A comparison of sexual and asexual replication strategies in a simplified model based on the yeast life cycle

This paper develops simplified mathematical models describing the mutation-selection balance for the asexual and sexual replication pathways in Saccharomyces cerevisiae, or Baker’s yeast. The simplified models are based on the single-fitness-peak approximation in quasispecies theory. We assume diploid genomes consisting of two chromosomes, and we assume that each chromosome is functional if and only if its base sequence is identical to some master sequence. The growth and replication of the yeast cells is modeled as a first-order process, with first-order growth rate constants that are determined by whether a given genome consists of zero, one, or two functional chromosomes. In the asexual pathway, we assume that a given diploid cell divides into two diploids. For the sake of generality, our model allows for mitotic recombination and asymmetric chromosome segregation. In the sexual pathway, we assume that a given diploid cell divides into two diploids, each of which then divide into two haploids. The resulting four haploids enter a haploid pool, where they grow and replicate until they meet another haploid with which to fuse. In the sexual pathway, we consider two mating strategies: (1) a selective strategy, where only haploids with functional chromosomes can fuse with one another; (2) a random strategy, where haploids randomly fuse with one another. When the cost for sex is low, we find that the selective mating strategy leads to the highest mean fitness of the population, when compared to all of the other strategies. When the cost for sex is low, sexual replication with random mating also has a higher mean fitness than asexual replication without mitotic recombination or asymmetric chromosome segregation. We also show that, at low replication fidelities, sexual replication with random mating has a higher mean fitness than asexual replication, as long as the cost for sex is low. If the fitness penalty for having a defective chromosome is sufficiently high and the cost for sex sufficiently low, then at low replication fidelities the random mating strategy has a mean fitness that is a factor of larger than the asexual mean fitness. We argue that for yeast, the selective mating strategy is the one that is closer to reality, which if true suggests that sex may provide a selective advantage under considerably more relaxed conditions than previous research has indicated. The results of this paper also suggest that S. cerevisiae switches from asexual to sexual replication when stressed, because stressful growth conditions provide an opportunity for the yeast to clear out deleterious mutations from their genomes. That being said, our model does not contradict theories for the evolution of sex that argue that sex evolved because it allows a population to more easily adapt to changing conditions.     

A quasispecies approach to the evolution of sexual replication in unicellular organisms

This study develops a simplified model describing the evolutionary dynamics of a population composed of obligate sexually and asexually reproducing, unicellular organisms. The model assumes that the organisms have diploid genomes consisting of two chromosomes, and that the sexual organisms replicate by first dividing into haploid intermediates, which then combine with other haploids, followed by the normal mitotic division of the resulting diploid into two new daughter cells. We assume that the fitness landscape of the diploids is analogous to the single-fitness-peak approach often used in single-chromosome studies. That is, we assume a master chromosome that becomes defective with just one point mutation. The diploid fitness then depends on whether the genome has zero, one, or two copies of the master chromosome. We also assume that only pairs of haploids with a master chromosome are capable of combining so as to produce sexual diploid cells, and that this process is described by second-order kinetics. We find that, in a range of intermediate values of the replication fidelity, sexually reproducing cells can outcompete asexual ones, provided the initial abundance of sexual cells is above some threshold value. The range of values where sexual reproduction outcompetes asexual reproduction increases with decreasing replication rate and increasing population density. We critically evaluate a common approach, based on a group selection perspective, used to study the competition between populations and show its flaws in addressing the evolution of sex problem.     

Diploidy and the selective advantage for sexual reproduction in unicellular organisms

