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Schematic representation of the design of Assay II. Schematic representation of the design of Assay II and the way of calculating mate choice and post-zygotic reproductive isolation on the example of a male's line 1. Procedures are described in the text. doi: 10.1371/journal.pone.0074971.g002
Source publication
Sexual conflict leading to sexual antagonistic coevolution has been hypothesized to drive reproductive isolation in allopatric populations and hence lead to speciation. However, the generality of this speciation mechanism is under debate. We used experimental evolution in the bulb mite Rhizoglyphusrobini to investigate whether sexual conflict promo...
Contexts in source publication
Context 1
... established groups of three individuals, each group consisting of one male, one female from the same line ("sympatric" female) and one female from another line within the same mating system ("allopatric" female). Between 16 and 20 males per line were used to form such groups, 4-5 for each of the four "allopatric" female lines (Figure 2). Hence, all possible line combinations were established within each mating system. ...
Context 2
... 14 days, the numbers of offspring produced by each female were counted. For each female line- male line combination (see Figure 2), we calculated an index I, the total number of offspring produced by the "allopatric" females from a given line divided by the total number of offspring produced by all females from this line. We then calculated the isolation index for each male line as a mean of those indexes (Figure 2). ...
Context 3
... each female line- male line combination (see Figure 2), we calculated an index I, the total number of offspring produced by the "allopatric" females from a given line divided by the total number of offspring produced by all females from this line. We then calculated the isolation index for each male line as a mean of those indexes (Figure 2). ...
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Citations
... To understand the origins of the postmating reproductive isolation in our study, it is necessary to explain how differences between replicates evolved and why this leads to reproductive isolation. It has been suggested that sexual conflict, driven either by female-male or male-male interactions, could result in replicate specific responses and thus reproductive isolation, but the empirical evidence has remained controversial [36][37][38][39][40]. In addition to selection also genetic drift can cause differences between replicate populations, even if they originate from the same founder population. ...
Background
Reproductive isolation can result from adaptive processes (e.g., ecological speciation and mutation-order speciation) or stochastic processes such as “system drift” model. Ecological speciation predicts barriers to gene flow between populations from different environments, but not among replicate populations from the same environment. In contrast, reproductive isolation among populations independently adapted to the same/similar environment can arise from both mutation-order speciation or system drift.
Results
In experimentally evolved populations adapting to a hot environment for over 100 generations, we find evidence for pre- and postmating reproductive isolation. On one hand, an altered lipid metabolism and cuticular hydrocarbon composition pointed to possible premating barriers between the ancestral and replicate evolved populations. On the other hand, the pronounced gene expression differences in male reproductive genes may underlie the postmating isolation among replicate evolved populations adapting to the same environment with the same standing genetic variation.
Conclusion
Our study confirms that replicated evolution experiments provide valuable insights into the mechanisms of speciation. The rapid emergence of the premating reproductive isolation during temperature adaptation showcases incipient ecological speciation. The potential evidence of postmating reproductive isolation among replicates gave rise to two hypotheses: (1) mutation-order speciation through a common selection on early fecundity leading to an inherent inter-locus sexual conflict; (2) system drift with genetic drift along the neutral ridges.
... Most evolution experiments designed to test the hypothesis that sexual selection drives speciation have not yielded any signs of reproductive isolation (reviewed by Plesnar -Bielak et al. 2013;White et al. 2020). One possible explanation for the negative results is that replicate populations exposed to the same selection regimes do not evolve in arbitrarily different directions. ...
... Similarly, an experimental evolution study in dung flies found that large populations with stronger sexual conflict diverged more than small populations with weaker conflict (Martin and Hosken, 2003). However, similar comparative (Carvalho et al., 2021) and experimental evolution studies in other species have failed to detect such a relationship (Gay et al., 2009;Wigby and Chapman, 2006;Plesnar-Bielak et al., 2013). Although interlocus sexual conflict can lead to population divergence and speciation, this may only occur when certain conditions are met and conflict is unconstrained in populations (Gavrilets, 2014). ...
... Hemiclonal analysis in D. melanogaster was later used to demonstrate a fundamental consequence of intralocus sexual conflict: a negative relationship between the fitness of parents and their opposite-sex offspring. In this study, higher fitness mothers produced lower fitness sons, and higher fitness fathers produced lower fitness daughters (Pischedda and Chippindale, 2006). Additional evidence for intralocus sexual conflict in D. melanogaster comes from experimental evolution studies in which genomes evolved exclusively in males ("male-limited" genomes), removing any potential counter-selection on alleles when expressed in females (Prasad et al., 2007;Rice, 1996). ...
