The evolution of obligate sex: the roles of sexual selection and recombination
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The evolution of sex is one of the greatest mysteries in evolutionary biology. An even greater mystery is the evolution of obligate sex, particularly when competing with facultative sex and not with complete asexuality. Here, we develop a stochastic simulation of an obligate allele invading a facultative population, where males are subject to sexual selection. We identify a range of parameters where sexual selection can contribute to the evolution of obligate sex: Especially when the cost of sex is low, mutation rate is high, and the facultative individuals do not reproduce sexually very often. The advantage of obligate sex becomes larger in the absence of recombination. Surprisingly, obligate sex can take over even when the population has a lower mean fitness as a result. We show that this is due to the high success of obligate males that can compensate the cost of sex.Keywords:
Obligate
Experimental Evolution
Males of
Outcrossing
Caenorhabditis
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Abstract. 1. Sexual selection is a powerful evolutionary force that is hypothesised to play an important role in the evolution of lifespan. Here we test for the potential contribution of sexual selection to the rapid evolution of male lifespan in replicated laboratory populations of the seed beetle, Callosobruchus maculatus . 2. For 35 generations, newly hatched virgin male beetles from eight different populations were allowed to mate for 24 h and then discarded. Sexual selection was removed in half of these populations by enforcing random monogamy. 3. Classic theory predicts that because of sexual competition, males from sexually selected lines would have higher age‐specific mortality rates and shorter lifespan than males from monogamous lines. 4. Alternatively, condition‐dependent sexual selection may also favour genes that have positive pleiotropic effects on lifespan and ageing. 5. Males from all eight populations evolved shorter lifespans compared with the source population. However, there was no difference in lifespan between males from populations with or without sexual selection. Thus, sexual selection did not contribute to the evolution of male lifespan despite the fact that such evolution did occur in our study populations.
Experimental Evolution
Sexual reproduction
Callosobruchus chinensis
Sexual maturity
Sexual dimorphism
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Artificial selection and experimental evolution document natural selection under controlled conditions. Collectively, these techniques are continuing to provide fresh and important insights into the genetic basis of evolutionary change, and are now being employed to investigate mating behaviour. Here, we focus on how selection techniques can reveal the genetic basis of post-mating adaptations to sexual selection and sexual conflict. Alteration of the operational sex ratio of adult Drosophila over just a few tens of generations can lead to altered ejaculate allocation patterns and the evolution of resistance in females to the costly effects of elevated mating rates. We provide new data to show how male responses to the presence of rivals can evolve. For several traits, the way in which males responded to rivals was opposite in lines selected for male-biased, as opposed to female-biased, adult sex ratio. This shows that the manipulation of the relative intensity of intra- and inter-sexual selection can lead to replicable and repeatable effects on mating systems, and reveals the potential for significant contemporary evolutionary change. Such studies, with important safeguards, have potential utility for understanding sexual selection and sexual conflict across many taxa. We discuss how artificial selection studies combined with genomics will continue to deepen our knowledge of the evolutionary principles first laid down by Darwin 150 years ago.
Experimental Evolution
Antagonistic Coevolution
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The ability of sexual conflict to facilitate speciation has been widely anticipated in speciation research. However, mathematical models based on mating rate predict only two scenarios that result in speciation out of six possible evolutionary outcomes of sexual conflict (Gavrilets and Hayashi, 2005). There have been only two instances where experimental evolutionary studies have convincingly demonstrated the possibility of speciation linked to sexual conflict (Martin and Hosken, 2003; Syed et al., 2017). The study by (Syed et al., 2017) involving replicates of Drosophila melanogaster populations under differential operational sex ratio have shown that both premating and postmating-prezygotic isolation evolved in the male biased (high sexual conflict) regime but not in the female biased regime (low sexual conflict). This indicates possibility of coevolution of sexual signals such as cuticular lipids in form of precopulatory isolating mechanism since they evolve rapidly and are involved in Drosophila mate recognition. We studied cuticular lipid divergence in the same Drosophila populations undergoing reproductive isolation and found that their cuticular lipid profiles are sexually dimorphic indicating past and/or ongoing sexually antagonistic coevolution. Although male biased replicates evolved isolation in reproductive traits due to high sexual conflict, the patterns of cuticular lipid divergence in high and low sexual conflict regimes suggest that sexual selection is the dominant selection pressure rather than sexual conflict affecting the cuticular lipid trait. Although there is evidence of divergence of cuticular lipid profiles among both sexes of male biased replicates, the divergence pattern is defined by ancestry of the different replicates and cannot be unambiguously credited to sexual conflict.
Antagonistic Coevolution
Reproductive isolation
Genetic algorithm
Coevolution
Ecological speciation
Divergence (linguistics)
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Abstract Sexual selection is a potent force shaping multiple aspects of the interaction between the sexes, including the characters underlying reproductive success and sexual conflict, and may play an important role in determining the viability of populations. Experimental evolution is a methodological approach in which researchers either act as selective agents or establish the selective pressures operating on individuals to investigate changes in traits across generations and the genetic underpinning of these changes. Experimental evolution replicates the evolutionary process under controlled conditions and, by doing so, offers exceptional insights into the role of variation, selection and adaptation in evolution. Applied to the study of pre‐copulatory (before mating) and post‐copulatory (after mating) sexual selection, experimental evolution proves critical to understand the evolutionary consequences of male–male competition and female mate choice, and the repercussions of concurrent or divergent interests between the sexes in regard to reproduction. Key Concepts: Experimental evolution is a methodological approach to study adaptation under controlled experimental conditions. Sexual selection shapes the characters underlying reproductive success. Experimental evolution is a powerful tool for understanding the evolutionary consequences of sexual selection and sexual conflict.
