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Polyphenisms and polymorphisms: Genetic variation in plasticity and color variation within and among bluefin killifish populations
Abstract
The presence of stable color polymorphisms within populations begs the question of how genetic variation is maintained. Consistent variation among populations in coloration, especially when correlated with environmental variation, raises questions about whether environmental conditions affect either the fulcrum of those balanced polymorphisms, the plastic expression of coloration, or both. Color patterns in male bluefin killifish provoke both types of questions. Red and yellow morphs are common in all populations. Blue males are more common in tannin‐stained swamps relative to clear springs. Here we combined crosses with a manipulation of light to explore how genetic variation and phenotypic plasticity shape these patterns. We found that the variation in coloration is attributable mainly to two axes of variation: (1) a red‐yellow axis with yellow being dominant to red, and (2) a blue axis that can override red‐yellow and is controlled by genetics, phenotypic plasticity, and genetic variation for phenotypic plasticity. The variation among populations in plasticity suggests it is adaptive in some populations but not others. The variation among sires in plasticity within the swamp population suggests balancing selection may be acting not only on the red‐yellow polymorphism but also on plasticity for blue coloration. This article is protected by copyright. All rights reserved
Three nominal species of the killifish genus Aplocheilus are reported from the lowlands of Sri Lanka. Two of these, Aplocheilus dayi and Aplocheilus werneri, are considered endemic to the island, whereas Aplocheilus parvus is reported from both Sri Lanka and Peninsular India. Here, based on a collection from 28 locations in Sri Lanka, also including a dataset of Asian Aplocheilus downloaded from GenBank, we present a phylogeny constructed from the mitochondrial cytochrome b (cytb), mitochondrial cytochrome c oxidase subunit 1 (cox1), and nuclear recombination activating protein 1 (rag1), and investigate the interrelationships of the species of Aplocheilus in Sri Lanka. The endemic Sri Lankan aplocheilid clade comprising A. dayi and A. werneri is recovered as the sister group to the clade comprising A. parvus from Sri Lanka and Aplocheilus blockii from Peninsular India. The reciprocal monophyly of A. dayi and A. werneri is not supported in our molecular phylogeny. A. dayi and A. werneri display strong sexual dimorphism, but species‐level differences are subtle, explained mostly by pigmentation patterns. Their phenotypes exhibit a parapatric distribution and may represent locally adapted forms of a single species. Alternatively, the present study does not rule out the possibility that A. dayi and A. werneri may represent an incipient species pair or that they have undergone introgression or hybridization in their contact zones. We provide evidence that the Nilwala‐Gin region of southwestern Sri Lanka may have acted as a drought refugium for these fishes.
For insects that exhibit wing polyphenic development, abiotic and biotic signals dictate the adult wing morphology of the insect in an adaptive manner such that in stressful environments the formation of a flight-capable morph is favored and in low stress environments a flightless morph is favored. While there is a relatively large amount known about the environmental cues that dictate morph formation in wing polyphenic hemipterans like planthoppers and aphids, whether those cues dictate the same morphs in non-hemipteran (i.e. cricket) wing polyphenic species has not been explicitly investigated. To experimentally test the generality of environmental cue determination of wing polyphenism across taxa with diverse life histories, in this study we tested the importance of food quantity, parasitic infection, and tactile cues on wing morph determination in the wing polyphenic sand field cricket, Gryllus firmus. Our results also show that certain stress cues, such as severe diet quantity limitation and parasitic infection, actually led to an increase in the production of flightless morph. Based on these findings, our results suggest that physiological and genetic constraints are important to an organism’s ability to respond to environmental variation in an adaptive manner beyond simple life history trade-offs.
Upside-down jellyfish ( Cassiopea sp. ) are highly tolerant to multiple abiotic stressors, including fluctuating temperatures associated with shallow marine habitats. This resilience may underlie the ability of Cassiopea sp. to inhabit a wide variety of tropical habitats across the globe. Additionally, Cassiopea sp. are marked by a conspicuous array of appendage coloration; individual medusae vary in the hue and number of oral appendages, which are often strikingly blue. The function of this coloration is not understood. We aimed to understand how extrinsic and intrinsic factors may shape thermal tolerance. Adult Cassiopea xamachana were collected from two sites that vary in daily temperature range within the Florida Keys and were subjected to acute lethal heat stress experiments. To quantify a whole-organism response to heat, we measured changes in bell pulsation, which likely plays a role in feeding, oxygen exchange, and symbiont uptake. Results show that C. xamachana from the two collection sites do not exhibit different responses to heat, suggesting that temperature fluctuations do not prime individuals for higher thermal tolerance. Additionally, C. xamachana with blue appendages survived significantly higher temperatures and exhibited less change in bell pulsation rates compared to non-blue individuals. Finally, color morphs were acclimated at either ambient (26 °C) or elevated (33 °C) temperatures. We found that acclimation at 33 °C, as well as appendage color in each treatment, led to higher survival under acute heat stress. Together, these findings highlight the importance of phenotypic plasticity and coloration in Cassiopea resilience during heat stress.
Female cichlid fish living in African great lakes are known to have sensory systems that are adapted to ambient light environments. These sensory system adaptations are hypothesized to have influenced the evolution of the diverse male nuptial coloration. In rock-dwelling Lake Malawi mbuna cichlids, however, the extent to which ambient light environments influence female sensory systems and potentially associated male nuptial coloration remains unknown. Yet, the ubiquitous blue flank coloration and UV reflection of male mbuna cichlids suggests the potential impacts of the blue-shifted ambient light environment on these cichlid’s visual perception and male nuptial coloration in the shallow water depth in Lake Malawi. In the present study, we explored whether and how the sensory bias of females influences intersexual communication in the mbuna cichlid, Metriaclima zebra. A series of choice experiments in various light environments showed that M. zebra females (i) have a preference for the blue-shifted light environment, (ii) prefer to interact with males in blue-shifted light environments, (iii) do not show a preference between dominant and subordinate males in full-spectrum, long-wavelength filtered, and short-wavelength filtered light environments, and (iv) show a ‘reversed’ preference for subordinate males in the UV-filtered light environment. These results suggest that the visual perception of M. zebra females may be biased to the ambient light spectra in their natural habitat by local adaptation and that this sensory bias may influence the evolution of blue and UV reflective patterns in male nuptial coloration.
