Strong inbreeding depression in a Daphnia metapopulation

The deleterious effects of inbreeding have long been known, and inbreeding can increase the risk of extinction for local populations in metapopulations. However, other consequences of inbreeding in metapopulations are still not well understood. Here we show the presence of strong inbreeding depression in a rockpool metapopulation of the planktonic freshwater crustacean Daphnia magna, which reproduces by cyclical parthenogenesis. We conducted three experiments in real and artificial rockpools to quantify components of inbreeding depression in the presence and the absence of competition between clonal lines of selfed and outcrossed genotypes. In replicated asexual populations, we recorded strong selection against clones produced by selfing in competition with clones produced by outcrossing. In contrast, inbreeding depression was much weaker in single-clone populations, that is, in the absence of competition between inbred and outbred clones. The finding of a competitive advantage of the outbred genotypes in this metapopulation suggests that if rockpool populations are inbred, hybrid offspring resulting from crosses between immigrants and local genotypes might have a strong selective advantage. This would increase the effective gene flow in the metapopulation. However, the finding of low inbreeding depression in the monoclonal populations suggests that inbred and outbred genotypes might have about equal chances of establishing new populations.     

Selection, load and inbreeding depression in a large metapopulation

The subdivision of a species into local populations causes its response to selection to change, even if selection is uniform across space. Population structure increases the frequency of homozygotes and therefore makes selection on homozygous effects more effective. However, population subdivision can increase the probability of competition among relatives, which may reduce the efficacy of selection. As a result, the response to selection can be either increased or decreased in a subdivided population relative to an undivided one, depending on the dominance coefficient F(ST) and whether selection is hard or soft. Realistic levels of population structure tend to reduce the mean frequency of deleterious alleles. The mutation load tends to be decreased in a subdivided population for recessive alleles, as does the expected inbreeding depression. The magnitude of the effects of population subdivision tends to be greatest in species with hard selection rather than soft selection. Population structure can play an important role in determining the mean fitness of populations at equilibrium between mutation and selection.     

Inbreeding depression and drift load in small populations at demographic disequilibrium

Inbreeding depression is a major driver of mating system evolution and has critical implications for population viability. Theoretical and empirical attention has been paid to predicting how inbreeding depression varies with population size. Lower inbreeding depression is predicted in small populations at equilibrium, primarily due to higher inbreeding rates facilitating purging and/or fixation of deleterious alleles (drift load), but predictions at demographic and genetic disequilibrium are less clear. In this study, we experimentally evaluate how lifetime inbreeding depression and drift load, estimated by heterosis, vary with census (N_c) and effective (estimated as genetic diversity, H_e) population size across six populations of the biennial Sabatia angularis as well as present novel models of inbreeding depression and heterosis under varying demographic scenarios at disequilibrium (fragmentation, bottlenecks, disturbances). Our experimental study reveals high average inbreeding depression and heterosis across populations. Across our small sample, heterosis declined with H_e, as predicted, whereas inbreeding depression did not vary with H_e and actually decreased with N_c. Our theoretical results demonstrate that inbreeding depression and heterosis levels can vary widely across populations at disequilibrium despite similar H_e and highlight that joint demographic and genetic dynamics are key to predicting patterns of genetic load in nonequilibrium systems.     

The different sources of variation in inbreeding depression, heterosis and outbreeding depression in a metapopulation of Physa acuta

Understanding how parental distance affects offspring fitness, i.e., the effects of inbreeding and outbreeding in natural populations, is a major goal in evolutionary biology. While inbreeding is often associated with fitness reduction (inbreeding depression), interpopulation outcrossing may have either positive (heterosis) or negative (outbreeding depression) effects. Within a metapopulation, all phenomena may occur with various intensities depending on the focal population (especially its effective size) and the trait studied. However, little is known about interpopulation variation at this scale. We here examine variation in inbreeding depression, heterosis, and outbreeding depression on life-history traits across a full-life cycle, within a metapopulation of the hermaphroditic snail Physa acuta. We show that all three phenomena can co-occur at this scale, although they are not always expressed on the same traits. A large variation in inbreeding depression, heterosis, and outbreeding depression is observed among local populations. We provide evidence that, as expected from theory, small and isolated populations enjoy higher heterosis upon outcrossing than do large, open populations. These results emphasize the need for an integrated theory accounting for the effects of both deleterious mutations and genetic incompatibilities within metapopulations and to take into account the variability of the focal population to understand the genetic consequences of inbreeding and outbreeding at this scale.     

