recent urban evolution studies reveal that museum specimens can be used for diverse research questions, but they are used infrequently. Further, although nearly all studies we analyzed generated resources that could be deposited in natural history collections (e.g. collected specimens), a minority (12%) of studies actually did so. Depositing such resources in collections is crucial to allow the scientific community to verify, replicate, and/or re‐visit prior research. Therefore, to ensure that adequate museum resources are available for future urban evolutionary biology research, the research community–– from practicing biologists to funding agencies and professional societies must make adjustments that prioritize the collection and deposition of urban specimens.
... Nevertheless, the exploration of adaptive processes of microbial communities, including changes in the total microbial structure and on specific groups remains challenging, because it requires a pertinacious effort to obtain detailed, accurate measurements of both physical and biological factors (Podell et al. 2014). The analysis of communities sampled at sequential moments can lend insight toward understanding the underlying environmental drivers causing the shifts in the communities' structure over time (Habel et al. 2014). Frequent and long-term observations of the biotic and abiotic components in HAAL are required, especially to know the seasonal variations of the microbiota in those extreme environments . ...
Chapter
Puna wetlands and salars are a unique extreme environment all over the world, since their locations are in high-altitude saline deserts, largely influenced by volcanic activity. Ultraviolet radiation, arsenic content, high salinity, and low dissolved oxygen content, together with extreme daily temperature fluctuations and oligotrophic conditions, shape an environment that recreates the early Earth and, even more so, extraterrestrial conditions. Microbes inhabiting extreme environments face these conditions with different strategies, including formation of intricate microbial communities with an increasing degree of complexity. In that way, biofilms, mats, endoevaporitic mats, domes, and microbialites have been found to exist in association with salars, lagoons, and even volcanic fumaroles in Central Andean extreme environments. They form microbial ecosystems, where light and O2 availability decrease with depth stratification, promoting functional group diversity. This microbial diversity, together with the geochemistry, may favor the precipitation of minerals. This chapter summarizes general concepts in the environmental microbiology of extreme Andean ecosystems, which are explored throughout this book.
... However, an intriguing issue that emerged over the last decades is related to the temporal dynamics of genetic changes, notably for demographically declining populations (Osborne, Carson, & Turner, 2012;Spielman et al., 2004). Most studies assessed genetic changes associated with demographic declines using snapshot approaches, but several authors started to claim that combining continuous-in-time genetic monitoring and demographic surveys would be the ideal design to assess the sustainability of wild (and endangered) populations (Habel, Husemann, Finger, Danley, & Zachos, 2014;Schwartz, Luikart, & Waples, 2007; but see Osborne et al., 2012). Demographic and genetic changes could either be linear over time or follow tipping point dynamics, which has very different consequences for the long-term viability of populations (Hoban et al., 2014). ...
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Rivers are fascinating ecosystems in which the eco-evolutionary dynamics of organisms are constrained by particular features, and biologists have developed a wealth of knowledge about freshwater biodiversity patterns. Over the last ten years, our group used a holistic approach to contribute to this knowledge by focusing on the causes and consequences of intraspecific diversity in rivers. We conducted empirical works on temperate permanent rivers from Southern France, and we broadened the scope of our findings using experiments, meta-analyses and simulations. We demonstrated that intraspecific (genetic) diversity follows a spatial pattern (downstream increase in diversity) that is repeatable across taxa (from plants to vertebrates) and river systems. This pattern can result from interactive processes that we teased apart using appropriate simulation approaches. We further experimentally showed that intraspecific diversity matters for the functioning of river ecosystems. It indeed affects community dynamics, but also key ecosystem functions such as litter degradation. This means that losing intraspecific diversity in rivers can yield major ecological effects. Our work on the impact of multiple human stressors on intraspecific diversity revealed that-in the studied rivers systems-stocking of domestic (fish) strains strongly and consistently alters natural spatial patterns of diversity. It also highlighted the need for specific analytical tools to tease apart spurious from actual relationships in the wild. Finally, we developed original conservation strategies at the basin scale based on the systematic conservation planning framework that appeared pertinent for preserving intraspecific diversity in rivers. We identified several important research avenues that should further facilitate our understanding of patterns of local adaptation in rivers, the identification of processes sustaining intraspecific biodiversity-ecosystem function relationships, and the setting of reliable conservation plans.
... These observations are reminiscent of sympatric subpopulations sharing the same spatially, but not temporally, defined locations 43 With certain caveats, our analysis of recent genetic migration rates and directionality in the NEA may suggest an asymmetrical pattern of immigration into the Irish Sea (IoM sampling area). However, as some assumptions of the inference model were not met (low, constant migration rates and high F ST differentiation 46 ), these findings should be interpreted as a merged Irish Sea (IoM) sample set representing all NEA individuals at one time point, rather than source-sink population dynamics. ...
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Migratory movements in response to seasonal resources often influence population structure and dynamics. Yet in mobile marine predators, population genetic consequences of such repetitious behaviour remain inaccessible without comprehensive sampling strategies. Temporal genetic sampling of seasonally recurring aggregations of planktivorous basking sharks, Cetorhinus maximus, in the Northeast Atlantic (NEA) affords an opportunity to resolve individual re-encounters at key sites with population connectivity and patterns of relatedness. Genetic tagging (19 microsatellites) revealed 18% of re-sampled individuals in the NEA demonstrated inter/multi-annual site-specific re-encounters. High genetic connectivity and migration between aggregation sites indicate the Irish Sea as an important movement corridor, with a contemporary effective population estimate (Ne) of 382 (CI = 241–830). We contrast the prevailing view of high gene flow across oceanic regions with evidence of population structure within the NEA, with early-season sharks off southwest Ireland possibly representing genetically distinct migrants. Finally, we found basking sharks surfacing together in the NEA are on average more related than expected by chance, suggesting a genetic consequence of, or a potential mechanism maintaining, site-specific re-encounters. Long-term temporal genetic monitoring is paramount in determining future viability of cosmopolitan marine species, identifying genetic units for conservation management, and for understanding aggregation structure and dynamics.
... Large reference collections of specimens are of paramount importance for both disciplines. They are required to confirm the status of new species by comparison with those that are already known, but also to infer species distributions, and to assess changes in species abundances and range shifts through time series (Habel et al. 2013). Such collections are principally held by natural history museums which today serve as libraries and infrastructure for biodiversity research. ...
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Scorpions have always inspired fear and fascination because of the potency of their venoms. Although this ancient arachnid group is relatively small (ca. 2400 species) and has been continuously studied for the past century, the taxonomy is still in a state of flux and the correct identification of species often remains difficult. With more than 725 species and 9000 specimens, the Zoological Museum in Hamburg (ZMH) holds one of the largest and most significant scorpion collections in the world. This collection also contains many historical types described by Karl Kraepelin in the early 20 th century. In order to contribute to a more stable scorpion taxonomy and to assist future scorpion researchers, we present an illustrated and annotated catalogue of the ZMH scorpion collections. The type specimens of 89 species belonging to 10 families are documented, imaged and assessed alongside their primary data. For practical reasons, only the taxa belonging to the parvorder Iurida Soleglad et Fet, 2003 are presented here whilst the Parvorder Buthida Soleglad et Fet, 2003 will be catalogued in a second publication.
