Search

Evolutionary biologists have endeavoured to explain the extraordinary diversity of sperm morphology across animals for more than a century. One hypothesis to explain sperm diversity is that sperm length is shaped by the environment where fertilization takes place (that is, fertilization mode). Evolutionary transitions in fertilization modes may transform how selection acts on sperm length, probably by affecting postcopulatory mechanisms of sperm competition and the scope for cryptic female choice. Here, we address this hypothesis by generating a macro-evolutionary view of how fertilization mode (including external fertilizers, internal fertilizers and spermcasters) influences sperm length diversification among 3,233 species from 21 animal phyla. We show that sperm are shorter in species whose sperm are diluted in aquatic environments (that is, external fertilizers and spermcasters) and longer in species where sperm are directly transferred to females (that is, internal fertilizers). We also show that sperm length evolves faster and with a greater number of adaptive shifts in species where sperm operate within females (for example, spermcasters and internal fertilizers). Our results demonstrate that fertilization mode is a key driver in the evolution of sperm length across animals, and we argue that a complex combination of postcopulatory forces has shaped sperm length diversification throughout animal evolution.

Sexual dimorphism is typically thought to result from sexual selection for elaborated male traits, as proposed by Darwin. However, natural selection could reduce expression of elaborated traits in females, as proposed by Wallace. Darwin and Wallace debated the origins of dichromatism in birds and butterflies, and although evidence in birds is roughly equal, if not in favor of Wallace's model, butterflies lack a similar scale of study. Here, we present a large-scale comparative phylogenetic analysis of the evolution of butterfly coloration, using all European non-hesperiid butterfly species (n = 369). We modeled evolutionary changes in coloration for each species and sex along their phylogeny, thereby estimating the rate and direction of evolution in three-dimensional color space using a novel implementation of phylogenetic ridge regression. We show that male coloration evolved faster than female coloration, especially in strongly dichromatic clades, with male contribution to changes in dichromatism roughly twice that of females. These patterns are consistent with a classic Darwinian model of dichromatism via sexual selection on male coloration, suggesting this model was the dominant driver of dichromatism in European butterflies.

Inbreeding depression, the reduced fitness of the offspring of related individuals, can affect males and females differently. Although a comprehensive theoretical framework describing the causes of sex-specific inbreeding depression is lacking, empirical evidence suggests that often one sex tends to be more vulnerable than the other. However, the generality, direction, and degree of sex-specific difference in inbreeding depression remains enigmatic as studies on this topic have reported conflicting results. Here, we conduct a meta-analysis to test for sex-specific differences in the magnitude of inbreeding depression. We synthetised 321 effect sizes of experimental studies across 47 species and found a small difference in inbreeding depression between the sexes: females suffered slightly higher inbreeding depression than males. Furthermore, a higher inbreeding coefficient was correlated with higher inbreeding depression. However, there was a large amount of heterogeneity that remained unexplained, even when considering different factors that could affect inbreeding between the sexes, such as sexual size dimorphism, heterogamety, the type of trait measured and whether animals were tested in a stressful environment. As such, we highlight the need to further explore inbreeding depression across different species to determine the occurrence and causes of sex differences to increase our understanding of the evolutionary consequences of sex-specific inbreeding depression.

Post-copulatory sexual selection, and sperm competition in particular, is a powerful selective force shaping the evolution of sperm morphology. Although mounting evidence suggests that post-copulatory sexual selection influences the evolution of sperm morphology among species, recent evidence also suggests that sperm competition influences variation in sperm morphology at the intraspecific level. However, contradictory empirical results and limited taxonomic scope have led to difficulty in assessing the generality of sperm morphological responses to variation in the strength of sperm competition. Here, we use phylogenetically controlled analyses to explore the effects of sperm competition on sperm morphology and variance in sharks, a basal vertebrate group characterized by wide variation in rates of multiple mating by females, and consequently sperm competition risk. Our analyses reveal that shark species experiencing greater levels of sperm competition produce sperm with longer flagella and that sperm flagellum length is less variable in species under higher sperm competition risk. In contrast, neither the length of the sperm head and midpiece nor variation in sperm head and midpiece length was associated with sperm competition risk. Our findings demonstrate that selection influences both the inter- and intraspecific variation in sperm morphology and suggest that the flagellum is an important target of sexual selection in sharks. These findings provide important insight into patterns of selection on the ejaculate in a basal vertebrate lineage.

