Clelia Gasparini

Cryptic female preference for genetically unrelated males is mediated by ovarian fluid in the guppy

As inbreeding is costly, it has been suggested that polyandry may evolve as a means to reduce the negative fitness consequences of mating with genetically related males. While several studies provide support for this hypothesis, evidence of pure post-copulatory mechanisms capable of biasing paternity towards genetically unrelated males is still lacking; yet these are necessary to support inbreeding avoidance models of polyandry evolution. Here we showed, by artificially inseminating a group of female guppies with an equal number of sperm from related (full-sib) and unrelated males, that sperm competition success of the former was 10 per cent lower, on average, than that of the unrelated male. The paternity bias towards unrelated males was not due to differential embryo survival, as the size of the brood produced by control females, which were artificially inseminated with the sperm of a single male, was not influenced by their relatedness with the male. Finally, we collected ovarian fluid (OF) from virgin females. Using computer-assisted sperm analysis, we found that sperm velocity, a predictor of sperm competition success in the guppy, was significantly lower when measured in a solution containing the OF from a sister as compared with that from an unrelated female. Our results suggest that sperm–OF interaction mediates sperm competition bias towards unrelated mates and highlight the role of post-copulatory mechanisms in reducing the cost of mating with relatives in polyandrous females.

Sperm number and velocity affect sperm competition success in the guppy ( Poecilia reticulata )

While both sperm number and quality are now recognized to be important in determining the outcome of sperm competition, very few studies have experimentally assessed the influence of these two parameters simultaneously. We studied the effect of sperm quality and number on competitive fertilization success in an internal-fertilizing fish, the guppy (Poecilia reticulata), which is characterized by high levels of sperm competition. We artificially inseminated virgin females with varying proportion of sperm from two competing males, while holding constant the total number of sperm transferred to the female. Sperm morphology and sperm swimming velocity were also determined prior to insemination. The paternity outcome of sperm competition trials was assessed through molecular analyses of the resulting offspring using polymorphic microsatellite loci. We found that both sperm number and sperm velocity affected the outcome of sperm competition, with males that contributed more and faster sperm achieving a greater paternity share.

Sperm Swimming Velocity Predicts Competitive Fertilization Success in the Green Swordtail Xiphophorus helleri

Sperm competition is expected to favour the evolution of traits that influence the performance of sperm when they compete to fertilize a females eggs. While there is considerable evidence that selection favours increases in sperm numbers, much less is known about how sperm quality contributes towards competitive fertilization success. Here, we determine whether variation in sperm quality influences competitive fertilization success in the green swordtail Xiphophorus helleri, a highly promiscuous livebearing fish. We use artificial insemination as a method of controlled sperm delivery and show that sperm swimming velocity is the primary determinant of fertilization success when ejaculates from two males compete to fertilize a females eggs. By contrast, we found no evidence that sperm length had any effect on siring success. We also found no evidence that pre- and postcopulatory sexual traits were phenotypically integrated in this species, suggesting that the previous observation that reproductive skew favours males with high mating rates is unlikely to be due to any direct association between sperm quality and male sexual ornamentation.

Copulation duration, insemination efficiency and male attractiveness in guppies

In polyandrous species, females may influence paternity by biasing sperm usage in favour of particular males. In the guppy, Poecilia reticulata , the number of sperm inseminated in a copulation depends on the females perception of male attractiveness. We videorecorded copulations in the laboratory to test the hypothesis that there is a positive correlation between the number of sperm inseminated and the duration of the copulation. Duration was positively correlated with the number of sperm retrieved from the females gonoduct. Once copulation duration was statistically controlled for, more sperm were retrieved from the gonoduct in courtship copulations than in coercive copulations, and in postpartum females than in virgin females. Copulation duration was positively correlated with the degree of carotenoid coloration of the male, suggesting that copulation duration might be the proximate mechanism of cryptic female choice in this species. The intensity of ‘jerking’, a postcopulatory behaviour of male guppies, was positively correlated with the number of sperm inseminated, suggesting a possible signalling function of this display.

Effect of male age on sperm traits and sperm competition success in the guppy (Poecilia reticulata).

Deleterious mutations can accumulate in the germline with age, decreasing the genetic quality of sperm and imposing a cost on female fitness. If these mutations also affect sperm competition ability or sperm production, then females will benefit from polyandry as it incites sperm competition and, consequently, minimizes the mutational load in the offspring. We tested this hypothesis in the guppy (Poecilia reticulata), a species characterized by polyandry and intense sperm competition, by investigating whether age affects post‐copulatory male traits and sperm competition success. Females did not discriminate between old and young males in a mate choice experiment. While old males produced longer and slower sperm with larger reserves of strippable sperm, compared to young males, artificial insemination did not reveal any effect of age on sperm competition success. Altogether, these results do not support the hypothesis that polyandry evolved in response to costs associated with mating with old males in the guppy.