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Natural History Collections (NHCs) represent the world’s largest repositories of long-term biodiversity datasets. Specimen collection and voucher deposition has been the backbone of NHCs since their inception, but recent decades have seen a drastic decline in rates of growth via active collecting. Amphibians and reptiles are amongst the most threatened zoological groups on the planet and are historically underrepresented in most worldwide NHCs. As part of an ongoing project to review the Portuguese zoological collections in the country’s NHCs, herpetological data from its three major museums and smaller collections was gathered and used to examine the coverage and representation of the different taxa extant in Portugal. These collections are not taxonomically, geographically, or temporally complete. Approximately 90% of the Portuguese herpetological taxa are represented in the country’s NHCs, and around half of the taxa are represented by less than 50 specimens. Geographically, the collections cover less than 30% of the country’s territory and almost all of the occurring taxa have less than 10% of their known distribution represented in the collections. A discussion on the implications for science of such incomplete collections and a review of the current status of Portuguese NHCs is presented.
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Temporally fluctuating environmental conditions are a ubiquitous feature of natural habitats. Yet, how finely natural populations adaptively track fluctuating selection pressures via shifts in standing genetic variation is unknown. We generated high-frequency, genome-wide allele frequency data from a genetically diverse population of Drosophila melanogaster in extensively replicated field mesocosms from late June to mid-December, a period of ~12 generations. Adaptation throughout the fundamental ecological phases of population expansion, peak density, and collapse was underpinned by extremely rapid, parallel changes in genomic variation across replicates. Yet, the dominant direction of selection fluctuated repeatedly, even within each of these ecological phases. Comparing patterns of allele frequency change to an independent dataset procured from the same experimental system demonstrated that the targets of selection are predictable across years. In concert, our results reveal fitness-relevance of standing variation that is likely to be masked by inference approaches based on static population sampling, or insufficiently resolved time-series data. We propose such fine-scaled temporally fluctuating selection may be an important force maintaining functional genetic variation in natural populations and an important stochastic force affecting levels of standing genetic variation genome-wide.
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Highly social species are successful because they cooperate in obligately integrated societies. We examined temporal genetic variation in the eusocial wasp Vespula maculifrons in order to gain a greater understanding of evolution in highly social taxa. First, we wished to test if effective population sizes of eusocial species were relatively low due to the reproductive division of labor that characterizes eusocial taxa. We thus estimated the effective population size of V. maculifrons by examining temporal changes in population allele frequencies. We sampled the genetic composition of a V. maculifrons population at three separate time points spanning a 13-year period. We found that effective population size ranged in the hundreds of individuals, which is similar to estimates in other, non-eusocial taxa. Second, we estimated levels of polyandry in V. maculifrons in different years in order to determine if queen mating system varied over time. We found no significant change in the number or skew of males mated to queens. In addition, mating skew was not significant within V. maculifrons colonies. Therefore, our data suggest that queen mate number may be subject to stabilizing selection in this taxon. Overall, our study provides novel insight into the selective processes operating in eusocial species by analyzing temporal genetic changes within populations.
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Hypersaline environments are considered to be hostile environments due to their extreme conditions, such as high salinity and temperature. However, unicellular organisms from the three domains of life—Bacteria, Archaea, and Eukarya—are present in high numbers in these habitats where salt precipitation occurs due to saturation. In this chapter, we analyze the microbial community inhabiting different athalassohaline environments (ranging from 29% to 44% salinity) located in the Argentinean Altiplano with an elevation of 1615–4560 m a.s.l. Recently, the description of the microbial diversity in sediments and brines of these high-altitude hypersaline Andean Lakes (HAAL) have been addressed using culture-dependent and -independent approaches, and the main findings will be further discussed here. Additionally, biodiversity has been explored for novel diversity and connectivity between communities, as well as the influence of the environmental parameters on the total structure of the community. The understanding of the specific microbial patterns, with the final aim of using these environments as models, may shed light on how the extreme selection pressures shaped this specific lifestyle.
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Next‐generation sequencing has greatly expanded the utility and value of museum collections by revealing specimens as genomic resources. As the field of museum genomics grows, so does the need for extraction methods that maximize DNA yields. For avian museum specimens, the established method of extracting DNA from toe pads works well for most specimens. However, for some specimens, especially those of birds that are very small or very large, toe pads can be a poor source of DNA. In this study, we apply two DNA extraction methods (phenol‐chloroform and silica column) to three different sources of DNA (toe pad, skin punch, and bone) from ten historical avian museum specimens. We show that a modified phenol‐chloroform protocol yielded significantly more DNA than a silica column protocol (e.g., Qiagen DNeasy Blood & Tissue Kit) across all tissue types. However, extractions using the silica column protocol contained longer fragments on average than those using the phenol‐chloroform protocol, likely a result of loss of small fragments through the silica column. While toe pads yielded more DNA than skin punches and bone fragments, skin punches proved to be a reliable alternative source of DNA and might be especially appealing when toe pad extractions are impractical. Overall, we found that historical bird museum specimens contain substantial amounts of DNA for genomic studies under most extraction scenarios, but that a phenol‐chloroform protocol consistently provides the high quantities of DNA required for most current genomic protocols. This article is protected by copyright. All rights reserved.
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Population genomics has the potential to improve studies of evolutionary genetics, molecular ecology and conservation biology, by facilitating the identification of adaptive molecular variation and by improving the estimation of important parameters such as population size, migration rates and phylogenetic relationships. There has been much excitement in the recent literature about the identification of adaptive molecular variation using the population-genomic approach. However, the most useful contribution of the genomics model to population genetics will be improving inferences about population demography and evolutionary history.
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We describe a procedure for rapid purification of high quality DNA from either fresh or dry Orthoptera, suitable for the PCR amplification of DNA regions more than 800 bp long (even from oldest specimens), which allows genetic analyses on animals from collections without the complete specimen disruption.
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The Eastern Afromontane cloud forests occur as geographically distinct mountain exclaves. The conditions of these forests range from large to small and from fairly intact to strongly degraded. For this study, we sampled individuals of the forest bird species, the Montane White-eye Zosterops poliogaster from 16 sites and four mountain archipelagos. We analysed 12 polymorphic microsatellites and three phenotypic traits, and calculated Species Distribution Models (SDMs) to project past distributions and predict potential future range shifts under a scenario of climate warming. We found well-supported genetic and morphologic clusters corresponding to the mountain ranges where populations were sampled, with 43% of all alleles being restricted to single mountains. Our data suggest that large-scale and long-term geographic isolation on mountain islands caused genetically and morphologically distinct population clusters in Z. poliogaster. However, major genetic and biometric splits were not correlated to the geographic distances among populations. This heterogeneous pattern can be explained by past climatic shifts, as highlighted by our SDM projections. Anthropogenically fragmented populations showed lower genetic diversity and a lower mean body mass, possibly in response to suboptimal habitat conditions. On the basis of these findings and the results from our SDM analysis we predict further loss of genotypic and phenotypic uniqueness in the wake of climate change, due to the contraction of the species' climatic niche and subsequent decline in population size.Heredity advance online publication, 9 April 2014; doi:10.1038/hdy.2014.15.