Salinization is a global phenomenon affecting ecosystems and forcing freshwater organisms to deal with increasing levels of ionic stress. However, our understanding of mechanisms that permit salt tolerance in amphibians is limited. This study investigates mechanisms of salt tolerance in locally adapted, coastal populations of a treefrog, Hyla cinerea. Using a common garden experiment, we (i) determine the extent that environment (i.e., embryonic and larval saltwater exposure) or genotype (i.e., coastal vs. inland) affects developmental benchmarks and transcriptome expression and (ii) identify genes that may underpin differences in saltwater tolerance. Differences in gene expression, survival, and plasma osmolality were most strongly associated with genotype. Population genetic analyses on expressed genes also delineated coastal and inland groups based on genetic similarity. Coastal populations differentially expressed osmoregulatory genes including ion transporters (atp1b1, atp6V1g2, slc26a), cellular adhesion components (cdh26, cldn1, gjb3, ocln), and cytoskeletal components (odc1‐a, tgm3). Several of these genes are the same genes expressed by euryhaline fish after exposure to freshwater, which is a novel finding for North American amphibians and suggests that these genes may be associated with local salinity adaptation. Coastal populations also highly expressed glycerol‐3‐phosphate dehydrogenase 1 (gpd1), which indicates they use glycerol as a compatible osmolyte to reduce water loss—another mechanism of saltwater tolerance previously unknown in frogs. These data signify that Hyla cinerea inhabiting coastal, brackish wetlands have evolved a salt‐tolerant ecotype, and highlights novel candidate pathways that can lead to salt tolerance in freshwater organisms facing habitat salinization.
Reptiles use pterin and carotenoid pigments to produce yellow, orange, and red colors. These conspicuous colors serve a diversity of signaling functions, but their molecular basis remains unresolved. Here, we show that the genomes of sympatric color morphs of the European common wall lizard (Podarcis muralis), which differ in orange and yellow pigmentation and in their ecology and behavior, are virtually undifferentiated. Genetic differences are restricted to two small regulatory regions near genes associated with pterin [sepiapterin reductase (SPR)] and carotenoid [beta-carotene oxygenase 2 (BCO2)] metabolism, demonstrating that a core gene in the housekeeping pathway of pterin biosynthesis has been coopted for bright coloration in reptiles and indicating that these loci exert pleiotropic effects on other aspects of physiology. Pigmentation differences are explained by extremely divergent alleles, and haplotype analysis revealed abundant transspecific allele sharing with other lacertids exhibiting color polymorphisms. The evolution of these conspicuous color ornaments is the result of ancient genetic variation and cross-species hybridization.
Bright, highly reflective iridescent colours can be seen across nature and are produced by the scattering of light from nanostructures. Heliconius butterflies have been widely studied for their diversity and mimicry of wing colour patterns. Despite iridescence evolving multiple times in this genus, little is known about the genetic basis of the colour and the development of the structures which produce it. Heliconius erato can be found across Central and South America, but only races found in Western Ecuador and Colombia have developed blue iridescent colour. Here, we use crosses between iridescent and non-iridescent races of H. erato to study phenotypic variation in the resulting F2 generation. Using measurements of blue colour from photographs, we find that iridescent structural colour is a quantitative trait controlled by multiple genes, with strong evidence for loci on the Z sex chromosome. Iridescence is not linked to the Mendelian colour pattern locus that also segregates in these crosses (controlled by the gene cortex). Small angle X-ray scattering data shows that spacing between longitudinal ridges on the scales, which affects the intensity of the blue reflectance, also varies quantitatively in F2 crosses.
Although the environment varies, adaptive trait plasticity is uncommon, which can be due to either costs or limitations. Currently there is little evidence for costs of plasticity; limitations are a more promising explanation, including information reliability. A possible cause for a decrease in information reliability is the channeling of environmental information through one trait that then affects the phenotype of a second trait, the information path. Using an individual‐based simulation model, I explored the ways in which configurations of trait interactions and patterns of environmental variation in space and time affect the evolution of phenotypic plasticity. I found that genotypes and phenotypes evolved to shorten and simplify the information path from the environment to fitness. A shortened path was characterized by a decrease in the amount of plasticity for traits that had a less direct connection between the environment of development and fitness. A simplified path was characterized by a decrease in the amount of plasticity for traits that had multiple paths between the environment and their phenotype. These results suggest that an eighth proposition be added to the theory of the evolution of phenotypic plasticity: Trait plasticity will evolve to minimize the information path between the environment and fitness.
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It has been 25 years since the formalization of the Sensory Drive hypothesis was published in the American Naturalist (1992). Since then, there has been an explosion of research identifying its utility in contributing to our understanding of inter- and intra-specific variation in sensory systems and signaling properties. The main tenet of Sensory Drive is that environmental characteristics will influence the evolutionary trajectory of both sensory (detecting capabilities) and signaling (detectable features and behaviors) traits in predictable directions. We review the accumulating evidence in 154 studies addressing these questions and categorized their approach in terms of testing for environmental influence on sensory tuning, signal characteristics or both. For the subset of studies that examined sensory tuning, there was greater support for Sensory Drive processes shaping visual than auditory tuning, and it was more prevalent in aquatic than terrestrial habitats. Terrestrial habitats and visual traits were the prevalent habitat and sensory modality in the 104 studies showing support for environmental influence on signaling properties. Meanwhile an additional 19 studies that found no supporting evidence for environmental influence on signaling traits were all based in terrestrial ecosystems and almost exclusively involved auditory signals. Only 29 studies examined the complete coevolutionary process between sensory and signaling traits and were dominated by fish visual communication. We discuss biophysical factors that may contribute to the visual and aquatic bias for Sensory Drive evidence, as well as biotic factors that may contribute to the lack of Sensory Drive processes in terrestrial acoustic signaling systems.