Intraspecific evidence from guppies for correlated patterns of male and female genital trait diversification

The role of sexual selection in fuelling genital evolution is becoming increasingly apparent from comparative studies revealing interspecific divergence in male genitalia and evolutionary associations between male and female genital traits. Despite this, we know little about intraspecific variance in male genital morphology, or how male and female reproductive traits covary among divergent populations. Here we address both topics using natural populations of the guppy, Poecilia reticulata, a livebearing fish that exhibits divergent patterns of male sexual behaviour among populations. Initially, we performed a series of mating trials on a single population to examine the relationship between the morphology of the males copulatory organ (the gonopodium) and the success of forced matings. Using a combination of linear measurements and geometric morphometrics, we found that variation in the length and shape of the gonopodium predicted the success of forced matings in terms of the rate of genital contacts and insemination success, respectively. We then looked for geographical divergence in these traits, since the relative frequency of forced matings tends to be greater in high-predation populations. We found consistent patterns of variation in male genital size and shape in relation to the level of predation, and corresponding patterns of (co)variation in female genital morphology. Together, these data enable us to draw tentative conclusions about the underlying selective pressures causing correlated patterns of divergence in male and female genital traits, which point to a role for sexually antagonistic selection.

Female presence influences sperm velocity in the guppy.

As sperm production is costly, males are expected to strategically allocate resources to sperm production according to mating opportunities. While sperm number adjustments have been reported in several taxa, only a few studies investigated whether sperm quality shows adaptive plasticity as well. We tested this prediction in the guppy, Poecilia reticulata. A total of 46 males were initially stripped of all retrievable sperm before being randomly allocated to one of two treatments simulating different levels of mating opportunities (visual contact with females or female deprived). After 3 days, males were stripped and sperm velocity was assayed using Computer Assisted Sperm Analysis. Males in the presence of females produced significantly faster sperm than their counterparts. Implications for the evolution of this ejaculate plasticity in the light of results of sperm competition studies are discussed.

Postmating Female Control: 20 Years of Cryptic Female Choice

Cryptic female choice (CFC) represents postmating intersexual selection arising from female-driven mechanisms at or after mating that bias sperm use and impact male paternity share. Although biologists began to study CFC relatively late, largely spurred by Eberhard’s book published 20 years ago, the field has grown rapidly since then. Here, we review empirical progress to show that numerous female processes offer potential for CFC, from mating through to fertilization, although seldom has CFC been clearly demonstrated. We then evaluate functional implications, and argue that, under some conditions, CFC might have repercussions for female fitness, sexual conflict, and intersexual coevolution, with ramifications for related evolutionary phenomena, such as speciation. We conclude by identifying directions for future research in this rapidly growing field.

Do unattractive friends make you look better? Context-dependent male mating preferences in the guppy

Recent theory predicts that in species where females tend to mate with the relatively most ornamented males, males may increase their attractiveness to females, and hence mating success, by preferentially associating with females that are surrounded by less ornamented competitors. Despite this prediction, we still lack explicit experimental evidence that males strategically prefer females surrounded by less attractive competitors to maximize their relative attractiveness. In this paper, we provide a comprehensive test of this hypothesis in the guppy (Poecilia reticulata), a species where a females perception of a males attractiveness depends on his coloration relative to that of surrounding males. We found that males preferentially associated with females that were surrounded by relatively drab competitors, and that the strength of an individual males preference was negatively correlated with his level of ornamentation. A series of control experiments made it possible to exclude the potentially confounding effects of male–male competition or social motivations when drawing these conclusions. The ability of males to choose social context to increase their relative attractiveness has important evolutionary consequences, for example, by contributing towards the maintenance of variability in male sexual ornamentation despite the strong directional selection exerted by female preferences.

Female guppies shorten brood retention in response to predator cues

Predation risk influences the duration of offspring development in many species where embryos develop from externally shed eggs. Surprisingly, such predator-mediated effects on offspring development have rarely been explored in live-bearers. In this paper, we use the guppy (Poecilia reticulata), a live-bearing freshwater fish, to test whether the duration of brood retention (the time from mating to parturition) is influenced by experimental changes in the perceived level of predation. Because the swimming performance of female guppies is impaired during late pregnancy, we predicted that females would withhold broods for shorter periods when they are exposed to cues that signal a heightened risk of predation on adults rather than on juveniles. We therefore simulated increased risk of predation on adults by using a combination of pike-shaped models (resembling natural predators that prey on adult guppies) and ‘alarm substances’ derived from the skin extracts of adult conspecific females. Our results revealed that, under simulated predation risk, female guppies produced broods significantly more quickly than their counterparts assigned to a control group where predator cues were absent. A subsequent evaluation of offspring swimming performance revealed a significant positive association between neonate swimming speeds and the duration of brood retention, suggesting that by accelerating parturition, females may produce offspring with impaired locomotor skills. These findings, in conjunction with similar results from other live-bearing species, suggest that the conditions experienced by gestating females can generate significant variation in the timing of offspring development with potentially important implications for offspring fitness.