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The Evolution of Self-Fertilization and Inbreeding Depression in Plants. I. Genetic Models
Abstract
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.
... The evolution of self-fertilization in the quantitative genetic model presented here is similar to the conclusions of previous published models assuming monomorphic populations and modifier locus (Lande and Schemske 1985;Lloyd 1992;Cheptou and Mathias 2001). Here, the evolution of self-fertilization results from the balance between inbreeding depression (captured by p self and p out ) , pollen limitation (captured by p pol ) and the twofold cost of outcrossing. ...
... 2 ). Evolutionary scenarios are dependent on the cost of outcrossing as classically considered in mating system evolution models (Lande and Schemske 1985). Because an individual can sire ovules devoted to outcrossing in the population through pollen export, its fitness depend on the mating strategies (and their frequencies) of individuals in the population i.e. the fitness is frequency dependent. ...
... Our model has however several limitations with regards to classical mating system models. First, inbreeding depression is considered as fixed during the evolution of self-fertilization, i.e. we did not allow the possibility of purging deleterious mutations (Lande and Schemske 1985;Charlesworth et al. 1991). We acknowledge that this is limitation of the model. ...
As reported by experimental studies, changes in pollination regime are expected to drive plant mating system evolution. In natural populations facing pollinator decline, plant-mating system is thus susceptible to evolve. We analyzed the demographic consequences of such evolution and if such evolution can rescue populations. We developed a quantitative genetic model for evolution after a pollinator crash and we analyzed the demographic consequences over a few dozens of generations. The model considers two sources of stochasticity. Contrary to classical models, inbreeding depression is considered as a probabilistic event affecting differentially inbred and outbred individuals (demographic stochasticity). Pollination is also considered as a probabilistic event (environmental stochasticity). The model is derived under (1) infinite population size and (2) finite population size. The results highlight three generic evolutionary scenarios. The evolution of selfing after a pollinator crash can rescue populations but can sometimes lead to evolutionary suicide. While the genetic variance of mating system traits determines the pace of evolution, initial population sizes determine the countdown for evolution to rescue population making stochastic extinction likely in small populations. Our model shows that evolution may not save populations due to frequency-dependent selection acting on mating system. We propose an alternative interpretation for the higher extinction rate of selfing taxa and we discuss its implications for plant conservation.
... Waller, 2021 emphasized this enigma and reviewed mechanisms that might account for it. Selective interference among loci might act to slow or block purging (Lande and Schemske, 1985;Winn et al., 2011). Recurrent mutations might also replenish the load fast enough to regenerate δ (B. ...
... Mutations erode from either end of the POD zone or the load becomes unbalanced enough to fix one haplotype. The importance of linkage and small mutational effects are evident in the radically enhanced purging seen in models that ignore linkage and assume major mutational effects (Lande and Schemske, 1985). We also found that new recessive mutations that occur elsewhere in the genome generate associations with load alleles within POD zones that enhance POD zone heterozygosity and persistence (Fig. 4). ...
... In these simple static models, inbreeding depression less than 0.5 would result in exclusive selfing while higher levels would favor exclusive outcrossing. More dynamic simple models that allow selection make mixed mating systems even more improbable by allowing inbreeding to purge deleterious mutations, generating "run-away" selection for ever-increasing levels of selfing (Lande and Schemske, 1985). If drift instead fixes many segregating mutations, similar effects emerge as this, too, causes inbreeding depression to decline. ...
Classical models that ignore linkage predict that deleterious recessive mutations should purge or fix within inbred populations, yet inbred populations often retain moderate to high segregating load. True overdominance could generate balancing selection strong enough to sustain inbreeding depression even within inbred populations, but this is considered rare. However, arrays of deleterious recessives linked in repulsion could generate appreciable pseudo-overdominance that would also sustain segregating load. We used simulations to explore how long pseudo-overdominant (POD) zones persist once created (e.g., by hybridization between populations fixed for alternative mildly deleterious mutations). Balanced haplotype loads, tight linkage, and moderate to strong cumulative selective effects all serve to maintain POD zones. Tight linkage is key, suggesting that such regions are most likely to arise and persist in low recombination regions (like inversions). Selection and drift unbalance the load, eventually eliminating POD zones, but this process is quite slow under strong pseudo-overdominance. Background selection accelerates the loss of weak POD zones but reinforces strong ones in inbred populations by disfavoring homozygotes. Models and empirical studies of POD dynamics within populations help us understand how POD zones may allow the load to persist, greatly affecting load dynamics and mating systems evolution
... Inbreeding Inbreeding depression is the reduction in the fitness of progeny produced by consanguineous mating compared with mating between unrelated parents (Wright, 1984). Inbreeding depression is important in crop production, conservation of natural populations, and mating system evolution (Lloyd, 1979;Lande & Schemske, 1985;Charlesworth & Willis, 2009;Frankham, 2010). While recessive deleterious mutations are thought to play a major role in inbreeding depression, overdominance has also been implicated (Wright, 1984;Charlesworth & Willis, 2009). ...
... While recessive deleterious mutations are thought to play a major role in inbreeding depression, overdominance has also been implicated (Wright, 1984;Charlesworth & Willis, 2009). Lande & Schemske (1985) considered the relationship between inbreeding depression and mating system evolution. Their theoretical work predicted that when there is selective purging of recessive lethal and near-lethal alleles, populations of self-fertilizing organisms should exhibit reduced equilibrium levels of inbreeding depression. ...
... Inbreeding depression is thought to be the main barrier to the evolution of self-pollination (Lloyd, 1979), and yet with selfpollination, purging of recessive load is expected (Lande & Schemske, 1985). In an earlier set of population surveys, Baldwin & Schoen (2017) found that some selfing likely does occur in populations of L. alabamica that had been previously characterized at SI. Between 6 and 18% of plants exhibit 'leaky selfincompatibility' in which pollen tubes from self-pollen penetrate the styles. ...
Inbreeding depression plays a fundamental role in evolution. To help detect and characterize the loci that underlie inbreeding depression, we used bud pollination and salt treatments to circumvent self‐incompatibility (SI) in plants from populations of Leavenworthia alabamica and produced families of progeny that were then genotyped at genetically mapped single‐nucleotide polymorphism (SNP) loci.
Using Bayesian inference, the segregation patterns for each SNP were used to explore support for different dominance and selection coefficients at linked viability loci in different genomic regions.
There was support for several partially recessive viability loci in one of the populations, and one such locus mapped to the genomic region of the novel SI locus in L. alabamica.
These results are consistent with earlier findings that showed purging of inbreeding depression for germination rate in L. alabamica. They are also consistent with expectations from evolutionary genetic theory that recessive, deleterious alleles linked to loci under balancing selection can be sheltered from selection.
... The ID coefficient d was calculated from five reproductive traits (fruit set, seed number, seed length, well-developed seed proportion, in vitro germination), both for entire inflorescences and division of inflorescence on three levels, using formulas by Ågren and Schemske (1993) and Lande and Schemske (1985). The formula d = 1 − (Ws/Wo) was used when Ws < Wo, and d = (Wo/ Ws) − 1 for Ws > Wo, where Ws represents the average fitness of selfed progeny and Wo represents that of outcrossed progeny. ...
... The formula d = 1 − (Ws/Wo) was used when Ws < Wo, and d = (Wo/ Ws) − 1 for Ws > Wo, where Ws represents the average fitness of selfed progeny and Wo represents that of outcrossed progeny. The estimation was carried out using data where Ws denotes the average fitness of selfed progeny from autogamy and geitonogamy treatments and Wo denotes the average fitness of manually outcrossed progeny (Lande and Schemske, 1985;Charlesworth & Charlesworth, 1987). Cumulative d values were calculated incorporating the correlation among data sets, using the approach by Husband & Schemske (1996): d = 1 − (Ws F /Wo F x Ws NS /Wo NS x Ws SL /Wo SL x Ws DS /Wo DS x Ws IV /Wo IV ), where F is fruit set; NS is seed number per fruit; SL is seed length, DS is frequency of properly developed seeds per fruit, and IV is proportion in vitro asymbiotic germinated seeds to protocorm. ...
Introduction
Inbreeding depression (ID) in food-deceptive plants have been reported previously, however, it has not been often proven that selfed seeds germinate better than outbred ones or that selfing affects ID. To resolved these issues, food-deceptive related Dactylorhiza majalis, D. incarnata var. incarnata and D. fuchsii orchids were investigated.
Methods
Hand pollination treatments and control pollination were conducted. Fruit set, number of seeds per fruit, seed length, number of well-developed seeds per fruit, and proportion of in vitro asymbiotic germination seeds, were analyzed in relation to inflorescence levels and used as fitness indicators for these orchids. The ID and pollen limitation were measured.
Results
The lowest ID (δ = −1.000) was in D. majalis, and present in combination with a high pollen limitation in its populations. D. fuchsii showed higher ID (δ = 0.366), and D. incarnata var. incarnata weak ID (δ = 0.065), although ID varied between its fitness components. The seed number per fruit differed significantly between the treatments and the inflorescence levels in treatments.
Discussion
This study emphasizes that the breeding system rather than the flower position on the inflorescence shaped the quality and quantity of reproductive output. The ID and its effect on germination of food-deceptive orchid seeds undoubtedly played an important role.
... Comparison of results for resource-and ovulelimited cases reveals a feature of classic matingsystem theory that has not been recognized previously. Standard mating-system models (e.g., Lande and Schemske 1985) and Lloyd's (1979) model of competing selfing assumed that self-pollination did not affect pollen export and so are equivalent to the case modelled here. These models suggested that self-pollination is favoured if inbreeding depression (d) after self-fertilization is < 0.5. ...
... The theory presented in this chapter follows Lloyd's (1979Lloyd's ( , 1992 lead of expanding the analysis of mating-system evolution beyond the traditional genetic approach, which emphasized inbreeding depression (e.g., Lande and Schemske 1985;Charlesworth and Charlesworth 1987), to consider the influences of ecological factors (also see Uyenoyama et al. 1993;Goodwillie et al. 2005;Chapters 2, 6, 8, 10 and 12). A specific contribution of our models is the recognition that the post-dispersal performance of selfed seeds relative to outcrossed seeds (d s /d x ) provides a more general criterion for mating system evolution than does lifetime inbreeding depression (see Table 4.3). ...
The reproductive organs and mating biology of angiosperms exhibit greater variety than those of any other group of organisms. Flowers and inflorescences are also the most diverse structures produced by angiosperms, and floral traits provide some of the most compelling examples of evolution by natural selection. Given that flowering plants include roughly 250,000 species, their reproductive diversity will not be explained easily by continued accumulation of case studies of individual species. ınstead a more strategic approach is now required, which seeks to identify general principles concerning the role of ecological function in the evolution of reproductive diversity. The Ecology and Evolution of Flowers uses this approach to expose new insights into the functional basis of floral diversity, and presents the very latest theoretical and empirical research on floral evolution. Floral biology is a dynamic and growing area and this book, written by the leading internationally recognized researchers in this field, reviews current progress in understanding the evolution and function of flowers. Chapters contain both new research findings and synthesis. Major sections in turn examine functional aspects of floral traits and sexual systems, the ecological influences on reproductive adaptation, and the role of floral biology in angiosperm diversification. Overall, this integrated treatment illustrates the role of floral function and evolution in the generation of angiosperm biodiversity. This advanced textbook is suitable for graduate level students taking courses in plant ecology, evolution, systematics, biodiversity and conservation. ıt will also be of interest and use to a broader audience of plant scientists seeking an authoritative overview of recent advances in floral biology.
... The inbreeding depression was calculated by using the formula; δ = 1 -Ws/Wo; Where δ = inbreeding depression, Ws = the result of progeny from self-pollination and Wo = the outcome of progeny from cross-pollination (Lande & Schemske, 1985). A delineation inbreeding depression value of δ = 0.5, signified that the selfing is preferred below the value and beyond which outcrossing is favoured (Lande & Schemske, 1985). ...
... The inbreeding depression was calculated by using the formula; δ = 1 -Ws/Wo; Where δ = inbreeding depression, Ws = the result of progeny from self-pollination and Wo = the outcome of progeny from cross-pollination (Lande & Schemske, 1985). A delineation inbreeding depression value of δ = 0.5, signified that the selfing is preferred below the value and beyond which outcrossing is favoured (Lande & Schemske, 1985). ...
