Feed‐backs among inbreeding,inbreeding depression in sperm traits,and sperm competition can drive evolution of costly polyandry

Ongoing ambitions are to understand the evolution of costly polyandry and its consequences for species ecology and evolution. Emerging patterns could stem from feed‐back dynamics between the evolving mating system and its genetic environment, defined by interactions among kin including inbreeding. However, such feed‐backs are rarely considered in nonselfing systems. We use a genetically explicit model to demonstrate a mechanism by which inbreeding depression can select for polyandry to mitigate the negative consequences of mating with inbred males, rather than to avoid inbreeding, and to elucidate underlying feed‐backs. Specifically, given inbreeding depression in sperm traits, costly polyandry evolved to ensure female fertility, without requiring explicit inbreeding avoidance. Resulting sperm competition caused evolution of sperm traits and further mitigated the negative effect of inbreeding depression on female fertility. The evolving mating system fed back to decrease population‐wide homozygosity, and hence inbreeding. However, the net overall decrease was small due to compound effects on the variances in sex‐specific reproductive success and paternity skew. Purging of deleterious mutations did not eliminate inbreeding depression in sperm traits or hence selection for polyandry. Overall, our model illustrates that polyandry evolution, both directly and through sperm competition, might facilitate evolutionary rescue for populations experiencing sudden increases in inbreeding.     

Inbreeding effects on fitness traits in the heterocarpic herb Leontodon autumnalis L. (Asteraceae)

Heterocarpic plants are characterized by the production of distinct types of fruits that usually differ in their ecological behavior. In the Asteraceae, differences are mainly found between peripheral non-dispersal and central dispersal achenes (single-seeded fruits). Inbreeding depression is considered as an evolutionary force as it may reduce several fitness traits, and in the case of heterocarpic plants, it could influence fitness traits (e.g., seed set, germination rate, growth rate) of each fruit morph, which may have important ecological and evolutionary consequences. In particular, differential effects on fitness traits and dispersal of selfed and outcrossed progeny can strongly determine the viability of extant populations and the potential to colonize new habitats. We conducted a hand-pollination experiment in greenhouse conditions to test whether inbreeding affects the fitness of achene morphs in the heterocarpic herb Leontodon autumnalis (Asteraceae). Results show that achene morphs significantly differ in their ecological behavior, peripheral achenes germinating more and faster than central achenes. The significant interaction between pollination treatment and achene morph for germination probability might indicate a link between dormancy and mating system in L. autumnalis: germination was higher for outcrossed achenes in central achenes whereas the opposite pattern was exhibited by peripheral achenes. Selfing dramatically reduced seed set, probably as a consequence of strong self-incompatibility mechanisms rather than inbreeding effects. Inbreeding depression significantly affected late life-cycle traits, such as growth rate and biomass at flowering. Overall, results suggest that inbreeding depression seems to be an important selective force maintaining outcrossing in L. autumnalis.     

Genetic load,inbreeding depression,and hybrid vigor covary with population size: An empirical evaluation of theoretical predictions

Reduced population size is thought to have strong consequences for evolutionary processes as it enhances the strength of genetic drift. In its interaction with selection, this is predicted to increase the genetic load, reduce inbreeding depression, and increase hybrid vigor, and in turn affect phenotypic evolution. Several of these predictions have been tested, but comprehensive studies controlling for confounding factors are scarce. Here, we show that populations of Daphnia magna, which vary strongly in genetic diversity, also differ in genetic load, inbreeding depression, and hybrid vigor in a way that strongly supports theoretical predictions. Inbreeding depression is positively correlated with genetic diversity (a proxy for N_e), and genetic load and hybrid vigor are negatively correlated with genetic diversity. These patterns remain significant after accounting for potential confounding factors and indicate that, in small populations, a large proportion of the segregation load is converted into fixed load. Overall, the results suggest that the nature of genetic variation for fitness‐related traits differs strongly between large and small populations. This has large consequences for evolutionary processes in natural populations, such as selection on dispersal, breeding systems, ageing, and local adaptation.     

