Genome-wide allele frequency changes reveal that dynamic metapopulations evolve differently.

Two important characteristics of metapopulations are extinction-(re)colonization dynamics and gene flow between subpopulations. These processes can cause strong shifts in genome-wide allele frequencies that are generally not observed in "classical" (large, stable, panmictic) populations. Subpopulations founded by one or a few individuals, the so-called propagule model, are initially expected to show intermediate allele frequencies at polymorphic sites until natural selection and genetic drift drive allele frequencies toward a mutation-selection-drift equilibrium characterized by a negative exponential-like distribution of the site frequency spectrum (SFS). We followed changes in SFS distribution in a natural metapopulation of the cyclically parthenogenetic pond-dwelling microcrustacean Daphnia magna using biannual pool-seq samples collected over a five-year period from 118 ponds occupied by subpopulations of known age. As expected under the propagule model, SFSs in newly founded subpopulations trended toward intermediate allele frequencies and shifted toward right skewed distributions as the populations aged. Immigration and subsequent hybrid vigor altered this dynamic. We show that the analysis of SFS dynamics is a powerful approach to understand evolution in metapopulations. It allowed us to disentangle evolutionary processes occurring in a natural metapopulation, where many subpopulations evolve in parallel. Thereby, stochastic processes like founder and immigration events lead to a pattern of subpopulation divergence, while genetic drift, leads to converging SFS distributions in the persisting subpopulations. The observed processes are well explained by the propagule model and highlight that metapopulations evolve differently from classical populations.

Genetic Drift Shapes the Evolution of a Highly Dynamic Metapopulation.

The dynamics of extinction and (re)colonization in habitat patches are characterizing features of dynamic metapopulations, causing them to evolve differently than large, stable populations. The propagule model, which assumes genetic bottlenecks during colonization, posits that newly founded subpopulations have low genetic diversity and are genetically highly differentiated from each other. Immigration may then increase diversity and decrease differentiation between subpopulations. Thus, older and/or less isolated subpopulations are expected to have higher genetic diversity and less genetic differentiation. We tested this theory using whole-genome pool-sequencing to characterize nucleotide diversity and differentiation in 60 subpopulations of a natural metapopulation of the cyclical parthenogen Daphnia magna. For comparison, we characterized diversity in a single, large, and stable D. magna population. We found reduced (synonymous) genomic diversity, a proxy for effective population size, weak purifying selection, and low rates of adaptive evolution in the metapopulation compared with the large, stable population. These differences suggest that genetic bottlenecks during colonization reduce effective population sizes, which leads to strong genetic drift and reduced selection efficacy in the metapopulation. Consistent with the propagule model, we found lower diversity and increased differentiation in younger and also in more isolated subpopulations. Our study sheds light on the genomic consequences of extinction-(re)colonization dynamics to an unprecedented degree, giving strong support for the propagule model. We demonstrate that the metapopulation evolves differently from a large, stable population and that evolution is largely driven by genetic drift.

Genetic control of male production in Daphnia pulex.

Daphnia normally reproduce by cyclical parthenogenesis, with offspring sex being determined by environmental cues. However, some females have lost the ability to produce males. Our results demonstrate that this loss of male-producing ability is controlled by a dominant allele at a single locus. We identified the locus by comparing whole-genome sequences of 67 nonmale-producing (NMP) and 100 male-producing (MP) clones from 5 Daphnia pulex populations, revealing 132 NMP-linked SNPs and 59 NMP-linked indels within a single 1.1-Mb nonrecombining region on chromosome I. These markers include 7 nonsynonymous mutations, all of which are located within one unannotated protein-coding gene (gene 8960). Within this single gene, all of the marker-linked NMP haplotypes from different populations form a monophyletic clade, suggesting a single origin of the NMP phenotype, with the NMP haplotype originating by introgression from a sister species, Daphnia pulicaria Methyl farnesoate (MF) is the innate juvenile hormone in daphnids, which induces the production of males and whose inhibition results in female-only production. Gene 8960 is sensitive to treatment by MF in MP clones, but such responsiveness is greatly reduced in NMP clones. Thus, we hypothesize that gene 8960 is located downstream of the MF-signaling pathway in D. pulex, with the NMP phenotype being caused by expression change of gene 8960.