The aim of this study was to estimate reproductive effort and success in tropical trees and to examine the effect of pollen limitation on reproductive success. Pollen limitation was assessed through pollen supplementation experiment to contrast the open pollination treatment. The taxa selected were Bombax ceiba, Erythrina stricta (ornithophilous trees), Lagerstroemia speciosa, Mesua ferrea and Schima wallichii (entomophilous trees). Index of pollen limitation was highest in Bombax ceiba and Erythrina stricta (both self-incompatible species). The remaining three species were partially self-incompatible with favouring selfing in Lagerstroemia speciosa and Mesua ferrea and supporting outcrossing in Schima wallichii . Therefore, the high index of pollen limitation in Bombax ceiba and Erythrina stricta might be due to the effect of either lacking quality pollen or lacking bird pollinators. All five species produce a large amount of pollen at individual tree level in the order of 108 ( Erythrina stricta ) to 1010 ( Mesua ferrea ). Fruit and seed set following pollen supplementation were higher than the open pollination (as control) in all studied species. Pollen limitation in this study is likely associated with the effectiveness of pollinator and their frequency, as all the studied species had produced ample pollen at tree crown level which ultimately leads to pollinator resource limitation in tropical trees.
... Uniquely among conifers, WRC uses a mixed mating system of outcrossing and self-fertilization (selfing), with a mean outcrossing rate of ∼70% (El-Kassaby et al. 1994;O'Connell et al. 2001O'Connell et al. , 2004, and appears to suffer very little inbreeding depression for fitness growth traits (Wang and Russell 2006;Russell and Ferguson 2008). Mating systems in plants, particularly rates of selfing (s) and its complement, outcrossing (1s), are of interest to evolutionary biologists owing to their implications for genetic diversity and fitness and have been investigated extensively over the past century (Stebbins 1957;Lande and Schemske 1985;Barrett and Eckert 1990; Barrett et al. 2003;Wright et al. 2013). Although inbreeding depression resulting from selfing can lead to negative fitness impacts, a benefit of selfing may include reproductive assurance (Fisher 1941;Baker 1955), which, in the absence of strong inbreeding depression, can allow self-compatible populations to expand their geographic range faster than obligate outcrossers (Lande and Schemske 1985). ...
... Mating systems in plants, particularly rates of selfing (s) and its complement, outcrossing (1s), are of interest to evolutionary biologists owing to their implications for genetic diversity and fitness and have been investigated extensively over the past century (Stebbins 1957;Lande and Schemske 1985;Barrett and Eckert 1990; Barrett et al. 2003;Wright et al. 2013). Although inbreeding depression resulting from selfing can lead to negative fitness impacts, a benefit of selfing may include reproductive assurance (Fisher 1941;Baker 1955), which, in the absence of strong inbreeding depression, can allow self-compatible populations to expand their geographic range faster than obligate outcrossers (Lande and Schemske 1985). Research on inbreeding in plants has mostly focused on mating strategies in angiosperms (Barrett and Eckert 1990;Jarne and Charlesworth 1993;Vogler and Kalisz 2001;Barrett et al. 2003;Kalisz et al. 2004;Wright et al. 2013). ...
We assembled the 9.8 Gbp genome of western redcedar (WRC, Thuja plicata ), an ecologically and economically important conifer species of the Cupressaceae. The genome assembly, derived from a uniquely inbred tree produced through five generations of self-fertilization (selfing), was determined to be 86% complete by BUSCO analysis - one of the most complete genome assemblies for a conifer. Population genomic analysis revealed WRC to be one of the most genetically depauperate wild plant species, with an effective population size of approximately 300 and no significant genetic differentiation across its geographic range. Nucleotide diversity, π, is low for a continuous tree species, with many loci exhibiting zero diversity, and the ratio of π at zero- to four-fold degenerate sites is relatively high (~ 0.33), suggestive of weak purifying selection. Using an array of genetic lines derived from up to five generations of selfing, we explored the relationship between genetic diversity and mating system. While overall heterozygosity was found to decline faster than expected during selfing, heterozygosity persisted at many loci, and nearly 100 loci were found to deviate from expectations of genetic drift, suggestive of associative overdominance. Nonreference alleles at such loci often harbor deleterious mutations and are rare in natural populations, implying that balanced polymorphisms are maintained by linkage to dominant beneficial alleles. This may account for how WRC remains responsive to natural and artificial selection, despite low genetic diversity.
... Theoretical and experimental work suggests that, in the absence of inbreeding depression and assuming that all individuals produce equal number of seeds, once selfing originates, the selfing phenotype should increase in frequency and eventually become fixed over time (Charlesworth et al., 1990;Fisher, 1941;Lande & Schemske, 1985). ...
Distyly, a floral dimorphism that promotes outcrossing, is controlled by a hemizygous genomic region known as the S ‐locus. Disruptions of genes within the S ‐locus are responsible for the loss of distyly and the emergence of homostyly, a floral monomorphism that favors selfing. Using whole‐genome resequencing data of distylous and homostylous individuals from populations of Primula vulgaris and leveraging high‐quality reference genomes of Primula we tested, for the first time, predictions about the evolutionary consequences of transitions to selfing on S ‐genes. Our results reveal a previously undetected structural rearrangement in CYPᵀ associated with the shift to homostyly and confirm previously reported, homostyle‐specific, loss‐of‐function mutations in the exons of the S ‐gene CYPᵀ . We also discovered that the promoter and intronic regions of CYPᵀ in distylous and homostylous individuals are conserved, suggesting that down‐regulation of CYPᵀ via mutations in its promoter and intronic regions is not a cause of the shift to homostyly. Furthermore, we found that hemizygosity is associated with reduced genetic diversity in S ‐genes compared with their paralogs outside the S ‐locus. Additionally, the shift to homostyly lowers genetic diversity in both the S ‐genes and their paralogs, as expected in primarily selfing plants. Finally, we tested, for the first time, long‐standing theoretical models of changes in S ‐locus genotypes during early stages of the transition to homostyly, supporting the assumption that two copies of the S ‐locus might reduce homostyle fitness.
... Selection of minimal coancestry matings has also prevented the recurrence of new bottlenecks and big subdivisions in the population. This may be due to the genetic purging process recently described in the mhorr gazelle population by López-Cortegano et al. (2021), a process by which alleles are removed by selection, thus improving some fitness traits over generations and reducing inbreeding depression (Lande & Schemske, 1985). The retention of enough genetic variability, maximizing the genetic representation of all the wild-caught founders, is essential for future adaptation, successful expansion and restoration of natural populations (Frankham, 1996;Hedrick & Miller, 1992). ...
Breeding programs have an essential role in the recovery of threatened populations through optimal genetic management and mating strategies. The dama gazelle ( Nanger dama ) is a North African ungulate listed as critically endangered. The mhorr subspecies is extinct in the wild and currently survives thanks to the creation in 1971 of an ex situ breeding program. The aim of the present study was to assess the evolution of genetic variability in this mhorr gazelle captive population, as well as the mating strategy used in two reference populations studied (Almeria and Europe). The entire pedigree, with 2739 animals, was analyzed to measure demographic characters, pedigree completeness level, probability of gene origin, level of relatedness and genetic structure of the population. The population size has been progressively increasing, with up to 264 individuals alive in Europe at the time of the study. The average number of equivalent complete generations was 5.55. The effective number of founders and ancestors was both 3, and the founder genome equivalent was 1.99. The genetic contributions of the four main ancestors were unbalanced. The average values of inbreeding and average relatedness for the whole pedigree were, respectively, 28.34% and 50.14%. The effective population size was 8.7 by individual increase in inbreeding and 9.8 by individual increase in coancestry. F ‐statistics evidenced a very small level of population subdivision ( F ST = 0.033370). The mating strategy used, based on the minimum coancestry of the individuals, has minimized the losses of genetic variability and helped to balance the genetic contributions between ancestors. The strategy also avoided large subdivisions within the population and the appearance of new bottlenecks. This study shows how pedigree analysis can both be used to determine the genetic variability of the population and to assess the influence of the mating strategy used in the breeding program on such variability.
... Lloyd's most important contribution to studies of mating-system evolution was to introduce a functional dimension to the topic by forcing researchers to consider how and why self-pollination occurs, and the demographic and environmental context in which mating takes place (Lloyd 1979b(Lloyd , 1980a(Lloyd , 1992a. This ecological perspective has balanced population genetic approaches, which have traditionally dominated research in this area (e.g., Nagylaki 1976;Charlesworth 1980;Lande and Schemske 1985). The integration of ecological and genetic aspects stimulated by Lloyd has been incorporated increasingly in studies of plant mating (Holsinger 1996;Barrett and Pannell 1999). ...
The reproductive organs and mating biology of angiosperms exhibit greater variety than those of any other group of organisms. Flowers and inflorescences are also the most diverse structures produced by angiosperms, and floral traits provide some of the most compelling examples of evolution by natural selection. Given that flowering plants include roughly 250,000 species, their reproductive diversity will not be explained easily by continued accumulation of case studies of individual species. ınstead a more strategic approach is now required, which seeks to identify general principles concerning the role of ecological function in the evolution of reproductive diversity. The Ecology and Evolution of Flowers uses this approach to expose new insights into the functional basis of floral diversity, and presents the very latest theoretical and empirical research on floral evolution. Floral biology is a dynamic and growing area and this book, written by the leading internationally recognized researchers in this field, reviews current progress in understanding the evolution and function of flowers. Chapters contain both new research findings and synthesis. Major sections in turn examine functional aspects of floral traits and sexual systems, the ecological influences on reproductive adaptation, and the role of floral biology in angiosperm diversification. Overall, this integrated treatment illustrates the role of floral function and evolution in the generation of angiosperm biodiversity. This advanced textbook is suitable for graduate level students taking courses in plant ecology, evolution, systematics, biodiversity and conservation. ıt will also be of interest and use to a broader audience of plant scientists seeking an authoritative overview of recent advances in floral biology.
... A widely discussed example from plant biology is the evolution of reproductive self-compatibility and self-fertilization in angiosperms. Self-compatibility can be adaptive when outcrossing opportunities are limited but may ultimately increase a lineage's probability of extinction through inbreeding depression or inability to respond rapidly to changes in selection pressures (Stebbins, 1957;Lande and Schemske, 1985;Takebayashi and Morrell, 2001;Igic and Busch, 2013). Phylogenetic estimates of macroevolutionary rates have provided empirical support for this hypothesis (Goldberg et al., 2010;Freyman andHöhna, 2019, Zenil-Ferguson et al., 2019), ...
Activity pattern has played a prominent role in discussions of primate evolutionary history. Most primates are either diurnal or nocturnal, but a small number are active both diurnally and nocturnally. This pattern—cathemerality—also occurs at low frequency across mammals. Using a large sample of mammalian species, this study evaluates two macroevolutionary hypotheses proposed to explain why cathemerality is less common than diurnality and nocturnality: (1) that cathemeral lineages have higher extinction probabilities (differential diversification), and (2) that transitions out of cathemerality are more frequent, making it a less persistent state (differential state persistence). Rates of speciation, extinction, and transition between character states were estimated using hidden-rates models applied to a phylogenetic tree containing 3013 mammals classified by activity pattern. The models failed to detect consistent differences in diversification dynamics among activity patterns, but there is strong support for differential state persistence. Transition rates out of cathemerality tend to be much higher than transition rates out of nocturnality. Transition rates out of diurnality are similar to those for cathemerality in most clades, with two important exceptions: diurnality is unusually persistent in anthropoid primates and sciurid rodents. These two groups combine very low rates of transition out of diurnality with high speciation rates. This combination has no parallels among cathemeral lineages, explaining why diurnality has become more common than cathemerality in mammals. Similarly, the combination of rates found in anthropoids is sufficient to explain the low relative frequency of cathemerality in primates, making it unnecessary to appeal to high extinction probabilities in cathemeral lineages in this clade. These findings support the hypothesis that the distribution of activity patterns across mammals has been influenced primarily by differential state persistence, whereas the effect of differential diversification appears to have been more idiosyncratic.
... However, in extremely tiny populations, the effect of removal is also quite limited [57]. There are few direct indications from natural populations that purification can eradicate inbreeding depression [58]. Studies have shown that deleterious alleles are eliminated over time [59]. ...
