Similarity Selection and the Evolution of Sex: Revisiting the Red Queen

For over 25 years, many evolutionary ecologists have believed that sexual reproduction occurs because it allows hosts to change genotypes each generation and thereby evade their coevolving parasites. However, recent influential theoretical analyses suggest that, though parasites can select for sex under some conditions, they often select against it. These models assume that encounters between hosts and parasites are completely random. Because of this assumption, the fitness of a host depends only on its own genotype (“genotypic selection”). If a host is even slightly more likely to encounter a parasite transmitted by its mother than expected by random chance, then the fitness of a host also depends on its genetic similarity to its mother (“similarity selection”). A population genetic model is presented here that includes both genotypic and similarity selection, allowing them to be directly compared in the same framework. It is shown that similarity selection is a much more potent force with respect to the evolution of sex than is genotypic selection. Consequently, similarity selection can drive the evolution of sex even if it is much weaker than genotypic selection with respect to fitness. Examination of explicit coevolutionary models reveals that even a small degree of mother–offspring parasite transmission can cause parasites to favor sex rather than oppose it. In contrast to previous predictions, the model shows that weakly virulent parasites are more likely to favor sex than are highly virulent ones. Parasites have figured prominently in discussions of the evolution of sex, but recent models suggest that parasites often select against sex rather than for it. With the inclusion of small and realistic exposure biases, parasites are much more likely to favor sex. Though parasites alone may not provide a complete explanation for sex, the results presented here expand the potential for parasites to contribute to the maintenance of sex rather than act against it

ASSORTATIVE MATING FOR FITNESS AND THE EVOLUTION OF RECOMBINATION

Abstract. To understand selection on recombination, we need to consider how linkage disequilibria develop and how recombination alters these disequilibria. Any factor that affects the development of disequilibria, including nonrandom mating, can potentially change selection on recombination. Assortative mating is known to affect linkage disequilibria but its effects on the evolution of recombination have not been previously studied. Given that assortative mating for fitness can arise indirectly via a number of biologically realistic scenarios, it is plausible that weak assortative mating occurs across a diverse set of taxa. Using a modifier model, we examine how assortative mating for fitness affects the evolution of recombination under two evolutionary scenarios: selective sweeps and mutation-selection balance. We find there is no net effect of assortative mating during a selective sweep. In contrast, assortative mating could have a large effect on recombination when deleterious alleles are maintained at mutation-selection balance but only if assortative mating is sufficiently strong. Upon considering reasonable values for the number of loci affecting fitness components, the strength of selection, and the mutation rate, we conclude that the correlation in fitness between mates is unlikely to be sufficiently high for assortative mating to affect the evolution of recombination in most species

An analysis of single clutch paternity in the burrower bug Sehirus cinctus using microsatellites

Recent studies of the burrower bug, Sehirus cinctus, have examined the genetic basis of parental care. An understanding of the burrower bug mating system, and the subsequent pattern of offspring relatedness that this system generates, is critical to further interpret genetic data. To this end, we developed three consistently amplifiable highly polymorphic microsatellite loci and used them to determine genotypic patterns at the level of both the population and the single clutch. We found that all clutches were sired by single males. Further, we find no evidence for inbreeding. We hypothesize that single paternity within a clutch may play an important role in reducing the potential for sibling rivalry, by increasing the relatedness among clutchmates

Increased Transmission of Mutations by Low-Condition Females: Evidence for Condition-Dependent DNA Repair

Evidence is mounting that mutation rates are sufficiently high for deleterious alleles to be a major evolutionary force affecting the evolution of sex, the maintenance of genetic variation, and many other evolutionary phenomena. Though point estimates of mutation rates are improving, we remain largely ignorant of the biological factors affecting these rates at the individual level. Of special importance is the possibility that mutation rates are condition-dependent with low-condition individuals experiencing more mutation. Theory predicts that such condition dependence would dramatically increase the rate at which populations adapt to new environments and the extent to which populations suffer from mutation load. Despite its importance, there has been little study of this phenomenon in multicellular organisms. Here, we examine whether DNA repair processes are condition-dependent in Drosophila melanogaster. In this species, damaged DNA in sperm can be repaired by maternal repair processes after fertilization. We exposed high- and low-condition females to sperm containing damaged DNA and then assessed the frequency of lethal mutations on paternally derived X chromosomes transmitted by these females. The rate of lethal mutations transmitted by low-condition females was 30% greater than that of high-condition females, indicating reduced repair capacity of low-condition females. A separate experiment provided no support for an alternative hypothesis based on sperm selection

Relative Effectiveness of Mating Success and Sperm Competition at Eliminating Deleterious Mutations in Drosophila melanogaster

Condition-dependence theory predicts that sexual selection will facilitate adaptation by selecting against deleterious mutations that affect the expression of sexually selected traits indirectly via condition. Recent empirical studies have provided support for this prediction; however, their results do not elucidate the relative effects of pre- and postcopulatory sexual selection on deleterious mutations. We used the Drosophila melanogaster model system to discern the relative contributions of pre- and postcopulatory processes to selection against deleterious mutations. To assess second-male ejaculate competition success (P2; measured as the proportion of offspring attributable to the experimental male) and mating success, mutant and wild-type male D. melanogaster were given the opportunity to mate with females that were previously mated to a standard competitor male. This process was repeated for males subjected to a diet quality manipulation to test for effects of environmentally-manipulated condition on P2 and mating success. While none of the tested mutations affected P2, there was a clear effect of condition. Conversely, several of the mutations affected mating success, while condition showed no effect. Our results suggest that precopulatory selection may be more effective than postcopulatory selection at removing deleterious mutations. The opposite result obtained for our diet manipulation points to an interesting discrepancy between environmental and genetic manipulations of condition, which may be explained by the multidimensionality of condition. Establishing whether the various stages of sexual selection affect deleterious mutations differently, and to what extent, remains an important issue to resolve