Sex ratio effects on reproductive success of male and female Daphnia.

The intensity of mating competition and the opportunity for sexual selection are thought to depend on the operational sex ratio, the ratio of sexually active males to fertilizable females. Cyclic parthenogens, organisms that alternate between sexual reproduction and female-only parthenogenesis, show particularly high variation in sex ratios in natural populations but the effects of this variation on mating competition and reproductive success of each sex are poorly understood. In a series of experiments with Daphnia magna, we experimentally imposed five sex ratio categories, varying from one male per 81 females to an even sex ratio. We found that, in males, reproductive success strongly and monotonically decreased with decreasing number of females per male. In females, in contrast, mating success and reproductive success were reduced only at the most female-biased sex ratio (1:81), when many females remained unmated and unfertilized, and then again at equal sex ratios, probably due to negative effects of high density or stress induced by numerous males. Our results suggest that females experienced male limitation at heavily female-biased sex ratios below one male to about 50 females. As this is well within the sex ratio variation observed in natural Daphnia populations, we conclude that mating competition and the opportunity for sexual selection may exist not only in males but, at least periodically, also in females.

Evolution of Gene Expression during a Transition from Environmental to Genetic Sex Determination.

Genetic sex determination (GSD) can evolve from environmental sex determination (ESD) via an intermediate state in which both coexist in the same population. Such mixed populations are found in the crustacean Daphnia magna, where non-male producers (NMP, genetically determined females) coexist with male producers (MP), in which male production is environmentally inducible and can also artificially be triggered by exposure to juvenile hormone. This makes Daphnia magna a rare model species for the study of evolutionary transitions from ESD to GSD. Although the chromosomal location of the NMP-determining mutation has been mapped, the actual genes and pathways involved in the evolution of GSD from ESD remain unknown. Here, we present a transcriptomic analysis of MP and NMP females under control (female producing) and under hormone exposure conditions. We found ∼100 differentially expressed genes between MP and NMP under control conditions. Genes in the NMP-determining chromosome region were especially likely to show such constitutive expression differences. Hormone exposure led to expression changes of an additional ∼100 (MP) to ∼600 (NMP) genes, with an almost systematic upregulation of those genes in NMP. These observations suggest that the NMP phenotype is not determined by a simple "loss-of-function" mutation. Rather, homeostasis of female offspring production under hormone exposure appears to be an active state, tightly regulated by complex mechanisms involving many genes. In a broader view, this illustrates that the evolution of GSD, while potentially initiated by a single mutation, likely leads to secondary integration involving many genes and pathways.

How clonal are clones? A quest for loss of heterozygosity during asexual reproduction in Daphnia magna.

Due to the lack of recombination, asexual organisms are predicted to accumulate mutations and show high levels of within-individual allelic divergence (heterozygosity); however, empirical evidence for this prediction is largely missing. Instead, evidence of genome homogenization during asexual reproduction is accumulating. Ameiotic crossover recombination is a mechanism that could lead to long genomic stretches of loss of heterozygosity (LOH) and unmasking of mutations that have little or no effect in heterozygous state. Therefore, LOH might be an important force for inducing variation among asexual offspring and may contribute to the limited longevity of asexual lineages. To investigate the genetic consequences of asexuality, here we used high-throughput sequencing of Daphnia magna for assessing the rate of LOH over a single generation of asexual reproduction. Comparing parthenogenetic daughters with their mothers at several thousand genetic markers generated by restriction site-associated DNA (RAD) sequencing resulted in high LOH rate estimation that largely overlapped with our estimates for the error rate. To distinguish these two, we Sanger re-sequenced the top 17 candidate RAD-loci for LOH, and all of them proved to be false positives. Hence, even though we cannot exclude the possibility that short stretches of LOH occur in genomic regions not covered by our markers, we conclude that LOH does not occur frequently during asexual reproduction in D. magna and ameiotic crossovers are very rare or absent. This finding suggests that clonal lineages of D. magna will remain genetically homogeneous at least over time periods typically relevant for experimental work.