Ammopiptanthus possesses ancestral traits and, as a tertiary relict, is one of the surviving remnants of the ancient Mediterranean retreat and climate drought. It is also the only genus of super xerophytic, evergreen, broad-leaved shrubs. Ammopiptanthus nanus, one of the two species in this genus, is predominantly found in extremely arid and frigid environments, and is increasingly threatened with extinction. Study of the species’ genetic diversity is thus beneficial for its survival and the efficacy of ex situ conservation efforts. Based on transcriptome data, 15 pairs of effective EST-SSR were screened to evaluate A. nanus genetic diversity. In all, 87 samples from three populations were evaluated, the results of which show that ex situ conservation in the Wuqia region needs to be supplemented. Conservation and breeding of individual A. nanus offspring should be strengthened in the future to ensure their progeny continue to exhibit high genetic diversity and variation.
... Second, recombination must be such that adapted haplotypes can emerge on most chromosomes. Purging a few, highly deleterious alleles is relatively simple (Lande and Schemske 1985;Charlesworth and Charlesworth 1999). Zhang et al. (2021) developed a genome design pipeline for identifying and eliminating large-effect deleterious alleles, but the task becomes difficult when there are many slightly deleterious alleles, which are often linked in repulsion (Fig. 1), a phenomenon identified over half a century ago and called the Hill-Robertson effect (Comeron et al. 2008;Hill and Robertson 1966). ...
Conversion of potato from a tetraploid, heterozygous, vegetatively propagated crop to a diploid F1 hybrid, propagated via botanical seed, would constitute a considerable advance for global agriculture, but faces multiple challenges. One such challenge is the difficulty in inbreeding potato, which involves purging deleterious alleles from its genome. This commentary discusses possible reasons for this difficulty and highlights a recent sequence-based effort to classify SNP variation, in potato germplasm, according to its deleterious potential. Tools and strategies connected to this database may facilitate development of F1 hybrids.
... 385Meta-analysis (Whitehead et al. 2018) suggests that variation of selfing rates among conspecific 386populations can be large in species with an intermediate mean selfing rate, while is relatively low in 387 predominantly outcrossing or selfing species. In fact, previous models predict that either completely selfing or 388 outcrossing is evolutionarily stable(Lloyd 1979, Lande andSchemske 1985), but populations with mixed mating 389 systems are common(Goodwillie et al. 2005), which may represent a transient stage during evolution from 390 outcrossing to selfing. Based on the fact of great among-population variation in selfing rates, the current results 391 ...
Phylogenetic analyses suggest that self-compatible lineages have higher speciation rates than self-incompatible lineages. However, the effects of selfing on speciation remain unclear. Although a selfing population can resist gene flow from other populations, selfing may increase gene flow from a focal population to other populations. This study investigates the effects of selfing rates of two populations on the waiting time to speciation through the accumulation of Dobzhansky-Muller incompatibilities (DMI). Generally, a higher mean selfing rate of two populations facilitates speciation when incompatibility-controlling alleles are recessive and are weakly selected, and when gene flow is mainly through pollen dispersal instead of seed dispersal. However, the selfing rate difference between two populations can retard speciation, especially when the selfing rate of immigrants remains unchanged after migration. When the selfing rates of two populations differ, speciation may be fastest when the mean selfing rate is intermediate. Given that selfing rates often vary among conspecific populations in plant species, the results indicate that lineages with higher mean selfing rates may not necessarily have higher rates of speciation through the accumulation of DMI, and also call for an estimation of the dependency of speciation rates on selfing rates.
... The data suggest that if inbreeding affects lifetime reproductive success in this population of seals, the effect is very minor. The estimated cost of inbreeding (δ sensu [86]) in lifetime reproductive success for mature individuals with an inbreeding coefficient of 0.25 (equivalent to a full sibling mating) was lower (0.137, 95% confidence interval from 0.032 to 0.260) than the average cost of inbreeding for mortality in wild (2.155 after standardizing for F = 0.25; [10]) or captive mammal populations (0.33; [9]). It is important to note that these costs of inbreeding are calculated at an inbreeding coefficient beyond any of the median values observed in our sample. ...
Inbreeding depression can reduce the viability of wild populations. Detecting inbreeding depression in the wild is difficult; developing accurate estimates of inbreeding can be time and labor intensive. In this study, we used a two-step modeling procedure to incorporate uncertainty inherent in estimating individual inbreeding coefficients from multilocus genotypes into estimates of inbreeding depression in a population of Weddell seals (Leptonychotes weddellii). The two-step modeling procedure presented in this paper provides a method for estimating the magnitude of a known source of error, which is assumed absent in classic regression models, and incorporating this error into inferences about inbreeding depression. The method is essentially an errors-in-variables regression with non-normal errors in both the dependent and independent variables. These models, therefore, allow for a better evaluation of the uncertainty surrounding the biological importance of inbreeding depression in non-pedigreed wild populations. For this study we genotyped 154 adult female seals from the population in Erebus Bay, Antarctica, at 29 microsatellite loci, 12 of which are novel. We used a statistical evidence approach to inference rather than hypothesis testing because the discovery of both low and high levels of inbreeding are of scientific interest. We found evidence for an absence of inbreeding depression in lifetime reproductive success, adult survival, age at maturity, and the reproductive interval of female seals in this population.
... However, the elevated homozygosity of selfers allows for the more efficient fixation of advantageous (Abu Awad & Roze, 2018), and removal of deleterious (Charlesworth, 1992), partially recessive (h < 0.5) mutations. As such, partially selfing populations can more effectively "purge" recessive (and likely highly deleterious mutations, as estimated in three model organisms; Agrawal & Whitlock, 2011;Crow, 1993;Huber et al., 2018;Mukai et al., 1972;Phadnis & Fry, 2005) mutations than can highly outcrossing populations (Lande & Schemske, 1985). So, all else equal, the selfing rate does not change the efficacy of selection on mutations with additive effect but facilitates the purging of (partially) recessive mutations. ...
Much theory has focused on how a population's selfing rate affects the ability of natural selection to remove deleterious mutations from a population. However, most such theory has focused on mutations of a given dominance and fitness effect in isolation. It remains unclear how selfing affects the purging of deleterious mutations in a genome-wide context where mutations with different selection and dominance coefficients co-segregate. Here, we use individual-based forward simulations and analytical models to investigate how mutation, selection and recombination interact with selfing rate to shape genome-wide patterns of mutation accumulation and fitness. In addition to recovering previously described results for how selfing affects the efficacy of selection against mutations of a given dominance class, we find that the interaction of purifying selection against mutations of different dominance classes changes with selfing and recombination rates. In particular, when recombination is low and recessive deleterious mutations are common, outcrossing populations transition from purifying selection to pseudo-overdominance, dramatically reducing the efficacy of selection. At these parameter combinations, the efficacy of selection remains low until populations hit a threshold selfing rate, above which it increases. In contrast, selection is more effective in outcrossing than (partial) selfing populations when recombination rates are moderate to high and recessive deleterious mutations are rare.
... The wide variety of mating systems observed in animals, plants, fungi and algae has multiple ecological and evolutionary consequences that might impact higher-level evolutionary processes such as species extinction and speciation. For instance, hermaphroditic species vary in their rate of self-fertilisation-spanning from obligate outcrossing via all degrees of mixed mating to predominant selfing species [2][3][4]-and this has long been argued to affect macroevolutionary processes [5][6][7][8][9]. Because selfing tends to reduce both the genetic diversity and the adaptive potential of populations, selfing lineages have been argued to be 'evolutionary deadends' as they can be expected to go extinct at faster rates than outcrossing lineages [5,8,10,11]. ...
Self-fertilisation is widespread among hermaphroditic species across the tree of life. Selfing has many consequences on the genetic diversity and the evolutionary dynamics of populations, which may in turn affect macroevolutionary processes such as speciation. On the one hand, because selfing increases genetic drift and reduces migration rate among populations, it may be expected to promote speciation. On the other hand, because selfing reduces the efficacy of selection, it may be expected to hamper ecological speciation. To better understand under which conditions and in which direction selfing affects the build-up of reproductive isolation, an explicit population genetics model is required. Here, we focus on the interplay between genetic drift, selection and genetic linkage by studying speciation without gene flow. We test how fast populations with different rates of selfing accumulate mutations leading to genetic incompatibilities. When speciation requires populations to pass through a fitness valley caused by underdominant and compensatory mutations, selfing reduces the depth and/or breadth of the valley, and thus overall facilitates the fixation of incompatibilities. When speciation does not require populations to pass through a fitness valley, as for Bateson-Dobzhanzky-Muller incompatibilities (BDMi), the lower effective population size and higher genetic linkage in selfing populations both facilitate the fixation of incompatibilities. Interestingly, and contrary to intuitive expectations, local adaptation does not always accelerate the fixation of incompatibilities in outcrossing relative to selfing populations. Our work helps to clarify how incompatibilities accumulate in selfing vs . outcrossing lineages, and has repercussions on the pace of speciation as well as on the genetic architecture of reproductive isolation.
... The formation of a stably reproducing population from newly originated rare polyploids can be promoted by a transition to self-fertilization . While a transition to selfing in diploids often leads to inbreeding depression when deleterious recessive mutations are exposed in homozygotes, in polyploids the negative impacts of selfing may be alleviated by additional allelic copies that mask recessive mutations and maintain high fitness (Lande and Schemske 1985;Comai 2005;Rosche et al. 2017). ...
Self-incompatibility systems based on self-recognition evolved in hermaphroditic plants to maintain genetic variation of offspring and mitigate inbreeding depression. Despite these benefits in diploid plants, for polyploids who often face a scarcity of mating partners, self-incompatibility can thwart reproduction. In contrast, self- compatibility provides an immediate advantage: a route to reproductive viability. Thus, diploid selfing lineages may facilitate the formation of new allopolyploid species. Here, we describe the mechanism of establishment of at least four allopolyploid species in Brassicaceae ( Arabidopsis suecica , Arabidopsis kamchatica, Capsella bursa-pastoris, and Brassica napus ), in a manner dependent on the prior loss of the self-incompatibility mechanism in one of the ancestors. In each case, the degraded S -locus from one parental lineage was dominant over the functional S -locus of the outcrossing parental lineage. Such dominant loss-of-function mutations promote an immediate transition to selfing in allopolyploids and may facilitate their establishment.
... Because flowering plants often exhibit high intraspecific variation in reproductive systems, they present novel opportunities to examine the role of breeding systems in influencing patterns of genetic diversity and divergence among populations (e.g., Culley & Stokes, 2012;Sun et al., 2002;Toczydlowski & Waller, 2019). For example, many flowering plants have the capacity for both crossand self-fertilization, a condition termed mixed-mating (Goodwillie et al., 2005;Lande & Schemske, 1985). Self-fertilization presents several benefits in the context of mate availability and range expansion (Baker, 1955;Busch & Delph, 2012). ...
Both intrinsic and extrinsic forces work together to shape connectivity and genetic variation in populations across the landscape. Here we explored how geography, breeding system traits, and environmental factors influence the population genetic patterns of Triodanis perfoliata, a widespread mix-mating annual plant in the contiguous US. By integrating population genomic data with spatial analyses and modeling the relationship between a breeding system and genetic diversity, we illustrate the complex ways in which these forces shape genetic variation. Specifically, we used 4705 single nucleotide polymorphisms to assess genetic diversity, structure, and evolutionary history among 18 populations. Populations with more obligately selfing flowers harbored less genetic diversity (π: R 2 = .63, p = .01, n = 9 populations), and we found significant population structuring (F ST = 0.48). Both geographic isolation and environmental factors played significant roles in predicting the observed genetic diversity: we found that corridors of suitable environments appear to facilitate gene flow between populations, and that environmental resistance is correlated with increased genetic distance between populations. Last, we integrated our genetic results with species distribution modeling to assess likely patterns of connectivity among our study populations. Our landscape and evolutionary genetic results suggest that T. perfoliata experienced a complex demographic and evolutionary history, particularly in the center of its distribution. As such, there is no singular mechanism driving this species' evolution. Together, our analyses support the hypothesis that the breeding system, geography, and environmental variables shape the patterns of diversity and connectivity of T. perfoliata in the US.