No evidence of inbreeding depression in sperm performance traits in wild song sparrows

Inbreeding is widely hypothesized to shape mating systems and population persistence, but such effects will depend on which traits show inbreeding depression. Population and evolutionary consequences could be substantial if inbreeding decreases sperm performance and hence decreases male fertilization success and female fertility. However, the magnitude of inbreeding depression in sperm performance traits has rarely been estimated in wild populations experiencing natural variation in inbreeding. Further, the hypothesis that inbreeding could increase within‐ejaculate variation in sperm traits and thereby further affect male fertilization success has not been explicitly tested. We used a wild pedigreed song sparrow (Melospiza melodia) population, where frequent extrapair copulations likely create strong postcopulatory competition for fertilization success, to quantify effects of male coefficient of inbreeding (f) on key sperm performance traits. We found no evidence of inbreeding depression in sperm motility, longevity, or velocity, and the within‐ejaculate variance in sperm velocity did not increase with male f. Contrary to inferences from highly inbred captive and experimental populations, our results imply that moderate inbreeding will not necessarily constrain sperm performance in wild populations. Consequently, the widely observed individual‐level and population‐level inbreeding depression in male and female fitness may not stem from reduced sperm performance in inbred males.     

Environment-dependent inbreeding depression in a hermaphroditic freshwater snail

Inbreeding depression was simultaneously studied under contrasted environments, laboratory and natural conditions, using individuals originating from 14 families of the freshwater snail Physa acuta. Both survival and growth of juveniles showed inbreeding depression under laboratory conditions. The same fitness components were monitored with mature snails either kept under laboratory conditions or released at a natural site and analysed using capture-mark-recapture models. Genetic composition of both samples was similar. Inbreeding depression on survival was highest in the laboratory while strong outbreeding depression was revealed in the field. Thus inbreeding depression may not be always higher under natural conditions, at the opposite of what is commonly assumed. We suggest that inbreeding depression is dependent on metabolic requirements imposed by the environment. Other evidences showing that inbreeding depression is environment-dependent are reviewed. We conclude that genetic models should include both genetic and environmental variance in inbreeding depression for studying mating system evolution.     

Inbreeding shapes the evolution of marine invertebrates

Inbreeding is a potent evolutionary force shaping the distribution of genetic variation within and among populations of plants and animals. Yet, our understanding of the forces shaping the expression and evolution of nonrandom mating in general, and inbreeding in particular, remains remarkably incomplete. Most research on plant mating systems focuses on self-fertilization and its consequences for automatic selection, inbreeding depression, purging, and reproductive assurance, whereas studies of animal mating systems have often assumed that inbreeding is rare, and that natural selection favors traits that promote outbreeding. Given that many sessile and sedentary marine invertebrates and marine macroalgae share key life history features with seed plants (e.g., low mobility, modular construction, and the release of gametes into the environment), their mating systems may be similar. Here, we show that published estimates of inbreeding coefficients (F_IS) for sessile and sedentary marine organisms are similar and at least as high as noted in terrestrial seed plants. We also found that variation in F_IS within invertebrates is related to the potential to self-fertilize, disperse, and choose mates. The similarity of F_IS for these organismal groups suggests that inbreeding could play a larger role in the evolution of sessile and sedentary marine organisms than is currently recognized. Specifically, associations between traits of marine invertebrates and F_IS suggest that inbreeding could drive evolutionary transitions between hermaphroditism and separate sexes, direct development and multiphasic life cycles, and external and internal fertilization.     

Inbreeding Avoidance Drives Consistent Variation of Fine-Scale Genetic Structure Caused by Dispersal in the Seasonal Mating System of Brandt’s Voles