Transition from Environmental to Partial Genetic Sex Determination in Daphnia through the Evolution of a Female-Determining Incipient W Chromosome.

Sex chromosomes can evolve during the evolution of genetic sex determination (GSD) from environmental sex determination (ESD). Despite theoretical attention, early mechanisms involved in the transition from ESD to GSD have yet to be studied in nature. No mixed ESD-GSD animal species have been reported, except for some species of Daphnia, small freshwater crustaceans in which sex is usually determined solely by the environment, but in which a dominant female sex-determining locus is present in some populations. This locus follows Mendelian single-locus inheritance, but has otherwise not been characterized genetically. We now show that the sex-determining genomic region maps to the same low-recombining peri-centromeric region of linkage group 3 (LG3) in three highly divergent populations of D. magna, and spans 3.6 Mb. Despite low levels of recombination, the associated region contains signs of historical recombination, suggesting a role for selection acting on several genes thereby maintaining linkage disequilibrium among the 36 associated SNPs. The region carries numerous genes involved in sex differentiation in other taxa, including transformer2 and sox9. Taken together, the region determining the genetic females shows characteristics of a sex-related supergene, suggesting that LG3 is potentially an incipient W chromosome despite the lack of significant additional restriction of recombination between Z and W. The occurrence of the female-determining locus in a pre-existing low recombining region illustrates one possible form of recombination suppression in sex chromosomes. D. magna is a promising model for studying the evolutionary transitions from ESD to GSD and early sex chromosome evolution.

Chromosomal rearrangements maintain a polymorphic supergene controlling butterfly mimicry.

Supergenes are tight clusters of loci that facilitate the co-segregation of adaptive variation, providing integrated control of complex adaptive phenotypes. Polymorphic supergenes, in which specific combinations of traits are maintained within a single population, were first described for 'pin' and 'thrum' floral types in Primula and Fagopyrum, but classic examples are also found in insect mimicry and snail morphology. Understanding the evolutionary mechanisms that generate these co-adapted gene sets, as well as the mode of limiting the production of unfit recombinant forms, remains a substantial challenge. Here we show that individual wing-pattern morphs in the polymorphic mimetic butterfly Heliconius numata are associated with different genomic rearrangements at the supergene locus P. These rearrangements tighten the genetic linkage between at least two colour-pattern loci that are known to recombine in closely related species, with complete suppression of recombination being observed in experimental crosses across a 400-kilobase interval containing at least 18 genes. In natural populations, notable patterns of linkage disequilibrium (LD) are observed across the entire P region. The resulting divergent haplotype clades and inversion breakpoints are found in complete association with wing-pattern morphs. Our results indicate that allelic combinations at known wing-patterning loci have become locked together in a polymorphic rearrangement at the P locus, forming a supergene that acts as a simple switch between complex adaptive phenotypes found in sympatry. These findings highlight how genomic rearrangements can have a central role in the coexistence of adaptive phenotypes involving several genes acting in concert, by locally limiting recombination and gene flow.

A high-density genetic map reveals variation in recombination rate across the genome of Daphnia magna.