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.     

Dynamics of an age‐structured population drawn from a random numbers table

I constructed age‐structured populations by drawing numbers from a random numbers table, the constraints being that within a cohort each number be smaller than the preceding number (indicating that some individuals died between one year and the next) and that the first two‐digit number following 00 or 01 ending one cohort’s life be the number born into the next cohort. Populations constructed in this way showed prolonged existence with total population numbers fluctuating about a mean size and with long‐term growth rate (r) ≈ 0. The populations’ birth rates and growth rates and the females’ per capita fecundity decreased significantly with population size, whereas the death rates showed no significant relationship to population size. These results indicate that age‐structured populations can persist for long periods of time with long‐term growth rates of zero in the absence of negative‐feedback loops between a population’s present or prior density and its birth rate, growth rate, and fecundity, contrary to the assumption of density‐dependent regulation hypotheses. Thus, a long‐term growth rate of zero found in natural populations need not indicate that a population’s numbers are regulated by density‐dependent factors.     

Joint effects of self-fertilization and population structure on mutation load, inbreeding depression and heterosis

Both the spatial distribution of organisms and their mode of reproduction have important effects on the change in allele frequencies within populations. In this article, we study the combined effect of population structure and the rate of partial selfing of organisms on the efficiency of selection against recurrent deleterious mutations. Assuming an island model of population structure and weak selection, we express the mutation load, the within- and between-deme inbreeding depression, and heterosis as functions of the frequency of deleterious mutants in the metapopulation; we then use a diffusion model to calculate an expression for the equilibrium probability distribution of this frequency of deleterious mutants. This allows us to derive approximations for the average mutant frequency, mutation load, inbreeding depression, and heterosis, the simplest ones being Equations 35-39 in the text. We find that population structure can help to purge recessive deleterious mutations and reduce the load for some parameter values (in particular when the dominance coefficient of these mutations is <0.2-0.3), but that this effect is reversed when the selfing rate is above a given value. Conversely, within-deme inbreeding depression always decreases, while heterosis always increases, with the degree of population subdivision, for all selfing rates.     

Multilocus heterozygosity and inbreeding depression in an insular house sparrow metapopulation

Inbreeding causes reduction of genetic variability that may have severe fitness consequences. In spite of its potentially huge impact on viability and evolutionary processes especially in small populations, quantitative demonstrations of genetic and demographic effects of inbreeding in natural populations are few. Here, we examine the relationship between individual inbreeding coefficients (F) and individual standardized multilocus heterozygosity (H) in an insular metapopulation of house sparrows (Passer domesticus) in northern Norway in order to evaluate whether H is a good predictor for F. We then relate variation in fitness (i.e. the probability of surviving from fledging to recruitment) to F and H, which enables us to examine whether inbreeding depression is associated with a reduction in genetic variability. The average level of inbreeding in the house sparrow metapopulation was high, and there was large inter-individual variation in F. As expected, standardized multilocus heterozygosity decreased with the level of inbreeding. The probability of recruitment was significantly negatively related to F, and, accordingly, increased with H. However, H explained no significant additional variation in recruitment rate than was explained by F. This suggests that H is a good predictor for F in this metapopulation, and that an increase in F is likely to be associated with a general increase in the level of homozygosity on loci across the genome, which has severe fitness consequences.     

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.     