Inbreeding depression is a major evolutionary and ecological force influencing population dynamics and the evolution of inbreeding-avoidance traits such as mating systems and dispersal. Mating systems and dispersal are fundamental determinants of population genetic structure. Resolving the relationships among genetic structure, seasonal breeding-related mating systems and dispersal will facilitate our understanding of the evolution of inbreeding avoidance. The goals of this study were as follows: (i) to determine whether females actively avoided mating with relatives in a group-living rodent species, Brandt’s voles (Lasiopodomys brandtii), by combined analysis of their mating system, dispersal and genetic structure; and (ii) to analyze the relationships among the variation in fine-genetic structure, inbreeding avoidance, season-dependent mating strategies and individual dispersal. Using both individual- and population-level analyses, we found that the majority of Brandt’s vole groups consisted of close relatives. However, both group-specific FISs, an inbreeding coefficient that expresses the expected percentage rate of homozygosity arising from a given breeding system, and relatedness of mates showed no sign of inbreeding. Using group pedigrees and paternity analysis, we show that the mating system of Brandt’s voles consists of a type of polygyny for males and extra-group polyandry for females, which may decrease inbreeding by increasing the frequency of mating among distantly-related individuals. The consistent variation in within-group relatedness, among-group relatedness and fine-scale genetic structures was mostly due to dispersal, which primarily occurred during the breeding season. Biologically relevant variation in the fine-scale genetic structure suggests that dispersal during the mating season may be a strategy to avoid inbreeding and drive the polygynous and extra-group polyandrous mating system of this species.     

Role of parasite transmission in promoting inbreeding: II. Pedigree reconstruction reveals sib‐transmission and consequent kin‐mating

Even though parasitic flatworms are one of the most species‐rich groups of hermaphroditic organisms, we know virtually nothing of their mating systems (selfing or kin‐mating rates) in nature. Hence, we lack an understanding of the role of inbreeding in parasite evolution. The natural mating systems of parasitic flatworms have remained elusive due to the inherent difficulty in generating progeny‐array data in many parasite systems. New developments in pedigree reconstruction allow direct inference of realized selfing rates in nature by simply using a sample of genotyped individuals. We built upon this advancement by utilizing the closed mating systems, that is, individual hosts, of endoparasites. In particular, we created a novel means to use pedigree reconstruction data to estimate potential kin‐mating rates. With data from natural populations of a tapeworm, we demonstrated how our newly developed methods can be used to test for cosibling transmission and inbreeding depression. We then showed how independent estimates of the two mating system components, selfing and kin‐mating rates, account for the observed levels of inbreeding in the populations. Thus, our results suggest that these natural parasite populations are in inbreeding equilibrium. Pedigree reconstruction analyses along with the new companion methods we developed will be broadly applicable across a myriad of parasite species. As such, we foresee that a new frontier will emerge wherein the diverse life histories of flatworm parasites could be utilized in comparative evolutionary studies to broadly address ecological factors or life history traits that drive mating systems and hence inbreeding in natural populations.     

Genetic components of variation in Nemophila menziesii undergoing inbreeding: morphology and flowering time.

The standard approaches to estimation of quantitative genetic parameters and prediction of response to selection on quantitative traits are based on theory derived for populations undergoing random mating. Many studies demonstrate, however, that mating systems in natural populations often involve inbreeding in various degrees (i.e. , self matings and matings between relatives). Here we apply theory developed for estimating quantitative genetic parameters for partially inbreeding populations to a population of Nemophila menziesii recently obtained from nature and experimentally inbred. Two measures of overall plant size and two of floral size expressed highly significant inbreeding depression. Of three dominance components of phenotypic variance that are defined under partial inbreeding, one was found to contribute significantly to phenotypic variance in flower size and flowering time, while the remaining two components contributed only negligibly to variation in each of the five traits considered. Computer simulations investigating selection response under the more complete genetic model for populations undergoing mixed mating indicate that, for parameter values estimated in this study, selection response can be substantially slowed relative to predictions for a random mating population. Moreover, inbreeding depression alone does not generally account for the reduction in selection response.     