Sensory drive predicts that the conditions under which signaling takes place have large effects on signals, sensory systems, and behavior. The coupling of an ecological genetics approach with sensory drive has been fruitful. An ecological genetics approach compares populations that experience different environments and asks whether population differences are adaptive and are the result of genetic and/or environmental variation. The multi-faceted effects of signaling environments are well-exemplified by the bluefin killifish. In this system, males with blue anal fins are abundant in tannin-stained swamps that lack UV/blue light but are absent in clear springs where UV/blue light is abundant. Past work indicates that lighting environments shape genetic and environmental variation in color patterns, visual systems, and behavior. Less is known about the selective forces creating the across population correlations between UV/blue light and the abundance of blue males. Here, we present three new experiments that investigate the roles of lighting environments on male competition, female mate choice, and predation. We found strong effects of lighting environments on male competition where blue males were more likely to emerge as dominant in tea-stained water than in clear water. Our preliminary study on predation indicated that blue males may be less susceptible to predation in tea-stained water than in clear water. However, there was little evidence for female preferences favoring blue males. The resulting pattern is one where the effects of lighting environments on genetic variation and phenotypic plasticity match the direction of selection and favor the expression of blue males in swamps.
How animals visually perceive the environment is key to understanding important ecological behaviors, such as predation, foraging, and mating. This study focuses on the visual system properties and visual perception of color in the largemouth bass Micropterus salmoides. This study (a) documents the number and spectral sensitivity of photoreceptors, (b) uses these parameters to model visual perception, and (c) tests the model of color perception using a behavioral assay. Bass possess single cone cells maximally sensitive at 535 nm, twin cone cells maximally sensitive at 614 nm, and rod cells maximally sensitive at 528 nm. A simple model of visual perception predicted that bass should not be able to discern between chartreuse yellow and white nor between green and blue. In contrast, bass should be able to discern red from all achromatic (i.e. gray scale) stimuli. These predictions were partially upheld in behavioral trials. In behavioral trials, bass were first trained to recognize a target color to receive a food reward, then tested on their ability to differentiate between their target color and a color similar in brightness. Bass trained to red and green could easily discern their training color from all other colors for target colors that were similar in brightness (white and black, respectively). This study shows that bass possess dichromatic vision and do use chromatic (i.e. color) cues in making visually-based decisions.
The maintenance of genetic variation in the face of natural selection is a long-standing question in evolutionary biology. In the bluefin killifish Lucania goodei, male coloration is polymorphic. Males can produce either red or yellow coloration in their anal fins, and both color morphs are present in all springs. These two morphs are heritable and how they are maintained in nature is unknown. Here, we tested two mechanisms for the maintenance of the red/yellow color morphs. Negative frequency dependent mating success predicts that rare males have a mating advantage over common males. Spatial variation in fitness predicts that different color morphs have an advantage in different microhabitat types. Using a breeding experiment, we tested these hypotheses by creating populations with different ratios of red to yellow males (5 Red: 1 Yellow; 1Red: 5 Yellow) and determining male mating success on shallow and deep spawning substrates. We found no evidence of negative frequency-dependent mating success. Common morphs tended to have higher mating success, and this was particularly so on shallow spawning substrates. However, on deep substrates, red males enjoyed higher mating success than yellow males, particularly so when red males were rare. However, yellow males did not have an advantage at either depth nor when rare. We suggest that preference for red males is expressed in deeper water, possibly due to alterations in the lighting environment. Finally, male pigment levels were correlated with one another and predicted male mating success. Hence, pigmentation plays an important role in male mating success.
Background
Efficient communication requires that signals are well transmitted and perceived in a given environment. Natural selection therefore drives the evolution of different signals in different environments. In addition, environmental heterogeneity at small spatial or temporal scales may favour phenotypic plasticity in signaling traits, as plasticity may allow rapid adjustment of signal expression to optimize transmission. In this study, we explore signal plasticity in the nuptial coloration of Lake Victoria cichlids, Pundamilia pundamilia and Pundamilia nyererei. These two species differ in male coloration, which mediates species-assortative mating. They occur in adjacent depth ranges with different light environments. Given the close proximity of their habitats, overlapping at some locations, plasticity in male coloration could contribute to male reproductive success but interfere with reproductive isolation.
Methods
We reared P. pundamilia , P. nyererei, and their hybrids under light conditions mimicking the two depth ranges in Lake Victoria. From photographs, we quantified the nuptial coloration of males, spanning the entire visible spectrum. In experiment 1, we examined developmental colour plasticity by comparing sibling males reared in each light condition. In experiment 2, we assessed colour plasticity in adulthood, by switching adult males between conditions and tracking coloration for 100 days.
Results
We found that nuptial colour in Pundamilia did respond plastically to our light manipulations, but only in a limited hue range. Fish that were reared in light conditions mimicking the deeper habitat were significantly greener than those in conditions mimicking shallow waters. The species-specific nuptial colours (blue and red) did not change. When moved to the opposing light condition as adults, males did not change colour.
Discussion
Our results show that species-specific nuptial colours, which are subject to strong divergent selection by female choice, are not plastic. We do find plasticity in green coloration, a response that may contribute to visual conspicuousness in darker, red-shifted light environments. These results suggest that light-environment-induced plasticity in male nuptial coloration in P. pundamilia and P. nyererei is limited and does not interfere with reproductive isolation.
Some species actively change color and pattern for camouflage on a range of background types. Such dynamic camouflage may be particularly advantageous for species inhabiting heterogeneous habitats, such as intertidal zones, where individuals are exposed to both terrestrial and marine predators depending on tides and wave action. Most studies of dynamic pattern camouflage have focused on relatively few species, and rarely species inhabiting the intertidal zone. We used image analysis and predator (avian) vision modelling to determine if rock gobies (Gobius paganellus) change their body pattern in response to their background, and to explore how background marking size influence pattern change. Rock gobies rapidly (within 1 min) changed their pattern when placed on checkerboards with different sized squares, and on backgrounds resembling natural substrates. On backgrounds resembling natural substrates, those with a small grain size, such as sand, elicited a larger degree of pattern change than those with a larger grain size. However, despite this, the majority of fish showed little or no improvement in background matching over time. Instead, the markings elicited are characteristic of disruptive coloration and may function primarily through breaking up the body outline rather than via improved match to the background pattern itself.