BACKGROUND: Recombination rate is an essential parameter for many genetic analyses. Recombination rates are highly variable across species, populations, individuals and different genomic regions. Due to the profound influence that recombination can have on intraspecific diversity and interspecific divergence, characterization of recombination rate variation emerges as a key resource for population genomic studies and emphasises the importance of high-density genetic maps as tools for studying genome biology. Here we present such a high-density genetic map for Daphnia magna, and analyse patterns of recombination rate across the genome. RESULTS: A F2 intercross panel was genotyped by Restriction-site Associated DNA sequencing to construct the third-generation linkage map of D. magna. The resulting high-density map included 4037 markers covering 813 scaffolds and contigs that sum up to 77 % of the currently available genome draft sequence (v2.4) and 55 % of the estimated genome size (238 Mb). Total genetic length of the map presented here is 1614.5 cM and the genome-wide recombination rate is estimated to 6.78 cM/Mb. Merging genetic and physical information we consistently found that recombination rate estimates are high towards the peripheral parts of the chromosomes, while chromosome centres, harbouring centromeres in D. magna, show very low recombination rate estimates. CONCLUSIONS: Due to its high-density, the third-generation linkage map for D. magna can be coupled with the draft genome assembly, providing an essential tool for genome investigation in this model organism. Thus, our linkage map can be used for the on-going improvements of the genome assembly, but more importantly, it has enabled us to characterize variation in recombination rate across the genome of D. magna for the first time. These new insights can provide a valuable assistance in future studies of the genome evolution, mapping of quantitative traits and population genetic studies.

Genes mirror geography in Daphnia magna.

Identifying the presence and magnitude of population genetic structure remains a major consideration in evolutionary biology as doing so allows one to understand the demographic history of a species as well as make predictions of how the evolutionary process will proceed. Next-generation sequencing methods allow us to reconsider previous ideas and conclusions concerning the distribution of genetic variation, and what this distribution implies about a given species evolutionary history. A previous phylogeographic study of the crustacean Daphnia magna suggested that, despite strong genetic differentiation among populations at a local scale, the species shows only moderate genetic structure across its European range, with a spatially patchy occurrence of individual lineages. We apply RAD sequencing to a sample of D. magna collected across a wide swath of the species' Eurasian range and analyse the data using principle component analysis (PCA) of genetic variation and Procrustes analytical approaches, to quantify spatial genetic structure. We find remarkable consistency between the first two PCA axes and the geographic coordinates of individual sampling points, suggesting that, on a continent-wide scale, genetic differentiation is driven to a large extent by geographic distance. The observed pattern is consistent with unimpeded (i.e. no barriers, landscape or otherwise) migration at large spatial scales, despite the fragmented and patchy nature of favourable habitats at local scales. With high-resolution genetic data similar patterns may be uncovered for other species with wide geographic distributions, allowing an increased understanding of how genetic drift and selection have shaped their evolutionary history.

Local adaptation of sex induction in a facultative sexual crustacean: insights from QTL mapping and natural populations of Daphnia magna.

Dormancy is a common adaptation in invertebrates to survive harsh conditions. Triggered by environmental cues, populations produce resting eggs that allow them to survive temporally unsuitable conditions. Daphnia magna is a crustacean that reproduces by cyclical parthenogenesis, alternating between the production of asexual offspring and the sexual reproduction of diapausing eggs (ephippia). Prior to ephippia production, males (necessary to ensure ephippia fertilization) are produced parthenogenetically. Both the production of ephippia and the parthenogenetic production of males are induced by environmental factors. Here, we test the hypothesis that the induction of D. magna resting egg production shows a signature of local adaptation. We postulated that Daphnia from permanent ponds would produce fewer ephippia and males than Daphnia from intermittent ponds and that the frequency and season of habitat deterioration would correlate with the timing and amount of male and ephippia production. To test this, we quantified the production of males and ephippia in clonal D. magna populations in several different controlled environments. We found that the production of both ephippia and males varies strongly among populations in a way that suggests local adaptation. By performing quantitative trait locus mapping with parent clones from contrasting pond environments, we identified nonoverlapping genomic regions associated with male and ephippia production. As the traits are influenced by two different genomic regions, and both are necessary for successful resting egg production, we suggest that the genes for their induction co-evolve.

No recombination suppression in asexually produced males of Daphnia pulex.