This article develops mathematical models describing the evolutionary dynamics of both asexually and sexually reproducing populations of diploid unicellular organisms. The asexual and sexual life cycles are based on the asexual and sexual life cycles in Saccharomyces cerevisiae, Baker’s yeast, which normally reproduces by asexual budding, but switches to sexual reproduction when stressed. The mathematical models consider three reproduction pathways: (1) Asexual reproduction, (2) self-fertilization, and (3) sexual reproduction. We also consider two forms of genome organization. In the first case, we assume that the genome consists of two multi-gene chromosomes, whereas in the second case, we consider the opposite extreme and assume that each gene defines a separate chromosome, which we call the multi-chromosome genome. These two cases are considered to explore the role that recombination has on the mutation-selection balance and the selective advantage of the various reproduction strategies. We assume that the purpose of diploidy is to provide redundancy, so that damage to a gene may be repaired using the other, presumably undamaged copy (a process known as homologous recombination repair). As a result, we assume that the fitness of the organism only depends on the number of homologous gene pairs that contain at least one functional copy of a given gene. If the organism has at least one functional copy of every gene in the genome, we assume a fitness of 1. In general, if the organism has l homologous pairs that lack a functional copy of the given gene, then the fitness of the organism is κ _l . The κ _l are assumed to be monotonically decreasing, so that κ₀ = 1 > κ₁ > κ₂ > ⋯ > κ_∞ = 0. For nearly all of the reproduction strategies we consider, we find, in the limit of large N, that the mean fitness at mutation-selection balance is max{2 e^-m-1, 0} ,\hbox{max}\{2 e^{-\mu}-1, 0\} , where N is the number of genes in the haploid set of the genome, ε is the probability that a given DNA template strand of a given gene produces a mutated daughter during replication, and μ = Nε. The only exception is the sexual reproduction pathway for the multi-chromosomed genome. Assuming a multiplicative fitness landscape where κ _l  = α ^l for α ∈ (0, 1), this strategy is found to have a mean fitness that exceeds the mean fitness of all the other strategies. Furthermore, while other reproduction strategies experience a total loss of viability due to the steady accumulation of deleterious mutations once μ exceeds ln2 ,\ln 2 , no such transition occurs in the sexual pathway. Indeed, in the limit as α → 1 for the multiplicative landscape, we can show that the mean fitness for the sexual pathway with the multi-chromosomed genome converges to e ^−2μ, which is always positive. We explicitly allow for mitotic recombination in this study, which, in contrast to previous studies using different models, does not have any advantage over other asexual reproduction strategies. The results of this article provide a basis for understanding the selective advantage of the specific meiotic pathway that is employed by sexually reproducing organisms. The results of this article also suggest an explanation for why unicellular organisms such as Saccharomyces cerevisiae (Baker’s yeast) switch to a sexual mode of reproduction when stressed. While the results of this article are based on modeling mutation-propagation in unicellular organisms, they nevertheless suggest that, in more complex organisms with significantly larger genomes, sex is necessary to prevent the loss of viability of a population due to genetic drift. Finally, and perhaps most importantly, the results of this article demonstrate a selective advantage for sexual reproduction with fewer and much less restrictive assumptions than those of previous studies.     

Cost of interacting with sexual partners in a facultative sexual microbe

The widespread occurrence of sexual organisms despite the high costs of sex has long intrigued biologists. The best-known costs are the twofold cost of producing males and the cost associated with producing traits to attract mates and to interact with mating partners, such as exaggerated sexual behaviors and morphological modifications. These costs have been inferred from studies of plants and animals but are thought to be absent in facultative sexual microbes. Here, using the facultative sexual fungus Cryptococcus neoformans, I provide experimental evidence showing that: (i) interactions with active sexual partners can be costly for vegetative fitness in a facultative sexual microbe; (ii) this cost is positively correlated to mating ability; (iii) this cost is composed of at least two distinct components, the cost of producing mating signals that exert effects on mating partners and that associated with responding to active mating partners; and (iv) extended asexual reproduction can reduce both components of the cost. This cost must have been compensated for by the production of zygotes and sexual spores to allow the initial evolution and spread of sexual reproduction in eukaryotes.     

Facultative sexual reproduction under frequency-dependent selection on a single locus

The evolution of a facultative sexual strategy that simultaneously produced sexual and asexual individuals was studied theoretically, under negative frequency-dependence of fitness. The organism was considered to be diploid, characterized by two loci concerning fitness and determining sexual strategy, between which a certain degree of linkage existed. The locus concerning fitness was assumed to involve two alleles, resulting in three genotypes, the relative fitness of an individual being defined by a decreasing function of frequency of its own genotype on this locus in the population. The sexual reproductive strategy was considered to be determined by three alleles; asexual, obligate sexual and facultative sexual. Simulations under various linkages between loci and level of frequency dependence of fitness showed that a facultative sexual strategy was generally able to invade and increase in the population. In particular, when the level of frequency dependence was high to some degree, the facultative strain producing many sexual individuals tended to exclusively occupy the population. Namely, the frequency-dependent selection resulted in a predominance of obligate sexual strategy over asexual strategy, simultaneously causing a subordination of the former to the facultative sexual strategy. This indicated that the evolution of sex should be considered carefully with respect to the possibility of invasion of facultative sex.     