Animal coloration has multiple functions including thermoregulation, camouflage, and social signaling, and the requirements of each function may sometimes conflict. Many terrestrial ectotherms accommodate the multiple functions of color through color change. However, the relative importance of these functions and how color-changing species accommodate them when they do conflict are poorly understood because we lack data on color change in the wild. Here, we show that the color of individual radio-tracked bearded dragon lizards, Pogona vitticeps, correlates strongly with background color and less strongly, but significantly, with temperature. We found no evidence that individuals simultaneously optimize camouflage and thermoregulation by choosing light backgrounds when hot or dark backgrounds when cold. In laboratory experiments, lizards showed both UV-visible (300?700 nm) and near-infrared (700?2,100 nm) reflectance changes in response to different background and temperature treatments, consistent with camouflage and thermoregulatory functions, respectively, but with no interaction between the two. Overall, our results suggest that wild bearded dragons change color to improve both thermoregulation and camouflage but predominantly adjust for camouflage, suggesting that compromising camouflage may entail a greater potential immediate survival cost.
Discovering the mutational events that fuel adaptation to environmental change remains an important challenge for evolutionary biology. The classroom example of a visible evolutionary response is industrial melanism in the peppered moth (Biston betularia): the replacement, during the Industrial Revolution, of the common pale typica form by a previously unknown black (carbonaria) form, driven by the interaction between bird predation and coal pollution(1). The carbonaria locus has been coarsely localized to a 200-kilobase region, but the specific identity and nature of the sequence difference controlling the carbonaria-typica polymorphism, and the gene it influences, are unknown(2). Here we show that the mutation event giving rise to industrial melanism in Britain was the insertion of a large, tandemly repeated, transposable element into the first intron of the gene cortex. Statistical inference based on the distribution of recombined carbonaria haplotypes indicates that this transposition event occurred around 1819, consistent with the historical record. We have begun to dissect the mode of action of the carbonaria transposable element by showing that it increases the abundance of a cortex transcript, the protein product of which plays an important role in cell-cycle regulation, during early wing disc development. Our findings fill a substantial knowledge gap in the iconic example of microevolutionary change, adding a further layer of insight into the mechanism of adaptation in response to natural selection. The discovery that the mutation itself is a transposable element will stimulate further debate about the importance of 'jumping genes' as a source of major phenotypic novelty(3).
The ability to change appearance over a range of timescales is widespread in nature, existing in many invertebrate and vertebrate groups. This can include color change occurring in seconds, minutes, and hours, to longer term changes associated with phenotypic plasticity and development. A major function is for camouflage against predators because color change and plasticity enables animals to match their surroundings and potentially reduce the risk of predation. Recently, we published findings (Stevens et al., 2014a) showing how shore crabs can change their appearance and better match the background to predator vision in the short term. This, coupled with a number of past studies, emphasizes the potential that animals have to modify their appearance for camouflage. However, the majority of studies on camouflage and color plasticity have focused on a small number of species capable of unusually rapid changes. There are many broad questions that remain about the nature, mechanisms, evolution, and adaptive value of color change and plasticity for concealment. Here, I discuss past work and outline six questions relating to color change and plasticity, as well as major avenues for future work.
Explaining the presence of conspicuous female ornaments that take the form of male-typical traits has been a longstanding challenge in evolutionary biology. Such female ornaments have been proposed to evolve via both adaptive and non-adaptive evolutionary processes. Determining the genetic underpinnings of female ornaments is important for elucidating the mechanisms by which such female traits arise and persist in natural populations, but detailed information about their genetic basis is still scarce. In this study, we investigated the genetic architecture of two ornaments, the orange-red throat and pelvic spine, in the threespine stickleback (Gasterosteus aculeatus). Throat coloration is male-specific in ancestral marine populations but has evolved in females in some derived stream populations, whereas sexual dimorphism in pelvic spine coloration is variable among populations. We find that ornaments share a common genetic architecture between the sexes. At least three independent genomic regions contribute to red throat coloration, and harbor candidate genes related to pigment production and pigment cell differentiation. One of these regions is also associated with spine coloration, indicating that both ornaments might be mediated partly via pleiotropic genetic mechanisms.
Disequilibrium has been estimated for alleles at pairs of loci controlling shell colour and banding in populations of Cepaea nemoralis from northern Europe. There is strong overall positive disequilibrium between pink/yellow colour and unbanded/banded (pink unbanded in excess) but not for colour and the band-modifying loci mid-banded and trifasciate. When the colour/banding data are divided into four equally sized sections (quadrants) representing, respectively, high and low yellow and high and low unbanded frequencies, there is significant interaction in disequilibrium between quadrants, with high positive disequilibrium contributed by populations in which pink and unbanded are at high frequency. We interpret this as indicating diversifying, rather than stabilizing, selection. Simulations show how the overall value and quadrant differences may have built up. The brown allele at the colour locus is known to be associated with much higher unbanded frequencies than the other two colours, owing to some intrinsic incompatibility between banding and ground colour. It is suggested that the same may apply, although to a lesser extent, with respect to pink and unbanded relative to yellow.