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Temporal changes in allele frequencies are often assumed in studies addressing the history of populations affected by different anthropogenic and natural impacts at different time scales. Yet, few studies directly compare the genetic composition of populations over time spans of more than 10 years. Therefore, to test the genetic effects of 15 years of population isolation in the butterfly Lycaena helle, we analysed 472 individuals from 27 samples, of which nine were collected in 1991 and 18 in 2006. Sampling was performed in five mountain regions (Pyrenees, Massif Central, Jura, Vosges and Ardennes). Genetic analyses were performed using five polymorphic microsatellites. Old and new samples of identical or neighbouring populations revealed similar genetic differentiations among these five mountain regions. A comparatively strong genetic differentiation among populations combined with a high amount of private alleles for each mountain area was detected, but mountain-specific alleles were in most cases identical in 1991 and 2006. Nevertheless, the obtained data also indicate moderate changes between 1991 and 2006 in the species' genetic structure - genetic differentiation among local populations increased marginally and allele frequencies showed corresponding modifications. A significant decline in genetic diversity was not detectable, and nine private alleles exclusive to a single mountain region were only detected in samples from the year 1991, whereas eleven were only observed in the individuals collected in 2006. These observations might indicate the results of genetic drift within isolated populations.
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Habitats often show similar present structuring, but contrasting histories: habitats occur naturally fragmented due to abiotic or biotic factors over long time periods, but may also have become fragmented only recently through transformation from interconnected to highly fragmented habitats within short time periods. Species and populations being faced with such contrasting habitat scenarios also show contrasting responses at species and intraspecific level. Organisms and populations from naturally fragmented habitats may show a reduction in their genetic load (purging) due to purifying selection in isolation. In contrast, sudden habitat transformations from interconnected to highly fragmented structures and the resulting transition from gene flow or panmixia to strong population differentiation often have negative effects on biota; while species occur in interconnected population networks (maintaining a high proportion of genetic diversity), a sudden breakdown of gene flow may lead to a severe loss of genetic diversity and the manifestation of weakly deleterious alleles. In consequence, fragmented habitats need not have a negative impact on species per se, but the history of habitat structures, particularly fast transformation processes, may severely affect the persistence and fitness of species.
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We analyzed mtDNA polymorphisms (a total of 741bp from a part of conserved control region, ND5, ND2, Cyt b and 12S) in 91 scats and 12 tissue samples of Bengal tiger (Panthera tigris tigris) populations across Terai Arc Landscape (TAL) located at the foothills of Himalayas in North Western India, Buxa Tiger Reserve (BTR), and North East India. In TAL and BTR, we found a specific haplotype at high frequency, which was absent elsewhere, indicating a genetically distinct population in these regions. Within the TAL region, there is some evidence for genetic isolation of the tiger populations west of river Ganges, i.e., in the western part of Rajaji National Park (RNP). Although the river itself might not constitute a significant barrier for tigers, recent human-induced changes in habitat and degradation of the Motichur-Chilla Corridor connecting the two sides of the tiger habitat of RNP might effectively prevent genetic exchange. A cohesive population is observed for the rest of the TAL. Even the more eastern BTR belongs genetically to this unit, despite the present lack of a migration corridor between BTR and TAL. In spite of a close geographic proximity, Chitwan (Nepal) constitutes a tiger population genetically different from TAL. Moreover, it is observed that the North East India tiger populations are genetically different from TAL and BTR, as well as from the other Bengal tiger populations in India.
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Salmonid fishes exhibit high levels of population differentiation. In particular, the brown trout (Salmo trutta L.) demonstrates complex within river drainage genetic structure. Increasingly, these patterns can be related to the underlying evolutionary models, of which three scenarios (member-vagrant hypothesis, metapopulation model and panmixia) facilitate testable predictions for investigations into population structure. We analysed 1225 trout collected from the River Dart, a 75 km long river located in southwest England. Specimens were collected from 22 sample sites across three consecutive summers (2001–2003) and genetic variation was examined at nine microsatellite loci. A hierarchical analysis of molecular variance revealed that negligible genetic variation was attributed among temporal samples. The highest levels of differentiation occurred among samples isolated above barriers to fish movement, and once these samples were removed, a significant effect of isolation-by-distance was observed. These results suggest that, at least in the short-term, ecological events are more important in shaping the population structure of Dart trout than stochastic extinction events, and certainly do not contradict the expectations of a member-vagrant hypothesis. Furthermore, individual-level spatial autocorrelation analyses support previous recommendations for the preservation of a number of spawning sites spaced throughout the tributary system to conserve the high levels of genetic variation identified in salmonid species.
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Scats from marine otters were collected from the entire Peruvian distribution range along the Pacific coast. Partial mtDNA control region sequences (265bp) were successfully amplified and analysed in 37 out of 87 samples. Based on spatial distribution and home range information of marine otters we assumed our final data set to represent at least 24 different individuals, yielding surprisingly high genetic variability (11 haplotypes, h=0.86, π=0.0117). No unequivocal evidence of genetic substructuring, a bottleneck or isolation by distance could be detected. This study presents the first genetic data in this endangered species and highlights the significance of the Peruvian gene pool for the establishment of reserves, potential future expansion, recolonisation or translocations. Keywords Lontra felina -Mitochondrial control region-Non-invasive genetic sampling-Peru
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Temporal genetic data may be used forestimating effective population size (N e) and for addressing the `temporal stability' of population structure, two issues of central importance for conservation and management. In this paper we assess the amount of spatio-temporal genetic variation at 17 di-allelic allozyme loci and estimate current N e in two populations of stream resident brown trout (Salmo trutta) using data collected over 20 years. The amount ofpopulation divergence was found to bereasonably stable over the studied time period.There was significant temporal heterogeneitywithin both populations, however, and N e was estimated as 19 and 48 for the twopopulations. Empirical estimates of theprobability of detecting statisticallysignificant allele frequency differencesbetween samples from the same populationseparated by different numbers of years wereobtained. This probability was found to befairly small when comparing samples collectedonly a few years apart, even for theseparticular populations that exhibit quiterestricted effective sizes. We discuss someimplications of the present results for browntrout population genetics and conservation, andfor the analysis of temporal genetic change inpopulations with overlapping generations ingeneral.
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Multi-locus monomorphism in microsatellites is practically non-existent, with one notable exception, the island fox (Urocyon littoralis dickeyi) population on San Nicolas island off the coast of southern California, having been called “the most monomorphic sexually reproducing animal population yet reported”. Here, we present the unprecedented long-term monomorphism in relict populations of the highly endangered Parnassius apollo butterfly, which is protected by CITES and classified as “threatened” by the IUCN. The species is disjunctly distributed throughout the western Palaearctic and has occurred in several small remnant populations outside its main distribution area. We screened 78 individuals from 1 such relict area (Mosel valley, Germany) at 16 allozyme and 6 microsatellite loci with the latter known to be polymorphic in this species elsewhere. From the same area, we also genotyped 55 museum specimens sampled from 1895 to 1989 to compare historical and present levels of genetic diversity. However, none of all these temporal populations yielded any polymorphism. Thus, present and historical butterflies were completely monomorphic for the same fixed allele. This is the second study to report multi-locus monomorphism for microsatellites in an animal population and the first one to prove this monomorphism not to be the consequence of recent factors. Possible explanations for our results are a very low long-term effective population size and/or a strong historic bottleneck or founder event. Since the studied population has just recovered from a recent population breakdown (second half of twentieth century) and no signs of inbreeding depression have been detected, natural selection might have purged the population of weakly deleterious alleles, thus rendering it less susceptible to the usual negative corollaries of high levels of homozygosity and low effective population size.
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DNA that has been recovered from archaeological and palaeontological remains makes it possible to go back in time and study the genetic relationships of extinct organisms to their contemporary relatives. This provides a new perspective on the evolution of organisms and DNA sequences. However, the field is fraught with technical pitfalls and needs stringent criteria to ensure the reliability of results, particularly when human remains are studied.