Understanding the classics: the unifying concepts of transgressive segregation,inbreeding depression and heterosis and their central relevance for crop breeding

Transgressive segregation and heterosis are the reasons that plant breeding works. Molecular explanations for both phenomena have been suggested and play a contributing role. However, it is often overlooked by molecular genetic researchers that transgressive segregation and heterosis are most simply explained by dispersion of favorable alleles. Therefore, advances in molecular biology will deliver the most impact on plant breeding when integrated with sources of heritable trait variation – and this will be best achieved within a quantitative genetics framework. An example of the power of quantitative approaches is the implementation of genomic selection, which has recently revolutionized animal breeding. Genomic selection is now being applied to both hybrid and inbred crops and is likely to be the major source of improvement in plant breeding practice over the next decade. Breeders’ ability to efficiently apply genomic selection methodologies is due to recent technology advances in genotyping and sequencing. Furthermore, targeted integration of additional molecular data (such as gene expression, gene copy number and methylation status) into genomic prediction models may increase their performance. In this review, we discuss and contextualize a suite of established quantitative genetics themes relating to hybrid vigour, transgressive segregation and their central relevance to plant breeding, with the aim of informing crop researchers outside of the quantitative genetics discipline of their relevance and importance to crop improvement. Better understanding between molecular and quantitative disciplines will increase the potential for further improvements in plant breeding methodologies and so help underpin future food security.     

Heterosis in age‐specific selected populations of a seed beetle: Sex differences in longevity and reproductive behavior

We tested mutation accumulation hypothesis for the evolution of senescence using short‐lived and long‐lived populations of the seed‐feeding beetle, Acanthoscelides obtectus (Say), obtained by selection on early‐ and late‐life for many generations. The expected consequence of the mutation accumulation hypothesis is that in short‐lived populations, where the force of natural selection is the strongest early in life, the late‐life fitness traits should decline due to genetic drift which increases the frequency of mutations with deleterious effects in later adult stages. Since it is unlikely that identical deleterious mutations will increase in several independent populations, hybrid vigor for late‐life fitness is expected in offspring obtained in crosses among populations selected for early‐life fitness traits. We tested longevity of both sexes, female fecundity and male reproductive behavior for hybrid vigor by comparing hybrid and nonhybrid short‐lived populations. Hybrid vigor was confirmed for male virility, mating speed and copulation duration, and longevity of both sexes at late ages. In contrast to males, the results on female fecundity in short‐lived populations did not support mutation accumulation as a genetic mechanism for the evolution of this trait. Contrary to the prediction of this hypothesis, male mating ability indices and female fecundity in long‐lived populations exhibited hybrid vigor at all assayed age classes. We demonstrate that nonhybrid long‐lived populations diverged randomly regarding female and male reproductive fitness, indicating that sexually antagonistic selection, when accompanied with genetic drift for female fecundity and male virility, might be responsible for overriding natural selection in the independently evolving long‐lived populations.     

The relative effects of mutation accumulation versus inbreeding depression on fitness in experimental populations of the housefly

Loss of fitness due to inbreeding depression in small captive populations of endangered species is widely appreciated. Populations of all sizes may also experience loss in fitness when environmental conditions are ameliorated because deleterious alleles may be rendered neutral and accumulate rapidly. Few data exist, however, to demonstrate loss in fitness due to relaxed selection. Loss of fitness in life‐history traits were compared between LARGE (N_e ≥ 500) and SMALL (N_e = 50) populations of the housefly Musca domestica L that were subjected to curtailed life span at 21 days to remove selection on late‐acting deleterious alleles. During the early part of the life history (≤21 days), the rate of decline in fecundity and progeny production over 24 generations was greater in the small (1.5%) than in the large populations <0.2%), but rate of loss in late‐life fecundity and progeny production (>21 days) was equivalent across populations, consistent with neutral theory, and amounted to 1.7% per generation. This rate of loss due to relaxed selection was equivalent to the rate of loss due to inbreeding in populations with an effective size of 50 individuals. Even if captive populations are kept large to avoid inbreeding, breeding them in benign environments where the forces of natural selection are curtailed may jeopardize the capability of these populations to exist in natural environments within few generations. Zoo Biol 20:145–156, 2001. © 2001 Wiley‐Liss, Inc.     