Choosing a mate is one of the most important decisions in an animal’s lifetime. Female mate choice is often guided by the presence or intensity of male sexual ornaments, which must be integrated and compared among potential mates. Individuals with greater cognitive abilities may be better at evaluating and comparing sexual ornaments, even when the difference in ornaments is small. While brain size is often used as a proxy for cognitive ability, its effect on mate choice has rarely been investigated. Here, we investigate the effect of brain size on mate preferences in the pygmy halfbeak Dermogenys collettei, a small freshwater fish that forms mixed-sex shoals where mating takes place. Pygmy halfbeaks are ideal models as their semi-transparent heads allow for external brain measurements. After validating the use of external measurements as a proxy for internal brain size, we presented females with large or small brains (relative to body length) with two males that had either a large or small difference in sexual ornamentation (measured by the total area of red coloration). Unexpectedly, neither total relative brain size nor relative telencephalon size affected any measured aspect of mate preference. However, the difference in male sexual ornamentation did affect preference, with females preferring males with a smaller area of red coloration when the difference in ornaments was large. This study highlights the complexities of mate choice and the importance of considering a range of stimuli when examining mate preferences., Does a bigger brain make you better at choosing a good mate? Using a small fish called a pygmy halfbeak, we show that females with bigger brains are not better at choosing mates compared to females with smaller brains. However, we discovered that female preference depends on how different males are—females prefer males with less red coloration on their bodies when there is a big difference between the two males.

Animals are usually expected to avoid mating with relatives (kin avoidance) as incestuous mating can lead to the expression of inbreeding depression. Yet, theoretical models predict that unbiased mating with regards to kinship should be common, and that under some conditions, the inclusive fitness benefits associated with inbreeding can even lead to a preference for mating with kin. This mismatch between empirical and theoretical expectations generates uncertainty as to the prevalence of inbreeding avoidance in animals. Here, we synthesized 677 effect sizes from 139 experimental studies of mate choice for kin versus non-kin in diploid animals, representing 40 years of research, using a meta-analytical approach. Our meta-analysis revealed little support for the widely held view that animals avoid mating with kin, despite clear evidence of publication bias. Instead, unbiased mating with regards to kinship appears widespread across animals and experimental conditions. The significance of a variety of moderators was explored using meta-regressions, revealing that the degree of relatedness and prior experience with kin explained some variation in the effect sizes. Yet, we found no difference in kin avoidance between males and females, choice and no-choice experiments, mated and virgin animals or between humans and animals. Our findings highlight the need to rethink the widely held view that inbreeding avoidance is a given in experimental studies.

Sperm competition is a powerful selective force that has shaped sexual traits throughout animal evolution. Yet, how fertilization mode (i.e. external versus internal fertilization) influences the scope and potential for sperm competition to act on ejaculates remains unclear. Here, I examine how fertilization mode shapes ejaculatory responses to sperm competition in fishes, a diverse group that constitute the majority of vertebrate biological diversity. Fishes are an ideal group for this examination because they exhibit a wide range of reproductive behaviours and an unparalleled number of transitions in fertilization mode compared to any other vertebrate group. Drawing on data from cartilaginous and bony fishes, I first show that rates of multiple paternity are higher in internally than externally fertilizing fishes, contrary to the prevailing expectation. I then summarize how sperm competition acts on sperm number and quality in internally and externally fertilizing fishes, highlighting where theoretical predictions differ between these groups. Differences in how ejaculates respond to sperm competition between fertilization modes are most apparent when considering sperm size and swimming performance. Clarifying how fertilization mode influences evolutionary responses in ejaculates will inform our understanding of ejaculate evolution across the animal tree of life. This article is part of the theme issue ‘Fifty years of sperm competition’.

Evolutionary biologists have endeavoured to explain the extraordinary diversity of sperm morphology across animals for more than a century. One hypothesis to explain sperm diversity is that sperm length is shaped by the environment where fertilization takes place (that is, fertilization mode). Evolutionary transitions in fertilization modes may transform how selection acts on sperm length, probably by affecting postcopulatory mechanisms of sperm competition and the scope for cryptic female choice. Here, we address this hypothesis by generating a macro-evolutionary view of how fertilization mode (including external fertilizers, internal fertilizers and spermcasters) influences sperm length diversification among 3,233 species from 21 animal phyla. We show that sperm are shorter in species whose sperm are diluted in aquatic environments (that is, external fertilizers and spermcasters) and longer in species where sperm are directly transferred to females (that is, internal fertilizers). We also show that sperm length evolves faster and with a greater number of adaptive shifts in species where sperm operate within females (for example, spermcasters and internal fertilizers). Our results demonstrate that fertilization mode is a key driver in the evolution of sperm length across animals, and we argue that a complex combination of postcopulatory forces has shaped sperm length diversification throughout animal evolution.