Inbreeding depresses short and long distance dispersal in three congeneric spiders

Dispersal is one of the most important precopulatory inbreeding avoidance mechanisms and subject to landscape related selection pressures. In small populations, inbreeding within and between populations may strongly affect population dynamics if it reduces fitness and gene‐flow. While inbreeding avoidance is generally considered to be a key evolutionary driver of dispersal, potential effects of inbreeding on the dispersal process, are poorly known. Here, I document how inbreeding within a population, so by mating among relatives, affects the survivorship and the dispersal behaviour of three congeneric spider Erigone species (Araneae: Linyphiidae) that differ in habitat preference and regional rarity. The three species were chosen as a model because they allow the assessment of both long and short distance dispersal motivation (respectively ballooning and rappelling) under laboratory conditions. Inbreeding reduced both long and short distance dispersal modes in the three congeneric species. Because survival was depressed after inbreeding, with a tendency of reduced survival loss in the rare and highly stenotopic species, energetic constraints are likely to be the underlying mechanism. Inbreeding consequently depresses silk‐related dispersal in three related spiders. This may induce an inbreeding depression vortex with important consequences for range expansion and metapopulation dynamics of aerially dispersing species from highly fragmented landscapes.     

Comparing the consequences of natural selection,adaptive phenotypic plasticity,and matching habitat choice for phenotype–environment matching,population genetic structure,and reproductive isolation in meta‐populations

Organisms commonly experience significant spatiotemporal variation in their environments. In response to such heterogeneity, different mechanisms may act that enhance ecological performance locally. However, depending on the nature of the mechanism involved, the consequences for populations may differ greatly. Building on a previous model that investigated the conditions under which different adaptive mechanisms (co)evolve, this study compares the ecological and evolutionary population consequences of three very different responses to environmental heterogeneity: matching habitat choice (directed gene flow), adaptive plasticity (associated with random gene flow), and divergent natural selection. Using individual‐based simulations, we show that matching habitat choice can have a greater adaptive potential than plasticity or natural selection: it allows for local adaptation while protecting genetic polymorphism despite global mating or strong environmental changes. Our simulations further reveal that increasing environmental fluctuations and unpredictability generally favor the emergence of specialist genotypes but that matching habitat choice is better at preventing local maladaptation by individuals. This confirms that matching habitat choice can speed up the genetic divergence among populations, cause indirect assortative mating via spatial clustering, and hence even facilitate sympatric speciation. This study highlights the potential importance of directed dispersal in local adaptation and speciation, stresses the difficulty of deriving its operation from nonexperimental observational data alone, and helps define a set of ecological conditions which should favor its emergence and subsequent detection in nature.     

Life-history plasticity and inbreeding depression under mate limitation and predation risk: cumulative lifetime fitness dissected with a life table response experiment

Environmental effects on the evolution of mating systems are increasingly discussed, but we lack many examples of how environmental conditions affect the expression and consequences of alternative mating systems. Variation in mate availability sets up a trade-off between reproductive assurance and inbreeding depression, but the consequences of both mate limitation and inbreeding may depend on other environmental conditions. Predation risk is common under natural conditions, and known to affect allocation to reproduction, but we know little about the effects of isolation and inbreeding under predation risk. We reared selfed and outcrossed hermaphroditic freshwater snails (Physa acuta) in four environments (predator cues present or absent crossed with mating partners available or not) and quantified life-history traits and cumulative lifetime fitness. Our results confirm that isolation from mates can increase longevity and growth, resulting in higher lifetime fecundity. Thus, we observed no evidence for mate limitation of reproduction. However, reproduction under isolation (i.e., selfing) resulted in inbreeding depression, which should counteract the benefits of selfing. Inbreeding depression in fitness occurred in both predator and no-predator environments, but there was no overall change in inbreeding depression with predator cues. This represents, to our knowledge, the first empirical estimate of the effect of predation risk on inbreeding depression in an animal. Cumulative fitness was most influenced by early survival and especially early fecundity. As predation risk and inbreeding (both ancestral and due to a lack of mates) reduced early fecundity, these effect are predicted to have important contributions to population growth under natural conditions. Therefore life-history plasticity (e.g., delayed reproduction) is likely to be very important to overall fitness.     