... In the extreme case of immediate and complete pollinator loss, an obligately outcrossing population will go extinct unless it adapts or colonizes a new environment with pollinators (Gomulkiewicz and Holt 1995;Thomann et al. 2013;Rodger et al. 2021). Given that the pollination symbiosis can be disrupted in many ways, it is not surprising that plants frequently evolve the capacity to self-fertilize, or mate with themselves (Stebbins 1957;Lande and Schemske 1985). Although transitions from outcrossing to selfing are among the most com-monly observed in the flowering plants (Barrett 2002), high selfing rates appear to negatively influence the diversification process (Goldberg et al. 2010); however, the ultimate causes of this macroevolutionary pattern are not well understood (Igic and Busch 2013;Wright et al. 2013;Hartfield et al. 2017). ...
Although selfing populations harbor little genetic variation limiting evolutionary potential, the causes are unclear. We experimentally evolved large, replicate populations of Mimulus guttatus for nine generations in greenhouses with or without pollinating bees and studied DNA polymorphism in descendants. Populations without bees adapted to produce more selfed seed yet exhibited striking reductions in DNA polymorphism despite large population sizes. Importantly, the genome‐wide pattern of variation cannot be explained by a simple reduction in effective population size, but instead reflects the complicated interaction between selection, linkage, and inbreeding. Simulations demonstrate that the spread of favored alleles at few loci depresses neutral variation genome wide in large populations containing fully selfing lineages. It also generates greater heterogeneity among chromosomes than expected with neutral evolution in small populations. Genome‐wide deviations from neutrality were documented in populations with bees, suggesting widespread influences of background selection. After applying outlier tests to detect loci under selection, two genome regions were found in populations with bees, yet no adaptive loci were otherwise mapped. Large amounts of stochastic change in selfing populations compromise evolutionary potential and undermine outlier tests for selection. This occurs because genetic draft in highly selfing populations makes even the largest changes in allele frequency unremarkable.
... Accordingly, a shift from selfing to outcrossing is difficult in flowering plants [40] despite the counteracting disadvantages resulting from inbreeding depression and pollen (ovule) discounting. Thus, selfing is generally considered to be an evolutionary 'dead end' or 'blind alley' [41,42]. ...
The transition from outcrossing to selfing is a common evolutionary trend in flowering plants, and floral traits change significantly with the evolution of selfing. Whether or not plant traits are subjected to selection remains an open question in species with mixed mating systems. We examined phenotypic selection in two populations of Halenia elliptica with different selfing rates. We found that the pollen–ovule ratio, seed size, plant height, spur length, and pollinator visitation rate in the population with the higher selfing rate were lower than those in the population with the lower selfing rate. Selfing provides reproductive assurance for populations when pollinator service is low, and the floral traits that are associated with selfing syndrome are evident in populations with a higher selfing rate but are subjected to weak selection in each of the two populations with different selfing rates. Directional selection for an early flowering time indicated that late blooming flowers could experience a risk of seed development in alpine environments, and for large plants, selection indicated that seed production could be limited by the available resources. The floral traits that are associated with pollinator attraction and specialization could be subjected to weak selection at the plant level as selfing evolves, and the selective pressures that are independent of pollinators might not change significantly; highlighting the selective biotic and abiotic pressures that shape the morphological traits of plant species and their independence from the mating system.
... However, inbreeding depression is caused by deleterious mutations and will often change with the selfing rate. Previous models and empirical evidence have shown that a higher selfing rate will lower the inbreeding depression at equilibrium (Lande and Schemske 1985;Roze 2015). Moreover, selection against deleterious mutations may inhibit fixation of a linked beneficial mutation, known as background selection (Charlesworth et al. 1993;Charlesworth 2012), which is more severe in selfing populations due to a reduced effective recombination rate. ...
Evolution of selfing is common in plant populations, but the genetic basis of selfing rate evolution remains unclear. Although the effects of genetic properties on fixation for mating‐unrelated alleles have been investigated, loci that modify the selfing rate (selfing modifiers) differ from mating‐unrelated loci in several aspects. Using population genetic models, I investigate the genetic basis of selfing rate evolution. For mating‐unrelated alleles, selfing promotes fixation only for recessive mutations, but for selfing modifiers, since the selection coefficient depends on the background selfing rate, selfing can promote fixation even for dominant modifiers. For mating‐unrelated alleles, the fixation probability from standing variation is independent of dominance and decreases with an increased background selfing rate. However, for selfing modifiers, the fixation probability peaks at an intermediate selfing rate and when alleles are recessive, because a change of its selection coefficient necessarily involves a change of the inbreeding coefficient, since both depend on the level of inbreeding depression. Furthermore, evolution of selfing involving multiple modifier loci is more likely when selfing is controlled by few large‐effect rather than many slight‐effect modifiers. I discuss how these characteristics of selfing modifiers have implications for the unidirectional transition from outcrossing to selfing and other empirical patterns. This article is protected by copyright. All rights reserved
How do biological networks evolve and expand? We study these questions in the context of the plant collaborative-non-self recognition self-incompatibility system. Self-incompatibility evolved to avoid self-fertilization among hermaphroditic plants. It relies on specific molecular recognition between highly diverse proteins of two families: female and male determinants, such that the combination of genes an individual possesses determines its mating partners. Though highly polymorphic, previous models struggled to pinpoint the evolutionary trajectories by which new specificities evolved. Here, we construct a novel theoretical framework, that crucially affords interaction promiscuity and multiple distinct partners per protein, as is seen in empirical findings disregarded by previous models. We demonstrate spontaneous self-organization of the population into distinct “classes” with full between-class compatibility and a dynamic long-term balance between class emergence and decay. Our work highlights the importance of molecular recognition promiscuity to network evolvability. Promiscuity was found in additional systems suggesting that our framework could be more broadly applicable.
Inbreeding depression refers to the reduced performance arising from increased homozygosity, a phenomenon that is the reverse of heterosis and exists among plants and animals. As a natural self-pollinated crop with strong heterosis, the mechanism of inbreeding depression in rice is largely unknown. To understand the genetic basis of inbreeding depression, we constructed a successive inbreeding population from the F2 to F4 generation and observed inbreeding depression of all heterotic traits in the progeny along with the decay of heterozygosity in each generation. The expected depression effect was largely explained by 13 QTLs showing dominant effects for spikelets per panicle, 11 for primary branches, and 12 for secondary branches, and these loci constitute the main correlation between heterosis and inbreeding depression. However, the genetic basis of inbreeding depression is also distinct from that of heterosis, such that a biased transmission ratio of alleles for QTLs with either dominant or additive effects in four segregation distortion regions would result in minor effects in expected depression. Noticeably, two-locus interactions may change the extent and direction of the depression effects of the target loci, and overall interactions would promote inbreeding depression among generations. Using an F2:3 variation population, the actual performance of the loci showing expected depression was evaluated considering the heterozygosity decay in the background after inbreeding. We found inconsistent or various degrees of background depression from the F2 to F3 generation assuming different genotypes of the target locus, which may affect the actual depression effect of the locus due to epistasis. The results suggest that the genetic architecture of inbreeding depression and heterosis is closely linked but also differs in their intrinsic mechanisms, which expand our understanding of the whole-genome architecture of inbreeding depression.
The breeding of Physalis peruviana is incipient in Brazil and is shown to be the most promising alternative for the development of productive genotypes with fruit quality. Therefore, the objective was to evaluate the combining ability between inbred lines of P. peruviana, thus indicating the selection of hybrids with fruit quality. Therefore, four populations from different origins were selfed for three generations and crossed in controlled hybridizations, resulting in 28 P. peruviana populations. The hybrid in relation to the parent performance, based on the effects of general and specific combining ability, was compared in a full diallel mating design (Griffing Method 1). In the analysis of variance, the factor genotype was partitioned into the following causes of variation: i) parents and F1 hybrids, ii) selfed generations and iii) Genotype × environment (GE) interaction. There were significant differences between Parents and F1 hybrids for the trait fruit polar diameter. Still, the interaction between specific combining ability x environment and, reciprocal effect x environment, was significant. However, for the Xanxerê environment, there was a reduction of approximately 3.0 mm in the polar diameter of the fruit in the hybrid Colombia x Peru and a reduction of 4.5 mm for the reciprocal (Peru x Colombia). In the comparison of the selfed generations S0 with S1, the fruit weight of the Lages population decreased by 0.380 g. There was also a reduction of 974.5 kg.ha-1 in the fruit yield of the Peruvian population. Thus, the performance of the P. peruviana populations in hybrid combinations is unpromising, indicating the existence of only one P. peruviana gene pool, with a restricted genetic basis.
A wide diversity of mating systems occur in nature, with frequent evolutionary transitions in mating-compatibility mechanisms. Basidiomycete fungi typically have two mating-type loci controlling mating compatibility, HD and PR, usually residing on different chromosomes. In Microbotryum anther-smut fungi, there have been repeated events of linkage between the two mating-type loci through chromosome fusions, leading to large non-recombining regions. By generating high-quality genome assemblies, we found that two sister Microbotryum species parasitizing Dianthus plants, M. superbum and M. shykoffianum, as well as the distantly related M. scorzonarae, have their HD and PR mating-type loci on different chromosomes, but with the PR mating-type chromosome fused with a part of the ancestral HD chromosome. Furthermore,progressive extensions of recombination suppression have generated evolutionary strata. In all three species, rearrangements suggest the existence of a transient stage of HD-PR linkage by whole chromosome fusion, and, unexpectedly, the HD genes lost their function. In M. superbum, multiple natural diploid strains were homozygous, and the disrupted HD2 alleles was hardly expressed. Mating tests confirmed that a single genetic factor controlled mating compatibility (i.e. PR) and that haploid strains with identical HD alleles could mate and produce infectious hyphae. The HD genes have therefore lost their function in the control of mating compatibility in these Microbotryum species. While the loss of function of PR genes in mating compatibility has been reported in a few basidiomycete fungi, these are the first documented cases for the loss of mating-type determination by HD genes in heterothallic fungi. The control of mating compatibility by a single genetic factor is beneficial under selfing and can thus be achieved repeatedly, through evolutionary convergence in distant lineages, involving different genomic or similar pathways.
Despite the potential for mechanical, developmental and/or chemical mechanisms to prevent self-fertilization, incidental self-fertilization is inevitable in many predominantly outcrossing species. In such cases, inbreeding can compromise individual fitness. Unquestionably, much of this inbreeding depression is maladaptive. However, we show that when reproductive compensation allows for the replacement of inviable embryos lost early in development, selection can favour deleterious recessive variants that induce ‘self-sacrificial’ death of inbred embryos. Our theoretical results provide numerous testable predictions which could challenge the assumption that inbreeding depression is always maladaptive. Our work is applicable any species that cannot fully avoid inbreeding, exhibits substantial inbreeding depression, and has the potential to compensate embryos lost early in development. In addition to its general applicability, our theory suggests that self-sacrificial variants might be responsible for the remarkably low realized selfing rates of gymnosperms with high primary selfing rates, as gymnosperms exhibit strong inbreeding depression, have effective reproductive compensation mechanisms, and cannot evolve chemical self-incompatibility.
Competition among pollen or sperm (gametic selection) can cause evolution. Mating systems shape the intensity of gametic selection by determining the competitors involved, which can in turn cause the mating system itself to evolve. We model the bidirectional relationship between gametic selection and mating systems, focusing on variation in female mating frequency (monandry-polyandry) and self-fertilisation (selfing-outcrossing). First, we find that monandry and selfing both reduce the efficiency of gametic selection in removing deleterious alleles. This means that selfing can increase mutation load, in contrast to cases without gametic selection where selfing purges deleterious mutations and decreases mutation load. Second, we explore how mating systems evolve via their effect on gametic selection. By manipulating gametic selection, polyandry can evolve to increase the fitness of the offspring produced. However, this indirect advantage of post-copulatory sexual selection is weak and is likely to be overwhelmed by any direct fitness effects of mating systems. Nevertheless, gametic selection can be potentially decisive for selfing evolution because it significantly reduces inbreeding depression, which favours selfing. Thus, the presence of gametic selection could be a key factor driving selfing evolution.