Spermatozoa are the most morphologically diverse cell type, leading to the widespread assumption that they evolve rapidly. However, there is no direct evidence that sperm evolve faster than other male traits. Such a test requires comparing male traits that operate in the same selective environment, ideally produced from the same tissue, yet vary in function. Here, we examine rates of phenotypic evolution in sperm morphology using two insect groups where males produce fertile and non-fertile sperm types (Drosophila species from the obscura group and a subset of Lepidoptera species), where these constraints are solved. Moreover, in Drosophila we test the relationship between rates of sperm evolution and the link with the putative selective pressures of fertilization function and postcopulatory sexual selection exerted by female reproductive organs. We find repeated evolutionary patterns across these insect groups—lengths of fertile sperm evolve faster than non-fertile sperm. In Drosophila, fertile sperm length evolved faster than body size, but at the same rate as female reproductive organ length. We also compare rates of evolution of different sperm components, showing that head length evolves faster in fertile sperm while flagellum length evolves faster in non-fertile sperm. Our study provides direct evidence that sperm length evolves more rapidly in fertile sperm, probably because of their functional role in securing male fertility and in response to selection imposed by female reproductive organs.

Mate choice can continue after mating via chemical communication between the female reproductive system and sperm. While there is a growing appreciation that females can bias sperm use and paternity by exerting cryptic female choice for preferred males, we know surprisingly little about the mechanisms underlying these post-mating choices. In particular, whether chemical signals released from eggs (chemoattractants) allow females to exert cryptic female choice to favour sperm from specific males remains an open question, particularly in species (including humans) where adults exercise pre-mating mate choice. Here, we adapt a classic dichotomous mate choice assay to the microscopic scale to assess gamete-mediated mate choice in humans. We examined how sperm respond to follicular fluid, a source of human sperm chemoattractants, from either their partner or a non-partner female when experiencing a simultaneous or non-simultaneous choice between follicular fluids. We report robust evidence under these two distinct experimental conditions that follicular fluid from different females consistently and differentially attracts sperm from specific males. This chemoattractant-moderated choice of sperm offers eggs an avenue to exercise independent mate preference. Indeed, gamete-mediated mate choice did not reinforce pre-mating human mate choice decisions. Our results demonstrate that chemoattractants facilitate gamete-mediated mate choice in humans, which offers females the opportunity to exert cryptic female choice for sperm from specific males.

Higher social status is expected to result in fitness benefits as it secures access to potential mates. In promiscuous species, male reproductive success is also determined by an individual’s ability to compete for fertilization after mating by producing high-quality ejaculates. However, the complex relationship between a male’s investment in social status and ejaculates remains unclear. Here, we examine how male social status influences ejaculate quality under a range of social contexts in the pygmy halfbeak Dermogenys collettei, a small, group-living, internally fertilizing freshwater fish. We show that male social status influences ejaculate traits, both in the presence and absence of females. Dominant males produced faster swimming and more viable sperm, two key determinants of ejaculate quality, but only under conditions with frequent male–male behavioral interactions. When male–male interactions were experimentally reduced through the addition of a refuge, differences in ejaculate traits of dominant and subordinate males disappeared. Furthermore, dominant males were in a better condition, growing faster, and possessing larger livers, highlighting a possible condition dependence of competitive traits. Contrary to expectations, female presence or absence did not affect sperm swimming speed or testes mass. Together, these results suggest a positive relationship between social status and ejaculate quality in halfbeaks and highlight that the strength of behavioral interactions between males is a key driver of social-status-dependent differences in ejaculate traits., The winner takes it all? In the pygmy halfbeak fish, males who win fights are also likely to win fertilization bouts by producing superior ejaculates. Socially dominant males have faster swimming sperm and more viable ejaculates than subordinates, challenging the common conception that males need to specialize. However, dominant halfbeaks can only surpass subordinates in ejaculate quality if there is ample opportunity for fighting. If fighting between males is infrequent, no differences in ejaculates emerge.

Female multiple mating provides the opportunity for sexual selection to continue after gamete release, generating strong selection on male reproductive traits. In particular, in species where femal ...

The domestication of animals and plants offers an exceptional opportunity to study evolutionary adaptations. In particular, domesticated animals display several behavioral alterations, including increased sociability and decreased fearfulness and aggression, when compared with their wild ancestors. However, studies quantifying simultaneous changes in multiple behaviors during domestication are lacking. Moreover, the role of human-directed play behavior has been largely neglected when studying the domestication process. Here we address these issues by examining behavioral changes during the domestication of the dog (Canis familiaris) from the gray wolf (Canis lupus) using a standardized behavioral test applied to wolf hybrids and several dog breeds. Contrary to expectations, our study provides little support for collective behavioral alterations. Specifically, although we found that wolf hybrids were less playful and overall more fearful than dogs, we did not detect any differences in sociability or aggression between wolf hybrids and dog breeds. Instead, our results suggest that behavioral alterations during domestication do not necessarily occur in concert and point to an important, but previously overlooked, role of selection on play behavior directed at humans during the domestication of dogs. (PsycINFO Database Record (c) 2018 APA, all rights reserved).