Obligate parthenogenesis (OP) is often thought to evolve by disruption of reductional meiosis and suppression of crossover recombination. In the crustacean Daphnia pulex, OP lineages, which have evolved from cyclical parthenogenetic (CP) ancestors, occasionally produce males that are capable of reductional meiosis. Here, by constructing high-density linkage maps, we find that these males show only slightly and nonsignificantly reduced recombination rates compared to CP males and females. Both meiosis disruption and recombination suppression are therefore sex-limited (or partly so), which speaks against the evolution of OP by disruption of a gene that is essential for meiosis or recombination in both sexes. The findings may be explained by female-limited action of genes that suppress recombination, but previously identified candidate genes are known to be expressed in both sexes. Alternatively, and equally consistent with the data, OP might have evolved through a reuse of the parthenogenesis pathways already present in CP and through their extension to all events of oogenesis. The causal mutations for the CP to OP transition may therefore include mutations in genes involved in oogenesis regulation and may not necessarily be restricted to genes of the "meiosis toolkit." More generally, our study emphasizes that there are many ways to achieve asexuality, and elucidating the possible mechanisms is key to ultimately identify the genes and traits involved.

Asexual male production by ZW recombination in Artemia parthenogenetica.

In some asexual species, parthenogenetic females occasionally produce males, which may strongly affect the evolution and maintenance of asexuality if they cross with related sexuals and transmit genes causing asexuality to their offspring ("contagious parthenogenesis"). How these males arise in the first place has remained enigmatic, especially in species with sex chromosomes. Here, we test the hypothesis that rare, asexually produced males of the crustacean Artemia parthenogenetica are produced by recombination between the Z and W sex chromosomes during non-clonal parthenogenesis, resulting in ZZ males through loss of heterozygosity at the sex determination locus. We used RAD-sequencing to compare asexual mothers with their male and female offspring. Markers on several sex-chromosome scaffolds indeed lost heterozygosity in all male but no female offspring, suggesting that they correspond to the sex-determining region. Other sex-chromosome scaffolds lost heterozygosity in only a part of the male offspring, consistent with recombination occurring at a variable location. Alternative hypotheses for the production of these males (such as partial or total hemizygosity of the Z) could be excluded. Rare males are thus produced because recombination is not entirely suppressed during parthenogenesis in A. parthenogenetica. This finding may contribute to explaining the maintenance of recombination in these asexuals.

Genetic estimates of population age in the water flea, Daphnia magna.

Genetic datasets can be used to date evolutionary events, even on recent time scales if sufficient data are available. We used statistics calculated from multilocus microsatellite datasets to estimate population ages in data generated through coalescent simulations and in samples from populations of known age in a metapopulation of Daphnia magna in Finland. Our simulation results show that age estimates improve with additional loci and define a time frame over which these statistics are most useful. On the most recent time scales, assumptions regarding the model of mutation (infinite sites vs. stepwise mutation) have little influence on estimated ages. In older populations, size homoplasy among microsatellite alleles results in a downwards bias for estimates based on the infinite sites model (ISM). In the Finnish D. magna metapopulation, our genetically derived estimated ages were biased upwards. Potential sources of this bias include the underlying model of mutation, gene flow, founder size, and the possibility of persistent source populations in the system. Our simulated data show that genetic age estimation is possible, even for very young populations, but our empirical data highlight the importance of factors such as migration when these statistics are applied in natural populations.

Nucleotide polymorphism at a gene (Pgi) under balancing selection in a butterfly metapopulation.