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The amounts of inbreeding depression upon selfing and of heterosis upon outcrossing determine the strength of selection on the selfing rate in a population when this evolves polygenically by small steps. Genetic models are constructed which allow inbreeding depression to change with the mean selfing rate in a population by incorporating both mutation to recessive and partially dominant lethal and sublethal alleles at many loci and mutation in quantitative characters under stabilizing selection. The models help to explain observations of high inbreeding depression (> 50%) upon selfing in primarily outcrossing populations, as well as considerable heterosis upon outcrossing in primarily selfing populations. Predominant selfing and predominant outcrossing are found to be alternative stable states of the mating system in most plant populations. Which of these stable states a species approaches depends on the history of its population structure and the magnitude of effect of genes influencing the selfing rate.
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Abstract Although studies of population genetic structure are very common, whether genetic structure is stable over time has been assessed for very few taxa. The question of stability over time is particularly interesting for frogs because it is not clear to what extent frogs exist in dynamic metapopulations with frequent extinction and recolonization, or in stable patches at equilibrium between drift and gene flow. In this study we collected tissue samples from the same five populations of leopard frogs, Rana pipens, over a 22–30 year time interval (11–15 generations). Genetic structure among the populations was very stable, suggesting that these population were not undergoing frequent extinction and colonization. We also estimated the effective size of each population from the change in allele frequencies over time. There exist few estimates of effective size for frog populations, but the data available suggest that ranid frogs may have much larger ratios of effective size (Ne) to census size (Nc) that toads (bufonidae). Our results indicate that R. pipiens populations have effective sizes on the order of hundreds to at most a few thousand frogs, and Nee/Nc ratios in the range of 0.1–1.0. These estimates of Ne/Nc are consistent with those estimated for other Rana species. Finally, we compared the results of three temporal methods for estimating Ne. Moment and pseudolikelihood methods that assume a closed population gave the most similar point estimates, although the moment estimates were consistently two to four times larger. Wang and Whitlock's new method that jointly estimates Ne and the rate of immigration into a population (m) gave much smaller estimates of Ne and implausibly large estimates of m. This method requires knowing allele frequencies in the source of immigrants, but was thought to be insensitive to inexact estimates. In our case the method may have failed because we did not know the true source of immigrants for each population. The method may be more sensitive to choice of source frequencies than was previously appreciated, and so should be used with caution if the most likely source of immigrants cannot be identified clearly.
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Next-generation sequencing technologies are making a substantial impact on many areas of biology, including the analysis of genetic diversity in populations. However, genome-scale population genetic studies have been accessible only to well-funded model systems. Restriction-site associated DNA sequencing, a method that samples at reduced complexity across target genomes, promises to deliver high resolution population genomic dataçthousands of sequenced markers across many individuals-for any organism at reasonable costs. It has found application in wild populations and non-traditional study species, and promises to become an important technology for ecological population genomics. © The Author 2011. Published by Oxford University Press. All rights reserved.
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The amounts of inbreeding depression upon selfing and of heterosis upon outcrossing determine the strength of selection on the selfing rate in a population when this evolves polygenically by small steps. Genetic models are constructed which allow inbreeding depression to change with the mean selfing rate in a population by incorporating both mutation to recessive and partially dominant lethal and sublethal alleles at many loci and mutation in quantitative characters under stabilizing selection. The models help to explain observations of high inbreeding depression (>50%) upon selfing in primarily outcrossing populations, as well as considerable heterosis upon outcrossing in primarily selfing populations. Predominant selfing and predominant outcrossing are found to be alternative stable states of the mating system in most plant populations. Which of these stable states a species approaches depends on the history of its population structure and the magnitude of effect of genes influencing the selfing rate.
Article
Anthropogenic impact such as overhunting and habitat fragmentation has reduced the total red deer population (Cervus elaphus) across Europe. In Germany remaining subpopulations are even confined to designated areas with limited or no gene flow among them. Red deer populations inhabiting the Bavarian–Bohemian forest ecosystem had been divided by a fortified State border between Germany and former Czechoslovakia. To assess red deer genetic diversity more than two decades after the removal of the fortifications, we analysed a population from the Bavarian Forest National Park, Germany, and one from the National Park Šumava, Czech Republic, using 11 microsatellite loci and a 910 bp long section of the mitochondrial control region (mtDNA). Bayesian analyses of microsatellite allele frequencies favoured the presence of a single population in the Bavarian-Bohemian forest ecosystem over other population genetic structures. This admixture was supported by a lack of population pairwise differentiation between German and Czech red deer microsatellite genotypes in the analysis of molecular variance (AMOVA, FST = 0.009, p = 0.383). Contrastingly, AMOVA revealed a highly significant matrilinear differentiation of mtDNA between the two samples (ΦST = 0.285, p = 0.002), whereby German red deer belonged predominantly to haplogroup A (western Europe) and Czech red deer predominantly to haplogroup C (eastern Europe). In combination, these findings indicated a high degree of philopatry by does and extensive gene flow across the former border mediated by stags. They also identified the Bavarian–Bohemian forest ecosystem as part of a suture zone between western and eastern European red deer matrilines.
Article
The distribution of genetic variation in Texas stream fishes has been shaped by a complex mix of historical and anthropogenic factors. Although Texas was not glaciated during the Pleistocene, the rise in sea level following this epoch isolated formerly connected drainages. More recently, the construction of dams, modifications of stream systems, and the release of commercially raised fish have influenced the patterns of genetic diversity. To examine how these different factors have impacted Texas stream fishes, we compared the genetic structure of five species of fish spanning two families and inhabiting two adjacent drainages: Lepomis megalotis, Lepomis cyanellus, Cyprinella lutrensis, Cyprinella venusta, and Campostoma anomalum. Our analyses of the mitochondrial D-Loop show that genetic patterns differ strongly across species. A phylogeographical split between the Brazos and Trinity drainages was seen in conspecific populations of Lepomis species and is probably the result of the historical separation of these river systems. In contrast, contemporary ecological and anthropogenic factors, such as the desiccation of streams during summer, and the translocation of bait fish, appear to have a stronger influence on the genetic patterns in the remaining species. The contrasting results demonstrate the importance of using a multi-species, comparative approach for landscape genetic studies as single species patterns may not be repre-sentative of others and thus may obscure differential effects of historical versus recent events as well as natural versus anthropogenic forces. By comparing closely related species that differ in their life history and economic importance it may be possible to disentangle the relative roles of historical, intrinsic, and anthropogenic influences on different organisms within a region. © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, • • , • • – • • .
Article
Maintaining genetic variation for future evolutionary change is an important issue for conservation biology. However, there is controversy over the effective population size (Ne) required for endangered species to retain their evolutionary potential, with proposed sizes ranging from 500 to 5000. The highest estimate is based on the assumption that 90% of mutations are deleterious. We review the arguments for an effective size of 5000 and conclude that it assumes effective mutation rates that are too low, and heritabilities that are, in general, very high. We conclude that an Ne of 500-1000 is appropriate at this time.
Article
In the ocean, large-scale dispersal and replenishment by larvae is a key process underlying biological changes associated with global warming. On tropical reefs, coral bleaching, degradation of habitat and declining adult stocks are also likely to change contemporary patterns of dispersal and gene flow and may lead to range contractions or expansions. On the Great Barrier Reef, where adjacent reefs form a highly interconnected system, we use allozyme surveys of c. 3000 coral colonies to show that populations are genetically diverse, and rates of gene flow for a suite of five species range from modest to high among reefs up to 1200 km apart. In contrast, 700 km further south on Lord Howe Island, genetic diversity is markedly lower and populations are genetically isolated. The virtual absence of long-distance dispersal of corals to geographically isolated, oceanic reefs renders them extremely vulnerable to global warming, even where local threats are minimal.