Plants exhibit diverse breeding systems, with populations capable of outcrossing, selfing, and/or asexual reproduction. However, interactions between the three reproductive pathways remain not fully clear. Sexual reproduction introduces segregation and recombination, but incurs several costs. Selfing can affect the relative costs and benefits of sexual vs. asexual reproduction. Building population genetic models, I explore how selfing affects the evolution of a sexual reproduction rate modifier via (1) indirect selection due to segregation, (2) indirect selection from changes in recombination rates, and (3) selection from the cost of meiosis and mate limitation. The dominant selective force mediating the evolution of sex is found to vary with the rate of sexual reproduction and selfing, but selective force (1) and (3) are generally stronger than selective force (2). A modifier enhancing sexual reproduction tends to be favored by indirect selection generated by partially recessive, small-effect deleterious mutations, while hindered by highly recessive lethal mutations. Overall, evolution towards higher sexual reproduction is hindered at low sexual reproduction rates and intermediate selfing rates, but favored under high selfing rates. The results suggest that asexual reproduction may precede the evolution of selfing, and offer insights into the evolution of mechanisms reducing geitonogamy in partially clonal populations.
The evolution of mating systems in plants is central for understanding the rise of their diversity on Earth. The transition towards self-fertilization is a well-known example of convergent evolution although the opposite direction is expected to be forbidden according to evolutionary theories. We suggest that the ploidy level could promote changes in the reproductive strategies through its effect on traits related to pollination.
We performed controlled crosses on several populations from the polyploid Erysimum incanum species complex, described as predominantly selfing, to evaluate the inbreeding depression. Additionally, we measured mating traits such as floral size, herkogamy, anther exertion, the relative investment in male and female components (P:O ratio) and genetic diversity.
We described three ploidy levels in the complex – hexaploids were unknown until now. We found significant differences in the self-pollination success among ploidies and even among populations within the same ploidy. Inbreeding depression was present in higher ploidies, accompanied by bigger flowers with higher anther exposure, increased herkogamy and P:O and genetic diversity.
These findings suggest that ploidy could be promoting alternative reproductive strategies to selfing, driving mating system diversification within a selfing species, which has not been previously described in the wild.
Reproductive biology is a very important and essential component for species diversity, and evolution from simpler to complex forms. The objective of this study is to explore the research landscape on plant reproductive biology (PRB) as published in the Scopus database from 1972 to 2022 (50 years). The bibliometric and knowledge map analyses were used to analyze the plant reproductive biology, current trends, hot topics, maps of co-citations, maps of co-occurrence, top ten countries with total published documents, total citations, average citations per document, and top ten journals with number of citations in the Scopus data base from 1972 to 2022. Total 1112 publications were published during the past 50 years. Our analysis indicates that conservation, genetics, evolution, pollination, and biodiversity are the critical topics related to plant reproductive biology. The findings showed that the USA, China, U.K., and Brazil were the most productive countries in terms of plant reproductive biology research publication. The level of collaboration between the countries was significantly high for this research topic. This research is an early effort to understand the development and evolution of plant reproductive biology in the last 50 years. The citation footprint and authorship networks which have been established during this study, will help in promoting research capacity, trend of research in this field, and contribute to improve research culture and awareness in this important area of conservation biology.
Premise:
What maintains mixed mating is an evolutionary enigma. Cleistogamy, the production of both potentially outcrossing chasmogamous, and obligately selfing cleistogamous flowers on the same individual plant, is an excellent system to study the costs of selfing. Inbreeding depression can prevent the evolution of greater selfing within populations, and heterosis in crosses between populations may further tip the balance in favor of outcrossing. Few empirical estimates of inbreeding depression and heterosis in the same system exist for cleistogamous species.
Methods:
We investigate the potential costs of selfing by quantifying inbreeding depression and heterosis in three populations of the cleistogamous perennial Ruellia humilis Nutt (Acanthaceae). We performed hand-pollinations to self, and outcross within and between populations, and measured seed number, germination, total flower production, and estimated cumulative fitness for the resulting progeny in a greenhouse experiment.
Key results:
We found moderate inbreeding depression for cumulative fitness (<30%) in two populations, but outbreeding depression for crosses within a third population (-26%). For between population crosses, there was weak to modest heterosis (11-47%) in two of the population combinations, but modest to strong outbreeding depression (-21 to -71%) in the other four combinations.
Conclusions:
Neither inbreeding depression nor heterosis was of sufficient magnitude to explain the continued production of CH flowers given the relative energetic advantage of CL flowers previously estimated for these populations. Outbreeding depression either within or between populations makes the maintenance of chasmogamous flowers even harder to explain. More information is needed on the genetic basis of cleistogamy in order to resolve this conundrum. This article is protected by copyright. All rights reserved.
Opisthopappus is a perennial, endemic herb of the Taihang Mountains in China. Two species of this genus (O. longilobus and O. taihangensis) are important wild genetic resources for Asteraceae; however, their reproductive biology has been lacking until now. This study is the first detailed report on the reproductive biology and breeding systems of two Opisthopappus species. Through field observations, the floral syndromes of O. longilobus and O. taihangensis were found to possess a similar pattern, although O. taihangensis has a relatively larger capitulum, more ray ligules, and disc florets. The flowers of both O. longilobus and O. taihangensis are protandrous, a character that can prevent autogamy at the single-flower level, and insects are required for pollination. Further, brightly ligules, brightly bisexual florets, unique fragrance, and amount of nectar suggest that these species propagate via an entomophilous pollination system. Hymenopteran and Diptera species were observed as the effective pollinators for these two species. The outcrossing index, pollen/ovule ratio and the results of hand pollination indicated that these Opisthopappus species might have a mixed mating system that combines cross-fertilization and partial self-fertilization for O. longilobus and O. taihangensis, outcrossing predominated in the breeding system, while self-pollination played an important role in seed production when insect pollination was unavailable, particularly in a harsh environment, such as the Taihang Mountains cliffs. Meanwhile, O. taihangensis might better adapt to severe surroundings with relatively complex floral syndromes, specifically through the attraction of visiting insects and a high seed set rate. The above results not only provide reference information toward a better understanding of the survival strategies of O. longilobus and O. taihangensis in the Taihang Mountains but also lay a solid foundation for further exploring the molecular mechanisms that underly their adaptation under cliff environments.
In haploid species, sexual reproduction by selfing lacks the common benefits from recombination and is indistinguishable from asexual reproduction at the genetic level. Nevertheless, the evolution of self-compatibility, known as homothallism in organisms with mating types, has occurred hundreds of times in fungi. Two main hypotheses have been proposed for the evolution of homothallism. First, that homothallism offers reproductive assurance, which is especially important when species have an obligatory sexual phase in their lifecycle. Second, that homothallism is associated with population level compatibility, increasing the chance of outbreeding. Here, we test these hypotheses using the fission yeast Schizosaccharomyces pombe, which is homothallic by mating-type switching, leveraging natural variation for switching efficiency in this species. Combining empirical tests with cellular automaton simulations, we show that homothallism by switching increases mating success of switching genotypes, but does not affect population level compatibility. Experiments show that outcrossing is actually reduced under homothallism. Our simulations explain these findings, because due to local mating, gametes that mated through intra-clonal selfing are no longer available for outcrossing. Our results suggest that the recurrent evolution of haploid self-compatibility is likely driven by selection for mating assurance, not to increase the potential for outcrossing.
Inbreeding depression occurs when individuals who are closely related mate and produce offspring with reduced fitness. Although inbreeding depression is a genetic phenomenon, the magnitude of inbreeding depression can be influenced by environmental conditions and parental effects. In this study, we tested whether size-based parental effects influence the magnitude of inbreeding depression in an insect with elaborate and obligate parental care (the burying beetle, Nicrophorus orbicollis). We found that larger parents produced larger offspring. However, larval mass was also influenced by the interaction between parental body size and larval inbreeding status: when parents were small, inbred larvae were smaller than outbred larvae, but when parents were large this pattern was reversed. In contrast, survival from larval dispersal to adult emergence showed inbreeding depression that was unaffected by parental body size. Our results suggest that size-based parental effects can generate variation in the magnitude of inbreeding depression. Further work is needed to dissect the mechanisms through which this might occur and to better understand why parental size influences inbreeding depression in some traits but not others.
Abstract
We tested whether parental body size influenced the magnitude of inbreeding depression in an insect with obligate parental care (Nicrophorus orbicollis). We found that when parents were small, inbred larvae were smaller than outbred larvae. This pattern was reversed with parents who were large. In contrast, survival to eclosion displayed inbreeding depression that was insensitive to parental size.
Inbreeding exposes deleterious recessive alleles in homozygotes, lowering fitness and generating inbreeding depression (ID). Both purging (via selection) and fixation (via drift) should reduce segregating deleterious mutations and ID in more inbred populations. These theoretical predictions are not well-tested in wild populations, which is concerning given purging/fixation have opposite fitness outcomes. We examined how individual- and population-level inbreeding and genomic heterozygosity affected maternal and progeny fitness within and among 12 wild populations of Impatiens capensis. We quantified maternal fitness in home sites, maternal multilocus heterozygosity (using 12,560 SNPs), and lifetime fitness of selfed and predominantly outcrossed progeny in a common garden. These populations spanned a broad range of individual- (fi = -0.17-0.98) and population-level inbreeding (FIS = 0.25-0.87). More inbred populations contained fewer polymorphic loci, less fecund mothers, and smaller progeny, suggesting higher fixed loads. However, despite appreciable ID (mean: 8.8 lethal equivalents per gamete), ID did not systematically decline in more inbred population. More heterozygous mothers were more fecund and produced fitter progeny in outcrossed populations, but this pattern unexpectedly reversed in highly inbred populations. These observations suggest that persistent overdominance or some other force acts to forestall purging and fixation in these populations.
Increased rates of self-fertilization are often found in plant colonies, but the factors driving the observed higher selfing rates remain unclear. Specifically, the higher selfing rates in colonist populations may be due to 1) source populations with a higher selfing rate being more likely to successfully establish colonies (a filter effect), 2) the in situ evolution of selfing rate or a plastic selfing rate increase rescuing the colony from extinction, 3) selfing rate evolution post establishment. Using individual-based simulations and eco-evo models, we show that under both single and multiple dispersal, colony establishment may often be driven by a filter effect, due to a higher initial selfing rate and lower genetic load, which are correlated since selfing can purge deleterious mutations. Moreover, the role of the filter effect is weaker under multiple dispersal than single dispersal. The evolution of a higher selfing rate is unlikely to contribute directly to colony establishment. Although selfing rate evolution occurs during the colonization process, most of the selfing rate evolution may occur post establishment. Plasticity in selfing rates is more effective in facilitating colony establishment than the evolution of selfing.
Macroevolutionary studies have estimated higher extinction rates of self-compatible lineages than self-incompatible ones. A leading explanation is that selfing may prevent adaptation, since models show that selfing can inhibit the fixation of adaptive alleles at a single locus (1-step adaptation). However, adaptation often involves changes at multiple loci (multi-step adaption), but the effects of selfing remain unclear because selfing increases homozygosity, which affects selection intensity, the effective population size, and the effective recombination rate. By modeling using population genetic models, I investigate the effects of selfing on adaption requiring fixation of 2 adaptive alleles, I show that intermediate selfing rates generally promote adaption, by increasing the fixation probability of the double-mutant haplotype once it is generated. In constant-sized populations, selfing increases the rate of adaptation through the fixation of new mutations even when both alleles are dominant. In demographically declining populations, the rescue probability rises sharply as the selfing rate increases from zero, but quickly drops to be low when it approaches 1.0. These findings are at odds with the hypothesis that higher extinction rates of self-compatible lineages result from reduced adaptive potential but may help explain why some studies have failed to detect relaxation of selection in selfers and also the prevalence of mixed-mating systems.
Introduced species often benefit from escaping their enemies when they are transported to a new range, an idea commonly expressed as the enemy release hypothesis. However, species might shed mutualists as well as enemies when they colonize a new range. Loss of mutualists might reduce the success of introduced populations, or even cause failure to establish. We provide the first quantitative synthesis testing this natural but often overlooked parallel of the enemy release hypothesis, which is known as the missed mutualist hypothesis. Meta-analysis showed that plants interact with 1.9 times more mutualist species, and have 2.3 times more interactions with mutualists per unit time in their native range than in their introduced range. Species may mitigate the negative effects of missed mutualists. For instance, selection arising from missed mutualists could cause introduced species to evolve either to facilitate interactions with a new suite of species or to exist without mutualisms. Just as enemy release can allow introduced populations to redirect energy from defence to growth, potentially evolving increased competitive ability, species that shift to strategies without mutualists may be able to reallocate energy from mutualism toward increased competitive ability or seed production. The missed mutualist hypothesis advances understanding of the selective forces and filters that act on plant species in the early stages of introduction and establishment and thus could inform the management of introduced species.