The genomic signature of sexual selection in the genetic diversity of the sex chromosomes and autosomes

Genomic levels of variation can help reveal the selective and demographic forces that have affected a species during its history. The relative amount of genetic diversity observed on the sex chromosomes as compared to the autosomes is predicted to differ among monogamous and polygynous species. Many species show departures from the expectation for monogamy, but it can be difficult to conclude that this pattern results from variation in mating system because forces other than sexual selection can act upon sex chromosome genetic diversity. As a critical test of the role of mating system, we compared levels of genetic diversity on the Z chromosome and autosomes of phylogenetically independent pairs of shorebirds that differed in their mating systems. We found general support for sexual selection shaping sex chromosome diversity because most polygynous species showed relatively reduced genetic variation on their Z chromosomes as compared to monogamous species. Differences in levels of genetic diversity between the sex chromosomes and autosomes may therefore contribute to understanding the long-term history of sexual selection experienced by a species.     

Antagonism between sexual and natural selection in experimental populations of Saccharomyces cerevisiae

Trade-offs between life-history components are a central concept of evolution and ecology. Sexual and natural selection seem particularly apt to impose antagonistic selective pressures. When sex is not integrated into reproduction, as in Saccharomyces cerevisiae, natural selection can impair or even eliminate it. In this study, a genetic trade-off between the sexual and asexual phases of the yeast life cycle was suggested by sharp declines in the mating and sporulation abilities of unrelated genotypes that were propagated asexually in minimal growth medium and in mice. When sexual selection was applied to populations that had previously evolved asexually, sexual fitness increased but asexual fitness declined. No such negative correlation was observed when sexual selection was applied to an ancestral strain: sexual and asexual fitness both increased. Thus, evolutionary history affected the evolution of genetic correlations, as fitness increases in a population already well adapted to the environment were more likely to come at the expense of sexual functions.     

Genetic variation and asexual reproduction in the facultatively parthenogenetic cockroach Nauphoeta cinerea: implications for the evolution of sex

Asexual reproduction could offer up to a two‐fold fitness advantage over sexual reproduction, yet higher organisms usually reproduce sexually. Even in facultatively parthenogenetic species, where both sexual and asexual reproduction is sometimes possible, asexual reproduction is rare. Thus, the debate over the evolution of sex has focused on ecological and mutation‐elimination advantages of sex. An alternative explanation for the predominance of sex is that it is difficult for an organism to accomplish asexual reproduction once sexual reproduction has evolved. Difficulty in returning to asexuality could reflect developmental or genetic constraints. Here, we investigate the role of genetic factors in limiting asexual reproduction in Nauphoeta cinerea, an African cockroach with facultative parthenogenesis that nearly always reproduces sexually. We show that when N. cinerea females do reproduce asexually, offspring are genetically identical to their mothers. However, asexual reproduction is limited to a nonrandom subset of the genotypes in the population. Only females that have a high level of heterozygosity are capable of parthenogenetic reproduction and there is a strong familial influence on the ability to reproduce parthenogenetically. Although the mechanism by which genetic variation facilitates asexual reproduction is unknown, we suggest that heterosis may facilitate the switch from producing haploid meiotic eggs to diploid, essentially mitotic, eggs.     

Emergence and Maintenance of Sex among Diploid Organisms Aided by Assortative Mating

Using computer simulations I studied the simultaneous effect of variable environments, mutation rates, ploidy, number of loci subject to evolution and random and assortative mating on various reproductive systems. The simulations showed that mutants for sex and recombination are evolutionarily stable, displacing alleles for monosexuality in diploid populations mating assortatively under variable selection pressure. Assortative mating reduced excessive allelic variance induced by recombination and sex, especially among diploids. Results suggest a novel adaptive value for sex and recombination. They show that the adaptive value of diploidy and that of the segregation of sexes is different to that of sex and recombination. The results suggest that the emergence of sex had to be preceded by the emergence of diploid monosexual organisms and provide an explanation for the emergence and maintenance of sex among diploids and for the scarcity of sex among haploid organisms.     