Article
Aim This paper has three aims: (1) to reconstruct the population history of a flightless silvicolous (forest) ground beetle in a region where strong anthropogenic activity has altered the connectivity of the landscape; (2) to estimate the effects of both contemporary and historical landscape structure on the genetics of populations; and (3) to investigate the reasons for clinal variation in one gene locus found in an earlier study carried out in the same geographical location. Location Münster (Westphalia), north-west Germany. Methods We investigated 26 populations of the ground beetle Carabus auronitens Fabricius, 1792 by analysing seven polymorphic microsatellite loci and an allozyme locus. Samples of at least 16 individuals per site were studied. These were obtained from dry pitfall traps placed at 23 sites and from three additional (refuge) populations. We used regression and correlation analyses to investigate the effects of both historical and contemporary landscape structure on the allele frequency distributions of the investigated loci. Spatial autocorrelation analysis was used to study possible clinal variations, and admixture rates were calculated in order to assess the genetic influence of populations from possible refuges. Possible reasons for the development of the cline were examined using simulation models. Results The allele frequency distributions at the investigated loci could not be explained by selection or isolation by distance. We found clinal variation in 50% of the investigated loci and our simulations indicated that this was unlikely to have developed by chance. Admixture rates show significant influences of the investigated refuge populations on the populations under study. Main conclusions The findings strongly suggest that the clinal variation is secondary. It results from recolonization of the area by C. auronitens from multiple refuges after anthropogenic landscape changes caused forest fragmentation and led to species isolation.
Article
Patterns of genetic diversity are strongly influenced by the history of populations, which is often ignored when examining the viability of populations. We studied the relationship of population size, genetic variation, and fitness in the perennial herb Vincetoxicum hirundinaria (Asclepiadaceae) in the southwestern archipelago of Finland, where this species occurs commonly on many of the islands and its distribution is highly fragmented. We measured the magnitude and distribution of genetic variation in this species to examine how patterns of genetic diversity reflect population history, especially the colonization pattern of the islands and the mating system. Additionally, we used the genetic data to interpret previous results that suggest that fitness variation among populations is not directly related to population size. We found a high level of genetic variation (He = 0.396) and a low level of genetic differentiation (FST = 0.052) among the populations. In contrast to several rare plant species, the level of genetic variation (H e) was not correlated with population size or with male or female fitness of the plants. Our results also indicated that inbreeding is common in all populations regardless of their size (mean FIS = 0.460) but that it does not correlate significantly with male or female fitness traits. The observed patterns of genetic variation suggest that this species has a mixed mating system. Taken together, these results indicate that the studied populations are of recent common ancestry but may also have relatively high levels of current gene flow. The differences between our results and those from previous studies of rare plant species with a fragmented distribution pattern emphasize the importance of considering whether fragmentation is caused by recent human activities or whether it reflects a distribution pattern characteristic of the species when evaluating the conservation needs of the species.
Article
Archived scales and otoliths constitute a unique source of DNA that potentially enables extension of the temporal scale of genetic studies of fish populations by decades and even centuries. We review recent insights into fish population and conservation genetics obtained using analysis of DNA from archived samples. This involves both new knowledge about demographic parameters and population structure in wild populations and insights into consequences of anthropogenic pressure resulting from over-harvesting, habitat degradation and stocking. We show that the latter category of studies have led to significant changes of management practices. Ongoing improvement of genetic methods will undoubtedly further expand the ability to utilize historical DNA samples. We envisage that temporal comparisons of large numbers of coding genes will lead to novel insights into selective responses of fish populations to anthropogenic challenges, particularly fisheries-induced selection and global warming. However, both acquisition and storage of historical DNA samples can be hurdles to temporal genetic analyses, while degradation and low copy number in historical DNA samples render genetic data from such sources prone to technical artefacts. We summarize recommendations for storage of samples and DNA extraction and provide checklists for validation of genotyping results. Finally, we stress that validation procedures also involve documentation of the time and population of origin of historical samples, and the inferences drawn should account for the technical and statistical uncertainties associated with historical DNA analysis.
Article
Population genetic studies on tunas are reviewed. These studies have focused on phylogenetic reconstructions, species identifications and stock delineation, and have used tools ranging from blood group and allozyme analysis to PCR-aided examination of mitochondrial DNA variation. Both allozyme and mtDNA approaches show tunas in the genus Thunnus to be very closely related to one another, but also indicate that the two presently recognized subspecies of northern bluefin tuna, Thunnus thynnus thynnus and T. t. orientalis, in fact may be worthy of species status. These techniques also permit the unequivocal recognition of specimens, which is not always possible on morphological grounds. However, it is arguable that, until recently, tunas have not received their due attention from geneticists given their commercial significance and the need for information on stock structure to ensure sustainable management. This may be because tunas are known to be highly vagile and therefore levels of population differentiation are expected to be low. None the less, population subdivision has been recorded in several species (skipjack, yellowfin, albacore), although this tends to be on a broad (intra- or inter-oceanic) rather than on a more local scale. New molecular tools, including the PCR-based analyses of nuclear genes and microsatellite loci, are yielding new, highly polymorphic markers, and will enable more powerful analyses of stock structure than have hitherto been possible.
Article
Most studies of the loss of genetic variation caused by bottlenecks in population size have used heterozygosity as a measure of genetic variation. In this paper, I compare the effects of bottlenecks on the loss of alleles, as well as the reduction in heterozygosity. Population bottlenecks of short duration will have little effect on heterozygosity but are expected to reduce severely the number of alleles present. Heterozygosity provides a good measure of the capability of a population to respond to selection immediately following a bottleneck. However, the number of alleles remaining is important for the long-term response to selection and survival of populations and species.
Article
Large populations, seemingly not at risk of extinction, can decline rapidly due to alteration of habitat. This appears to be the case of the butterfly Chazara briseis, which is declining in all of Central and Eastern Europe, even from apparently large areas of its steppe grassland habitats. We combined mark–recapture, allozyme electrophoresis and adult behaviour observation to study the last remaining metapopulation of this once-widespread butterfly in the Czech Republic. The total population estimate was 1300 males and 1050 females in 10 colonies within a 70 km2 landscape. Adults were long-lived, and inseminated females required several weeks before they started ovipositing. Models using realistic lengths of the preoviposition period estimated that due to background mortality, only 25–55% of the female census population lived long enough to contribute to the next generation. This demographic load was unlikely to be balanced by an increased fecundity. Allozyme electrophoresis of 22 loci revealed much higher allelic variation than in most other studies of butterflies living in small populations (mean heterozygosity: 20.7%). If expressed as per individual colony, the genetic variation did not correlate with population density, survival or longevity. This was probably due to frequent movements among colonies; during 8 weeks of adult flight, 5.1% of recaptured males and 3.6% of recaptured females moved between colonies. The high preoviposition mortality indicates that populations of this species must contain more individuals compared with populations not suffering this additional demographic load. The high allelic diversity of each single colony suggests that the population as a whole has not undergone genetic bottlenecks, but now may be facing risks of inbreeding depression due to allele frequency shifts and the possible increase of weakly deleterious alleles. In the past, high effective population sizes were maintained by frequent dispersal in dense networks of steppic grasslands. Generous habitat restoration is necessary to safeguard populations of this specialized, yet formerly common species.