Identifying mechanisms of reproductive isolation is key to understanding speciation. Among the putative mechanisms underlying reproductive isolation, sperm-female interactions (postmating-prezygotic barriers) are arguably the hardest to identify, not least because these are likely to operate at the cellular or molecular level. Yet sperm-female interactions offer great potential to prevent the transfer of genetic information between different populations at the initial stages of speciation. Here we provide a preliminary test for the presence of a putative postmating-prezygotic barrier operating between three populations of Trinidadian guppies (Poecilia reticulata), an internally fertilizing fish that inhabits streams with different levels of connectivity across Trinidad. We experimentally evaluate the effect of female ovarian fluid on sperm velocity (a predictor of competitive fertilization success) according to whether males and females were from the same (native) or different (foreign) populations. Our results reveal the potential for ovarian fluid to act as a postmating-prezygotic barrier between two populations from different drainages, but also that the strength of this barrier is different among populations. This result may explain the previous finding that, in some populations, sperm from native males have precedence over foreign sperm, which could eventually lead to reproductive isolation between these populations. This article is protected by copyright. All rights reserved.

The nurse shark, Ginglymostoma cirratum (Bonnaterre, 1778) is one of the most studied species of elasmobranchs. However, the knowledge of their reproductive biology is still relatively rare, particularly in the western South Atlantic. This study aimed to describe the morphology of the uterus and the ovary of G. cirratum, based on specimens caught off at the Fortaleza/CE coast, northeast Brazil. Samples were collected from September 2012 to June 2013, from regular landings of artisanal fishing, which commercialize this species freely. A total of ten females were collected. The methodologies followed for analyzing the ovaries and uterus of those females included both macroscopic and histological analysis. G. cirratum has internal type ovary morphology, with invaginations of connective tissue, which defines compartments and separate oocyte groups in ovigerous lots. The epithelium lining the ovary changes from simple columnar ciliated in the area without ovigerous lots, which turns into a simple cubic epithelium in the coating portion of the epigonal organ where ovarian tissue is absent. The uterine mucosa has secretory cells denoted by Alcian Blue staining, indicating the production of mucopolysaccharides, even in immature individuals. This lecithotrophic shark has a uterine vascularized mucosa that is one characteristic of viviparous elasmobranch species. RESUMO: O tubarão-lixa, Ginglymostoma cirratum (Bonnaterre, 1778) é uma das espécies mais estudadas de elasmobrânquios. O conhecimento de sua biologia reprodutiva, no entanto, ainda é relativamente raro, particularmente no Oeste do Atlântico Sul. Este estudo objetivou a descrição morfológica do útero e ovário de G. cirratum, baseado em espécimes capturados na costa de Fortaleza/CE, no Nordeste do Brasil. Um total de dez fêmeas foi coletado de setembro de 2012 a junho de 2013, nos desembarques regulares da pesca artesanal, que comercializam essa espécie livremente. A metodologia foi de acordo com as analises macroscópica e histológica dos ovários e útero. G. cirratum tem o tipo de morfologia de ovário interno, com invaginações de tecido conjuntivo, que define compartimentos e separa grupos de oócitos em lotes ovígeros. O epitélio que reveste o ovário varia de epitélio simples colunar ciliado na área que não apresenta lotes ovígeros para epitélio simples cúbico na porção de revestimento do órgão epigonal, onde o tecido ovariano é ausente. A mucosa uterina possui células secretoras, evidenciadas pela coloração em Alcian Blue, indicando a produção de mucopolissacarídeos, mesmo em indivíduos imaturos. Este tubarão lecitotrófico apresenta a mucosa uterina vascularizada, sendo esta uma característica de espécies de elasmobrânquios vivíparos.

Reproductive competition generates episodes of both pre- and postcopulatory sexual selection. Theoretical models of sperm competition predict that as the fitness gains from expenditure on the weapons of male combat increase, males should increase their expenditure on weapons and decrease their expenditure on traits that contribute to competitive fertilization success. Although traits subject to sexual selection are known to have accelerated evolutionary rates of phenotypic divergence, it is not known whether the competing demands of investment into pre- and postcopulatory traits affect their relative rates of evolutionary divergence. We use a comparative approach to estimate the rates of divergence in pre- and postcopulatory traits among onthophagine dung beetles. Weapons evolved faster than body size while testes mass and sperm length evolved more slowly than body size, suggesting that precopulatory competition is the stronger episode of sexual selection acting on these beetles. Although horns evolved faster than testes, evolutionary increases in horn length were not associated with evolutionary reductions in testes mass. Our data for onthophagines support the notion that in taxa where males are unable to monopolize paternity, expenditure on both weapons and testes should both be favored.