Genetics of dispersal

Dispersal is a process of central importance for the ecological and evolutionary dynamics of populations and communities, because of its diverse consequences for gene flow and demography. It is subject to evolutionary change, which begs the question, what is the genetic basis of this potentially complex trait? To address this question, we (i) review the empirical literature on the genetic basis of dispersal, (ii) explore how theoretical investigations of the evolution of dispersal have represented the genetics of dispersal, and (iii) discuss how the genetic basis of dispersal influences theoretical predictions of the evolution of dispersal and potential consequences. Dispersal has a detectable genetic basis in many organisms, from bacteria to plants and animals. Generally, there is evidence for significant genetic variation for dispersal or dispersal‐related phenotypes or evidence for the micro‐evolution of dispersal in natural populations. Dispersal is typically the outcome of several interacting traits, and this complexity is reflected in its genetic architecture: while some genes of moderate to large effect can influence certain aspects of dispersal, dispersal traits are typically polygenic. Correlations among dispersal traits as well as between dispersal traits and other traits under selection are common, and the genetic basis of dispersal can be highly environment‐dependent. By contrast, models have historically considered a highly simplified genetic architecture of dispersal. It is only recently that models have started to consider multiple loci influencing dispersal, as well as non‐additive effects such as dominance and epistasis, showing that the genetic basis of dispersal can influence evolutionary rates and outcomes, especially under non‐equilibrium conditions. For example, the number of loci controlling dispersal can influence projected rates of dispersal evolution during range shifts and corresponding demographic impacts. Incorporating more realism in the genetic architecture of dispersal is thus necessary to enable models to move beyond the purely theoretical towards making more useful predictions of evolutionary and ecological dynamics under current and future environmental conditions. To inform these advances, empirical studies need to answer outstanding questions concerning whether specific genes underlie dispersal variation, the genetic architecture of context‐dependent dispersal phenotypes and behaviours, and correlations among dispersal and other traits.     

Plant population dynamics, pollinator foraging, and the selection of self-fertilization

Many flowering plants rely on pollinators, self-fertilization, or both for reproduction. We model the consequences of these features for plant population dynamics and mating system evolution. Our mating systems-based population dynamics model includes an Allee effect. This often leads to an extinction threshold, defined as a density below which population densities decrease. Reliance on generalist pollinators who primarily visit higher density plant species increases the extinction threshold, whereas autonomous modes of selfing decrease and can eliminate the threshold. Generalist pollinators visiting higher density plant species coupled with autonomous selfing may introduce an effect where populations decreasing in density below the extinction threshold may nonetheless persist through selfing. The extinction threshold and selfing at low density result in populations where individuals adopting a single reproductive strategy exhibit mating systems that depend on population density. The ecological and evolutionary analyses provide a mechanism where prior selfing evolves even though inbreeding depression is greater than one-half. Simultaneous consideration of ecological and evolutionary dynamics confirms unusual features (e.g., evolution into extinction or abrupt increases in population density) implicit in our separate consideration of ecological and evolutionary scenarios. Our analysis has consequences for understanding pollen limitation, reproductive assurance, and the evolution of mating systems.     

Reduced inbreeding depression in peripheral relative to central populations of a monocarpic herb

Many temperate taxa were confined to warmer latitudes during the last glacial maximum. As their ranges expanded when climates warmed, genetic drift and inbreeding in relatively small peripheral populations are expected to have reduced genetic diversity and the segregating genetic load. Therefore, inbreeding depression in peripheral populations might be lower than in centrally located sites. We evaluated the consequences of inbreeding for fitness traits in six central and six northern peripheral populations of the herb Campanulastrum americanum. Inbreeding reduced performance for all traits. Inbreeding depression in peripheral populations was lower than in central populations. This difference increased across the life cycle from similar levels for germination, to central populations having three times the inbreeding depression for adult traits. Geographical patterns of inbreeding depression suggest that mating system variation and potential future mating system evolution in many temperate taxa might reflect, at least in part, nonequilibrium conditions associated with historic range changes.     

Ecology and evolution of plant mating

Plants exhibit complex mating patterns because of their immobility, hermaphroditism and reliance on vectors for pollen transfer. Research on plant mating attempts to determine who mates with whom in plant populations and how and why mating patterns become evolutionarily modified. Most theoretical models of mating-system evolution have focused on the fitness consequences of selling and outcrossing, stimulating considerable empirical work on the ecology and genetics of inbreeding depression. Less attention has been given to how the mechanics of pollen dispersal influence the transmission of self and outcross gametes. Recent work on the relation between pollen dispersal and mating suggests that many features of floral design traditionally interpreted as anti-selling mechanisms may function to reduce the mating costs associated with large floral displays.     