The Glanville fritillary butterfly (Melitaea cinxia, Nymphalidae) has a large, well-studied metapopulation in the Aland Islands in Finland. Previous studies have found that the common allozyme genotypes at the phosphoglucose isomerase (PGI) locus are associated with individual variation in performance and fitness, with phenotypic data suggesting ongoing balancing selection via heterozygote advantage. Here, we analyze nucleotide polymorphism in the coding region of the Pgi gene. Pgi is exceptionally polymorphic, in contrast to three other metabolic genes (Mdh, Idh, and Gapdh) with low levels of polymorphism. Most of the variation is due to two common haplotype clades, which are highly divergent and exhibit extensive linkage disequilibrium. These two clades correspond to the two most common allozyme alleles previously studied. Molecular tests of selection and coalescence simulations indicate that patterns of nucleotide polymorphism depart from neutrality and are consistent with long-term balancing selection. The split between the two main haplotype clades is estimated to predate the last common ancestor of a clade of five extant Melitaea species. Comparative structural analysis of Pgi polymorphism in M. cinxia and the unrelated Colias eurytheme butterfly suggests a similar but not identical target of balancing selection. Our results indicate convergent evolution between these two species at both the phenotypic and molecular levels.

Not so clonal asexuals: Unraveling the secret sex life of Artemia parthenogenetica.

The maintenance of sex is paradoxical as sexual species pay the "twofold cost of males" and should thus quickly be replaced by asexual mutants reproducing clonally. However, asexuals may not be strictly clonal and engage in "cryptic sex," challenging this simple scenario. We study the cryptic sex life of the brine shrimp Artemia parthenogenetica, which has once been termed an "ancient asexual" and where no genetic differences have ever been observed between parents and offspring. This asexual species rarely produces males, which can hybridize with sexual females of closely related species and transmit asexuality to their offspring. Using such hybrids, we show that recombination occurs in asexual lineages, causing loss-of-heterozygosity and parent-offspring differences. These differences cannot generally be observed in field-sampled asexuals because once heterozygosity is lost, subsequent recombination leaves no footprint. Furthermore, using extensive paternity tests, we show that hybrid females can reproduce both sexually and asexually, and transmit asexuality to both sexually and asexually produced offspring in a dominant fashion. Finally, we show that, contrary to previous reports, field-sampled asexual females also rarely reproduce sexually (rate ∼2‰). Overall, most previously known facts about Artemia asexuality turned out to be erroneous. More generally, our findings suggest that the evidence for strictly clonal reproduction of asexual species needs to be reconsidered, and that rare sex and consequences of nonclonal asexuality, such as gene flow within asexuals, need to be more widely taken into account in more realistic models for the maintenance of sex and the persistence of asexual lineages.

Nucleotide polymorphism and within-gene recombination in Daphnia magna and D. pulex, two cyclical parthenogens.

Theory predicts that partially asexual organisms may make the "best of both worlds": for the most part, they avoid the costs of sexual reproduction, while still benefiting from an enhanced efficiency of selection compared to obligately asexual organisms. There is, however, little empirical data on partially asexual organisms to test this prediction. Here we examine patterns of nucleotide diversity at eight nuclear loci in continentwide samples of two species of cyclically parthenogenetic Daphnia to assess the effect of partial asexual reproduction on effective population size and amount of recombination. Both species have high nucleotide diversities and show abundant evidence for recombination, yielding large estimates of effective population sizes (300,000-600,000). This suggests that selection will act efficiently even on mutations with small selection coefficients. Divergence between the two species is less than one-tenth of previous estimates, which were derived using a mitochondrial molecular clock. As the two species investigated are among the most distantly related species of the genus, this suggests that the genus Daphnia may be considerably younger than previously thought. Daphnia has recently received increased attention because it is being developed as a model organism for ecological and evolutionary genomics. Our results confirm the attractiveness of Daphnia as a model organism, because the high nucleotide diversity and low linkage disequilibrium suggest that fine-scale mapping of genes affecting phenotypes through association studies should be feasible.

Ecological differentiation between coexisting sexual and asexual strains of Daphnia pulex.