Characterization of the reproductive anatomy of elasmobranchs (sharks, skates, rays, and sawfish) offers unique insights into the evolution of reproductive traits in animals due to their phylogenetic position at the base of the vertebrate tree of life. Yet, despite advances in our understanding of male elasmobranch reproductive physiology and testes histology, very little is known about how testes histomorphometrics varies with male maturation. In this study, we characterize and contrast testes morphology and histomorphology of males at different maturation stages in three shark species with diametric testes development: Prionaceglauca, Rhizoprionodon lalandii, and Mustelus canis. All stages of spermatogenesis were observed in P. glauca and R. lalandii, while for M. canis, only males at early stages of maturation were examined and therefore all the spermatogenesis cells lineage were not present. The number of Sertoli cells increased with cell development by six times in R. lalandii and roughly four times in P. glauca, and were statistically different among stages of spermatogenesis cysts in both species. Statistical differences in cyst diameter and Sertoli cell numbers were observed between P. glauca and R. lalandii. The increase of spermatocyte II cell diameter described for R. Lalandii in this study was not usual to elasmobranch species as compared, for example, to P. glauca. This information proves the importance of studying the testicular development and the process of spermatogenesis is necessary for understanding the reproductive biology of the species, including life cycles and history, variation of reproductive morphology. Anat Rec, 299:759-768, 2016. © 2016 Wiley Periodicals, Inc.

In the version of this Article originally published, references were missing from the column "Source(s) for mating and parental care system data" in Supplementary Table 1. The following references have now been added to the relevant species: Brichard 1989 has been added to Chalinochromis popelini, Chalinochromis brichardi and Julidochromis dickfeldi; Clabaut et al. 2007 to Altolamprologus calvus and Julidochromis regani; Konings 1998 to Neolamprologus hecqui; and Kuwamura 1997 to Chalinochromis popelini.

Male genitalia exhibit patterns of divergent evolution driven by sexual selection. In contrast, for many taxonomic groups, female genitalia are relatively uniform and their patterns of evolution remain largely unexplored. Here we quantify variation in the shape of female genitalia across onthophagine dung beetles, and use new comparative methods to contrast their rates of divergence with those of male genitalia. As expected, male genital shape has diverged more rapidly than a naturally selected trait, the foretibia. Remarkably, female genital shape has diverged nearly three times as fast as male genital shape. Our results dispel the notion that female genitalia do not show the same patterns of divergent evolution as male genitalia, and suggest that female genitalia are under sexual selection through their role in female choice., Although male genital shape is known to evolve rapidly in response to sexual selection, relatively little is known about the evolution of female genital shape. Here, the authors show that across onthophagine dung beetles, female genital shape has diverged much more rapidly than male genital shape.

Using the plainfin midshipman fish Porichthys notatus, a species with alternative reproductive tactics (ARTs), we investigated how sperm maturation shapes sperm competitive abilities. We compared sperm performance and morphology before and after final sperm maturation by sampling sperm from the testes and stripped ejaculates of guarders and sneakers. In accordance with sperm competition risk theory, ejaculates from sneaker males had three times as much sperm as ejaculates from guarder males and sneaker males produced faster swimming sperm than guarder males, but this was only the case after final sperm maturation had occurred. Additionally, fully mature sperm found in ejaculates had larger heads and midpieces than sperm found in the testes. These results emphasize the important role played by non-sperm components of an ejaculate in mediating sperm performance and potentially also morphology.

Mate choice plays a well-known role in the evolution of secondary sexual traits important in precopulatory competition. However, few studies have linked mate choice with the evolution of postcopulatory competitive traits. Here, we explore how variation in male mating behaviors and female mate choice insuences male investment in reproductive traits that enhance sperm competition, a for m of postcopulatory maleÐmale competition. By combining ecological and physiological data from wild plainÞn midshipman ( Porichthys notatus ), a marine Þsh species with 2 alternative reproductive tactics (guarder and sneaker males), we show that female mate choice is associated with uneven sperm competition risk between male reproductive tactics as well as among males using the same repro -ductive tactic. Larger guarder males attracted more females and experienced higher rates of attempted cuckoldry compared with smaller guarder males. In turn, larger guarder males appear adapted to this increased sperm competition risk, producing faster sperm than smaller guarder males. Sneaker males (the smallest males of all) had faster swimming sperm, with larger sperm midpieces and smaller sperm heads than did guarder males. These results suggest that female choice can amplify the selection gradient acting on males both between and within reproductive tactics.

In many species, the negative fitness effects of inbreeding have facilitated the evolution of a wide range of inbreeding avoidance mechanisms. Although avoidance mechanisms operating prior to mating are well documented, evidence for postcopulatory mechanisms of inbreeding avoidance remain scarce. Here, we examine the potential for paternity biases to favour unrelated males when their sperm compete for fertilizations though postcopulatory inbreeding avoidance mechanisms in the guppy, Poecilia reticulata. To test this possibility, we used a series of artificial inseminations to deliver an equal number of sperm from a related (either full sibling or half sibling) and unrelated male to a female while statistically controlling for differences in sperm quality between rival ejaculates. In this way, we were able to focus exclusively on postcopulatory mechanisms of inbreeding avoidance and account for differences in sperm competitiveness between rival males. Under these carefully controlled conditions, we report a significant bias in paternity towards unrelated males, although this effect was only apparent when the related male was a full sibling. We also show that sperm competition generally favours males with highly viable sperm and thus that some variance in sperm competitiveness can be attributed to difference in sperm quality. Our findings for postcopulatory inbreeding avoidance are consistent with prior work on guppies, revealing that sperm competition success declines linearly with the level of relatedness, but also that such effects are only apparent at relatedness levels of full siblings or higher. These findings reveal that postcopulatory processes alone can facilitate inbreeding avoidance.