Stabilizing selection,mutational bias,and the evolution of sex*

Stabilizing selection around a fixed phenotypic optimum is expected to disfavor sexual reproduction, since asexually reproducing organisms can maintain a higher fitness at equilibrium, while sex disrupts combinations of compensatory mutations. This conclusion rests on the assumption that mutational effects on phenotypic traits are unbiased, that is, mutation does not tend to push phenotypes in any particular direction. In this article, we consider a model of stabilizing selection acting on an arbitrary number of polygenic traits coded by bialellic loci, and show that mutational bias may greatly reduce the mean fitness of asexual populations compared with sexual ones in regimes where mutations have weak to moderate fitness effects. Indeed, mutation and drift tend to push the population mean phenotype away from the optimum, this effect being enhanced by the low effective population size of asexual populations. In a second part, we present results from individual‐based simulations showing that positive rates of sex are favored when mutational bias is present, while the population evolves toward complete asexuality in the absence of bias. We also present analytical (QLE) approximations for the selective forces acting on sex in terms of the effect of sex on the mean and variance in fitness among offspring.     

To self or not to self? Absence of mate choice despite costly outcrossing in the fungus Podospora anserina

Fungi have a large potential for flexibility in their mode of sexual reproduction, resulting in mating systems ranging from haploid selfing to outcrossing. However, we know little about which mating strategies are used in nature, and why, even in well-studied model organisms. Here, we explored the fitness consequences of alternative mating strategies in the ascomycete fungus Podospora anserina. We measured and compared fitness proxies of nine genotypes in either diploid selfing or outcrossing events, over two generations, and with or without environmental stress. We showed that fitness was consistently lower in outcrossing events, irrespective of the environment. The cost of outcrossing was partly attributed to non-self recognition genes with pleiotropic effects on fertility. We then predicted that when presented with options to either self or outcross, individuals would perform mate choice in favour of the reproductive strategy that yields higher fitness. Contrary to our prediction, individuals did not seem to avoid outcrossing when a choice was offered, in spite of the fitness cost incurred. Our results suggest that, although functionally diploid, P. anserina does not benefit from outcrossing in most cases. We outline different explanations for the apparent lack of mate choice in face of high fitness costs associated with outcrossing, including a new perspective on the pleiotropic effect of non-self recognition genes.     

The evolution of sex chromosomes in organisms with separate haploid sexes

The evolution of dimorphic sex chromosomes is driven largely by the evolution of reduced recombination and the subsequent accumulation of deleterious mutations. Although these processes are increasingly well understood in diploid organisms, the evolution of dimorphic sex chromosomes in haploid organisms (U/V) has been virtually unstudied theoretically. We analyze a model to investigate the evolution of linkage between fitness loci and the sex‐determining region in U/V species. In a second step, we test how prone nonrecombining regions are to degeneration due to accumulation of deleterious mutations. Our modeling predicts that the decay of recombination on the sex chromosomes and the addition of strata via fusions will be just as much a part of the evolution of haploid sex chromosomes as in diploid sex chromosome systems. Reduced recombination is broadly favored, as long as there is some fitness difference between haploid males and females. The degeneration of the sex‐determining region due to the accumulation of deleterious mutations is expected to be slower in haploid organisms because of the absence of masking. Nevertheless, balancing selection often drives greater differentiation between the U/V sex chromosomes than in X/Y and Z/W systems. We summarize empirical evidence for haploid sex chromosome evolution and discuss our predictions in light of these findings.     

On the Adaptive Value of Some Mate Selection Strategies

Results of an agent-based computer simulation of the evolution of diploid sexual organisms showed that several mate selection strategies confer much higher average fitness to the simulated populations, and higher evolutionary stability to the alleles coding for these strategies, than random mating. Strategies which select for 'good genes' were very successful, and so were strategies based on assortative mating. The results support the hypothesis that mating is not likely to be random in nature and that the most successful mate selection strategies are those based on assortative mating or on advantageous genes.     

The conservation of redundancy in genetic systems: effects of sexual and asexual reproduction