Heterostyly, a plant sexual polymorphism controlled by the S‐locus supergene, has evolved numerous times among angiosperm lineages and represents a classic example of convergent evolution in form and function. Determining whether underlying molecular convergence occurs could provide insights on constraints to floral evolution. Here, we investigated S‐locus genes in distylous Gelsemium (Gelsemiaceae) to determine whether there is evidence of molecular convergence with unrelated distylous species.
We used several approaches, including anatomical measurements of sex‐organ development and transcriptome and whole‐genome sequencing, to identify components of the S‐locus supergene. We also performed evolutionary analysis with candidate S‐locus genes and compared them with those reported in Primula and Turnera.
The candidate S‐locus supergene of Gelsemium contained four genes, of which three appear to have originated from gene duplication events within Gelsemiaceae. The style‐length genes GeCYP in Gelsemium and CYP734A50 in Primula likely arose from duplication of the same gene, CYP734A1. Three out of four S‐locus genes in Gelsemium elegans were hemizygous, as previously reported in Primula and Turnera.
We provide genomic evidence on the genetic convergence of the supergene underlying distyly among distantly related angiosperm lineages and help to illuminate the genetic architecture involved in the evolution of heterostyly.
There have been many studies of morphological and genetic variation in island plant radiations, but few have shown how the mating system has shaped the patterns of variation. In this study, outcrossing rates and paternity in eight populations of the Madeiran endemic Tolpis macrorhiza were estimated using genome-wide RADseq genotyping. The species is believed to have evolved early in the geological history of the island, and we here examine mating system evolution during colonization and establishment of populations across Madeira. The mating system is highly outcrossing in seven populations and mixed mating in one. Some maternal plants in highly outcrossing populations were inbred, suggesting that mating system varies temporally as well as spatially. This mating system may provide flexibility for establishment of new populations in the dynamic landscapes of oceanic islands while maintaining genetic diversity within populations. Multiple paternity is prevalent in populations, indicating that compatible mates are not limited to a few sires. Our analyses of T. macrorhiza were enabled by several methodological advances included in the v.3 release of the BORICE estimation program. These include SNP filtering programs to generate valid likelihoods and post-processing scripts to partition mating system variation among populations and among maternal plants within populations.
Theoretical models were developed to propose a new mechanism enhancing mixed mating (reproduction by both outcrossing and selfing) in hermaphroditic plants; mixed mating can be maintained if there exists among-parent variation in early-acting inbreeding depression in embryos and parents can replace dead embryos by overproduction of ovules. In the two main models developed, the number of embryos produced is allowed to evolve, parents may overproduce embryos, and among-parent variation in early-acting inbreeding depression does not exist or exists. I found that mixed mating does not evolve if among-parent variation in early-acting inbreeding depression does not exist, whereas it evolves if it exists. If the degree of early-acting inbreeding depression in embryos is variable among parents, parents with the same selfing strategy suffer different effects of early-acting inbreeding depression. Specifically, overproduction of embryos may be insufficient when inbreeding depression is severe but wasteful when it is weak. Hence, it is advantageous to produce a moderate number of embryos to reduce waste of resources. Mixed mating is then advantageous to avoid great reductions in seed number caused by massive loss of selfed embryos in cases of severe inbreeding depression.
Self-fertilisation is widespread among hermaphroditic species across the tree of life. Selfing has many consequences on the genetic diversity and the evolutionary dynamics of populations, which may in turn affect macroevolutionary processes such as speciation. On the one hand, because selfing increases genetic drift and reduces migration rate among populations, selfing may be expected to promote speciation. On the other hand, because selfing reduces the efficacy of selection, selfing may be expected to hamper ecological speciation. To better understand under which conditions and in which direction selfing affects the build-up of reproductive isolation, an explicit population genetics model is required. Here, we focus on the interplay between genetic drift, selection and genetic linkage by studying speciation without gene flow. We test how fast populations with different rates of selfing accumulate mutations leading to genetic incompatibilities. When speciation requires the population to pass through a fitness valley caused by underdominant and compensatory mutations, selfing reduces the depth and/or breadth of the valley, and thus overall facilitates the fixation of incompatibilities. When speciation does not require the population to pass through a fitness valley, as for Bateson-Dobzhanzky-Muller incompatibilities (BDMi), the lower effective population size and higher genetic linkage in selfing populations facilitates the fixation of incompatibilities. Interestingly, and contrary to intuitive expectations, local selection does not always accelerate the build-up of reproductive isolation in outcrossing relative to selfing populations. Our work helps to clarify how selfing lineages may speciate and diversify over time, and emphasizes the need to account for interactions among segregating mutations within populations to better understand macroevolutionary dynamics.
Author summary
Hermaphroditic organisms may use their male gametes to fertilise their own female gametes, and species vary greatly in how much they self-fertilise. Self-fertilisation induces many genetic modifications in the population, which may ultimately affect the rates at which lineages diversify. Here we aim to build predictions on how self-fertilisation affects the rate at which reproductive isolation arises between geographically isolated populations. Specifically, we develop theoretical models in which populations varying in their rates of self-fertilisation may fixate mutations leading to reproductive isolation. We first explored scenarios in which reproductive isolation is made by mutations whose fixations necessitate the population to experience temporally deleterious effects (i.e., a fitness valley), and found that self-fertilisation reduces the breadth and depth of the fitness valley and thereby overall facilitates the accumulation of such mutations. Second, we explored scenarios in which genetic incompatibilities are caused by interactions between derived alleles of different genes (i.e., BDMi). By allowing the BDMi to occur within populations, we found that self-fertilisation reduces the manifestation of BDMi within population, and thereby facilitates their fixation. This effect prevails even in the face of local adaptation. Thus, our study clarifies how fast species are expected to arise in self-fertilisation lineages.
Background: Argemone ochroleuca is a worldwide invasive weed but is also highly valuable for their chemical compounds. Knowledge about its reproduction will help create plans for its control or its propagation.
Questions: Does A. ochroleuca has an incompatibility system like other Papaveraceae species? Which are the reproductive strategies that favor the seed formation in A. ochroleuca?
Studied species: A. ochroleuca is an annual species with bisexual flowers.
Study site and dates: Mexico City, Mexico. The fieldwork was performed from February to May in 2013, 2014, and 2017.
Methods: Direct observations were made to describe the flower cycle of A. ochroleuca. We used self-pollinated flowers to analyze if this species is self-incompatible by following the pollen tube growth through gynoecium. Controlled pollinations were made to quantify and compare the number of seeds produced per treatment to know the mating system and explore if the species presents a mechanism of reproductive assurance through autogamy, or exhibits inbreeding depression.
Results: A. ochroleuca is self-compatible and exhibits a mixed mating system. Although outcrossing is how more seeds are produced, both autogamy and pseudocleistogamy are present as reproductive assurance mechanisms. Naturally pollinated flowers produce the maximum number of seeds, but inbreeding depression is present in the population. Thus, the number of seeds will be affected by continuous selfing.
Conclusions: This study highlights the mixed mating system and reproductive assurance mechanisms as successful strategies for A. ochroleuca, a common pattern in invasive weeds.
Premise:
To avoid inbreeding depression, plants have evolved diverse breeding systems to favor outcrossing, such as self-incompatibility. However, changes in biotic and abiotic conditions can result in selective pressures that lead to a breakdown in self-incompatibility. The shift to increased selfing is commonly associated with reduced floral features, lower attractiveness to pollinators, and increased inbreeding. We tested the hypothesis that the loss of self-incompatibility, a shift to self-fertilization (autogamy), and concomitant evolution of the selfing syndrome (reduction in floral traits associated with cross-fertilization) will lead to increased inbreeding and population differentiation in Oenothera primiveris. Across its range, this species exhibits a shift in its breeding system and floral traits from a self-incompatible population with large flowers to self-compatible populations with smaller flowers.
Methods:
We conducted a breeding system assessment, evaluated floral traits in the field and under controlled conditions, and measured population genetic parameters using RADseq data.
Results:
Our results reveal a bimodal transition to the selfing syndrome from the west to the east of the range of O. primiveris. This shift includes variation in the breeding system and the mating system, a reduction in floral traits (flower diameter, herkogamy, and scent production), a shift to greater autogamy, reduced genetic diversity, and increased inbreeding.
Conclusions:
The observed variation highlights the importance of range-wide studies to understand breeding system variation and the evolution of the selfing syndrome within populations and species.
Cleistogamy is a mode of reproduction which promotes self-pollination as the flower remains closed even after anthesis. This system avoids contamination of foreign pollen to outcross the clesitogamous flower. In nature, under suboptimal environmental condition, few plant species produce cleistogamous flower which requires fewer resources to reproduction. Three different types of cleistogamy occur in plants namely dimorphic cleistogamy, induced cleistogamy, and complete cleistogamy. This kind of sexual reproduction maintains the locally adopted gene complex and homogeneity of the genes in the population. This system of reproduction helps in achieving the genetic purity of any species. This system can be transferred to other species to exploit the cleistogamous nature of reproduction.
There is an ongoing societal debate about plant breeding systems and their impact on stakeholders in food systems. Hybrid breeding and hybrid seed have become controversial topics as they are believed to mostly serve high-tech agricultural systems. This article focuses on the perspective of commercial plant breeders when developing new cultivars of food crops. Arguably, hybrid breeding is the most effective breeding system for genetic improvement of crops, enhancing yields, improving product quality and increasing resistance against (a)biotic stresses. Nonetheless, hybrid breeding is not commercially applied in all crops. We analyse how biological and economic factors determine whether a commercial plant breeder opts for the hybrid system or not. We show that the commercial feasibility of hybrid breeding depends on the crop and business case. In conclusion, the commercial application of hybrid breeding in crops seems to be hampered mostly by high costs of seed production. Case studies regarding the hybrid transitions in maize, wheat and potato are included to illustrate these findings. This Perspective analyses how biological and economic factors determine whether a commercial plant breeder will opt for a hybrid breeding system, and finds that the cost of seed production is a key factor.
In view of the ongoing rarity of Ecbolium ligustrinum there is an urgent need for conservation of the species. For this, a detailed work was carried out regarding the untold story of its reproductive ecology. The work was done for three consecutive years (2015–2017) at Midnapore, West Bengal over three different populations collected from three different areas of West Bengal. Field data were also recorded from these three wild populations. The species produces gullet flowers with bi-labiate corolla having long slender tubes. The flowers exhibit one day of longevity. The flowers are visited by 10 species of insects. Among those, four species viz. Eristalis tenax , a Dipteran member and three ant species of Hymenoptera such as Camponotus sp., Formica sp. and Monomorium sp. are the effective pollinators. As per pollination efficiency, Eristalis tenax (PE i = 0.76) is the most successful one. The flowers are shortly protandrous (dichogamous) and passed by three distinct reproductive (male, bisexual and female) phases. The breeding system clearly depicts that the species is facultatively xenogamous supported by myophilous mode of pollination. However, geitonogamous type of pollination is also observed through myrmecophily, an atypical instance found in plants. Lastly, the plant retained some sort of autogamy through ‘fail-safe’ mechanism of pollination, an adaptation which might be developed in absence of pollinators. Therefore, undoubtedly it can be concluded that E. ligustrinum is a partially self-incompatible (ISI = 0.27) species having a mixed mating system, adapted for xenogamy through specialised mode of plant-pollinator interactions.
The coexistence of different mating strategies, whereby a species can reproduce both by selfing and outcrossing, is an evolutionary enigma. Theory predicts two predominant stable mating states: outcrossing with strong inbreeding depression or selfing with weak inbreeding depression. As these two mating strategies are subject to opposing selective forces, mixed breeding systems are thought to be a rare transitory state yet can persist even after multiple speciation events. We hypothesise that if each mating strategy plays a distinctive role during some part of the species life history, opposing selective pressures could be balanced, permitting the stable co-existence of selfing and outcrossing sexual morphs. In this scenario, we would expect each morph to be specialised in their respective roles. Here we show, using behavioural, physiological and gene expression studies, that the selfing (hermaphrodite) and outcrossing (female) sexual morphs of the trioecious nematode Auanema freiburgensis have distinct adaptations optimised for their different roles during the life cycle. A. freiburgensis hermaphrodites are known to be produced under stressful conditions and are specialised for dispersal to new habitat patches. Here we show that they exhibit metabolic and intestinal changes enabling them to meet the cost of dispersal and reproduction. In contrast, A. freiburgensis females are produced in favourable conditions and facilitate rapid population growth. We found that females compensate for the lack of reproductive assurance by reallocating resources from intestinal development to mate-finding behaviour. The specialisation of each mating system for its role in the life cycle could balance opposing selective forces allowing the stable maintenance of both mating systems in A. freiburgensis.
