Tommaso Pizzari

Postcopulatory sexual selection.

The female reproductive tract is where competition between the sperm of different males takes place, aided and abetted by the female herself. Intense postcopulatory sexual selection fosters inter-sexual conflict and drives rapid evolutionary change to generate a startling diversity of morphological, behavioural and physiological adaptations. We identify three main issues that should be resolved to advance our understanding of postcopulatory sexual selection. We need to determine the genetic basis of different male fertility traits and female traits that mediate sperm selection; identify the genes or genomic regions that control these traits; and establish the coevolutionary trajectory of sexes.

Sperm competition and ejaculate economics

Sperm competition was identified in 1970 as a pervasive selective force in post‐copulatory sexual selection that occurs when the ejaculates of different males compete to fertilise a given set of ova. Since then, sperm competition has been much studied both empirically and theoretically. Because sperm competition often favours large ejaculates, an important challenge has been to understand the evolution of strategies through which males invest in sperm production and economise sperm allocation to maximise reproductive success under competitive conditions. Sperm competition mechanisms vary greatly, depending on many factors including the level of sperm competition, space constraints in the sperm competition arena, male mating roles, and female influences on sperm utilisation. Consequently, theoretical models of ejaculate economics are complex and varied, often with apparently conflicting predictions. The goal of this review is to synthesise the theoretical basis of ejaculate economics under sperm competition, aiming to provide empiricists with categorised model assumptions and predictions. We show that apparent contradictions between older and newer models can often be reconciled and there is considerable consensus in the predictions generated by different models. We also discuss qualitative empirical support for some of these predictions, and detail quantitative matches between predictions and observations that exist in the yellow dung fly. We argue that ejaculate economic theory represents a powerful heuristic to explain the diversity in ejaculate traits at multiple levels: across species, across males and within individual males. Future progress requires greater understanding of sperm competition mechanisms, quantification of trade‐offs between ejaculate allocation and numbers of matings gained, further knowledge of mechanisms of female sperm selection and their associated costs, further investigation of non‐sperm ejaculate effects, and theoretical integration of pre‐ and post‐copulatory episodes of sexual selection.

Female feral fowl eject sperm of subdominant males

Paternity is often determined by competition between the ejaculates of different males. Males can also use particular behaviours or structures to manipulate how females use sperm. However, the ability of females to bias sperm utilization in favour of preferred males independently of male manipulation has not been demonstrated. Females are predicted to respond differentially to the sperm of different males when the reproductive interests of the sexes differ and when females are coerced into copulating. Here we show that in female feral fowl most copulations are coerced, and that females consistently bias sperm retention in favour of the preferred male phenotype. Females prefer to copulate with dominant males, but when sexually coerced by subordinate males, they manipulate the behaviour of dominant males to reduce the likelihood of insemination. If this fails, females differentially eject ejaculates according to male status in the absence of any male manipulation and preferentially retain the sperm of dominant males.

Sophisticated sperm allocation in male fowl

When a female is sexually promiscuous, the ejaculates of different males compete for the fertilization of her eggs; the more sperm a male inseminates into a female, the more likely he is to fertilize her eggs. Because sperm production is limited and costly, theory predicts that males will strategically allocate sperm (1) according to female promiscuity, (2) saving some for copulations with new females, and (3) to females producing more and/or better offspring. Whether males allocate sperm in all of these ways is not known, particularly in birds where the collection of natural ejaculates only recently became possible. Here we demonstrate male sperm allocation of unprecedented sophistication in the fowl Gallus gallus. Males show status-dependent sperm investment in females according to the level of female promiscuity; they progressively reduce sperm investment in a particular female but, on encountering a new female, instantaneously increase their sperm investment; and they preferentially allocate sperm to females with large sexual ornaments signalling superior maternal investment. Our results indicate that female promiscuity leads to the evolution of sophisticated male sexual behaviour.

6 – Sperm competition and sperm phenotype

Publisher Summary Sperm competition is the competition between the ejaculates of different males for the fertilization of a given set of ova. Charles Darwin (1871) proposed sexual selection as a process that operates on variation in male ability to compete with other males for access to reproductive opportunities, and which promotes traits that confer an advantage in reproductive competition. In most taxa individual females may copulate (or spawn) with multiple males (i.e., are polyandrous). As a consequence, the ejaculates of different males may co-occur around a set of ova at the time of fertilization, resulting in sperm competition. Sperm competition introduces variation in male reproductive success determined by the relative competitive fertilizing efficiency of the ejaculates of different males, and generates postcopulatory, intrasexual selection, which promotes traits that increase the fertilization success of an ejaculate under competitive conditions. A second consequence of polyandry is the potential for intersexual selection to continue after copulation through mechanisms that enable females (or ova) to bias the outcome of sperm competition in favor of the sperm of certain males, a process known as sperm selection or cryptic female choice. The past three decades have seen an explosion of interest in postcopulatory sexual selection that has highlighted the importance of sperm competition and cryptic female choice as engines of evolutionary change. This chapter reviews recent empirical and theoretical advances to discuss various ways in which sperm competition may shape the evolution of sperm and ejaculate traits.