This study reports a novel form of testicular development in nurse sharks (Ginglymostoma cirratum) and provides the first histological description of spermatogenesis in this species. Radially structured testes developed from the caudal to the cranial regions, a pattern that appears to be unique among shark species. Testes from immature males had spermatogonia and Sertoli cells, while in testes of developing and capable to reproduce males, the nuclei of Sertoli cells were evident in basal positions of spermatocyst. The spermatogonia divide to form primary spermatocytes, secondary spermatocytes divide to produce spermatids, and spermatids then move to the periphery of the spermatocyst. Subsequently, the cysts with spermatids were observed at different stages of maturation, and spermatids became spermatozoa. In the final stage of spermatogenesis, spermatozoa had their heads directed towards the basal membrane and flagella directed towards the lumen. Examinations of testes development in a broad range of shark species are now required to determine whether this novel form of testes development observed in nurse sharks is shared by other elasmobranch species.

Sperm velocity is a key determinant of competitive fertilization success in many species. Selection is therefore expected to favour the evolution of faster sperm when the level of sperm competition is high. However, several aspects can determine the direction and strength of selection acting on this key performance trait, including ecological factors that influence both sperm competition and the strength of selection acting on correlated traits that may constrain evolutionary responses in sperm velocity. Here, we determine how a key ecological variable, the level of predation, shapes sperm swimming speed across 18 Trinidadian populations of guppies ( Poecilia reticulata ). We use performance analysis, a statistical tool akin to the familiar methods of multivariate selection analyses, to determine how the level of predation influences sperm velocity (modelled as a performance trait) when accounting for correlated pre- and postcopulatory traits that are also impacted by predation. We show that predation affects the combination of pre- and postcopulatory traits that ultimately predict sperm performance. Overall, we report evidence for disruptive relationships between sperm performance and combinations of ornaments and sperm morphology, but the specific combinations of traits that predict sperm velocity depended on the level of predation. These analyses underscore the complex nonlinear interrelationships among pre- and postcopulatory traits and the importance of considering ecological factors that may ultimately change the way in which multiple traits interact to determine a trait's performance value. As such, our results are likely to be broadly applicable across systems where selection is influenced by ecological conditions.

It is often assumed that longer sperm, by virtue of their increased swimming speed, have a fertilization advantage over shorter sperm when in competition to fertilize eggs. However, there is surprisingly little evidence for a positive correlation between sperm length and speed. Here we use an approach that accounts for within-male variation in sperm traits to examine the relationships between sperm length and sperm speed across a broad range of species, including three internally fertilizing species and three externally fertilizing species. Our results reveal that correlations between sperm size and speed are indeed present and possibly more common than currently thought. However, the direction of the correlations between sperm length and speed, which are more prevalent within a male's ejaculate than among males, were influenced by fertilization mode in contrasting and unexpected ways. Broadly, the patterns revealed that in externally fertilizing species sperm with longer flagellum and shorter heads relative to their flagellum swam faster, whereas in internally fertilizing species sperm with shorter flagellum and longer heads relative to their flagellum swam faster. We discuss these results in light of sperm competition theory and contrast the intraspecific patterns observed in this study with macroevolutionary patterns of sperm evolution reported elsewhere.

Recent and future climate change alters the thermal habitat of aquatic species on a global scale, generating novel environmental challenges during all life stages, including reproduction. Changes in water temperature profoundly influence the performance of ectothermic aquatic organisms. This is an especially crucial issue for migratory fish, because they traverse multiple environments in order to reproduce. In externally fertilizing migratory fish, gametes are affected by water temperature indirectly, within the reproductive organ in which they are produced during migration, as well as directly upon release into the surrounding medium upon arrival at their spawning grounds. Both direct (after release) and indirect (during production) thermal impacts on gamete quality have been investigated, but never in conjunction. Here, we assessed the cumulative influence of temperature on brown trout, Salmo trutta, sperm quality during sperm production (male acclimation temperature) as well as upon release (sperm activation water temperature) on two consecutive dates during the brown trout spawning season. Early in the season, warm acclimation of males reduced their fertilization probability (lower sperm velocity) when compared to cold acclimated males, especially when activation water temperature was also increased beyond the thermal optimum (resulting in a lower proportion of motile sperm with lower velocity). Later in the season, sperm quality was unaffected by acclimation temperature and thermal sensitivity of sperm was reduced. These results give novel insights into the complex impacts of climate change on fish sperm, with implications for the reproduction and management of hatchery and wild trout populations in future climate scenarios.