Pigmentation varies within and between species and is often adaptive. The amount of pigmentation on the abdomen of Drosophila melanogaster is a relatively simple morphological trait, which serves as a model for mapping the genetic basis of variation in complex phenotypes. Here, we assessed natural variation in female abdominal pigmentation in 175 sequenced inbred lines of the Drosophila melanogaster Genetic Reference Panel, derived from the Raleigh, NC population. We quantified the proportion of melanization on the two most posterior abdominal segments, tergites 5 and 6 (T5, T6). We found significant genetic variation in the proportion of melanization and high broad-sense heritabilities for each tergite. Genome-wide association studies identified over 150 DNA variants associated with the proportion of melanization on T5 (84), T6 (34), and the difference between T5 and T6 (35). Several of the top variants associated with variation in pigmentation are in tan, ebony, and bric-a-brac1, genes known to affect D. melanogaster abdominal pigmentation. Mutational analyses and targeted RNAi-knockdown showed that 17 out of 28 (61%) novel candidate genes implicated by the genome-wide association study affected abdominal pigmentation. Several of these genes are involved in developmental and regulatory pathways, chitin production, cuticle structure, and vesicle formation and transport. These findings show that genetic variation may affect multiple steps in pathways involved in tergite development and melanization. Variation in these novel candidates may serve as targets for adaptive evolution and sexual selection in D. melanogaster.
There is considerable interest in the occurrence and molecular mechanisms of phenotypic plasticity and genotype-by-environment interactions (G x E) in plant populations. The emergence of genomic tools, including quantitative trait locus (QTL) mapping and transcriptome studies, provides opportunities to identify G x E patterns and mechanisms across a diversity of phenotypes, species, and environments. We review progress in evaluating the presence and characterizing the mechanisms of G x E using genomic studies of abiotic responses in plants. Our review reveals that G x E is common, often caused by changes in the magnitude of genetic effects in response to the environment, and associated with diverse genetic factors and molecular variants. We illustrate this diversity with an examination of transcriptome studies and discussion of cloned genes underlying G x E. We discuss the caveats associated with existing studies and outline future directions for better understanding G x E and its impact on local adaptation and plant improvement.
Significance
Environmental variation is becoming more frequent and unpredictable as a consequence of climate change, yet we currently lack the tools to evaluate the extent to which organisms may adapt to this phenomenon. Here we develop a model that explores these issues and use it to study how changes in the timescale and predictability of environmental variation may ultimately affect population viability. Our model indicates that, although populations can often cope with fairly large changes in these environmental parameters, on occasion they will collapse abruptly and go extinct. We characterize the conditions under which these evolutionary tipping points occur and discuss how vulnerability to such cryptic threats may depend on the genetic architecture and life history of the organisms involved.
There is a bewildering diversity of signals, sensory systems, and signaling behavior. A consideration of how these traits affect each other's evolution explains some of this diversity. Natural selection favors signals, receptors, and signaling behavior that maximize the received signals relative to background noise and minimize signal degradation. Properties of sensory systems bias the direction of evolution of the signals that they receive. For example, females may prefer males whose signals they can perceive more easily, and this will lead to the spread of more easily perceived male traits. Environmental conditions during signal transmission and detection also affect signal perception. Specific environmental conditions will bias the evolutionary direction of behavior, which affects the time and place of signaling as well as microhabitat preferences. Increased specialization of microhabitats and signaling behavior may lead to biased evolution of the sensory systems to work more efficiently. Thus, sensory systems, signals, signaling behavior, and habitat choice are evolutionarily coupled. These suites of traits should coevolve in predictable directions, determined by environmental biophysics, neurobiology, and the genetics of the suites of traits--hence the term "sensory drive." Because conditions vary in space and time, diversity will be generated
To understand empirical patterns of phenotypic plasticity, we need to explore the complexities of environmental heterogeneity and how it interacts with cue reliability. I consider both temporal and spatial variation separately and in combination, the timing of temporal variation relative to development, the timing of movement relative to selection, and two different patterns of movement: stepping-stone and island. Among-generation temporal heterogeneity favors plasticity, while within-generation heterogeneity can result in cue unreliability. In general, spatial variation more strongly favors plasticity than temporal variation, and island migration more strongly favors plasticity than stepping-stone migration. Negative correlations among environments between the time of development and selection can result in seemingly maladaptive reaction norms. The effects of higher dispersal rates depend on the life history stage when dispersal occurs and the pattern of environmental heterogeneity. Thus, patterns of environmental heterogeneity can be complex and can interact in unforeseen ways to affect cue reliability. Proper interpretation of patterns of trait plasticity requires consideration of the ecology and biology of the organism. More information on actual cue reliability and the ecological and developmental context of trait plasticity is needed.
Many plants display characteristic phytochrome-mediated stem elongation responses to crowding and vegetation shade, commonly referred to as the shade avoidance syndrome. We tested the hypothesis that this elongation is a form of adaptive plasticity by comparing the relative performance at high and low density of wild-type plants and transgenic and mutant plants in which the shade avoidance response was disabled. Transgenic tobacco plants in which elongation in response to neighbors was blocked by expression of the oat PHYA gene had decreased relative fitness when grown in competition with elongated wild-type plants. In contrast, constitutively elongated Brassica ein mutant plants, deficient in light-stable phytochrome, had lower fitness relative to nonelongated wild type at low density than in competition with elongated wild type at high density. The observation that phytochrome-mediated elongation is advantageous in dense stands, but disadvantageous for uncrowded plants, indicates that a response to foliage shade allows plants to develop an appropriate morphology for the level of competition they experience. This observation supports the adaptive plasticity hypothesis for this ecologically important trait.
Evolutionary Ecology simultaneously unifies conceptual and empirical advances in evolutionary ecology and provides a volume that can be used as either a primary textbook or a supplemental reading in an advanced undergraduate or graduate course. The focus of the book is on current concepts in evolutionary ecology, and the empirical study of these concepts. The editors have assembled a group of prominent biologists who have made significant contributions to this field. They both synthesize the current state of knowledge and identity areas for future investigation. Evolutionary Ecology will be of general interest to researchers and students in both ecology and evolutionary biology. Researchers in evolutionary ecology that want an overview of the current state of the field, and graduate students that want an introduction the field, will find this book very valuable. This volume can also be used as a primary textbook or supplemental reading in both upper division and graduate courses/seminars in Evolutionary Ecology.