Estimating the ratio of effective to actual size of an age‐structured population from individual demographic data

The effective population size is a central concept for understanding evolutionary processes in a finite population. We employ Fisher's reproductive value to estimate the ratio of effective to actual population size for an age‐structured population with two sexes using random samples of individual vital rates. The population may be subject to environmental stochasticity affecting the vital rates. When the mean sex ratio at birth is known, improved efficiency is obtained by utilizing the records of total number of offspring rather than considering separately female and male offspring. We also show how to incorporate uncertain paternity.     

Demography,life history and the evolution of age‐dependent social behaviour

Since the inception of modern social evolution theory, a vast majority of studies have sought to explain cooperation using relatedness‐driven hypotheses. Natural populations, however, show a substantial amount of variation in social behaviour that is uncorrelated with relatedness. Age offers a major alternative explanation for variation in behaviour that remains unaccounted for. Most natural populations are structured into age‐classes, with ageing being a nearly universal feature of most major taxa, including eukaryotic and prokaryotic organisms. Despite this, the theoretical underpinnings of age‐dependent social behaviour remain limited. Here, I investigate how group age‐composition, demography and life history shape trajectories of age‐dependent behaviours that are expressed conditionally on an actor and recipient's age. I show that demography introduces novel age‐dependent selective pressures acting on social phenotypes. Furthermore, I find that life history traits influence the costs and benefits of cooperation directly, but also indirectly. Life history has a strong impact not only on the genetic structure of the population but also on the distribution of group age‐compositions, with both of these processes influencing the expression of age‐dependent cooperation. Age of peak reproductive performance, in particular, is of chief importance for the evolution of cooperation, as this will largely determine the age and relatedness of social partners. Moreover, my results suggest that later‐life reproductive senescence may occur because of demographic effects alone, which opens new vistas on the evolution of menopause and related phenomena.     

Genetic decline and inbreeding depression in an extremely rare tree

Many endangered species have small population sizes, with less than 10 remaining individuals in some extreme situations. Although the consequences of a small population size have received considerable research attention, few studies have examined the fate of extremely rare plants. Ostrya rehderiana is one such species, with only 5 naturally-regenerated surviving individuals and less than 150 artificially-regenerated progeny. Using amplified fragment length polymorphisms (AFLPs), we found that there was a low percentage of polymorphic loci but moderate heterozygosity in the 5 wild individuals. A severe decline in genetic diversity was observed in the progeny, with a decrease of 36.7% in heterozygosity and of 12% in the number of markers that were amplified per individual compared with the parental generation, a result which was caused by genetic drift and inbreeding. The effective population size was estimated to be 1. A significant positive relationship between parental genetic dissimilarity and the number of surviving offspring was observed, which indicated that inbreeding depression might have purged more inbred offspring. Implications for protection and recovery of the genetic variation of extremely rare plants, such as O. rehderiana, are proposed.     

Using heterozygosity–fitness correlations to study inbreeding depression in an isolated population of white‐tailed deer founded by few individuals

A heterozygosity–fitness correlations (HFCs) may reflect inbreeding depression, but the extent to which they do so is debated. HFCs are particularly likely to occur after demographic disturbances such as population bottleneck or admixture. We here study HFC in an introduced and isolated ungulate population of white‐tailed deer Odocoileus virginianus in Finland founded in 1934 by four individuals. A total of 422 ≥ 1‐year‐old white‐tailed deer were collected in the 2012 hunting season in southern Finland and genotyped for 14 microsatellite loci. We find significant identity disequilibrium as estimated by g₂. Heterozygosity was positively associated with size‐ and age‐corrected body mass, but not with jaw size or (in males) antler score. Because of the relatively high identity disequilibrium, heterozygosity of the marker panel explained 51% of variation in inbreeding. Inbreeding explained approximately 4% of the variation in body mass and is thus a minor, although significant source of variation in body mass in this population. The study of HFC is attractive for game‐ and conservation‐oriented wildlife management because it presents an affordable and readily used approach for genetic monitoring that allowing identification of fitness costs associated with genetic substructuring in what may seem like a homogeneous population.     

