Selection acting on males can reduce mutation load of sexual relative to asexual populations, thus mitigating the twofold cost of sex, provided that it seeks and destroys the same mutations as selection acting on females, but with higher efficiency. This could happen due to sexual selection-a potent evolutionary force that in most systems predominantly affects males. We used replicate populations of red flour beetles (Tribolium castaneum) to study sex-specific selection against deleterious mutations introduced with ionizing radiation. We found no evidence for selection being stronger in males than in females; in fact, we observed a nonsignificant trend in the opposite direction. This suggests that selection on males does not reduce mutation load below the level expected under the (hypothetical) scenario of asexual reproduction. Additionally, we employed a novel approach, based on a simple model, to quantify the relative contributions of sexual and offspring viability selection to the overall selection observed in males. We found them to be similar in magnitude; however, only the offspring viability component was statistically significant. In summary, we found no support for the hypothesis that selection on males in general, and sexual selection in particular, contributes to the evolutionary maintenance of sex.
The maintenance of males and outcrossing is widespread, despite considerable costs of males. By enabling recombination between distinct genotypes, outcrossing may be advantageous during adaptation to novel environments and if so, it should be selected for under environmental challenge. However, a given environmental change may influence fitness of male, female, and hermaphrodite or asexual individuals differently, and hence the relationship between reproductive system and dynamics of adaptation to novel conditions may not be driven solely by the level of outcrossing and recombination. This has important implications for studies investigating the evolution of reproductive modes in the context of environmental changes, and for the extent to which their findings can be generalized. Here, we use Caenorhabditis elegans—a free-living nematode species in which hermaphrodites (capable of selfing but not cross-fertilizing each other) coexist with males (capable of fertilizing hermaphrodites)—to investigate the response of wild type as well as obligatorily outcrossing and obligatorily selfing lines to stressfully increased ambient temperature. We found that thermal stress affects fitness of outcrossers much more drastically than that of selfers. This shows that apart from the potential for recombination, the selective pressures imposed by the same environmental change can differ between populations expressing different reproductive systems and affect their adaptive potential.
Radical shifts in reproductive systems result in radical changes in selective pressures acting on reproductive traits. Nematode Caenorhabditis elegans constitutes one of rare model systems where such shifts can be experimentally induced, providing an opportunity for studying the evolution of reproductive phenotypes in real time. Evolutionary history of predominantly selfing reproduction in has led to degeneration of traits involved outcrossing, making it inefficient. Here, we introduced obligatory outcrossing into isogenic lines of C. elegans and allowed replicate populations to evolve under the new reproductive system. We predicted that they should evolve higher outcrossing efficiency, leading to increased fitness relative to unevolved ancestors. To test this prediction, we assayed fitness of both ancestral and evolved outcrossing populations. To control for the potentially confounding effect of adaptation to laboratory conditions, we also assayed populations with wild-type (selfing) reproductive system. In five experimental blocks, we measured competitive fitness of 12 evolved populations (6 outcrossing, 6 selfing) after ca. 95 generations of evolution, along with their respective ancestors. On average, we found that fitness increased by 0.72 SD (± 0.3 CI) in outcrossing and by 0.52 (± 0.35 CI) in selfing populations, suggesting further adaptation to laboratory conditions in both types. Contrary to predictions, fitness increase was not significantly higher in outcrossing populations, suggesting no detectable adaptation to the changed reproductive system. Importantly, the results for individual populations varied strongly between experimental blocks, in some cases even differing in effect direction. This emphasises the importance of experimental replication in avoiding reporting false findings.
According to theory, sexual selection in males may efficiently purge mutation load of sexual populations, reducing or fully compensating 'the cost of males'. For this to occur, mutations not only need to be deleterious to both sexes, they also must affect males more than females. A frequently overlooked problem is that relative strength of selection on males versus females may vary between environments, with social conditions being particularly likely to affect selection in males and females differently. Here, we induced mutations in red flour beetles (Tribolium castaneum) and tested their effect in both sexes under three different operational sex ratios (1:2, 1:1 and 2:1). Induced mutations decreased fitness of both males and females, but their effect was not stronger in males. Surprisingly, operational sex ratio did not affect selection against deleterious mutations nor its relative strength in the sexes. Thus, our results show no support for the role of sexual selection in the evolutionary maintenance of sex.
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