The definition of sexual selection : a response to comments on Shuker and Kvarnemo

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The definition of sexual selection

The work was supported by Vetenskapsrådet (2020-04992) to C.K.Sexual selection is a key component of evolutionary biology. However, from the very formulation of sexual selection by Darwin, the nature and extent of sexual selection have been controversial. Recently, such controversy has led back to the fundamental question of just what sexual selection is. This has included how we incorporate female-female reproductive competition into sexual or natural selection. In this review, we do four things. First, we examine what we want a definition to do. Second, we define sexual selection: sexual selection is any selection that arises from fitness differences associated with nonrandom success in the competition for access to gametes for fertilization. An important outcome of this is that as mates often also offer access to resources, when those resources are the targets of the competition, rather than their gametes, the process should be considered natural rather than sexual selection. We believe this definition encapsulates both much of Darwin’s original thinking about sexual selection, and much of how contemporary biologists use the concept of sexual selection. Third, we address alternative definitions, focusing in some detail on the role of female reproductive competition. Fourth, we challenge our definition with a number of scenarios, for instance where natural and sexual selection may align (as in some forms of endurance rivalry), or where differential allocation means teasing apart how fecundity and access to gametes influence fitness. In conclusion, we emphasize that whilst the ecological realities of sexual selection are likely to be complex, the definition of sexual selection is rather simple.Publisher PDFPeer reviewe

Immigrant reproductive dysfunction facilitates ecological speciation

The distributions of species are not only determined by where they can survive – they must also be able to reproduce. Although immigrant inviability is a well-established concept, the fact that immigrants also need to be able to effectively reproduce in foreign environments has not been fully appreciated in the study of adaptive divergence and speciation. Fertilization and reproduction are sensitive life-history stages that could be detrimentally affected for immigrants in non-native habitats. We propose that “immigrant reproductive dysfunction” is a hitherto overlooked aspect of reproductive isolation caused by natural selection on immigrants. This idea is supported by results from experiments on an externally fertilizing fish (sand goby, Pomatoschistus minutus). Growth and condition of adults were not affected by non-native salinity whereas males spawning as immigrants had lower sperm motility and hatching success than residents. We interpret these results as evidence for local adaptation or acclimation of sperm, and possibly also components of paternal care. The resulting loss in fitness, which we call “immigrant reproductive dysfunction,” has the potential to reduce gene flow between populations with locally adapted reproduction, and it may play a role in species distributions and speciation

Effects of salinity on nest-building behaviour in a marine fish

Background: Parental allocation and reproductive success are often strongly influenced by environmental factors. In this respect, salinity is a key factor influencing species distributions and community structure in aquatic animals. Nevertheless, the effects of salinity on reproductive behaviours are not well known. Here, we used the sand goby (Pomatoschistus minutus), a small fish inhabiting a range of different salinities, to experimentally assess the effects of changes in salinity on nesting behaviour, a key component of reproduction in sand gobies and many other taxa. Results: We found that salinity levels influenced some aspects of male nesting behaviour (i.e. nest entrance size) but not others (i.e. latency to build a nest, choice of nest site, sand on top of nest) and that small and large individuals were differently affected. In particular, the importance of body size in adjustment of nest entrance depended on the salinity level. Conclusion: The results support the prediction that geographically widespread aquatic species, such as sand gobies, are able to perform well under a range of salinity levels. The phenotype by environment interaction found between male size and behavioural responses to salinity can, in turn, help to explain the notable variation observed in nest-building (and other) behaviours closely linked to reproduction.Peer reviewe

Socially induced tactic change in 2 types of sand goby sneaker males

Male alternative reproductive tactics, like satellite or sneaking tactics, typically parasitize reproductively on a larger resource-holding tactic. In the sand goby, Pomatoschistus minutus, 2 types of sneaker males are known. Sneaker males with melanization, a typical male breeding coloration, have small testes and large sperm-duct glands, and sneaker males without melanization have large testes and small sperm-duct glands. We tested their potential to change into the nest-holding tactic experimentally by keeping them with or without a large nest-holding male. With nest-holding males, neither sneaker male type built nests. However, without nest-holding males, a large proportion of both types of sneaker males built nests and became nest-holders, and all the nest-building nonmelanized sneaker males developed melanization. Furthermore, nest-building nonmelanized sneaker males had larger sperm-duct glands (used to produce a sperm-containing mucus) than nonnest-building nonmelanized sneaker males. However, contrary to our expectation, treatment did not affect testes size. Compared with melanized sneaker males nonmelanized sneaker males tended to have a lower proportion of nest-building males and showed significantly less reproductive activity, especially in the early experimental period. Finally, in a separate experiment, we confirmed that nonmelanized sneaker males that build nests can spawn and tend eggs normally. Taken together, our results suggest that these tactics are not genetically or ontogenetically fixed but condition dependent. However, this does not exclude an underlying genetic variation in phenotype expression