Antagonistic pleiotropy and mutation accumulation contribute to age‐related decline in stress response

As organisms age, the effectiveness of natural selection weakens, leading to age‐related decline in fitness‐related traits. The evolution of age‐related changes associated with senescence is likely influenced by mutation accumulation (MA) and antagonistic pleiotropy (AP). MA predicts that age‐related decline in fitness components is driven by age‐specific sets of alleles, nonnegative genetic correlations within trait across age, and an increase in the coefficient of genetic variance. AP predicts that age‐related decline in a trait is driven by alleles with positive effects on fitness in young individuals and negative effects in old individuals, and is expected to lead to negative genetic correlations within traits across age. We build on these predictions using an association mapping approach to investigate the change in additive effects of SNPs across age and among traits for multiple stress‐response fitness‐related traits, including cold stress with and without acclimation and starvation resistance. We found support for both MA and AP theories of aging in the age‐related decline in stress tolerance. Our study demonstrates that the evolution of age‐related decline in stress tolerance is driven by a combination of alleles that have age‐specific additive effects, consistent with MA, as well as nonindependent and antagonistic genetic architectures characteristic of AP.     

Cryptic inbreeding depression in a growing population of a long‐lived species

Genetic effects are often overlooked in endangered species monitoring, and populations showing positive growth are often assumed to be secure. However, the continued reproductive success of a few individuals may mask issues such as inbreeding depression, especially in long‐lived species. Here, we test for inbreeding depression in little spotted kiwi (Apteryx owenii) by comparing a population founded with two birds to one founded with 40 birds, both from the same source population and both showing positive population growth. We used a combination of microsatellite genotypes, nest observations and modelling to examine the consequences of assessing population viability exclusively via population growth. We demonstrate (i) significantly lower hatching success despite significantly higher reproductive effort in the population with two founders; (ii) positive growth in the population with two founders is mainly driven by ongoing chick production of the founding pair; and (iii) a substantial genetic load in the population founded with two birds (10–15 diploid lethal equivalents). Our results illustrate that substantial, cryptic inbreeding depression may still be present when a population is growing, especially in long‐lived species with overlapping generations.     

spip 1.0: a program for simulating pedigrees and genetic data in age‐structured populations

We present the program spip for simulating multilocus genetic data on individuals in age‐structured populations. In addition to genetic data on sampled individuals, the pedigree connecting all individuals in the population is recorded. This allows investigation of the relationship between family structure and population parameters. We foresee that spip will be useful for evaluating multilocus estimators of pairwise relatedness and population structure, and for simulating the distribution of relatedness in populations with varying demographies. It also provides a method for simulating genetic drift in complex populations.     

Heterosis and inbreeding depression in bottlenecked populations: a test in the hermaphroditic freshwater snail Lymnaea stagnalis

Small population size is expected to induce heterosis, due to the random fixation and accumulation of mildly deleterious mutations, whereas within‐population inbreeding depression should decrease due to increased homozygosity. Population bottlenecks, although less effective, may have similar consequences. We tested this hypothesis in the self‐fertile freshwater snail Lymnaea stagnalis, by subjecting experimental populations to a single bottleneck of varied magnitude. Although patterns were not strong, heterosis was significant in the most severely bottlenecked populations, under stressful conditions. This was mainly due to hatching rate, suggesting that early acting and highly deleterious alleles were involved. Although L. stagnalis is a preferential outcrosser, inbreeding depression was very low and showed no clear relationship with bottleneck size. In the less reduced populations, inbreeding depression for hatching success increased under high inbreeding. This may be consistent with the occurence of synergistic epistasis between fitness loci, which may contribute to favour outcrossing in L. stagnalis.