Sperm mobility: mechanisms of fertilizing efficiency, genetic variation and phenotypic relationship with male status in the domestic fowl, Gallus gallus domesticus

When females are sexually promiscuous, sexual selection continues after insemination through sperm competition and cryptic female choice, and male traits conveying an advantage in competitive fertilization are selected for. Although individual male and ejaculate traits are known to influence paternity in a competitive scenario, multiple mechanisms co‐occur and interact to determine paternity. The way in which different traits interact with each other and the mechanisms through which their heritability is maintained despite selection remain unresolved. In the promiscuous fowl, paternity is determined by the number of sperm inseminated into a female, which is mediated by male social dominance, and by the quality of the sperm inseminated, measured as sperm mobility. Here we show that: (i) the number of sperm inseminated determines how many sperm reach the female sperm‐storage sites, and that sperm mobility mediates the fertilizing efficiency of inseminated sperm, mainly by determining the rate at which sperm are released from the female storage sites, (ii) like social status, sperm mobility is heritable, and (iii) subdominant males are significantly more likely to have higher sperm mobility than dominant males. This study indicates that although the functions of social status and sperm mobility are highly interdependent, the lack of phenotypic integration of these traits may maintain the variability of male fitness and heritability of fertilizing efficiency.

PERSPECTIVE: SEXUAL CONFLICT AND SEXUAL SELECTION: CHASING AWAY PARADIGM SHIFTS

Abstract.— Traditional models of sexual selection propose that partner choice increases both average male and average female fitness in a population. Recent theoretical and empirical work, however, has stressed that sexual conflict may be a potent broker of sexual selection. When the fitness interests of males and females diverge, a reproductive strategy that increases the fitness of one sex may decrease the fitness of the other sex. The chase‐away hypothesis proposes that sexual conflict promotes sexually antagonistic, rather than mutualistic, coevolution, whereby manipulative reproductive strategies in one sex are counteracted by the evolution of resistance to such strategies in the other sex. In this paper, we consider the criteria necessary to demonstrate the chase‐away hypothesis. Specifically, we review sexual conflict with particular emphasis on the chase‐away hypothesis; discuss the problems associated with testing the predictions of the chase‐away hypothesis and the extent to which these predictions and the predictions of traditional models of sexual selection are mutually exclusive; discuss misconceptions and mismeasures of sexual conflict; and suggest an alternative approach to demonstrate sexual conflict, measure the intensity of sexually antagonistic selection in a population, and elucidate the coevolutionary trajectories of the sexes.

Chicken genomics: Feather-pecking and victim pigmentation

Feather-pecking in domestic birds is associated with cannibalism and severe welfare problems. It is a dramatic example of a spiteful behaviour in which the victims fitness is reduced for no immediate direct benefit to the perpetrator and its evolution is unexplained. Here we show that the plumage pigmentation of a chicken may predispose it to become a victim: birds suffer more drastic feather-pecking when the colour of their plumage is due to the expression of a wild recessive allele at PMEL17, a gene that controls plumage melanization, and when these birds are relatively common in a flock. These findings, obtained using an intercross between a domestic fowl and its wild ancestor, have implications for the welfare of domestic species and offer insight into the genetic changes associated with the evolution of feather-pecking during the early stages of domestication.

Social competitiveness associated with rapid fluctuations in sperm quality in male fowl.

When females copulate with multiple males, paternity is determined by the competitive ability of a male to access females and by the ability of its ejaculates to out-compete those of other males over fertilization. The relationship between the social competitiveness of a male and the fertilizing quality of its sperm has therefore crucial implications for the evolution of male reproductive strategies in response to sexual selection. Here, we present a longitudinal experimental study of the relationship between social status and sperm quality. We monitored sperm quality in socially naive male domestic fowl, Gallus gallus domesticus, before and after exposure to a social challenge which comprised two stages. In the first stage, social dominance was established in male pairs divergent in sperm quality, and in the second, social status was experimentally manipulated by re-shuffling males across pairs. We show that sperm quality fluctuates within males both before and after a social challenge. Importantly, such fluctuations followed consistently different patterns in males that displayed different levels of social competitiveness in the social challenge. In particular, following the social challenge, sperm quality dropped in males that won both contests while the sperm quality of males that lost both contests remained constant. Together, these results indicate that males of different social competitiveness are predisposed to specific patterns of fluctuations in sperm quality. These rapid within-male fluctuations may help explain the recent findings of trade-offs between male social and gametic competitive abilities and may help maintain phenotypic variability in these traits.

Sex-specific, counteracting responses to inbreeding in a bird

Inbreeding often depresses offspring fitness. Because females invest more than males in a reproductive event, inbreeding is expected to be more costly to mothers than fathers, creating a divergence between the reproductive interests of each sex and promoting sex–specific inbreeding strategies. Males and females may bias the probability of inbreeding by selecting copulation partners, and, in sexually promiscuous species, through male strategic sperm investment in different females and female selection of the sperm of different males. However, these processes are often difficult to study, and the way that different male and female strategies interact to determine inbreeding remains poorly understood. Here we demonstrate sex–specific, counteracting responses to inbreeding in the promiscuous red junglefowl, Gallus gallus. First, a male was just as likely to copulate with his full–sib sister as with an unrelated female. In addition, males displayed a tendency to: (i) initiate copulation faster when exposed to an unrelated female than when exposed to a sister, and (ii) inseminate more sperm into sisters than into unrelated females. Second, females retained fewer sperm following insemination by brothers, thus reducing the risk of inbreeding and counteracting male inbreeding strategies.