... Intersexual conflict has been predicted to be an important driver of speciation (Gavrilets, 2014). There are two studies that find evidence for incipient speciation via intersexual conflict (Martin & Hosken, 2003, Syed et al., 2017 but also see Bacigalupe et al., 2007, Gay et al., 2009, Plesnar-Bielak et al., 2013. Syed et al. (2017), using male-biased (high sexual conflict) and female-biased (low sexual conflict) operational sex ratio regimes of Drosophila melanogaster, showed that within 105 generations of evolution, the replicate populations of the high sexual conflict regime evolved both premating and postmating prezygotic isolation among themselves. ...
In experimental evolutionary studies, altering sex ratio in populations imposes sex‐biased intrasexual and intersexual interactions, which is useful to study the effect of sexual selection and sexual conflict in such populations. We studied cuticular hydrocarbon (CHC) patterns of 170 generations‐old operational sex ratio‐altered Drosophila melanogaster population to investigate the evolutionary outcomes of such selection lines. Our results indicate that the competing sex in each of the selection lines has less variable CHC profile than the less abundant sex, potentially due to sexual selection. The intensity of sexual selection is possibly influenced by intense competition among the abundant sex as well as potential mate choice due to easy availability of mates for the rarer sex in the population. This result is even more striking since the male‐biased replicates were previously shown to have diverged in terms of mate preferences due to sexually antagonistic coevolution (SAC). The precopulatory isolating mechanism underlying such divergent mate preference could be sexual signals such as CHCs since they evolve rapidly and are involved in D. melanogaster mate recognition. Therefore, we also investigate whether CHC profiles diverged in male‐biased replicates in comparison to female‐biased replicates. We found no evidence that cuticular hydrocarbon profiles of male‐biased and female‐biased populations have evolved due to SAC. This study indicates that the differentiation of sexual traits may not be credited to sexual conflict despite populations isolated due to high sexual conflict evolve divergent cuticular hydrocarbon profiles.
... However, unless the hybrid disadvantage is sufficiently great, it will be in male interest to mate (Kokko & Ots, 2006;Parker, 1974;Parker, 1979;Waser, Austad & Keane, 1986); a wide parameter zone exists over which sexual conflict applies and in this zone selection on females acts as a force favouring speciation by restricting gene flow, but selection on males acts as a force resisting speciation by promoting gene flow. While some empirical studies suggest that sexual conflict promotes speciation, others do not (Gavrilets, 2014;Plesnar-Bielak et al., 2013). ...
In recent years, the field of sexual selection has exploded, with advances in theoretical and empirical research complementing each other in exciting ways. This perspective piece is the product of a ''stock-taking'' workshop on sexual selection and sexual conflict. Our aim is to identify and deliberate on outstanding questions and to stimulate discussion rather than provide a comprehensive overview of the entire field. These questions are organized into four thematic sections we deem essential to the field. First we focus on the evolution of mate choice and mating systems. Variation in mate quality can generate both competition and choice in the opposite sex, with implications for the evolution of mating systems. Limitations on mate choice may dictate the importance of direct vs. indirect benefits in mating decisions and consequently, mating systems, especially with regard to polyandry. Second, we focus on how sender and receiver mechanisms shape signal design. Mediation of honest signal content likely depends on integration of temporally variable social and physiological costs that are challenging to measure. We view the neuroethology of sensory and cognitive receiver biases as the main key to signal form and the 'aesthetic sense' proposed by Darwin. Since a receiver bias is sufficient to both initiate and drive ornament or armament exaggeration, without a genetically correlated or even coevolving receiver, this may be the appropriate 'null model' of sexual selection. Thirdly, we focus on the genetic architecture of sexually selected traits. Despite advances in modern molecular techniques, the number and identity of genes underlying performance, display and secondary sexual traits remains largely unknown. In-depth investigations into the genetic basis of sexual dimorphism in the context of long-term field studies will reveal constraints and trajectories of sexually selected trait evolution. Finally, we focus on sexual selection and conflict as drivers of speciation. Population divergence and speciation are often influenced by an interplay between sexual and natural selection. The extent to which sexual selection promotes How to cite this article Lindsay WR, Andersson S, Bererhi B, Höglund J, Johnsen A, Kvarnemo C, Leder EH, Lifjeld JT, Ninnes CE, Ols-son M, Parker GA, Pizzari T, Qvarnström A, Safran RJ, Svensson O, Edwards SV. 2019. Endless forms of sexual selection. PeerJ 7:e7988 http://doi.org/10.7717/peerj.7988 or counteracts population divergence may vary depending on the genetic architecture of traits as well as the covariance between mating competition and local adaptation. Additionally, post-copulatory processes, such as selection against heterospecific sperm, may influence the importance of sexual selection in speciation. We propose that efforts to resolve these four themes can catalyze conceptual progress in the field of sexual selection, and we offer potential avenues of research to advance this progress.