Article
Inbreeding is common in plants and can have considerable effects on population viability, because of inbreeding depression. Understanding what determines the magnitude of inbreeding depression is of fundamental importance for conservation biology. We used meta-analysis of 116 studies and 107 plant species to investigate the effects of population size, test environment, life history characteristics and stage on the magnitude of inbreeding depression in 13 different fitness traits. We found that inbreeding depression levels significantly increase with population size. This may be a consequence of either, or both, a higher baseline of the level of inbreeding or increased impact of purging in small populations; unfortunately the available data did not allow distinguishing between these potential explanations. In general, inbreeding depression was found to be common across species and environments, and was significant in all traits examined. Yet, the magnitude of inbreeding depression was significantly influenced by plant longevity and life-history stage, and varied depending on how plant fitness was measured. Our findings highlight the fundamental role of population size in influencing the magnitude of inbreeding depression in plants. This clearly has important implications for conservation biology. Moreover, our findings on the overall generality of inbreeding depression confirm that inbreeding depression is one of the key factors reducing plant population fitness and viability. Hence, we need a better understanding on the architecture of inbreeding depression, how different ecological and historical conditions influence the levels of inbreeding depression in natural plant populations, and its impacts on community dynamics.
Article
1. Metapopulation dynamics – the recurrent extinction and colonization in spatially discrete habitats – is expected to strongly affect within and between population genetic diversity. So far, however, accounts of true plant metapopulations are extremely scarce. 2. We monitored the colonization and extinction dynamics of an assemblage of populations of the annual Erysimum cheiranthoides on stony river banks during three consecutive years. Each year, winter flooding drives some populations to extinction, while vacant banks may become colonized. We describe the dynamics of these ephemeral populations using amplified fragment length polymorphism (AFLP) markers to quantify changes in the metapopulation genetic structure over time, and assessing the direction and relative amount of migration and colonization events. 3. Average extinction and colonization rates were high (0.39 and 0.34, respectively). While population genetic differentiation (F ST) tripled from 0.06 in 2005 to 0.17 in 2007, total metapopulation genetic diversity remained fairly constant through the years. Genetic assignment analyses allowed assigning more than 50% of the genotyped individuals to populations extant the year before. Colonizing individuals originated from different source populations (ϕ << 1) and there was considerable evidence of upstream seed dispersal. 4. The degree and pattern of spatial genetic structure varied between years and was related to variation in the flooding intensity of the Meuse River through the years. Possibly, activation of the soil seed bank also played a role in structuring the genetic make-up of the populations. 5. Because migration and colonization events were qualitatively equal, and colonizing individuals originated from different sources, the increase in F ST was in agreement with previous theoretical work. Very high migration and colonization rates, and the short monitoring period, may explain why there was no loss of genetic diversity from the metapopulation through recurrent extinction and colonization events. 6. Synthesis. This study gives one of the first accounts of the dynamics of a true plant meta-population. Temporal monitoring of genetic variation gave evidence of extensive and bidirectional seed dispersal, highly variable and increasing genetic differentiation, and rather constant within population genetic diversity. An important suggestion from this research is to include a dormant seed stage in further theoretical work on (meta) population genetics.
Article
Genetic diversity is one of the three forms of biodiversity recognized by the World Conservation Union (IUCN) as deserving conservation. The need to conserve genetic diversity within populations is based on two arguments: the necessity of genetic diversity for evolution to occur, and the expected relation-ship between heterozygosity and population fitness. Because loss of genetic diversity is related to inbreed-ing, and inbreeding reduces reproductive fitness, a correlation is expected between heterozygosity and pop-ulation fitness. Long-term effective population size, which determines rates of inbreeding, should also be correlated with fitness. However, other theoretical considerations and empirical observations suggest that the correlation between fitness and heterozygosity may be weak or nonexistent. We used all the data sets we could locate (34) to perform a meta-analysis and resolve the issue. Data sets were included in the study, provided that fitness, or a component of fitness, was measured for three or more populations along with heterozygosity, heritability, and/or population size. The mean weighted correlation between measures of genetic diversity, at the population level, and population fitness was 0.4323. The correlation was highly sig-nificant and explained 19% of the variation in fitness. Our study strengthens concerns that the loss of het-erozygosity has a deleterious effect on population fitness and supports the IUCN designation of genetic di-versity as worthy of conservation. Correlación entre Adaptabilidad y Diversidad Genética Resumen: La diversidad genética es una de las tres formas de biodiversidad reconocidas por la Unión de Conservación Mundial (IUCN) que merecen ser conservadas.
Article
Relationships between plant population size, fitness and within‐population genetic diversity are fundamental for plant ecology, evolution and conservation. We conducted meta‐analyses of studies published between 1987 and 2005 to test whether these relationships are generally positive, whether they are sensitive to methodological differences among studies, whether they differ between species of different life span, mating system or rarity and whether they depend on the size ranges of the studied populations. Mean correlations between population size, fitness and genetic variation were all significantly positive. The positive correlation between population size and female fitness tended to be stronger in field studies than in common garden studies, and the positive correlation between genetic variation and fitness was significantly stronger in DNA than in isoenzyme studies. The strength and direction of correlations between population size, fitness and genetic variation were independent of plant life span and the size range of the studied populations. The mean correlations tended to be stronger for the rare species than for common species. Expected heterozygosity, the number of alleles and the number or proportion of polymorphic loci significantly increased with population size, but the level of inbreeding F IS was independent of population size. The positive relationship between population size and the number of alleles and the number or proportion of polymorphic loci was stronger in self‐incompatible than in self‐compatible species. Furthermore, fitness and genetic variation were positively correlated in self‐incompatible species, but independent of each other in self‐compatible species. The close relationships between population size, genetic variation and fitness suggest that population size should always be taken into account in multipopulation studies of plant fitness or genetic variation. The observed generality of the positive relationships between population size, plant fitness and genetic diversity implies that the negative effects of habitat fragmentation on plant fitness and genetic variation are common. Moreover, the stronger positive associations observed in self‐incompatible species and to some degree in rare species, suggest that these species are most prone to the negative effects of habitat fragmentation.
Article
We amplified microsatellite DNA from museum specimens over 100 years old of the adonis blue butterfly, Polyommatus bellargus. These results were compared with butterfly samples taken from the same site near Folkestone in southern UK in 1998/9, 200 generations later, and with samples from other extant UK populations. Dramatic changes in allele frequencies have occurred over time, which is indicative of substantial genetic drift or extinction/recolonization. Patterns of heterozygosity in the 1998/9 sample are indicative of a past bottleneck, and one was known to have occurred in the late 1970s in this and many other UK populations. One allele present at high frequency in 1896 was not detected in any extant UK population, suggesting that it may have been lost from the UK (a ‘ghost’ allele), although the allele may well persist elsewhere within the range of the species. Although the present study is relatively small in scale (20 museum specimens from one site), it serves to reinforce the enormous potential of museum specimens in well represented taxa such as butterflies for examining the effects of demographic events spanning many years. © 2006 The Linnean Society of London, Biological Journal of the Linnean Society, 2006, 88, 447–452.