When Charles Darwin and Alfred Russell Wallace proposed their theory of evolution by natural selection, the concepts of evolution and speciation were not new. Darwin introduced The Origin with “An Historical Sketch,” in which he summarized the work of 34 previous authors who had speculated on evolution and the origin of species. What was new about Darwin and Wallace’s proposition was natural selection as the mechanism of evolutionary change. Darwin further proposed that natural selection was a unifying process that accounts for adaptation, for speciation, and hence for the diversity of life on earth. Darwin and Wallace proposed natural selection as a process that caused evolution. Adaptations are features of organisms that were shaped by this process. The modern version of Darwin and Wallace’s theory allows for other agents of evolution, such as genetic drift, migration, and mutation, but adaptation remains a product of natural selection alone. The virtue of their proposal is that it allows us to develop testable hypotheses about cause-and-effect relationships between features of the environment and presumed adaptations. Natural selection immediately became a source of controversy, although the nature of the controversy has shifted over time. First, there has been considerable debate about the definition of adaptation (e.g., Reeve and Sherman 1993). We do not wish to add to or summarize this debate because we feel that Darwin got it right the first time. Besides defining a cause-and-effect relationship between selection and adaptation, Darwin emphasized that we should not expect organisms to be perfectly adapted to their environment. In fact, this emphasis was a large component of his argument against divine creation. For example, Darwin recognized, through his experience with artificial selection, that different aspects of morphology were in some way “tied” to one another so that selection on one trait would cause correlated changes in others that were not necessarily adaptive. He also recognized that organisms were subject to constraints that might limit their ability to adapt. Finally, he argued that how organisms evolved was a function of their history, so that the response to selection on the same trait would vary among lineages. A more telling criticism considers the application of cause-and-effect reasoning to the interpretation of features of organisms as adaptations, and hence to the empirical study of adaptation.
Visual ecology is the study of how animals use visual systems to meet their ecological needs, how these systems have evolved, and how they are specialized for particular visual tasks. This book provides the first up-to-date synthesis of the field to appear in more than three decades. Featuring some 225 illustrations, including more than 140 in color, spread throughout the text, the book begins by discussing the basic properties of light and the optical environment. It then looks at how photoreceptors intercept light and convert it to usable biological signals, how the pigments and cells of vision vary among animals, and how the properties of these components affect a given receptor's sensitivity to light. The book goes on to examine how eyes and photoreceptors become specialized for an array of visual tasks, such as navigation, evading prey, mate choice, and communication. A timely and much-needed resource for students and researchers alike, the book also includes a glossary and a wealth of examples drawn from the full diversity of visual systems.
Coloration is an easily quantifiable visual trait that has proven to be a highly tractable system for genetic analysis and for studying adaptive evolution. The application of genomic approaches to evolutionary studies of coloration is providing new insight into the genetic architectures underlying colour traits, including the importance of large-effect mutations and supergenes, the role of development in shaping genetic variation and the origins of adaptive variation, which often involves adaptive introgression. Improved knowledge of the genetic basis of traits can facilitate field studies of natural selection and sexual selection, making it possible for strong selection and its influence on the genome to be demonstrated in wild populations. Colour traits have been useful for studying the genetics underlying adaptive evolution. This Review discusses how genomic technologies are providing a deeper understanding of these traits, revealing fresh insights into their genetic architecture, evolvability and origins of adaptive variation.
Environmentally transmitted parasites spend time in the abiotic environment, where they are subjected to a variety of stressors. Learning how they face this challenge is essential if we are to understand how host‐parasite interactions may vary across environmental gradients. We used a zooplankton‐bacteria host‐parasite system where availability of sunlight (solar radiation) influences disease dynamics to look for evidence of parasite local adaptation to sunlight exposure. We also examined how variation in sunlight tolerance among parasite strains impacted host reproduction. Parasite strains collected from clearer lakes (with greater sunlight penetration) were most tolerant of the negative impacts of sunlight exposure, suggesting local adaptation to sunlight conditions. This adaptation came with both a cost and a benefit for parasites: parasite strains from clearer lakes produced relatively fewer transmission stages (spores) but these strains were more infective. After experimental sunlight exposure, the most sunlight‐tolerant parasite strains reduced host fecundity just as much as spores that were never exposed to sunlight. Sunlight availability varies greatly among lakes around the world. Our results suggest that the selective pressure sunlight exposure exerts on parasites may impact both parasite and host fitness, potentially driving variation in disease epidemics and host population dynamics across sunlight availability gradients. This article is protected by copyright. All rights reserved
Phenotypic plasticity has been hypothesized to precede and facilitate adaptation to novel environments [1, 2, 3, 4, 5, 6, 7, 8], but examples of plasticity preceding adaptation in wild populations are rare (but see [9, 10]). We studied a population of side-blotched lizards, Uta stansburiana, living on a lava flow that formed 22,500 years ago [11] to understand the origin of their novel melanic phenotype that makes them cryptic on the black lava. We found that lizards living on and off of the lava flow exhibited phenotypic plasticity in coloration but also appeared to have heritable differences in pigmentation. We sequenced the exomes of 104 individuals and identified two known regulators of melanin production, PREP and PRKAR1A, which had markedly increased levels of divergence between lizards living on and off the lava flow. The derived variants in PREP and PRKAR1A were only found in the lava population and were associated with increased pigmentation levels in an experimental cohort of hatchling lizards. Simulations suggest that the derived variants in the PREP and PRKAR1A genes arose recently and were under strong positive selection in the lava population. Overall, our results suggest that ancestral plasticity for coloration facilitated initial survival in the lava environment and was followed by genetic changes that modified the phenotype in the direction of the induced plastic response, possibly through de novo mutations. These observations provide a detailed example supporting the hypothesis that plasticity aids in the initial colonization of a novel habitat, with natural selection subsequently refining the phenotype with genetic adaptations to the new environment.
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In bluefin killifish (Lucania goodei), a genetic color polymorphism is present where red and yellow anal fin morphs coexist in clear springs. The source of balancing selection is unknown. In a field study, vertical distributions did not differ between the morphs. Likewise, there was little evidence that lighting environments qualitatively differed over the 200 centimeters at which fish were collected. A greenhouse study showed that both morphs preferred to spawn at shallow depths. Thus, vertical distribution and spawning site choice are unlikely to explain the maintenance of the color polymorphism.