... However, unless the hybrid disadvantage is sufficiently great, it will be in male 978 interest to mate (Kokko & Ots 2006;Parker 1974;Parker 1979;Waser et al. 1986); a wide 979 parameter zone exists over which sexual conflict applies and in this zone selection on females 980 acts as a force favouring speciation by restricting gene flow, but selection on males acts as a 981 force resisting speciation by promoting gene flow. While some empirical studies suggest that 982 sexual conflict promotes speciation, others do not (Gavrilets 2014;Plesnar-Bielak et al. 2013). ...
In recent years, the field of sexual selection has exploded, with advances in theoretical and empirical research complementing each other in exciting ways. This perspective piece is the product of a “stock-taking” workshop on sexual selection and conflict. Our aim is to identify and deliberate on outstanding questions and to stimulate discussion rather than provide a comprehensive overview of the entire field. These questions are organized into four thematic sections we deem essential to the field. First we focus on the evolution of mate choice and mating systems. Variation in mate quality can generate both competition and choice in the opposite sex, with implications for the evolution of mating systems. Limitations on mate choice may dictate the importance of direct vs. indirect benefits in mating decisions and consequently, mating systems, especially with regard to polyandry. Second, we focus on how sender and receiver mechanisms shape signal design. Mediation of honest signal content likely depends on integration of temporally variable social and physiological costs that are challenging to measure. We view the neuroethology of sensory and cognitive receiver biases as the main key to signal form and the ‘aesthetic sense’ proposed by Darwin. Since a receiver bias is sufficient to both initiate and drive ornament or armament exaggeration, without a genetically correlated or even coevolving receiver, this may be the appropriate ‘null model’ of sexual selection. Thirdly, we focus on the genetic architecture of sexually selected traits. Despite advances in modern molecular techniques, the number and identity of genes underlying performance, display and secondary sexual traits remains largely unknown. In-depth investigations into the genetic basis of sexual dimorphism in the context of long-term field studies will reveal constraints and trajectories of sexually selected trait evolution. Finally, we focus on sexual selection and conflict as drivers of speciation. Population divergence and speciation are often influenced by an interplay between sexual and natural selection. The extent to which sexual selection promotes or counteracts population divergence may vary depending on the genetic architecture of traits as well as the covariance between mating competition and local adaptation. Additionally, post-copulatory processes, such as selection against heterospecific sperm, may influence the importance of sexual selection in speciation. We propose that efforts to resolve these four themes can catalyze conceptual progress in the field of sexual selection, and we offer potential avenues of research to advance this progress.
... Fry found equivocal support for sexual selection generating RI [8]. Subsequent work on sexual selection and speciation continues to fail to find significant RI [14][15][16][17], even when manipulating genetic variation and population size to increase the likelihood of response [14] and assessing different RI barriers [15]. One species, Drosophila melanogaster, has been tested independently in two laboratories but only one study found RI [18,19]. ...
... Fry found equivocal support for sexual selection generating RI [8]. Subsequent work on sexual selection and speciation continues to fail to find significant RI [14][15][16][17], even when manipulating genetic variation and population size to increase the likelihood of response [14] and assessing different RI barriers [15]. One species, Drosophila melanogaster, has been tested independently in two laboratories but only one study found RI [18,19]. ...
Speciation is the result of evolutionary processes that generate barriers to gene flow between populations, facilitating reproductive isolation. Speciation is typically studied via theoretical models and “snap-shot” tests in natural populations. Experimental speciation enables real-time direct tests of speciation theory and has been long-touted as a critical complement to other approaches. We argue that, despite its promise to elucidate the evolution of reproductive isolation, experimental speciation has been underutilised and lags behind other contributions to speciation research. We review recent experiments and outline a framework for how experimental speciation can be implemented to address current outstanding questions that are otherwise challenging to answer. Greater uptake of this approach is necessary to rapidly advance understanding of speciation.