Article
A fundamental assumption underlying the importance of genetic risks within conservation biology is that inbreeding increases the extinction probability of populations. Although inbreeding has been shown to have a detrimental impact on individual fitness, its contribution to extinction is still poorly understood. We have studied the consequences of different levels of prior inbreeding for the persistence of small populations using Drosophila melanogaster as a model organism. To this end, we determined the extinction rate of small vial populations differing in the level of inbreeding under both optimal and stress conditions, i.e. high temperature stress and ethanol stress. We show that inbred populations have a significantly higher short-term probability of extinction than non-inbred populations, even for low levels of inbreeding, and that the extinction probability increases with increasing inbreeding levels. In addition, we observed that the effects of inbreeding become greatly enhanced under stressful environmental conditions. More importantly, our results show that the impact of environmental stress becomes significantly greater for higher inbreeding levels, demonstrating explicitly that inbreeding and environmental stress are not independent but can act synergistically. These effects seem long lasting as the impact of prior inbreeding was still qualitatively the same after the inbred populations had been expanded to appreciable numbers and maintained as such for approximately 50 generations. Our observations have significant consequences for conservation biology.
Chapter
Insular middle mountains of Central Europe, such as Jesenik Mts. (max. altitude 1,495 m) and Krkonose Mts. (1,602 m), both in the Sudeten system, are poor in relic species, but the relic populations are suitable for studying the population responses to recent climatic change. There are two relic butterflies that are native to Jesenik Mts., each traditionally classified as an endemic subspecies: Erebia sudetica sudetica (Staudinger, 1851), a species protected by the EU Habitat Directive, and E. epiphron silesiana Meyer & Dür, 1852. Whereas Jesenik E. epiphron forms continuous populations, restricted to summit Nardus-dominated grasslands and not entering forested elevations, the distribution of Jesenik E. sudetica forms an archipelago at wet timberline sites and at clearings within mountain forests. Although both species avoid mountain forests, their lower distribution limits seem to be mediated by a limited range of available habitats, rather than of direct ecophysiological constraints. A non-native population of E. epiphron in Krkonose, transferred from the Jesenik in the 1930s, descends to ca 1,100 m, colonizing large clearings with cultural hay meadows within the forest belt. There is also behavioral and molecular evidence that E. epiphron cannot disperse through continuous forest. On the other hand, E. sudetica has a better dispersal power, and recent monitoring of its native Jesenik distribution suggests active colonization of woodland clearings. Thus, both butterflies can survive an altitudinal increase of the timberline, provided open habitats within the forests are secured. This conjecture suggests that these two and other alpine species survived past warmer periods of the Holocene in mountains, such as Jesenik owing to disturbance dynamics that never allowed complete forest closure. In the higher Krkonose, in contrast, they probably lacked suitable open habitats because of the encroachment of such sites by Pinus mugo dwarf pine, which is native to Krkonose but non-native to Jesenik.
Article
Human activities are simultaneously decreasing the size of wildlife populations (causing inbreeding) and increasing the level of stress that wildlife populations must face. Inbreeding reduces population fitness and increases extinction risk. However, very little information on the impact of stressful environments on extinction risk under inbreeding is available. We evaluated the impact of full sib inbreeding on extinction risk, using Drosophila melanogaster, in a benign and three stressful environments. The three stressful environments involved the addition to the medium of copper sulfate, methanol or alternating copper sulfate and methanol. There were 128 replicate populations for each of the four treatments. Under inbreeding, extinction rates were significantly higher in all three stressful environments compared with the benign environment. The percent extinct at generation eight (F = 0.826) for the four treatments were: 62.5% in the benign environment, 75.8%in the copper sulfate environment, 82.8% in the methanol environment, and 83.6% in the variable stress environment. However, the extinction rate in the variable stress environment did not differ significantly from the constant stress environments. Highly significant differences, among lineages, in extinction risk were detected. The results of this study indicate that wild populations are more vulnerable to inbreeding than indicated by extrapolation from captive environments.
Article
Historic data in the form of pinned specimens in entomological collections offer the potential to determine trends in genetic diversity of bumble bees (Bombus). We screened eight microsatellite loci in pinned bumble bee specimens from the U. S. National Pollinating Insects Collection. We tested three species (Bombus appositus, Bombus huntii and Bombus occidentalis) representing three subgenera of bumble bees (Subterraneobombus, Pyrobombus and Bombus sensu stricto) respectively. Bombus occidentalis is a species of particular concern for conservation biologists. Single mid-legs of ninety-six individuals from each species were assayed to determine microsatellite amplification success rates of historic material in a museum collection. Microsatellite alleles amplified in specimens up to 101 years old, but the rate of amplification success was significantly lower in material over 60 years of age. Loci with shorter allele sizes amplified more frequently than relatively longer alleles in samples from all age classes.We correlate the age of specimens to the age at which loci fail to amplify and discuss potential impacts of using certain markers for population genetic studies of museum specimens.
Article
In the present study, we analysed 18 red deer specimens from a small (N = 50) and isolated population in Schleswig-Holstein, northern Germany, with respect to variability at nine polymorphic microsatellite loci and 439bp of the mitochondrial DNA control region. Several cases of brachygnathy (shortened lower jaw), commonly associated with inbreeding depression, have been recorded in the population. Genetic variability was very low compared with other European red deer populations including the neighbouring population from which the population under study was derived some 130years ago. The effective population size was estimated to be seven individuals corresponding to an increase in inbreeding (or a loss of heterozygosity) of 7% each generation. This value is seven times higher than the theoretical threshold level up to which natural selection is believed to counteract the fixation of deleterious alleles in the gene pool. As a consequence, the population urgently needs genetic input from other populations to overcome the negative effects of random drift and inbreeding. To our knowledge, this study is one of the first to genetically analyse a red deer population showing strong signs of inbreeding depression.
Article
Allozyme and microsatellite data from numerous populations of Drosophila buzzatii have been used (i) to determine to what degree N e varies among generations within populations, and among populations, and (ii) to evaluate the congruence of four temporal and five single‐sample estimators of N e . Effective size of different populations varied over two orders of magnitude, most populations are not temporally stable in genetic composition, and N e showed large variation over generations in some populations. Short‐term N e estimates from the temporal methods were highly correlated, but the smallest estimates were the most precise for all four methods, and the most consistent across methods. Except for one population, N e estimates were lower when assuming gene flow than when assuming populations that were closed. However, attempts to jointly estimate N e and immigration rate were of little value because the source of migrants was unknown. Correlations among the estimates from the single‐sample methods generally were not significant although, as for the temporal methods, estimates were most consistent when they were small. These single‐sample estimates of current N e are generally smaller than the short‐term temporal estimates. Nevertheless, population genetic variation is not being depleted, presumably because of past or ongoing migration. A clearer picture of current and short‐term effective population sizes will only follow with better knowledge of migration rates between populations. Different methods are not necessarily estimating the same N e , they are subject to different bias, and the biology, demography and history of the population(s) may affect different estimators differently.