Experimental Evolution
Sexual reproduction
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Sexual interactions are often rife with conflict. Conflict between members of the same sex over opportunities to mate has long been understood to effect evolution via sexual selection. Although conflict between males and females is now understood to be widespread, such conflict is seldom considered in the same light as a general agent of sexual selection. Any interaction between males or females that generates variation in fitness, whether due to conflict, competition or mate choice, can potentially influence sexual selection acting on a range of male traits. Here we seek to address a lack of direct experimental evidence for how sexual conflict influences sexual selection more broadly. We manipulate a major source of sexual conflict in the black field cricket, Teleogryllus commodus, and quantify the resulting changes in the nature of sexual selection using formal selection analysis to statistically compare multivariate fitness surfaces. In T. commodus, sexual conflict occurs over the attachment time of an external spermatophore. By experimentally manipulating the ability of males and females to influence spermatophore attachment, we found that sexual conflict significantly influences the opportunity, form, and intensity of sexual selection on male courtship call and body size. When males were able to harass females, the opportunity for selection was smaller, the form of selection changed, and sexual selection was weaker. We discuss the broader evolutionary implications of these findings, including the contributions of sexual conflict to fluctuating sexual selection and the maintenance of additive genetic variation.
Spermatophore
Field cricket
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Male and female genital morphology varies widely across many taxa, and even among populations.Disentangling potential sources of selection on genital morphology is problematic because each sex is predicted to respond to adaptations in the other due to reproductive conflicts of interest.To test how variation in this sexual conflict trait relates to variation in genital morphology we used our previously developed artificial selection lines for high and low repeated mating rates.We selected for high and low repeated mating rates using monogamous pairings to eliminate contemporaneous female choice and male-male competition.Male and female genital shape responded rapidly to selection on repeated mating rate.High and low mating rate lines diverged from control lines after only 10 generations of selection.We also detected significant patterns of male and female genital shape coevolution among selection regimes.We argue that because our selection lines differ in sexual conflict, these results support the hypothesis that sexually antagonistic coevolution can drive the rapid divergence of genital morphology.The greatest divergence in morphology corresponded with lines in which the resolution of sexual conflict over mating rate was biased in favor of male interests.
Antagonistic Coevolution
Sex organ
Coevolution
Trait
Experimental Evolution
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Conflicts of interest between mates can promote the evolution of male traits that reduce female fitness and that drive coevolution between the sexes. The rate of adaptation depends on the intensity of selection and its efficiency, which depends on drift and genetic variability. This leads to the largely untested prediction that coevolutionary adaptations such as those driven by sexual conflict should evolve faster in large populations. We tested this using the bruchid beetle Callosobruchus maculatus, a species where harm inflicted by males is well documented. Although most experimental evolution studies remove sexual conflict, we reintroduced it in populations in which it had been experimentally removed. Both population size and standing genetic variability were manipulated in a factorial experimental design. After 90 generations of relaxed conflict (monogamy), the reintroduction of sexual conflicts for 30 generations favored males that harmed females and females that were more resistant to the genital damage inflicted by males. Males evolved to become more harmful when population size was large rather than when initial genetic variation was enriched. Our study shows that sexual selection can create conditions in which males can benefit from harming females and that selection may tend to be more intense and effective in larger populations.
Experimental Evolution
Coevolution
Callosobruchus maculatus
Genetic Variability
Antagonistic Coevolution
Effective population size
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Despite the key functions of the genitalia in sexual interactions and fertilization, the role of sexual selection and conflict in shaping genital traits remains poorly understood. Seed beetle (Callosobruchus maculatus) males possess spines on the intromittent organ, and females possess a thickened reproductive tract wall that also bears spines. We investigated the role of sexual selection and conflict by imposing monogamous mating on eight replicate populations of this naturally polygamous insect, while maintaining eight other populations under polygamy. To establish whether responses to mating system manipulation were robust to ecological context, we simultaneously manipulated life‐history selection (early/late reproduction). Over 18–21 generations, male genital spines evolved relatively reduced length in large males (i.e., shallower static allometry) in monogamous populations. Two nonintromittent male genital appendages also evolved in response to the interaction of mating system and ecology. In contrast, no detectable evolution occurred in female genitalia, consistent with the expectation of a delayed response in defensive traits. Our results support a sexually antagonistic role for the male genital spines, and demonstrate the evolution of static allometry in response to variation in sexual selection opportunity. We argue that further advances in the study of genital coevolution will require a much more detailed understanding of the functions of male and female genital traits.
Antagonistic Coevolution
Sex organ
Female sperm storage
Allometry
Aedeagus
Experimental Evolution
Coevolution
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Citations (86)
Although sexual selection can provide benefits to both sexes, it also can be costly because of expanded opportunities for intersexual conflict. We evaluated the role of sexual selection in a naturally promiscuous species, Drosophila melanogaster . In two replicate populations, sexual selection was removed through enforced monogamous mating with random mate assignment or retained in promiscuous controls. Monogamous mating constrains the reproductive success of mates to be identical, thereby converting prior conflicts between mates into opportunities for mutualism. Random mate assignment removes the opportunity for females to choose beneficial qualities in their mate. The mating treatments were maintained for 47 generations, and evolution was allowed to proceed naturally within the parameters of the design. In the monogamous populations, males evolved to be less harmful to their mates, and females evolved to be less resistant to male-induced harm. The monogamous populations also evolved a greater net reproductive rate than their promiscuous controls. These results indicate a potentially widespread cost of sexual selection caused by conflicts inherent to promiscuity.
Antagonistic Coevolution
Promiscuity
Experimental Evolution
Coevolution
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Citations (635)