... However, there is no empirical evidence favouring this. Despite multiple studies testing the hypothesis in different organisms, the study by Martin and Hosken remains the only direct evidence of SAC as a driver of RI so far [16][17][18][19][20] , and the idea of sexual conflict as an 'engine of speciation' remains controversial 21 . ...
... A number of studies -while testing if SAC drives reproductive isolation using experimental evolution -have measured postmating isolation extensively in terms of difference in fecundity 17 , offspring number 19,20 , offspring viability 17,18 or offspring sterility 18 , but found no evidence of isolation in those traits. While important, most of them are measures of post-zygotic isolation, which, as these and other studies 7 suggest, are less likely to manifest within tens of generations of selection. ...
Promiscuity can drive the evolution of sexual conflict before and after mating occurs. Post mating, the male ejaculate can selfishly manipulate female physiology, leading to a chemical arms race between the sexes. Theory suggests that drift and sexually antagonistic coevolution can cause allopatric populations to evolve different chemical interactions between the sexes, thereby leading to postmating reproductive barriers and speciation. There is, however, little empirical evidence supporting this form of speciation. We tested this theory by creating an experimental evolutionary model of Drosophila melanogaster populations undergoing different levels of interlocus sexual conflict. We found that allopatric populations under elevated sexual conflict show assortative mating, indicating premating reproductive isolation. Further, these allopatric populations also show reduced copulation duration and sperm defense ability when mating happens between individuals across populations compared to that within the same population, indicating postmating prezygotic isolation. Sexual conflict can cause reproductive isolation in allopatric populations through the coevolution of chemical (postmating prezygotic) as well as behavioural (premating) interactions between the sexes. Thus, to our knowledge, we provide the first comprehensive evidence of postmating (as well as premating) reproductive isolation due to sexual conflict.
... For example, how often does conflict lead to coevolution, diversification, and speciation? There is suggestive and mixed evidence for all of these larger scale outcomes Martin and Hosken 2004;Rice et al. 2005; but see Plesnar-Bielak et al. 2013). Even smaller scale questions remain open. ...
Sexual conflict occurs whenever there is sexually antagonistic selection on shared traits. When shared traits result from interactions (e.g., mating rate) and have a different genetic basis in each sex (i.e., interlocus conflict), then sex-specific traits that shift the value of these interaction traits toward the sex-specific optimum will be favored. Male traits can be favored that increase the fitness of their male bearers, but decrease the fitness of interacting females. Likewise, female traits that reduce the costs of interacting with harmful males may simultaneously impose costs on males. If the evolution of these antagonistic traits changes the nature of selection acting on the opposite sex, interesting coevolutionary dynamics will result. Here we examine three current issues in the study of sexually antagonistic interactions: the female side of sexual conflict, the ecological context of sexual conflict, and the strength of evidence for sexually antagonistic coevolution.
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... However, similar subsequent experiments have largely failed to provide evidence for the evolution of reproductive isolation. These include experiments with D. melanogaster (Wigby and Chapman 2006, but see Ghosh and Joshi 2012), Drosophila pseudoobscura (Bacigalupe et al. 2007), bruchid beetle populations Callosobruchus maculatus (Gay et al. 2009), water strider Gerris gillettei (Gagnon and Turgeon 2011), and the bulb mite Rhizoglyphus robini (Plesnar-Bielak et al. 2013). ...
At the end of the last century, sexual conflict was identified as a powerful engine of speciation, potentially even more important than ecological selection. Earlier work that followed-experimental, comparative, and mathematical-provided strong initial support for this assertion. However, as the field matures, both the power of sexual conflict and constraints on the evolution of reproductive isolation as driven by sexual conflict are becoming better understood. From theoretical studies, we now know that speciation is only one of several possible evolutionary outcomes of sexual conflict. In line with these predictions, both experimental evolution studies and comparative analyses of fertilization proteins and of species richness show that sexual conflict leads to, or is associated with, reproductive isolation and speciation in some cases but not in others. Increased genetic variation (especially in females) without reproductive isolation is an underappreciated consequence of sexually antagonistic selection.