Article
Habitat fragmentation and changed land use have seriously reduced population size in many tropical forest tree species. Formerly widespread species with limited gene flow may be particularly vulnerable to the negative genetic effects of forest fragmentation and small population size. Vateriopsis seychellarum (Dipterocarpaceae) is a formerly widespread canopy tree of the Seychelles, but is now reduced to 132 adult individuals distributed in eleven sites. Using ten microsatellite loci, a genetic inventory of all adult trees and a sample of 317 progeny, we demonstrate that despite its restricted range, overall genetic diversity was relatively high (H(E) : 0.56). The juvenile cohort, however, had significantly lower allelic richness (adults R(S) : 3.91; juveniles R(S) : 2.83) and observed heterozygosity than adult trees (adults H(O) : 0.62; juveniles H(O) : 0.48). Rare alleles were fewer and kinship between individuals was stronger in juveniles. Significant fine-scale spatial genetic structure was observed in remnant adults, and parentage analysis indicated that more than 90% of sampled progeny disperse <25 m and pollen dispersed <50 m. The molecular data confirmed that two populations were derived entirely from self-fertilized offspring from a single surviving mother tree. These populations produce viable offspring. Despite this extreme genetic bottleneck, self-compatibility may provide V. seychellarum with some resistance to the genetic consequences of habitat fragmentation, at least in the short term. We discuss our findings in the context of other rare and threatened dipterocarp species which are vulnerable to miss-management of genetic resources and population fragmentation.
Article
The loggerhead sea turtle is an endangered species exposed to many anthropogenic hazards in the Pacific. It is widely held that pelagic longline fisheries pose the major risk for Pacific loggerheads but the effects of other risk factors such as human-induced global climate change have rarely been considered. So we used generalised additive regression modelling and autoregressive-prewhitened cross-correlation analysis to explore whether regional ocean temperatures affect the long-term nesting population dynamics for the 2 Pacific loggerhead genetic stocks (Japan, Australia). We found that both Pacific stocks have been exposed to slowly increasing trends in mean annual sea surface temperature in their respective core regional foraging habitats over the past 50 years. We show that irrespective of whether a population was decreasing or increasing that there was an inverse correlation between nesting abundance and mean annual sea surface temperature in the core foraging region during the year prior to the summer nesting season. Cooler foraging habitat ocean temperatures are presumably associated with increased ocean productivity and prey abundance and consequently increased loggerhead breeding capacity. So warming regional ocean temperatures could lead to long-term decreased food supply and reduced nesting and recruitment unless Pacific loggerheads adapt by shifting their foraging habitat to cooler regions. So the gradual warming of the Pacific Ocean over the past 50 years is a major risk factor that must be considered in any meaningful diagnosis of the long-term declines apparent for some Pacific loggerhead nesting populations.
Article
AbstractFormaldehyde was first prepared in 1859, and since then has been in widespread use for fixing and preserving medical and biological specimens. The value of such archival material has increased considerably because several methods for extracting DNA from formaldehyde-fixed animal tissue have been developed. Most of these, however, either require large amounts of tissue (rarely available) or recover only short fragments of DNA. Here we summarize current knowledge of and experience with such published methods, look at some of the known problems, and develop an additional method based on embedding the tissue in agarose prior to treatment with proteinase-K and GeneReleaser. With this method we have obtained mitochondrial DNA useful for PCR reactions from as little as 3 mg tissue of more than 30 years old formaldehyde-fixed aplacophoran molluscs. We examine the conditions under which obtaining relatively high-quality DNA from formaldehyde-fixed material is possible, making previously collected samples accessible for molecular studies in genetics, systematics and related fields. The purpose of this short review is to acquaint molecular systematists with some of the methodological advances and considerations in using formaldehyde-preserved material.
Article
The role of genetic factors in extinction has been a controversial issue, especially since Lande’s paper [Genetics and demography in biological conservation, Science 241 (1988) 1455–1460] paper in Science. Here I review the evidence on the contribution of genetic factors to extinction risk. Inbreeding depression, loss of genetic diversity and mutation accumulation have been hypothesised to increase extinction risk. There is now compelling evidence that inbreeding depression and loss of genetic diversity increase extinction risk in laboratory populations of naturally outbreeding species. There is now clear evidence for inbreeding depression in wild species of naturally outbreeding species and strong grounds from individual case studies and from computer projections for believing that this contributes to extinction risk. Further, most species are not driven to extinction before genetic factors have time to impact. The contributions of mutation accumulation to extinction risk in threatened taxa appear to be small and to require very many generations. Thus, there is now sufficient evidence to regard the controversies regarding the contribution of genetic factors to extinction risk as resolved. If genetic factors are ignored, extinction risk will be underestimated and inappropriate recovery strategies may be used.
Article
Over the past two decades, new molecular genetic techniques have had substantial impacts on the fields of ecology, evolution and conservation. However, our current toolbox of genetic methodologies remains inadequate for answering many questions and there are significant technological and analytical limitations. We review the possible uses of single nucleotide polymorphisms (SNPs) as novel genetic markers for common questions in population genetics. Furthermore, we evaluate the potential of SNPs relative to frequently used genetic markers, such as microsatellite loci and mitochondrial DNA (mtDNA) sequences, and we discuss statistical power, analytical approaches, and technological improvements and limitations. Although ascertainment bias is a problem for some applications, SNPs can often generate equivalent statistical power whilst providing broader genome coverage and higher quality data than can either microsatellites or mtDNA, suggesting that SNPs could become an efficient and cost-effective genetic tool.
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Article
Rare plant species are vulnerable to genetic erosion and inbreeding associated with small population size and isolation due to increasing habitat fragmentation. The degree to which these problems undermine population viability remains debated. We explore genetic and reproductive processes in the critically endangered long-lived tropical tree Medusagyne oppositifolia, an endemic to the Seychelles with a naturally patchy distribution. This species is failing to recruit in three of its four populations. We evaluate whether recruitment failure is linked to genetic problems associated with fragmentation, and if genetic rescue can mitigate such problems. Medusagyne oppositifolia comprises 90 extant trees in four populations, with only the largest (78 trees) having successful recruitment. Using 10 microsatellite loci, we demonstrated that genetic diversity is high (H(E) : 0.48-0.63; H(O) : 0.56-0.78) in three populations, with only the smallest population having relatively low diversity (H(E) : 0.26 and H(O) : 0.30). All populations have unique alleles, high genetic differentiation, and significant within population structure. Pollen and seed dispersal distances were mostly less than 100 m. Individuals in small populations were more related than individuals in the large population, thus inbreeding might explain recruitment failure in small populations. Indeed, inter-population pollination crosses from the large donor population to a small recipient population resulted in higher reproductive success relative to within-population crosses. Our study highlights the importance of maintaining gene flow between populations even in species that have naturally patchy distributions. We demonstrate the potential for genetic and ecological rescue to support conservation of plant species with limited gene flow.
Article
Currently, there exists a limited knowledge on the extent of temporal variation in population genetic parameters of natural populations. Here, we study the extent of temporal variation in population genetics by genotyping 151 genome-wide SNP markers polymorphic in 466 individuals collected from nine populations of the annual plant Arabidopsis thaliana during 4 years. Populations are located along an altitudinal climatic gradient from Mediterranean to subalpine environments in NE Spain, which has been shown to influence key demographic attributes and life cycle adaptations. Genetically, A. thaliana populations were more variable across space than over time. Common multilocus genotypes were detected several years in the same population, whereas low-frequency multilocus genotypes appeared only 1 year. High-elevation populations were genetically poorer and more variable over time than low-elevation populations, which might be caused by a higher overall demographic instability at higher altitudes. Estimated effective population sizes were low but also showed a significant decreasing trend with increasing altitude, suggesting a deeper impact of genetic drift at high-elevation populations. In comparison with single-year samplings, repeated genotyping over time captured substantially higher amount of genetic variation contained in A. thaliana populations. Furthermore, repeated genotyping of populations provided novel information on the genetic properties of A. thaliana populations and allowed hypothesizing on their underlying mechanisms. Therefore, including temporal genotyping programmes into traditional population genetic studies can significantly increase our understanding of the dynamics of natural populations.