The relationship between probability of survival and the number of deleterious mutations in the genome is investigated using three different models of highly redundant systems that interact with a threatening environment. Model one is a system that counters a potentially lethal infection; it has multiple identical components that act in sequence and in parallel. Model two has many different overlapping components that provide three-fold coverage of a large number of vital functions. The third model is based on statistical decision theory: an ideal detector, following an optimum decision strategy, makes crucial decisions in an uncertain world. The probability of a fatal error is reduced by a redundant sampling system, but the chance of error rises as the system is impaired by deleterious mutations. In all three cases the survival profile shows a synergistic pattern in that the probability of survival falls slowly and then more rapidly. This is different than the multiplicative or independent survival profile that is often used in mathematical models. It is suggested that a synergistic profile is a property of redundant systems. Model one is then used to study the conservation of redundancy during sexual and asexual reproduction. A unicellular haploid organism reproducing asexually retains redundancy when the mutation rate is very low (0001 per cell division), but tends to lose high levels of redundancy if the mutation rate is increased (001 to 01 per cell division). If a similar unicellular haploid organism has a sexual phase then redundancy is retained for mutation rates between 0001 and 01 per cell division. The sexual organism outgrows the asexual organism when the above mutation rates apply. If they compete for finite resources the asexual organism will be extinguished. Variants of the sexual organism with increased redundancy will outgrow those with lower levels of redundancy and the sexual process facilitates the evolution of more complex forms. There is a limit to the extent that complexity can be increased by increasing the size of the genome and in asexual organisms this leads to progressive accumulation of mutations with loss of redundancy and eventual extinction. If complexity is increased by using genes in new combinations, the asexual form can reach a stable equilibrium, although it is associated with some loss of redundancy. The sexual form, by comparison, can survive, with retention of redundancy, even if the mutation rate is above one per generation. The conservation and evolution of redundancy, which is essential for complexity, depends on the sexual process of reproduction.     

The scale‐of‐choice effect and how estimates of assortative mating in the wild can be biased due to heterogeneous samples

The mode in which sexual organisms choose mates is a key evolutionary process, as it can have a profound impact on fitness and speciation. One way to study mate choice in the wild is by measuring trait correlation between mates. Positive assortative mating is inferred when individuals of a mating pair display traits that are more similar than those expected under random mating while negative assortative mating is the opposite. A recent review of 1134 trait correlations found that positive estimates of assortative mating were more frequent and larger in magnitude than negative estimates. Here, we describe the scale‐of‐choice effect (SCE), which occurs when mate choice exists at a smaller scale than that of the investigator's sampling, while simultaneously the trait is heterogeneously distributed at the true scale‐of‐choice. We demonstrate the SCE by Monte Carlo simulations and estimate it in two organisms showing positive (Littorina saxatilis) and negative (L. fabalis) assortative mating. Our results show that both positive and negative estimates are biased by the SCE by different magnitudes, typically toward positive values. Therefore, the low frequency of negative assortative mating observed in the literature may be due to the SCE's impact on correlation estimates, which demands new experimental evaluation.     

EVOLUTION OF THE NUMBER OF SEXES

In sexually reproducing isogamous organisms, gametes (or diploid cells in ciliates) are classified into two or more groups called sexes, and mating occurs only between cells of different sexes. We have studied the evolutionary stability of the number of sexes maintained in a population by examining population-genetic models. For models in which the diploid genome determines the sex of conjugal cells, a one-locus system with three alleles of pecking-order dominance is assumed. Unlike traditional bisexual models, the genetic dynamics then depend on a rule, called mating kinetics, which determines the proportion of matings between each pair of sexes for given proportions of cells of the three sexes. The evolutionary consequences greatly depend on the mating kinetics assumed. Of the four mating kinetics examined, two give a large advantage to rare sexes whose cells quickly find heterosexual partners, which implies an evolutionary increase in the number of sexes. In contrast, the other two mating kinetics, in which gametes wait for suitable mates without being eliminated from the gamete pool during this waiting period, produce neutrally stable dynamics with curves or a surface of equilibria. Then random drift or differential fitness among sexes would result in the loss of sex alleles until only two remain in the population. This suggests a turnover of sexes; a new sex invades and replaces resident sexes after temporary coexistence. Similar results are obtained in models with haploid sex-determination and with autogamy. These two processes, however, may help to maintain many sexes indirectly by preventing the accumulation of recessive lethal mutations on sex chromosomes. The relationship of these models to models of self-sterility factors in plants and sex factors in honeybees is discussed. To summarize, the number of sexes should increase when conjugal cells must find mates during a limited period of time, otherwise a two-sex system should evolve. We conclude that there may be more isogamous species with three or more sexes than are currently known.     