Heterozygosity-fitness correlations (HFCs) have been examined in a wide diversity of contexts, and the results are often used to infer the role of inbreeding in natural populations. Although population demography, reflected in population-level genetic parameters such as allelic diversity or identity disequilibrium, is expected to play a role in the emergence and detectability of HFCs, direct comparisons of variation in HFCs across many populations of the same species, with different genetic histories, are rare. Here, we examined the relationship between individual microsatellite heterozygosity and a range of sexually selected traits in 660 male guppies from 22 natural populations in Trinidad. Similar to previous studies, observed HFCs were weak overall. However, variation in HFCs among populations was high for some traits (although these variances were not statistically different from zero). Population-level genetic parameters, specifically genetic diversity levels (number of alleles, observed/expected heterozygosity) and measures of identity disequilibrium (g2 and heterozygosity-heterozygosity correlations), were not associated with variation in population-level HFCs. This latter result indicates that these metrics do not necessarily provide a reliable predictor of HFC effect sizes across populations. Importantly, diversity and identity disequilibrium statistics were not correlated, providing empirical evidence that these metrics capture different essential characteristics of populations. A complex genetic architecture likely underpins multiple fitness traits, including those associated with male fitness, which may have reduced our ability to detect HFCs in guppy populations. Further advances in this field would benefit from additional research to determine the demographic contexts in which HFCs are most likely to occur.

The selective forces that drive the evolution of cooperation have been intensely debated. Evolutionary transitions to cooperative breeding, a complex form of cooperation, have been hypothesized to be linked to low degrees of promiscuity, which increases intragroup relatedness and the indirect (that is, kin selected) benefits of helping. However, ecological factors also promote cooperative breeding, and may be more important than relatedness in some contexts. Identifying the key evolutionary drivers of cooperative breeding therefore requires an integrated assessment of these hypotheses. Here we show, using a phylogenetic framework that explicitly evaluates mating behaviours and ecological factors, that evolutionary transitions to cooperative breeding in cichlid fishes were not associated with social monogamy. Instead, group living, biparental care and diet type directly favoured the evolution of cooperative breeding. Our results suggest that cichlid fishes exhibit an alternative path to the evolution of complex societies compared to other previously studied vertebrates, and these transitions are driven primarily by direct fitness benefits.

Male reproductive success is influenced by competitive interactions during precopulatory and postcopulatory selective episodes. Consequently, males can gain reproductive advantages during precopulatory contest competition by investing in weaponry and during postcopulatory sperm competition by investing in ejaculates. However, recent theory predicts male expenditure on weaponry and ejaculates should be subject to a trade-off, and should vary under increasing risk and intensity of sperm competition. Here, we provide the first comparative analysis of the prediction that expenditure on weaponry should be negatively associated with expenditure on testes mass. Specifically, we assess how sexual selection influences the evolution of primary and secondary sexual traits among pinnipeds (seals, sea lions, and walruses). Using recently developed comparative methods, we demonstrate that sexual selection promotes rapid divergence in body mass, sexual size dimorphism (SSD), and genital morphology. We then show that genital length appears to be positively associated with the strength of postcopulatory sexual selection. However, subsequent analyses reveal that both genital length and testes mass are negatively associated with investment in precopulatory weaponry. Thus, our results are congruent with recent theoretical predictions of contest-based sperm competition models. We discuss the possible role of trade-offs and allometry in influencing patterns of reproductive trait evolution in pinnipeds.

The size of the vertebrate brain is shaped by a variety of selective forces. Although larger brains (correcting for body size) are thought to confer fitness advantages, energetic limitations of this costly organ may lead to trade-offs, for example as recently suggested between sexual traits and neural tissue. Here, we examine the patterns of selection on male and female brain size in pinnipeds, a group where the strength of sexual selection differs markedly among species and between the sexes. Relative brain size was negatively associated with the intensity of sexual selection in males but not females. However, analyses of the rates of body and brain size evolution showed that this apparent trade-off between sexual selection and brain mass is driven by selection for increasing body mass rather than by an actual reduction in male brain size. Our results suggest that sexual selection has important effects on the allometric relationships of neural development.

Assessing how selection operates on several, potentially interacting, components of the ejaculate is a challenging endeavor. Ejaculates can be subject to natural and/or sexual selection, which can impose both linear (directional) and nonlinear (stabilizing, disruptive, and correlational) selection on different ejaculate components. Most previous studies have examined linear selection of ejaculate components and, consequently, we know very little about patterns of nonlinear selection on the ejaculate. Even less is known about how selection acts on the ejaculate as a functionally integrated unit, despite evidence of covariance among ejaculate components. Here, we assess how selection acts on multiple ejaculate components simultaneously in the broadcast spawning sessile invertebrate Mytilus galloprovincialis using the statistical tools of multivariate selection analyses. Our analyses of relative fertilization rates revealed complex patterns of selection on sperm velocity, motility, and morphology. Interestingly, the most successful ejaculates were made up of slower swimming sperm with relatively low percentages of motile cells, and sperm with smaller head volumes that swam in highly pronounced curved swimming trajectories. These results are consistent with an emerging body of literature on fertilization kinetics in broadcast spawners, and shed light on the fundamental nature of selection acting on the ejaculate as a functionally integrated unit.