How polymorphisms are maintained within populations over long periods of time remains debated, because genetic drift and various forms of selection are expected to reduce variation. Here, we study the genetic architecture and maintenance of phenotypic morphs that confer crypsis in Timema cristinae stick insects, combining phenotypic information and genotyping-by-sequencing data from 1360 samples across 21 populations. We find two highly divergent chromosomal variants that span megabases of sequence and are associated with color polymorphism. We show that these variants exhibit strongly reduced effective recombination, are geographically widespread, and probably diverged millions of generations ago. We detect heterokaryotype excess and signs of balancing selection acting on these variants through the species’ history. A third chromosomal variant in the same genomic region likely evolved more recently from one of the two color variants and is associated with dorsal pattern polymorphism. Our results suggest that large-scale genetic variation associated with crypsis has been maintained for long periods of time by potentially complex processes of balancing selection. This article is protected by copyright. All rights reserved.
Signal evolution is thought to depend on both a signal's detectability or conspicuousness (signal design) as well as any extractable information it may convey to a potential receiver (signal content). While theoretical and empirical work in sexual selection has largely focused on signal content, there has been a steady accrual of evidence that signal design is also important for trait evolution. Despite this, relatively little attention has been paid to spatial variation in the conspicuousness of a given signal, especially over small spatial scales (relative to an organism's dispersal distance). Here, we show that visual signals of male threespine stickleback vary in conspicuousness, depending on a male's nest depth within a given lake. Deeper-nesting males were typically more chromatically conspicuous than shallow nesting males. This trend is partly because all male stickleback are more conspicuous in deep optical environments. However, deep males are even more conspicuous than environmentally-driven null expectations, while shallow males tend to be disproportionally cryptic. Experimental manipulation of male nesting depth induced plastic changes in nuptial color that replicated the natural gradients in conspicuousness. We discuss a number of potential mechanisms that could produce depth gradients in conspicuousness in male stickleback, including concomitant depth gradients in diet, predation pressure, male/female density, female preference and opportunity for sexual selection. This article is protected by copyright. All rights reserved.
Sailfin mollies (Poecilia latipinna) display marked interdemic variation in body size. We employed "common-garden" experiments in field enclosures to explore the potential role of environmental factors in determining the interdemic phenotypic variation in growth rate, age at maturity, and size at maturity. The largest single, consistent source of variation for all traits was family identity within populations. Environmental effects acted predominantly through family x environment interactions. There was little evidence for any intrinsic variation among populations once family heterogeneity had been accounted for. In general, when statistically significant differences existed, fish raised in a saltwater pond grew faster than their broodmates raised in a freshwater pond. Both males and females tended to mature at a smaller size and later in the freshwater pond than in the saltwater pond. The effects of the environmental conditions differed among the three years in which we performed these studies. In only one year was there a substantial difference between fish raised under the two environmental conditions. These results indicate that direct environmental effects are not strong enough to account for the differences in body size among natural populations and that intrinsic differences among natural populations are due to different frequency distributions of genotypes that are present in all populations.
Studies of spatial variation in the environment have primarily focused on how genetic variation can be maintained. Many one-locus genetic models have addressed this issue, but, for several reasons, these models are not directly applicable to quantitative (polygenic) traits. One reason is that for continuously varying characters, the evolution of the mean phenotype expressed in different environments (the norm of reaction) is also of interest. Our quantitative genetic models describe the evolution of phenotypic response to the environment, also known as phenotypic plasticity (Gause, 1947), and illustrate how the norm of reaction (Schmalhausen, 1949) can be shaped by selection. These models utilize the statistical relationship which exists between genotype-environment interaction and genetic correlation to describe evolution of the mean phenotype under soft and hard selection in coarse-grained environments. Just as genetic correlations among characters within a single environment can constrain the response to simultaneous selection, so can a genetic correlation between states of a character which are expressed in two environments. Unless the genetic correlation across environments is ± 1, polygenic variation is exhausted, or there is a cost to plasticity, panmictic populations under a bivariate fitness function will eventually attain the optimum mean phenotype for a given character in each environment. However, very high positive or negative correlations can substantially slow the rate of evolution and may produce temporary maladaptation in one environment before the optimum joint phenotype is finally attained.
Optics--a field of physics focusing on the study of light--is also central to many areas of biology, including vision, ecology, botany, animal behavior, neurobiology, and molecular biology.The Optics of Lifeintroduces the fundamentals of optics to biologists and nonphysicists, giving them the tools they need to successfully incorporate optical measurements and principles into their research. S nke Johnsen starts with the basics, describing the properties of light and the units and geometry of measurement. He then explores how light is created and propagates and how it interacts with matter, covering topics such as absorption, scattering, fluorescence, and polarization. Johnsen also provides a tutorial on how to measure light as well as an informative discussion of quantum mechanics. The Optics of Lifefeatures a host of examples drawn from nature and everyday life, and several appendixes that offer further practical guidance for researchers. This concise book uses a minimum of equations and jargon, explaining the basic physics of light in a succinct and lively manner. It is the essential primer for working biologists and for anyone seeking an accessible introduction to optics.
The descriptive analysis of multivariate data is, in classical applications, mostly a univariate and bivariate description of the marginals. This is an inappropriate approach for compositional data, because the parts of a composition are intrinsically linked to each other: the dataset is multivariate in nature, not by decision of the analyst. Following the principle of working in coordinates and the golden rule of working with log ratios, we can structure a meaningful descriptive analysis of a compositional dataset in the following steps. In the first step, descriptive statistics for central tendency, global spread, and codependence are computed. The second step is a preliminary look at a set of predefined “marginals”, i.e., some ternary diagrams, to uncover relations between more than two parts. The third step is the exploration of the codependence structure through the biplot, a joint optimal representation of the variables and of the observations of a composition. Biplots are nevertheless explained in Chap. 6, because of their connection with principal component analysis. One of the aims of all the preceding phases should be to select a reasonable set of projections, or the selection of a basis: if this is achieved, the fourth step should be a classical univariate analysis of each coordinate.