Evolution of sex: Why do organisms shuffle their genotypes

de ual species, the extent of genetic mixing caused by sex Genetic associations are conventionally defined is reduced by the complete suppression of recombina-tion in some individuals; for example, there is no re-combination in male Drosophila melanogaster. These observations suggest that reproduction with less or no genetic mixing is possible. Nonetheless, some such that positive values indicate alleles are packaged into individuals in such a way that increases the allelic variance among individuals, whereas negative values indicate alleles are organized in such a way that de-creases the allelic variance among individuals (Box 1 and figure in Box 2). Characterizing a population by its allele frequencies and patterns of associations makes it simpler to understand how genetic mixing affect

The Evolution of Sex with Exposure to Maternally Transmitted Parasites

<p>Darkly shaded regions indicate parameter values under which increased sex evolved in simulations. Lightly shaded regions indicate parameter values that selected against sex. A detailed description of the simulations is presented in <a href="http://www.plosbiology.org/article/info:doi/10.1371/journal.pbio.0040265#sd003" target="_blank">Protocol S3</a>. The effect of the modifier was assumed to be additive, i.e., <i>h_σ</i> = ½. Left: two-locus IMA model with <i>d_R</i> = 0.25. Right: two-locus Gene-For-Gene (GFG) model with a cost of resistance alleles of <i>c</i> = 0.05 <i>v</i> and cost of infectious alleles of <i>k</i> = 0.3. Resistance alleles were assumed to be completely dominant. MA model results were very similar to IMA model results (unpublished data). For the IMA model, the parameter combination with <i>σ</i> = 0.5, <i>v</i> = 0.2, <i>λ</i> = 1, and <i>ϕ</i> = 0.1, increased sex evolved in 90% of replicates; increased sex evolved in 95% of replicates the parameter combination with <i>σ</i> = 0.1, <i>v</i> = 0.8, <i>λ</i> = 10, and <i>ϕ</i> = 0.05; for other parameter combinations, sex evolved in all replicates in the direction indicated by shading. </p

Data from: Variation in the strength of inbreeding depression across environments: effects of stress and density dependence

In what types of environments should we expect to find strong inbreeding depression? Previous studies indicate that inbreeding depression, δ, is positively correlated with the stressfulness of the environment in which it is measured. However, it remains unclear why stress, per se, should increase δ. To our knowledge, only “competitive stress” has a logical connection to δ. Through competition for resources, better quality (outbred) individuals make the environment worse for lower quality (inbred) individuals, accentuating the differences between them. For this reason, we expect inbreeding depression to be stronger in environments where the fitness of individuals is more sensitive to the presence of conspecifics (i.e., where fitness is more density dependent). Indeed, some studies suggest a role for competition within environments but this idea has not been tested in the context of understanding variation in δ across environments. Using Drosophila melanogaster, we estimated δ for viability in 22 different environments. These environments were simultaneously characterized for (i) stressfulness and (ii) density dependence. Though stress and density dependence are moderately correlated with each other, inbreeding depression is much more strongly correlated with density dependence. These results suggest that mean selection across the genome is stronger in environments where competition is intense, rather than in environments that are stressful for other reasons

Data from: Male-biased fitness effects of spontaneous mutations in Drosophila melanogaster

In populations with males and females, sexual selection may often represent a major component of overall selection. Sexual selection could act to eliminate deleterious alleles in concert with other forms of selection, thereby improving the fitness of sexual populations. Alternatively, the divergent reproductive strategies of the sexes could promote the maintenance of sexually-antagonistic variation, causing sexual populations to be less fit. The net impact of sexual selection on fitness is not well understood, due in part to limited data on the sex-specific effects of spontaneous mutations on total fitness. Using a set of mutation accumulation lines of Drosophila melanogaster, we found that mutations were deleterious in both sexes and had larger effects on fitness in males than in females. This pattern is expected to reduce the mutation load of sexual females and promote the maintenance of sexual reproduction

Data from: The effect of deleterious mutations and age on recombination in Drosophila melanogaster

At the population level, recombination mediates the efficiency with which selection can eliminate deleterious mutations. At the individual level, deleterious alleles may influence recombination, which would change the rate at which linkage disequilibrium is eroded and thereby alter the efficiency with which deleterious alleles are purged. Here we test whether the presence of a deleterious allele on one autosome affects recombination on another autosome. We find that deleterious alleles not only alter the rate but also the pattern of recombination. However, there is little support that different deleterious alleles affect recombination in a consistent manner. Because we have detailed information on individual females across their life times, we are able to examine how recombination patterns change with age and find that these patterns are also affected by the presence of deleterious alleles. The differences among genotypes or among age classes is large enough to add substantial noise to genetic mapping experiments that do not consider these sources of variation