In numerous species, egg chemoattractants play a critical role in guiding sperm towards unfertilized eggs (sperm chemotaxis). Until now, the known functions of sperm chemotaxis include increasing the effective target size of eggs, thereby promoting sperm–egg encounters, and facilitating species recognition. Here, we report that in the broadcast spawning mussel, Mytilus galloprovincialis , egg chemoattractants may play an unforeseen role in sexual selection by enabling sperm to effectively ‘choose’ between the eggs of different conspecific females. In an initial experiment, we confirmed that sperm chemotaxis occurs in M. galloprovincialis by showing that sperm are attracted towards unfertilized eggs when given the choice of eggs or no eggs in a dichotomous chamber. We then conducted two cross-classified mating experiments, each comprising the same individual males and females crossed in identical male × female combinations, but under experimental conditions that offered sperm ‘no-choice’ (each fertilization trial took place in a Petri dish and involved a single male and female) or a ‘choice’ of a female's eggs (sperm were placed in the centre of a dichotomous choice chamber and allowed to choose eggs from different females). We show that male-by-female interactions characterized fertilization rates in both experiments, and that there was remarkable consistency between patterns of sperm migration in the egg-choice experiment and fertilization rates in the no-choice experiment. Thus, sperm appear to exploit chemical cues to preferentially swim towards eggs with which they are most compatible during direct sperm-to-egg encounters. These results reveal that sperm differentially select eggs on the basis of chemical cues, thus exposing the potential for egg chemoattractants to mediate mate choice for genetically compatible partners. Given the prevalence of sperm chemotaxis across diverse taxa, our findings may have broad implications for sexual selection in other mating systems.

Within animal societies, the ecological and social underpinnings of mating system variation can be related to resource dispersion, sexual conflict between breeders, and the effects of non-breeders. Here, we conducted a broad-scale investigation into the evolution of mating systems in the cooperatively breeding cichlid, Neolamprologus pulcher, a species that exhibits both monogamy and polygyny within populations. Using long-term field data, we showed that polygynous groups were more spatially clustered and held by larger competitively superior males than were monogamous groups, supporting the role of resource dispersion. To explore the role of sexual conflict, we forced polygynous males to become experimentally monogamous (EM) in the field. EM males spent more time on their remaining territory than naturally polygynous males but otherwise did not change behaviorally or physiologically. Females mated to EM males performed more submissive acts, and in a forced choice experiment, females did not preferentially associate with the larger of two unmated males. Females may therefore incur an unexpected cost from mating monogamously with a large and competitively superior male, a cost that mitigates sexual conflict over the mating system. Helpers were more closely related in monogamous groups but did not behave differently under monogamy or polygyny. Helpers therefore seem neither to be affected by nor affect the mating system of breeders. Our results demonstrate the roles of resource availability and conflict mitigation in determining the mating system, and highlight the importance of experimental manipulation for revealing hidden costs of hypothetical mating patterns. Key words: cooperative breeding, mating system, monogamy, polygyny, resource dispersion, sexual conflict. [Behav Ecol]

Natural environmental periodicity that occurs on both the small scale like day length, or larger scale like lunar light can provide animals with valuable information about resource availability and predation risk. Such environmental cycles are often linked to the timing of reproduction. Here, using the circulating androgen concentrations, gonadal investment patterns and detailed behavioral observations we show that wild populations of the group-living cichlid, Neolamprologus pulcher from Lake Tanganyika, have marked diurnal differences in behavior and lunar synchronicity in their reproductive physiology and behavior. Female ovarian investment peaked in the first quarter of the lunar cycle. In males, plasma steroid hormone levels and sperm swimming speed were highest at this same lunar stage, supporting the idea that egg laying occurs during this phase and that young will emerge at full moon, perhaps because nocturnal predators can be best detected then. Female subordinate group members' gonadal investment patterns mirrored the lunar pattern observed in dominant female breeders. In contrast, male subordinates did not show a change in gonadal investment or in steroid hormone concentrations across the lunar cycle, suggesting that female subordinates, but not male subordinates, reproduce within the social group. Neolamprologus pulcher demonstrated diurnal cycles in behavior, with higher rates of feeding in the morning. Male and female breeding pairs were strongly size matched potentially as a result of size-assortative mating; also the gonadal investment of male and female mated pairs was strongly correlated indicating within-pair reproductive synchronicity. In general, this study provides evidence for the impact of environmental cues (sunlight and moonlight) on circulating hormones and reproduction in a small tropical freshwater fish. © 2011 The Authors. Journal of Zoology © 2011 The Zoological Society of London.