The ecology and genetics of fitness in Chlamydomonas. XII. Repeated sexual episodes increase rates of adaptation to novel environments

Abstract.— We investigated the dynamics of adaptation of the unicellular chlorophyte Chlamydomonas reinhardtii to new and hostile conditions of growth provided by novel carbon substrates in the dark. The experiment was designed to contrast perennially asexual lines with lines that had experienced one or more sexual episodes. All lines were capable of adapting to the novel environment. The sexual lines, however, showed greater adaptation over the course of the experiment, especially in more complex environments. Moreover, the effect of sex on adaptation increased with the number of successive sexual episodes. The time-course of adaptation showed that sex initially caused an increase in the standardized variance of fitness and an initial drop in mean fitness, at least after a second or third sexual episode. These short-term effects were followed by a period of recovery during which the fitness of sexual lines eventually exceeded that of asexual lines. The increase in mean fitness was mirrored by a decrease in the standardized variance of fitness relative to asexuals, suggesting that directional selection used up the variation generated by meiotic recombination and thereby conferred a fitness advantage to the sexual lines. These results support the Weismann-Fisher-Muller hypothesis for the maintenance of sex in natural populations.     

QUANTITATIVE GENETICS AND POPULATION DYNAMICS

This study examines the dynamics of a competition and a host-parasite model in which the interactions are determined by quantitative characters. Both models are extensions of one-dimensional difference equations that can exhibit complicated dynamics. Compared to these basic models, the phenotypic variability given by the quantitative characters reduces the size of the density fluctuations in asexual populations. With sexual reproduction, which is described by modeling the genetics of the quantitative character explicitly with many haploid loci that determine the character additively, this reduction in fitness variance is magnified. Moreover, quantitative genetics can induce simple dynamics. For example, the sexual population can have a two-cycle when the asexual system is chaotic. This paper discusses the consequences for the evolution of sex. The higher mean growth rate implied by the lower fitness variance in sexual populations is an advantage that can overcome a twofold intrinsic growth rate of asexuals. The advantage is bigger when the asexual population contains only a subset of the phenotypes present in the sexual population, which conforms with the tangled bank theory for the evolution of sex and shows that tangled bank effects also occur in host-parasite systems. The results suggest that explicitly describing the genetics of a quantitative character leads to more flexible models than the usual assumption of normal character distributions, and therefore to a better understanding of the character's impact on population dynamics.     

The costs of sex due to deleterious intracellular parasites

A major problem in evolutionary theory is to explain the widespread occurrence of sexual recombination. This is particularly difficult in anisogamous species where the familiar ‘two-fold cost of sex’ is encountered. Another cost has recently been identified: that fusion of gametes allows intracellular parasites or deleterious ‘selfish’ genomes to invade a population. These costs of anisogamy and the ability of cytoplasmic agents to invade a sexual population are quantified, allowing the costs and consequences of different modes of reproduction to be compared. It is found that the costs of selfish elements are likely to be very high and, in particular, that isogamous sexual reproduction (the putative ‘primitive’ form) is not cost-free, but incurs a fitness reduction of the order of 90%; thus a large selective disadvantage occurs in the initial evolution of sex which is ignored in standard analysis. Even once anisogamy has evolved, the low levels of ‘paternal leakage’ observed in many extant organisms may allow selfish cytoplasmic elements to spread, resulting in moderate to large decreases in host population fitness. However, much of the cost of selfish elements is avoided in sexual lifecycles with a large number of asexual cellular divisions between sexual reproduction: this greatly impedes the spread of selfish agents and reduces the fitness loss attributable to selfish elements.     

INBREEDING DEPRESSION VARIES WITH INVESTMENT IN SEX IN A FACULTATIVE PARTHENOGEN

The reproductive mode of facultative parthenogens allows recessive mutations that accumulate during the asexual phase to be unmasked following sexual reproduction. Longer periods of asexual reproduction should increase the accumulation of deleterious mutations within individuals, reduce population-level genetic diversity via competition and increase the probability of mating among close relatives. Having documented that the investment in sexual reproduction differs among populations and clones of Daphnia pulicaria , we ask if this variation is predictive of the level of inbreeding depression across populations. In four lake populations that vary in sex investment, we raised multiple families (mother, field-produced daughter, laboratory-produced daughter) on high food and estimated the fitness reduction in both sexually produced offspring relative to the maternal genotype. Inbred individuals had lower fitness than their field-produced siblings. The magnitude of fitness reduction in inbred offspring increased as population-level investment in sex decreased. However, there was less of a fitness reduction following sex in the field-produced daughters, suggesting that many field-collected mothers were involved in outcross mating.