Sperm adaptation in relation to salinity in three goby species

In externally fertilizing species, the gametes of both males and females are exposed to the influences of the environment into which they are released. Sperm are sensitive to abiotic factors such as salinity, but they are also affected by biotic factors such as sperm competition. In this study, the authors compared the performance of sperm of three goby species, the painted goby, Pomatoschistus pictus, the two-spotted goby, Pomatoschistus flavescens, and the sand goby, Pomatoschistus minutus. These species differ in their distributions, with painted goby having the narrowest salinity range and sand goby the widest. Moreover, data from paternity show that the two-spotted goby experiences the least sperm competition, whereas in the sand goby sperm competition is ubiquitous. The authors took sperm samples from dissected males and exposed them to high salinity water (31 PSU) representing the North Sea and low salinity water (6 PSU) representing the brackish Baltic Sea Proper. They then used computer-assisted sperm analysis to measure the proportion of motile sperm and sperm swimming speed 10 min and 20 h after sperm activation. The authors found that sperm performance depended on salinity, but there seemed to be no relationship to the species' geographical distribution in relation to salinity range. The species differed in the proportion of motile sperm, but there was no significant decrease in sperm motility during 20 h. The sand goby was the only species with motile sperm after 72 h

Till death (or an intruder) do us part: intrasexual-competition in a monogamous Primate

Polygynous animals are often highly dimorphic, and show large sex-differences in the degree of intra-sexual competition and aggression, which is associated with biased operational sex ratios (OSR). For socially monogamous, sexually monomorphic species, this relationship is less clear. Among mammals, pair-living has sometimes been assumed to imply equal OSR and low frequency, low intensity intra-sexual competition; even when high rates of intra-sexual competition and selection, in both sexes, have been theoretically predicted and described for various taxa. Owl monkeys are one of a few socially monogamous primates. Using long-term demographic and morphological data from 18 groups, we show that male and female owl monkeys experience intense intra-sexual competition and aggression from solitary floaters. Pair-mates are regularly replaced by intruding floaters (27 female and 23 male replacements in 149 group-years), with negative effects on the reproductive success of both partners. Individuals with only one partner during their life produced 25% more offspring per decade of tenure than those with two or more partners. The termination of the pair-bond is initiated by the floater, and sometimes has fatal consequences for the expelled adult. The existence of floaters and the sporadic, but intense aggression between them and residents suggest that it can be misleading to assume an equal OSR in socially monogamous species based solely on group composition. Instead, we suggest that sexual selection models must assume not equal, but flexible, context-specific, OSR in monogamous species.Wenner-Gren Foundation, L.S.B. Leakey Foundation, the National Geographic Society, National Science Foundation (BCS- 0621020), the University of Pennsylvania Research Foundation and the Zoological Society of San Diego, German Science Foundation (HU 1746-2/1

Endless forms of sexual selection

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\u27\u27 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 \u27aesthetic sense\u27 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 \u27null model\u27 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

Molecular, behavioural and morphological comparisons of sperm adaptations in a fish with alternative reproductive tactics

In species with alternative reproductive tactics, there is much empirical support that parasitically spawning males have larger testes and greater sperm numbers as an evolved response to a higher degree of sperm competition, but support for higher sperm performance (motility, longevity and speed) by such males is inconsistent. We used the sand goby (Pomatoschistus minutus) to test whether sperm performance differed between breeding-coloured males (small testes, large mucus-filled sperm-duct glands; build nests lined with sperm-containing mucus, provide care) and parasitic sneaker-morph males (no breeding colouration, large testes, rudimentary sperm-duct glands; no nest, no care). We compared motility (per cent motile sperm), velocity, longevity of sperm, gene expression of testes and sperm morphometrics between the two morphs. We also tested if sperm-duct gland contents affected sperm performance. We found a clear difference in gene expression of testes between the male morphs with 109 transcripts differentially expressed between the morphs. Notably, several mucin genes were upregulated in breeding-coloured males and two ATP-related genes were upregulated in sneaker-morph males. There was a partial evidence of higher sperm velocity in sneaker-morph males, but no difference in sperm motility. Presence of sperm-duct gland contents significantly increased sperm velocity, and nonsignificantly tended to increase sperm motility, but equally so for the two morphs. The sand goby has remarkably long-lived sperm, with only small or no decline in motility and velocity over time (5 min vs. 22 h), but again, this was equally true for both morphs. Sperm length (head, flagella, total and flagella-to-head ratio) did not differ between morphs and did not correlate with sperm velocity for either morph. Thus, other than a clear difference in testes gene expression, we found only modest differences between the two male morphs, confirming previous findings that increased sperm performance as an adaptation to sperm competition is not a primary target of evolution.</p

Post-glacial establishment of locally adapted fish populations over a steep salinity gradient

Studies of colonization of new habitats that appear from rapidly changing environments are interesting and highly relevant to our understanding of divergence and speciation. Here, we analyse phenotypic and genetic variation involved in the successful establishment of a marine fish (sand goby,Pomatoschistus minutus) over a steep salinity drop from 35 PSU in the North Sea (NE Atlantic) to two PSU in the inner parts of the post-glacial Baltic Sea. We first show that populations are adapted to local salinity in a key reproductive trait, the proportion of motile sperm. Thereafter, we show that genome variation at 22,190 single nucleotide polymorphisms (SNPs) shows strong differentiation among populations along the gradient. Sequences containing outlier SNPs and transcriptome sequences, mapped to a draft genome, reveal associations with genes with relevant functions for adaptation in this environment but without overall evidence of functional enrichment. The many contigs involved suggest polygenic differentiation. We trace the origin of this differentiation using demographic modelling and find the most likely scenario is that at least part of the genetic differentiation is older than the Baltic Sea and is a result of isolation of two lineages prior to the current contact over the North Sea-Baltic Sea transition zone