Multivariate statistical methods are derived for measuring selection solely from observed changes in the distribution of phenotypic characters in a population within a generation. Selective effects are readily detectable in characters that do not change with age, such as meristic traits or adult characters in species with determinate growth. Ontogenetic characters, including allometric growth rates, can be analyzed in longitudinal studies where individuals are followed through time. Following an approach pioneered by Pearson (1903), this analysis helps to reveal the target(s) of selection, and to quantify its intensity, without identifying the selective agent(s). By accounting for indirect selection through correlated characters, separate forces of directional and stabilizing (or disruptive) selection acting directly on each character can be measured. These directional and stabilizing selection coefficients are respectively the parameters that describe the best linear and quadratic approximations to the selective surface of individual fitness as a function of the phenotypic characters. The theory is illustrated by estimating selective forces on morphological characters influencing survival in pentatomid bugs and in house sparrows during severe weather conditions.
The potentialities of diploid and tetraploid organisms for conserving variation which is genetical information are compared. While tetraploidy enhances the conservation of variation, it does not in general appear to do so by a factor of two, which might have been expected from the difference in the amount of genetic material.
This chapter discusses the effects of inbreeding in terms of genetic models of steadily increasing complexity. It correlates theoretical effects with observations and measurements that show that inbreeding populations contain large amounts of genetic variability and that this variability is organized into highly integrated and flexible systems. The observed structure of inbreeding populations results from an appropriate integration of inbreeding into the constellation of genetic and ecological factors that are involved in the regulation of variability and maintenance of flexibility. An understanding of the genetic structure of inbreeding species derives from the combining analyses of theoretical models with studies on experimental and natural populations. Inbreeding can arise in populations either as a result of various mechanisms that affect the mating system, or from restrictions in actual or effective population size. The theoretical effects of inbreeding are introduced in terms of single-locus population models in which population size is assumed sufficiently large to avoid sampling effects and in which it is assumed that selective values, mating system parameters, and other population parameters are constant in all environments. The effects on population structure of linkage and epistatic interactions among different polymorphisms are considered in terms of multilocus genetic models involving deviations from a fixed optimum, heterotic models, and mixed optimum-heterotic models.
All species are self-compatible, and require a treefall gap for germination and establishment. Self-pollination resulted in lower seed output in all species; this difference was significant for Costus allenii and C. laevis. Seedling growth of selfed, outcrossed and naturally-pollinated Costus allenii, C. laevis and C. guanaiensis in sun and shade habitats in the greenhouse was unaffected by breeding system, but significantly affected by habitat, with reduced growth in shade. Selfed progeny had the lowest biomass in all treatments, with inbreeding depression for growth ranging from 8-25% compared to out-crossed performance. Reduced growth and greater variation in growth for selfed, as compared to out-crossed, progeny are consistent with the hypothesis that inbreeding depression in these species results from homozygosity of rare, deleterious alleles which are not expressed in the heterozygous state. Relative biomass production varied more between sun and shade habitats for selfed, than outcrossed or naturally-pollinated progeny, suggesting that increased homozygosity following inbreeding reduces genotypic versatility.-from Author
Leptosporangiate ferns have apical meristems based upon tetrahedral apical cells. Computer simulation studies predict that such apical meristems are more likely to accumulate somatic mutations than the more stochastic apical meristems found in seed plants (Klekowski and Fukshansky, 1984a, 1984b). Clones of the ferns O sensibilis and M. struthiopteris were studied for genetic mosaicism for lethal and deleterious mutations expressed in the gametophyte generation. Clones which were genetic chimeras were common in both species. The frequency of such clones was used to calculate the forward mutation rate for gametophytic mutations on a per ramet basis. This mutation rate almost exactly predicted the level of genetic load for sporophytic lethals in O sensibilis. These data indicate that the occurrence of sporophytic lethals in fern populations is not in itself evidence for heterotic selection in these plants.
A sample from a cohort of oysters was analyzed electrophoretically for seven enzyme loci and the resulting information was related to individual weight. The cohort consisted of individuals of one year of age grown under uniform conditions. There is a deficit in the numbers of heterozygotes expected from Hardy-Weinberg ratios. The deficit varies from locus to locus, but locus-specific deficits do not change from cohort to cohort. If the sample is divided in weight-classes, the frequency of the most common allele in the sample decays with increasing weight class. An individual's weight is positively correlated with the number of loci for which it is heterozygous. The variance in weight is lower among individuals of high degree of heterozygosity Several hypotheses were examined in an attempt to account for these observations. Overdominance in growth rate appears to be the most plausible explanation for the correlation between weight and degree of heterozygosity, but it will not account for the deficit in the number of heterozygotes. The latter phenomenon results either from the breeding structure of the population, or from preferential mortality of heterozygotes at an early pre-settlement age. The alternative hypothesis that the allozyme markers are linked to genes recessive for growth rate is less likely in view of the fact that such linkages must exist for alleles at all loci examined.
Demographic data were collected in an experimental population of Gilia achilleifolia (Polemoniaceae) established in the field. The experimental population originated from seeds obtained after 0 (S0), 1 (S1) and 2 (S2) generations of artificial self-pollination of individuals from a nearby and normally outcrossing population. Seedling establishment was unaffected by inbreeding; however, interfamily variation in seedling establishment was detected. Life tables and fecundity schedules for the S0, S1 and S2 groups yielded estimates of net reproductive rates (R0), from which relative fitnesses were calculated. Relative fitnesses for the S0, S1 and S2 groups were 1.00, 0.56 and 0.57. The differences in relative fitness among the groups were due to survivorship. The magnitudes of the observed inbred fitnesses are slightly greater than those predicted by several models for outcrossing populations. Two possible explanations for this incongruity are discussed.
Conifers are wind pollinated with no reported restrictions on self pollination and self fertilization. Nevertheless, most species show large inbreeding depression in growth; and the frequency of self seedlings in wind-pollination progeny is generally low. In this paper the influence of embryo viability, polyembryony, and pregermination embryo selection on the relationship between natural self pollination and proportion of self seedlings is investigated. Species with low (coastal Douglas-fir) and high (noble fir) self-embryo viabilities are used as examples. In Douglas-fir, the main factor reducing the effects of self pollination is low viability of self embryos. Polyembryony and the potential for pregermination selection augment the effect of low self-embryo viability. Natural self pollination can reach 40-60% of total pollination without greatly increasing the proportion of self seedlings in the seedling population. In noble fir, polyembryony allows for embryo selection; but frequency of self seedlings increases nearly proportionately to any increase in natural self pollination. Other aspects of the mating system may limit natural self pollination or self fertilization in this species.
1) Limnanthes floccosa is an autogamous derivative of the outcrosser, L. alba. Limnanthes floccosa comprises five subspecies of which three are facultatively autogamous, and two are predominantly autogamous. 2) In Limnanthes floccosa the increases in chiasma frequency that have paralleled the evolution of autogamy indicate that autogamy has arisen not because of the effects self-pollination has on population structure, but because it serves as an adaptation to secure survival. 3) Hypotheses bearing on the evolution of autogamy are discussed and categorized according to whether the change from outcrossing to autogamy has occurred in relation to the prefertilization or the genetic effects of self-pollination. 4) Fluctuations in pollinator availability and seasonal variations in soil drying in marginal populations of Limnanthes alba indicate that autogamy in L. floccosa has arisen in relation to its prefertilization effect of securing seed set under circumstances in which insect-mediated cross pollination is unreliable. 5) Several arguments against the likelihood that autogamy arises in relation to the genetic effects of self-pollination are given.
Populations of Gilia achilleifolia were studied to assess the extent of variation for protandry, stigma exsertion, flower size, and fruit set in the absence of pollinators. Seven of these populations were further examined to determine the outcrossing rate using allozyme loci as marker genes. Average outcrossing rate estimates in this species ranged from 0.15-0.96. Outcrossing rate is positively correlated with an index of the degree of protandry, and negatively correlated with the proportion of fruit set in the absence of pollinators. Outcrossing rate is uncorrelated with stigma exsertion and flower size. Progeny tests of plants in two populations revealed significant intrapopulation heritable variation for degree of protandry, suggesting that evolutionary change in the breeding system proceeded through selection acting on the variation in this floral characteristic.
A bimodal distribution of outcrossing rates was observed for natural plant populations, with more primarily selfing and primarily outcrossing species, and fewer species with intermediate outcrossing rate than expected by chance. This distrbution is argued to result from selection for the maintenance of outcrossing in historically large, outcrossing populations with substantial inbreeding depression, and from selection for selfing when increased inbreeding, due to pollinator failure or population bottlenecks, reduces the level of inbreeding depression. Few species or populations are fixed at complete selfing or complete outcrossing. A low level of selfing in primarily outcrossing species is unlikely to be selectively advantageous, but will not reduce inbreeding depression to the level where selfing is selectively favored particularly if accompanied by reproductive compensation. Similarly, occasional outcrossing in primarily selfing species is unlikely to regularly provide sufficient heterosis to maintain selection for outcrossing through individual selection. Genetic, morphological and ecological constraints may limit the potential for outcrossing rates in selfers to be reduced below some minimum level. -Authors
A B S T R A C T Evidence is presented that a geographically peripheral population of the annual Stephanomeria exigua ssp. coronaria (Compositae), a widespread and ecologically diverse species, has recently given rise by a process of sympatric speciation to a diploid species presently designated "Malheurensis." The new species comprises less than 250 individuals and is found only at a single locality in eastern Oregon where it grows interspersed with its parental population. Stephanomeria exigua ssp. coronaria is an obligate outcrosser and "Malheurensis" is highly self-pollinating. Reproductive isolation is maintained by differences in breeding system, a crossability barrier that reduces seed set following cross-pollination between them, and reduction in hybrid fertility caused by chromosomal structural differences. They are very similar morphologically. Electrophoretic analyses of seven enzyme systems demonstrate that all the alleles but one at the controlling 13 gene loci in "Malheurensis" are identical to alleles in ssp. coronaria. The new species displays certain maladapted features including loss of the specific requirements for seed germination characteristic of the progenitor population of ssp. coronaria. The origin of "Malheurensis" appears to be an exception to the theory of geographical speciation because spatial isolation is not necessary at any time for the origin or establishment of its reproductive isolating barriers. The nature of these barriers plus the genetic homogeneity of the species are compatible with the hypothesis that it derives from a single progenitor individual. Very little genetic change is involved initially in this mode of speciation.
Quantitative genetic models of phenotypic evolution in small isolated populations are presented, from the initial founding event to continued random genetic drift and natural selection toward a new optimum phenotype. The basic features of complex morphologies included are polygenic inheritance with multiple allelism, pleiotropy, recombination and mutation. Gene flow, inbreeding depression, gene interaction, and genetic homeostasis are also discussed. Simpson's adaptive zones for phenotypes (analogous to Wright's adaptive topography for gene frequencies) are formulated probabilistically for small populations. It is concluded that Mayr's theory of allopatric speciation overemphasized both the genetic cohesion of widespread species and the founder effect on heterozygosity and quantitative genetic variation. However, data on the strength of natural selection and the spontaneous mutability of quantitative characters, in conjunction with the models, provide a feasible microevolutionary mechanism for substantial...