1. The widespread occurrence of sexual reproduction indicates that the benefits of sex can overcome its costs relative to asexual reproduction. Many closely related sexual and asexual taxa have different geographic distributions suggesting that their relative fitness may depend on the environment. However, support for such ecological differentiation is mainly based on correlative evidence, with experimental support being scarce, especially from the wild. 2. We studied ecological differentiation between asexual (obligate parthenogenetic) and sexual (cyclical parthenogenetic) Daphnia pulex in Southern Finland, where the two forms ('reproduction types') coexist regionally in a metapopulation. We found differences in several environmental factors between ponds inhabited by sexual and asexual populations (pH, calcium, oxygen, conductivity and absorbance). 3. A reciprocal competition experiment carried out directly in the natural ponds confirmed that sexuals and asexuals were ecologically differentiated; their relative fitness was found to depend on pH and calcium titres of the ponds. 4. Our study provides clear experimental evidence for the coexistence of closely related sexual and asexual taxa being mediated by ecological differentiation. In addition, the results of our competition experiment suggest that each of the reproduction types has a larger fundamental niche (absence of competition) than a realized niche (presence of competition). Thus, by temporarily creating competition-free space, metapopulation turnover may allow the reproduction types to occur in a wider range of habitats than under more stable population dynamics, and may thus further contribute to stabilize regional coexistence.

Parasite-driven replacement of a sexual by a closely related asexual taxon in nature.

Asexual species are thought to suffer more from coevolving parasites than related sexuals. Yet a variety of studies do not find the patterns predicted by theory. Here, to shine light on this conundrum, we investigate one such case of an asexual advantage in the presence of parasites. We follow the frequency dynamics of sexual and asexual Daphnia pulex in a natural pond that was initially dominated by sexuals. Coinciding with an epidemic of a microsporidian parasite infecting both sexuals and asexuals, the pond was rapidly taken over by the initially rare asexuals. With experiments comparing multiple sexual and asexual clones from across the local metapopulation, we confirm that asexuals are less susceptible and also suffer less from the parasite once infected. These results are consistent with the parasite-driven, ecological replacement of dominant sexuals by closely related, but more resistant asexuals, ultimately leading to the extinction of the formerly superior sexual competitor. Our study is one of the clearest examples from nature, backed up by experimental verification, showing a parasite-mediated reversal of competition dynamics. The experiments show that, across the metapopulation, asexuals have an advantage in the presence of parasites. In this metapopulation, asexuals are relatively rare, likely due to their recent invasion. While we cannot rule out other reasons for the observed patterns, the results are consistent with a temporary parasite-mediated advantage of asexuals due to the fact that they are rare, which is an underappreciated aspect of the Red Queen Hypothesis.

Genetic load in sexual and asexual diploids: segregation, dominance and genetic drift.

In diploid organisms, sexual reproduction rearranges allelic combinations between loci (recombination) as well as within loci (segregation). Several studies have analyzed the effect of segregation on the genetic load due to recurrent deleterious mutations, but considered infinite populations, thus neglecting the effects of genetic drift. Here, we use single-locus models to explore the combined effects of segregation, selection, and drift. We find that, for partly recessive deleterious alleles, segregation affects both the deterministic component of the change in allele frequencies and the stochastic component due to drift. As a result, we find that the mutation load may be far greater in asexuals than in sexuals in finite and/or subdivided populations. In finite populations, this effect arises primarily because, in the absence of segregation, heterozygotes may reach high frequencies due to drift, while homozygotes are still efficiently selected against; this is not possible with segregation, as matings between heterozygotes constantly produce new homozygotes. If deleterious alleles are partly, but not fully recessive, this causes an excess load in asexuals at intermediate population sizes. In subdivided populations without extinction, drift mostly occurs locally, which reduces the efficiency of selection in both sexuals and asexuals, but does not lead to global fixation. Yet, local drift is stronger in asexuals than in sexuals, leading to a higher mutation load in asexuals. In metapopulations with turnover, global drift becomes again important, leading to similar results as in finite, unstructured populations. Overall, the mutation load that arises through the absence of segregation in asexuals may greatly exceed previous predictions that ignored genetic drift.