Male bluefin killifish (Lucania goodei) exhibit extensive color variation in their fins, but the utility of this variation has not yet been determined. We collected males from multiple populations and spectrophotometrically determined the pigment types responsible for fin coloration. We determined that the orange coloration in the caudal fin is caused by carotenoid pigmentation. In contrast, color in the anal fin is either pterin based (yellow and red) or structural (blue) with a melanic fin border. As these colors have different developmental origins, the potential for complex signaling is high. Therefore, we sought to determine whether behavior, reproductive success, or health correlated with pigmentation. Males with more melanin on the anal fin were more dominant and had higher spawning success. Male-male aggression was greater between males with similar-sized melanic borders, indicating that melanic markings function as badges of status between males. Caudal carotenoid pigmentation did not correlate with dominance, but this highly labile ornament was correlated with body condition, parasite infection, and spawning success, suggesting a role in intersexual selection by signaling health to potential mates. Similar results were found for caudal fin coloration using digital photography. Pterin pigmentation in the anal fin was not related to dominance but was related to overall spawning levels and parasite infection, suggesting that pterin pigmentation may also signal immune status. Thus, the coloration of male bluefin killifish provides multiple messages to multiple receivers through these 3 pigments (melanin, pterin, and carotenoid) that have distinct developmental origins.
Phenotypic responses to photon flux density (PFD) by five populations of the herbaceous perennial Prunella vulgaris L. were compared. Plants from each population were grown in two light environments, and we measured the effect of PFD on overall performance (size) as well as the responses of several physiological traits to PFD. Both measures of size and physiological traits differed significantly between light environments and among populations. Significant population-by-environment interaction was detected for measures of size but not for any physiological traits. These results indicate significant differences among populations in the extent to which size is reduced by a decrease in PFD. However, these differences are not the result of variation in the responses of the physiological traits we measured. A comparison of the patterns of correlations among traits in the two light environments indicated signficant similarity of correlation structure between environments. This result contrasts with those of studies showing strong environmental dependence of phenotypic relationships between traits.
Data describing amounts of components of specimens are compositional if the size of each specimen is constant or irrelevant. Ideally compositional data is given by relative portions summing up to 1 or 100 %. But more often compositional data appear disguised in several ways: different components might be reported in different physical units, different cases might sum up to different totals, and almost never all relevant components are reported. Nevertheless, the constraints of constant sum and relative meaning of the portions have important implications for their statistical analysis, contradicting the typical assumptions of usual uni- and multivariate statistical methods and thus rendering their direct application spurious. A comprehensive statistical methodology, based on a vector space structure of the mathematical simplex, has only been developed very recently, and several software packages are now available to treat compositional data within it. This book is at the same time a textbook on compositional data analysis from a modern perspective and a sort of manual on the R-package “compositions”: both R and “compositions” are available for download as free software. This chapter discusses the need of an own statistical methodology for compositions, the historic background of compositional data analysis, and the software needs for compositional data analysis.
Often more than one quantitative trait is measured on each person in a set of pedigrees. The present paper suggests a class of covariance components models that will allow investigators to explore the genetic and environmental relationships between two quantitative traits. The theoretical framework for the models is given and criticized. We also discuss specific maximum likelihood methods for parameter estimation and hypothesis testing.
The mechanisms and functions of reversible colour change in arthropods are highly diverse despite, or perhaps due to, the presence of an exoskeleton. Physiological colour changes, which have been recorded in 90 arthropod species, are rapid and are the result of changes in the positioning of microstructures or pigments, or in the refractive index of layers in the integument. By contrast, morphological colour changes, documented in 31 species, involve the anabolism or catabolism of components (e.g. pigments) directly related to the observable colour. In this review we highlight the diversity of mechanisms by which reversible colour change occurs and the evolutionary context and diversity of arthropod taxa in which it has been observed. Further, we discuss the functions of reversible colour change so far proposed, review the limited behavioural and ecological data, and argue that the field requires phylogenetically controlled approaches to understanding the evolution of reversible colour change. Finally, we encourage biologists to explore new model systems for colour change and to engage scientists from other disciplines; continued cross-disciplinary collaboration is the most promising approach to this nexus of biology, physics, and chemistry.
Abstract Determining the degree to which variation in traits is controlled by genetics and/or environment is fundamental to understanding adaptation. In this study, we examine the genetic and environmental influences on color pattern expression in male bluefin killifish, Lucania goodei. This is a compelling system because both male color patterns and vision physiology are correlated with basic properties of the environment. Across populations, males with blue anal fins are more abundant in waters with low transmission of UV and blue wavelengths. Here, we present results from two paternal half-sib breeding experiments (one in the laboratory, one in the greenhouse) in which offspring were raised under light treatments that mimicked natural variation in the spectral composition of light. In both experiments, we found that red-versus-yellow expression is controlled by an autosomal locus of large effect where yellow (Y) is dominant over red (y). There was little blue expression in the laboratory. In the greenhouse, we found higher expression of blue anal fin morphs when males were raised in tea-stained water (low transmission UV/ blue) than when raised in clear water (high transmission UV/blue). We also found genetic effects of sires and an interaction between sire and lighting environment (i.e. heritable plasticity). These results show that a relatively simple, environmentally dependent, epistatic interaction can produce a large amount of variation in male color patterns that presumably function in sexual selection.
This book describes the sexual behavior of guppies and examines how mate choice by females leads to the evolution of the conspicuous colors and the courtship displays for which guppies are widely recognized. The author shows that female guppies prefer males with bright color patterns, especially those with orange spots, and that the mating preferences of females lead to sexual selection on both color patterns and courtship displays of males. Houde's work addresses a number of areas that are of interest in sexual selection, including the remarkable degree of plasticity and evolutionary lability of sexual behavior in guppies, geographic variation in mating preferences, possible mechanisms for the evolution of female mating preferences, and the role of sexual selection in speciation. In conclusion, the author explores the implications of her findings for behavioral ecologists who study sexual selection in other species.