The fitnesses of two phenotypes which differ in their frequency of self-fertilization are expressed exactly in terms of various parameters, including the relative fitness of progeny from selfing, i, and the proportion of available ovules fertilized with the aid of an external agent, e. Strategic models of natural selection find stationary conditions where the two phenotypes have the same fitness. Conditions when selfing is advantageous to populations and to individuals are not usually identical. Conditions favoring self-fertilization are more stringent when selfing competes with crossing (for individual selection, i > 1/2) and less stringent when selfing occurs prior to crossing (i > e/2). When selfing is delayed until after all opportunities for crossing, it is always advantageous if the parameters vary independently. Some functional interactions between parameters, as when an increase in selfing simultaneously reduces the efficiency of external pollinating agents, result in stationary conditions with mixed self- and cross-fertilization under certain conditions. Following a change in the level of self-fertilization, certain evolutionary adjustments increase the advantage of the acquired mode of fertilization. The models demonstrate that the evolution of various levels of self-fertilization in plants can be explained by individual selection without recourse to postulates of long-term advantages to populations.
Thirty-five coastal Douglas-fir trees were evaluated for embryonic genetic load from comparisons of sound seed set following self- and cross-pollinations, that is, from determinations of relative self-fertility. Estimates for the 35 trees ranged from about 3 to about 27 lethal equivalents per zygote active in the embryo stage, with the median tree carrying about 10 lethal equivalents per zygote. Relative self-fertility of Douglas-fir was compared with that reported for other coniferous species, and genetic load was compared with that reported for Drosophila, Tribolium, and man.
Genotypic differences among forms of Lupinus nanus were established for the reproductive traits of flowering time, flower size, pollen production, ovule production, length of anthers, length of stigmatic hairs, coherence between keel margins, blue reflectance from corollas, honey guide marking, and autofertility These forms outcrossed at significantly different rates when exposed to the same pollination environment. Attempts are made to relate reproductive traits to reproductive mode.
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IT was shown several decades ago that the reduction in genetic heterozygosity produced by inbreeding in domesticated plants and animals is accompanied by an increase in morphological variability1,2. While studies of laboratory populations and results of plant and animal breeding have been instrumental in identifying the relationship between genetic heterozygosity and morphological variability, such investigations often involved substantial changes in genetic heterozygosity, such as are produced when entire chromosomes are made homozygous. For this reason their relevance to the levels of heterozygosity in natural populations is unclear. Until recently attempts to examine this relationship in natural populations were hindered by the inability to routinely estimate levels of genetic heterozygosity in nature. However, determinations of genetic heterozygosity at specific enzyme-loci can now be made by electrophoresis. Recently Mitton3 found that heterozygotes for a set of five enzyme-loci had reduced multivariate variances for a set of morphological characters when compared to homozygotes at the same loci in populations of the killifish, Fundulus heteroclitus. It is very important to determine the generality of this observation for other species populations. I have now examined the relationship between genetic heterozygosity, as identified by electrophoresis, and the variance of morphological characters in the monarch butterfly, Danaus plexippus. Study of six polymorphic enzyme-loci in the monarch shows that once again heterozygotes have smaller variances for morphological characters when compared to homozygotes at the same locus.
Genetic load data for two homosporous ferns are summarized and the mean frequency of recessive sporophytic lethals per zygote calculated. Fifty-one spore collections of Onoclea sensibilis had a mean of 0587 lethals per zygote, and 129 spore collections of Osmunda regalis had a mean of 239 lethals per zygote. Each spore collection represents a meiotic sample from a single individual (genet). Both species form hermaphroditic gametophytes with extensive capacities for simple polyembryony. Simple polyembryony results in a form of soft selection in panmictic populations and thus higher equilibrium frequencies for lethals are possible than in organisms without simple polyembryony. When ferns are inbred, the high load levels are expressed. Load levels in ferns may reflect a balance between soft selection in panmictic populations and hard selection under conditions of inbreeding. The sheltering effect of simple poly-embryony is demonstrated for both mutational and heterotic load.
The rates of outcrossing in sympatric populations of Ipomoea purpurea and I, hederacea were estimated (using electrophoretic markers) to be 70% and 7% respectively. The difference in outcrossing rate is not apparently due to differences in pollinator service received by the species, but is associated with differences in anther-stigma distance. In I. purpurea stigmas are generally exserted and there is much genetic variation for anther-stigma distance. Variation in this character has a significant effect on the ease with which selfpollination occurs. In contrast there is no variation for the character in the I. hederacea population, the anthers being invariably held at the same level as the stigma, an arrangement promoting self-pollination.
L. pimpinellifolium is a highly heterogeneous species, exhibiting pronounced trends from one end of its linear distribution to the other in nearly every studied genetic locus. Drastic differences between populations were also detected in genetic variability and rates of outcrossing. Highly significant positive correlations exist in every possible comparison between flower size, degree of stigma exsertion, heterozygosity, and allelic polymorphism. The hypothesis most compatible with observations proposes that the very uniform, highly self-pollinated biotypes originated from the more primitive, more variable, facultatively allogamous forms.
The formulae for the mean and variance of squared deviations from an optimum are given for the cases of no dominance and of
complete dominance, first assuming no environmental complications but later removing this restriction. The variance in each
case is analysed into contributions due to (1) additive gene effects, (2) dominance deviations, (3) epistatic deviations,
(4) environmental effects and (5) nonadditive joint effects of heredity and environment. In the case of complete dominance,
formulae are developed which apply to epistatic relations in general. These lead to formulae for the correlations between
parent and offspring and between two offspring.
It appears that in a population in which the mean of some measurable character is at the optimum, the parent-offspring and
fraternal correlations in adaptive value are approximately the squares of the corresponding correlations with respect to the
character itself, whatever environmental complications there may be. Where the mean is not at the optimum, there is less difference
between the correlations in adaptive value and the corresponding ones with respect to the character itself.
This review encompasses a decade of studies of enzyme polymorphism in plant populations, in the light of both general theory and specific, simplified models. The patterns of the observed frequency of heterozygotes, compared with panmictic expectations adjusted only for inbreeding, are summarised for 23 outbreeding and 7 inbreeding plant species. There is a trend for outbreeders to show less heterozygosity than expected, and inbreeders to show more, despite the contrary evolutionary pressures on the mating system (the so-called heterozygosity paradox). An annual life cycle and pollination by animal vectors seem to increase the discrepancy in outbreeders. Of the several forces which might account for this paradox, the effects of intense microgeographic differentiation, of low gene flow, of self compatibility and of overdominance of linked segments are predominant. The evidence indicates that inbreeding plant species show more intense geographic and microgeographic differentiation, and more intense multilocus associations than outbreeders. Recent attempts to describe selection operating on variants by the analysis of life cycle components, of physiological processes, and of genetic demography are discussed. The fundamental importance of mating systems and their variation, as a distinctive feature of plant populations is already clear from the studies in hand. Therefore a closer integration of the joint microevolution of mating systems, and of genetic variation is required in both theoretical and experimental studies.
We have examined a model proposed by East (1929) for the evolution of gametophytic self-incompatibility allele systems, starting from populations with a self-fertility allele. The original self-fertility allele is not eliminated from the population when three active S alleles have been incorporated, but self-fertility alleles can coexist with S alleles. In order to examine this co-existence more fully, we studied the invasion of self-incompatible populations containing various numbers of S alleles (all assumed to be equally frequent) by three possible types of self-compatibility factors that could arise by mutation at the S locus. We find that there is always some critical number of active S alleles that ensures the elimination of mutant alleles with no activity in pollen; this number depends on die inbreeding depression. Alleles abolishing the stigma activity can spread, irrespective of how many active alleles are present, provided the inbreeding depression is small enough. Some of the biological implications of these results are discussed.
Population genetic studies of the evolution of breeding systems in flowering plants are reviewed. The selective advantage of a gene's increasing the selfing rate is stressed. In the evolution of outbreeding mechanisms, some strong disadvantage to selfing must therefore be acting; it is suggested that this disadvantage is inbreeding depression. Populations with no absolute barrier to selfing, and with intermediate levels of self-fertilization, appear to be the most likely starting state for the evolution of outbreeding mechanisms. There is some evidence for inbreeding depression in such populations. The evolution of distyly and dioecy are considered in some detail. An explanation for the existence of supergenes controlling these systems is proposed. The breakdown of distyly and tristyly are also considered. The evolution of recombination rates in selfing and outcrossing species is examined briefly.
THERE is little consensus among evolutionary biologists on the roles of morphological and protein variation within populations, and little consideration is given to their covariation. Morphological variation is known to be influenced by both the genetics of individuals and the environments in which they develop. Crosses between domesticated strains of plants and animals suggest that highly heterozygous individuals have enhanced developmental homeostasis1, but the implications of this phenomenon for natural populations have not been extensively explored. Reported here is an examination of the relationship between genetic heterozygosity of proteins and morphological variation in natural populations of the killifish, Fundulus heteroclitus. Results indicate that individuals heterozygous for an enzyme locus are likely to be less morphologically variable than individuals homozygous for that locus.
The contribution to the inbreeding depression from a digenic tetrasomic locus upon self-fertilization involves three genotypic interaction effects which may be thought of as a generalization of the dominance deviation for a diploid locus. It is shown how this contribution may be expressed in terms of these genotypic interaction effects, the gene frequencies and the number of generations of selfing.
It was shown in a simple model that a gene for selfing will be established in a population if and only if at least one of the selfing genotypes also contributes to random fertilization. The same conclusion is valid for vegetative reproduction and ameiotic parthenogenesis. This connection between selfing and the mating system is consistent with the much greater frequency of uniparental reproduction among plants than animals.
Most quantitative traits in most populations exhibit heritable genetic variation. Lande proposed that high levels of heritable variation may be maintained by mutation in the face of stabilizing selection. Several analyses have appeared of two distinct models with n additive polygenic loci subject to mutation and stabilizing selection. Each is reviewed and a new analysis and model are presented. Lande and Fleming analyzed extensions of a model originally treated by Kimura which assumes a continuum of possible allelic effects at each locus. Latter and Bulmer analyzed a model with diallelic loci. The published analyses of these models lead to qualitatively different predictions concerning the dependence of the equilibrium genetic variance on the underlying biological parameters. A new asymptotic analysis of the Kimura model shows that the different predictions are not consequences of the number of alleles assumed but rather are attributable to assumptions concerning the relative magnitudes of per locus mutation rates, the phenotypic effects of mutation, and the intensity of selection. This conclusion is reinforced by analysis of a model with triallelic loci. None of the approximate analyses presented are mathematically rigorous. To quantify their accuracy and display the domains of validity for alternative approximations, numerically determined equilibria are presented. In addition, empirical estimates of mutation rates and selection intensity are reviewed, revealing weaknesses in both the data and its connection to the models. Although the mathematical results and underlying biological requirements of my analyses are quite different from those of Lande , the results do not refute his hypothesis that considerable additive genetic variance may be maintained by mutation-selection balance. However, I argue that the validity of this hypothesis can only be determined with additional data and mathematics.
Several reports have shown that greater heterozygosity (both between individuals and between populations) is associated with lower morphological variance and asymmetry. Most previous work concerned poikilothermic organisms (for example, fish, butterflies, lizards, shellfish, salamanders and plants). Reports concerning two homoiotherms gave conflicting results. The report by Handford on a songbird, Zonotrichia capensis, failed to support the relationship, although these results have been questioned in the literature. Handford suggested that the lack of relationship in Zonotrichia could indicate a fundamental difference between homoiotherms and poikilotherms, reflected in their apparent differences in heterozygosity. However, we report here on electrophoretic and morphometric studies on another songbird species (Passer domesticus), in which the relationship appears to be upheld. We find consistently, among four locality samples, that the class of individuals of greatest allozyme heterozygosity nearly always exhibits the lowest multivariate morphological variance, and the class of greatest homozygosity nearly always exhibits the highest.
This paper analyses some models of selection for asexual reproduction, orincreased rates of self-fertilisation, in a variety of mating systems. It is shown that mutations to asexual modes of reproduction have a strong advantage in dioecious species and outbreeding hermaphrodites. This advantage is lost if the sex-ratio is heavily biased in favour of females (with dioecy), or if there is a high level of inbreeding (with hermaphroditism). It is also shown that there may be an advantage to asexuality, but not to increased self-fertilisation, in isogamous species. The biological implications of the results are discussed.
Ourload of mutations. Amer
- H J Muller
MULLER, H. J. 1950. Ourload of mutations. Amer. J. Hum. Genet. 2:111-176.
Selection in One-and Two-Locus Systems
- N Y De Nettancourt
Selection in One-and Two-Locus Systems. Springer-Verlag, N.Y. DE NETTANCOURT, D. 1977. Incompatibility in