Alessandro Devigili

Multivariate selection drives concordant patterns of pre- and postcopulatory sexual selection in a livebearing fish.

In many species, females mate with multiple partners, meaning that sexual selection on male traits operates across a spectrum that encompasses the competition for mates (that is, before mating) and fertilizations (after mating). Despite being inextricably linked, pre- and postcopulatory sexual selection are typically studied independently, and we know almost nothing about how sexual selection operates across this divide. Here we bridge this knowledge gap using the livebearing fish Poecilia reticulata. We show that both selective episodes, as well as their covariance, explain a significant component of variance in male reproductive fitness. Moreover, linear and nonlinear selection simultaneously act on pre- and postcopulatory traits, and interact to generate multiple phenotypes with similar fitness.

CROSS‐GENERATIONAL EFFECTS OF SEXUAL HARASSMENT ON FEMALE FITNESS IN THE GUPPY

Sexual harassment is a common outcome of sexual conflict over mating rate. A large number of studies have identified several direct costs to females of sexual harassment including energy expenditure and reduced foraging ability. However, the fitness consequences of sexual harassment for descendants have rarely been investigated. Here, we manipulated the level of sexual harassment and mating rate in two groups of female guppies, Poecilia reticulata, a live‐bearing fish in which sexual conflict over mating rate is particularly pronounced. Each female was allowed to interact with three males for one day (low sexual harassment, LSH) or for eight days (high sexual harassment, HSH) during each breeding cycle throughout their life. Female lifetime fecundity did not differ between the groups, but we found a strong effect on offspring fitness. HSH females produced (1) daughters with smaller bodies and (2) sons with shorter gonopodia, which were less attractive to females and less successful in coercive matings than their LSH counterparts. Although these results may be influenced by the indirect effects of sex ratio differences between treatments, they suggest that sexual harassment and elevated mating rate can have negative cross‐generational fitness effects and more profound evolutionary consequences than currently thought.

Pattern of inbreeding depression, condition dependence, and additive genetic variance in Trinidadian guppy ejaculate traits

In polyandrous species, a males reproductive success depends on his fertilization capability and traits enhancing competitive fertilization success will be under strong, directional selection. This leads to the prediction that these traits should show stronger condition dependence and larger genetic variance than other traits subject to weaker or stabilizing selection. While empirical evidence of condition dependence in postcopulatory traits is increasing, the comparison between sexually selected and ‘control’ traits is often based on untested assumption concerning the different strength of selection acting on these traits. Furthermore, information on selection in the past is essential, as both condition dependence and genetic variance of a trait are likely to be influenced by the pattern of selection acting historically on it. Using the guppy (Poecilia reticulata), a livebearing fish with high levels of multiple paternity, we performed three independent experiments on three ejaculate quality traits, sperm number, velocity, and size, which have been previously shown to be subject to strong, intermediate, and weak directional postcopulatory selection, respectively. First, we conducted an inbreeding experiment to determine the pattern of selection in the past. Second, we used a diet restriction experiment to estimate their level of condition dependence. Third, we used a half-sib/full-sib mating design to estimate the coefficients of additive genetic variance (CVA) underlying these traits. Additionally, using a simulated predator evasion test, we showed that both inbreeding and diet restriction significantly reduced condition. According to predictions, sperm number showed higher inbreeding depression, stronger condition dependence, and larger CVA than sperm velocity and sperm size. The lack of significant genetic correlation between sperm number and velocity suggests that the former may respond to selection independently one from other ejaculate quality traits. Finally, the association between sperm number and condition suggests that this trait may mediate the genetic benefits of polyandry which have been shown in this species.

Directional postcopulatory sexual selection is associated with female sperm storage in Trinidadian guppies

Female sperm storage (FSS) is taxonomically widespread and often associated with intense sperm competition, yet its consequences on postcopulatory sexual selection (PCSS) are poorly known. Theory predicts that FSS will reduce the strength of PCSS, because sperm characteristics favored before and after FSS may be traded‐off, and opportunities for nondirectional PCSS should increase. We explored these questions in the guppy (Poecilia reticulata), by allowing females to mate multiply and by comparing the paternity pattern in two successive broods. Contrary to predictions, the variance in male fertilization success increased after FSS, driven by a change in male paternity share across broods. This change was positively associated with sperm velocity (measured before FSS) but not with the duration of FSS, indirectly suggesting that faster sperm were better in entering female storage organs, rather than in persisting within them. Other male traits, such as male size and orange color, heterozygosity, and relatedness to the female, did not influence paternity after FSS. These results indicate that processes associated with FSS tend to reinforce the strength of PCSS in guppies, rather than weaken it. Further work is necessary to test whether this pattern changes in case of more prolonged FSS.

Artificial insemination unveils a first-male fertilization advantage in the guppy

Several factors are involved in determining the outcome of sperm competition. In addition to sperm number, sperm quality and male phenotype, insemination order is often associated with skewed paternity share. Patterns of sperm precedence can be produced by the mechanics of sperm storage and fertilization, or by active processes under male or female control. However, as males and females always interact during copulation, it is difficult to identify the mechanism responsible. The Trinidadian guppy, Poecilia reticulata, is a polyandric species characterized by last-male sperm precedence in natural matings. During such matings, females allow attractive males to inseminate more sperm by controlling copulation duration. We used artificial insemination to clarify the extent to which female control of sperm transfer influences the observed pattern of sperm precedence in this species. This technique allowed us to experimentally manipulate the number of sperm transferred and the timing of insemination. We found a significant first-male fertilization advantage. This advantage, however, declined as the time between insemination and parturition increased. Presumably, the anatomy and the physiology of the female genital tract favour egg fertilization by the first ejaculate inseminated, whereas sperm mixing is likely to be responsible for the reduction in first-male advantage associated with longer insemination–parturition intervals. Our results suggest that the last-male precedence detected after two consecutive natural matings is caused by cryptic female preference for attractive males associated with a female trading-up strategy (i.e. the second male is more frequently more attractive than the first male), rather than by insemination order per se. As the pattern of sperm precedence has important consequences for male reproductive strategies (for example mate guarding and male mate choice copying), unravelling its dynamic represents an important contribution to understanding the sexual behaviour of this model species.

Possible glimpses into early speciation: the effect of ovarian fluid on sperm velocity accords with post-copulatory isolation between two guppy populations

Identifying mechanisms of reproductive isolation is key to understanding speciation. Among the putative mechanisms underlying reproductive isolation, sperm–female interactions (post‐mating–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 post‐mating–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 post‐mating–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.

Population demography and heterozygosity-fitness correlations in natural guppy populations: An examination using sexually selected fitness traits

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.

Postcopulatory cost of immune system activation in Poecilia reticulata

The function and maintenance of the immune system impose costs that can take the form of energy consumption and/or physiological side effects. These, in turn, can affect the expression of several traits, including traits closely related to fitness. The interaction of the immune system with other life-history traits (e.g. growth and survival) and with precopulatory sexually selected traits (e.g. male ornaments) has been widely studied, whereas little is known about its interplay with postcopulatory sexually selected traits, such as sperm characteristics. We studied the effects of an immune challenge on the expression of precopulatory and postcopulatory traits in the guppy, Poecilia reticulata. We injected two groups of males with a lipopolysaccharide (LPS) solution or a saline solution (control) and compared the effects of the immune system activation on traits’ expression. The results showed a specific negative effect of the LPS injection on sperm traits, whereas precopulatory ornaments were lowered merely by manipulation (injection). We discuss the possible mechanisms underlying our findings, and the evolutionary implications that follow.