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

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

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

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

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Mating system variation drives rapid evolution of the female transcriptome in Drosophila pseudoobscura

Interactions between the sexes are believed to be a potent source of selection on sex-specific evolution. The way in which sexual interactions influence male investment is much studied, but effects on females are more poorly understood. To address this deficiency, we examined gene expression in virgin female Drosophila pseudoobscura following 100 generations of mating system manipulations in which we either elevated polyandry or enforced monandry. Gene expression evolution following mating system manipulation resulted in 14% of the transcriptome of virgin females being altered. Polyandrous females elevated expression of a greater number of genes normally enriched in ovaries and associated with mitosis and meiosis, which might reflect female investment into reproductive functions. Monandrous females showed a greater number of genes normally enriched for expression in somatic tissues, including the head and gut and associated with visual perception and metabolism, respectively. By comparing our data with a previous study of sex differences in gene expression in this species, we found that the majority of the genes that are differentially expressed between females of the selection treatments show female-biased expression in the wild-type population. A striking exception is genes associated with male-specific reproductive tissues (in D. melanogaster), which are upregulated in polyandrous females. Our results provide experimental evidence for a role of sex-specific selection arising from differing sexual interactions with males in promoting rapid evolution of the female transcriptome

Variation in pre- and post-copulatory sexual selection on male genital size in two species of lygaeid bug

This study was funded by the Natural Environmental Research Council (DTG studentship 1109354 to LRD).Sexual selection has been shown to be the driving force behind the evolution of the sometimes extreme and elaborate genitalia of many species. Sexual selection may arise before and/or after mating, or vary according to other factors such as the social environment. However, bouts of selection are typically considered in isolation. We measured the strength and pattern of selection acting on the length of the male intromittent organ (or processus) in two closely related species of lygaeid seed bug: Lygaeus equestris and Lygaeus simulans. In both species, we measured both pre- and post-copulatory selection. For L. equestris, we also varied the experimental choice design used in mating trials. We found contrasting pre- and post-copulatory selection on processus length in L. equestris. Furthermore, significant pre-copulatory selection was only seen in mating trials in which two males were present. This selection likely arises indirectly due to selection on a correlated trait, as the processus does not interact with the female prior to copulation. In contrast, we were unable to detect significant pre- or post-copulatory selection on processus length in L. simulans. However, a formal meta-analysis of previous estimates of post-copulatory selection on processus length in L. simulans suggests that there is significant stabilising selection across studies, but the strength of selection varies between experiments. Our results emphasise that the strength and direction of sexual selection on genital traits may be multifaceted and can vary across studies, social contexts and different stages of reproduction.Publisher PDFPeer reviewe

Developmental temperature affects the expression of ejaculatory traits and the outcome of sperm competition in Callosobruchus maculatus

The outcome of post-copulatory sexual selection is determined by a complex set of interactions between the primary reproductive traits of two or more males and their interactions with the reproductive traits of the female. Recently, a number of studies have shown the primary reproductive traits of both males and females express phenotypic plasticity in response to the thermal environment experienced during ontogeny. However, how plasticity in these traits affects the dynamics of sperm competition remains largely unknown. Here, we demonstrate plasticity in testes size, sperm size and sperm number in response to developmental temperature in the bruchid beetle Callosobruchus maculatus. Males reared at the highest temperature eclosed at the smallest body size and had the smallest absolute and relative testes size. Males reared at both the high- and low-temperature extremes produced both fewer and smaller sperm than males reared at intermediate temperatures. In the absence of sperm competition, developmental temperature had no effect on male fertility. However, under conditions of sperm competition, males reared at either temperature extreme were less competitive in terms of sperm offence (P2), whereas those reared at the lowest temperature were less competitive in terms of sperm defence (P1). This suggests the developmental pathways that regulate the phenotypic expression of these ejaculatory traits are subject to both natural and sexual selection: natural selection in the pre-ejaculatory environment and sexual selection in the post-ejaculatory environment. In nature, thermal heterogeneity during development is commonplace. Therefore, we suggest the interplay between ecology and development represents an important, yet hitherto underestimated component of male fitness via post-copulatory sexual selection

Geographic variation in breeding system and environment predicts melanin-based plumage ornamentation of male and female Kentish plovers

Sexual selection determines the elaboration of morphological and behavioural traits and thus drives the evolution of phenotypes. Sexual selection on males and females can differ between populations, especially when populations exhibit different breeding systems. A substantial body of literature describes how breeding systems shape ornamentation across species, with a strong emphasis on male ornamentation and female preference. However, whether breeding system predicts ornamentation within species and whether similar mechanisms as in males also shape the phenotype of females remains unclear. Here, we investigate how different breeding systems are associated with male and female ornamentation in five geographically distinct populations of Kentish plovers Charadrius alexandrinus. We predicted that polygamous populations would exhibit more elaborate ornaments and stronger sexual dimorphism than monogamous populations. By estimating the size and intensity of male (n = 162) and female (n = 174) melanin-based plumage ornaments, i.e. breast bands and ear coverts, we show that plumage ornamentation is predicted by breeding system in both sexes. A difference in especially male ornamentation between polygamous (darker and smaller ornaments) and monogamous (lighter and larger) populations causes the greatest sexual dimorphism to be associated with polygamy. The non-social environment, however, may also influence the degree of ornamentation, for instance through availability of food. We found that, in addition to breeding system, a key environmental parameter, rainfall, predicted a seasonal change of ornamentation in a sex-specific manner. Our results emphasise that to understand the phenotype of animals, it is important to consider both natural and sexual selection acting on both males and females

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