The genetic consequences of fluctuating inbreeding depression and the evolution of plant selfing rates

The magnitude of inbreeding depression, a central parameter in the evolution of plant mating systems, can vary depending on environmental conditions. However, the underlying genetic mechanisms causing environmental fluctuations in inbreeding depression, and the consequences of this variation for the evolution of self‐fertilization, have been little studied. Here, we consider temporal fluctuations of the selection coefficient in an explicit genetic model of inbreeding depression. We show that substantial variance in inbreeding depression can be generated at equilibrium by fluctuating selection, although the simulated variance tends to be lower than has been measured in experimental studies. Our simulations also reveal that purging of deleterious mutations does not depend on the variance in their selection coefficient. Finally, an evolutionary analysis shows that, in contrast to previous theoretical approaches, intermediate selfing rates are never evolutionarily stable when the variation in inbreeding depression is due to fluctuations in the selection coefficient on deleterious mutations.     

Evidence for an epigenetic role in inbreeding depression

Inbreeding depression (i.e. negative fitness effects of inbreeding) is central in evolutionary biology, affecting numerous aspects of population dynamics and demography, such as the evolution of mating systems, dispersal behaviour and the genetics of quantitative traits. Inbreeding depression is commonly observed in animals and plants. Here, we demonstrate that, in addition to genetic processes, epigenetic processes may play an important role in causing inbreeding effects. We compared epigenetic markers of outbred and inbred offspring of the perennial plant Scabiosa columbaria and found that inbreeding increases DNA methylation. Moreover, we found that inbreeding depression disappears when epigenetic variation is modified by treatment with a demethylation agent, linking inbreeding depression firmly to epigenetic variation. Our results suggest an as yet unknown mechanism for inbreeding effects and demonstrate the importance of evaluating the role of epigenetic processes in inbreeding depression.     

How is dispersal integrated in life histories: a quantitative analysis using butterflies

As dispersal plays a key role in gene flow among populations, its evolutionary dynamics under environmental changes is particularly important. The inter-dependency of dispersal with other life history traits may constrain dispersal evolution, and lead to the indirect selection of other traits as a by-product of this inter-dependency. Identifying the dispersal's relationships to other life-history traits will help to better understand the evolutionary dynamics of dispersal, and the consequences for species persistence and ecosystem functioning under global changes. Dispersal may be linked to other life-history traits as their respective evolutionary dynamics may be inter-dependent, or, because they are mechanistically related to each other. We identify traits that are predicted to co-vary with dispersal, and investigated the correlations that may constrain dispersal using published information on butterflies. Our quantitative analysis revealed that (1) dispersal directly correlated with demographic traits, mostly fecundity, whereas phylogenetic relationships among species had a negligible influence on this pattern, (2) gene flow and individual movements are correlated with ecological specialisation and body size, respectively and (3) routine movements only affected short-distance dispersal. Together, these results provide important insights into evolutionary dynamics under global environmental changes, and are directly applicable to biodiversity conservation.     

Inbreeding depression and genetic load of sexually selected traits: how the guppy lost its spots

To date, few studies have investigated the effects of inbreeding on sexually selected traits, although inbreeding depression on such traits can play an important role in the evolution and ecology of wild populations. Sexually selected traits such as ornamentation and courtship behaviour may not be primary fitness characters, but selection and dominance coefficients of their mutations will resemble those of traits under natural selection. Strong directional selection, for instance, through female mate-choice, purges all but the most recessive deleterious mutations, and the remaining dominance variation will result in inbreeding depression once populations undergo bottlenecks. We analysed the effects of inbreeding on sexually selected traits (colour pattern and courtship behaviour) in the male guppy, Poecilia reticulata, from Trinidad, and found a significant decline in the frequency of mating behaviour and colour spots. Such effects occurred although the genetic basis of these traits, many of which are Y-linked and hemizygous, would be expected to leave relatively little scope for inbreeding depression. Findings suggest that these sexually selected traits could reflect the genetic condition or health of males, and thus may be informative mate-cue characters for female choice as suggested by the 'good genes' model.