Paula Stockley

SPERM COMPETITION IN FISHES: THE EVOLUTION OF TESTIS SIZE AND EJACULATE CHARACTERISTICS

Fishes show one of the widest ranges of sperm competition intensity of any animal group. Here we present a comparative study whose aim is to investigate the effect of relative intensity of sperm competition on investment in spermatogenesis and the number and size of sperm produced. We find that both the gonadosomatic index (GSI = [gonad weight/body weight] x 100) and sperm numbers increase with intensity of sperm competition across species but that sperm length decreases. These new findings are consistent with a raffle‐based mode of sperm competition in fishes. Most of these results (positive correlation of the GSI and sperm number with sperm competition intensity) concur with the predictions of current sperm competition theory. However, we also find that sperm longevity decreases with sperm length across species. Current models for continuous fertilization suggest that if length increases a sperms speed but decreases its longevity, sperm length should increase with sperm competition intensity, whereas models for instant fertilization suggest that sperm length should remain constant. The negative relationship found between sperm competition and sperm length therefore does not fit predictions of either model.

Sperm competition games: a prospective analysis of risk assessment.

We develop the logic of assessment of sperm competition risk by individual males where the mechanism of sperm competition follows a ‘loaded raffle’ (first and second inseminates of a female have unequal prospects). Male roles (first or second to mate) are determined randomly. In model 1, males have no information about the risk associated with individual females and ejaculation strategy depends only on the probability, q, that females mate twice. Evolutionarily stable strategy (ESS) ejaculate expenditure increases linearly from zero with q, and reduces with increasing inequality between ejaculates, though the direction of the loading (which role is favoured) is unimportant. In model 2, males have perfect information and can identify each of three risk states: females that will (1) mate just once (‘no risk’), (2) mate twice but have not yet mated (‘future risk’), and (3) mate twice and have already mated (‘past risk’). The ESS is to ejaculate minimally with ‘no risk’ females, and to expend equally with ‘past’ and ‘future’ risk females; the direction of the competitive loading is again unimportant. Expenditure again increases with risk, but is now non–zero at extremely low risk. Model 3 examines three cases of partial information where males can identify only one of the three risk states and cannot distinguish between the other two: they therefore have just two information sets or ‘contexts’. Expenditure in both contexts typically rises non–linearly from zero with q, but (whatever the loading direction) expenditure is higher in the context with higher risk (e.g. if contexts are ‘mated’ and ‘virgin’, males spend more with mated females). However, in highly loaded raffles, sperm expenditure can decrease over part of the range of risk. Also, the direction of the loading now affects expenditure. Biological evidence for the predictions of the models is summarized and discussed.

Sperm competition games: individual assessment of sperm competition intensity by group spawners

A distinction is made between sperm competition risk (where there is typically a low probability of competition between two ejaculates) and sperm competition intensity (where typically two or more ejaculates compete). The relation between sperm competition intensity and sperm expenditure can be radically different across species from that within a species. Across species, the average ejaculate expenditure will increase with the average intensity of sperm competition. But within a species, the reverse trend is generally predicted for greater than two males competing for the same set of eggs. These effects are demonstrated with three sperm competition game models. They are devised mainly for externally fertilizing group-spawning species such as many fish, in which males group around a female and ejaculate when the female sheds her eggs. Fertilization is assumed to be instantaneous and each male gains a proportion of the eggs equal to his sperm number divided by the total sperm. In the first model, males cannot assess the number of competitors, and their ejaculate effort is shaped by the average number of males for the species or locally isolated deme. The proportion of reproductive effort expended on the ejaculate is predicted to increase as ( N — 1) / N, where N = the mean number of competing males present at a spawning. Thus if N is large, ejaculate expenditure dominates reproductive effort. In the second model, males can estimate whether there are more or less than average numbers of competitors present at a spawning, and in the third model, males can assess the number of competitors exactly. As in the first model, these models confirm that the mean ejaculate effort should increase with the mean number of competitors for the species. However, they predict that males should decrease their sperm expenditure as the estimated number of competitors present at a given spawning increases above two. These conclusions do not apply to sperm competition risk: there is thus no conflict with earlier models based on risk.

Sexual conflict resulting from adaptations to sperm competition.

Recent research on diverse animal taxa has revealed that male adaptations to sperm competition often lead to a conflict with female interests. That is, male attempts to increase their own fertilization success can result in a reduction of female fitness. This sexual conflict has led to selection for a variety of female adaptations that apparently reduce male-imposed costs. Understanding the causes and consequences of sexual conflict arising from adaptations to sperm competition offers much potential for new insight into the coevolution of male and female sexual strategies.

Female competition and its evolutionary consequences in mammals

Following Darwins original insights regarding sexual selection, studies of intrasexual competition have mainly focused on male competition for mates; by contrast, female reproductive competition has received less attention. Here, we review evidence that female mammals compete for both resources and mates in order to secure reproductive benefits. We describe how females compete for resources such as food, nest sites, and protection by means of dominance relationships, territoriality and inter‐group aggression, and by inhibiting the reproduction of other females. We also describe evidence that female mammals compete for mates and consider the ultimate causes of such behaviour, including competition for access to resources provided by mates, sperm limitation and prevention of future resource competition. Our review reveals female competition to be a potentially widespread and significant evolutionary selection pressure among mammals, particularly competition for resources among social species for which most evidence is currently available.

Benefits of Polyandry: A Life History Perspective

Bateman’s principle has been widely interpreted to imply that females gain no fitness benefits from polyandry (Bateman, 1948) and, therefore, should not be expected to mate multiply (here defined as mating with more than one male). Nevertheless, it is increasingly clear that females of many, if not most, taxa do copulate with multiple males (e.g. Birkhead and Wier, 1998). Moreover, polyandry is widespread despite considerable costs, including wasted time and energy, increased risk of predation and disease, potential damage caused by male seminal fluids and copulatory organs, and even death (Keller and Reeve, 1995; Eberhard, 1996). Despite these associated costs, females of diverse taxa not only accept several mates but also actively solicit multiple copulations in many instances (Birkhead and Moller, 1998). As evidence of diverse potential benefits associated with polyandry now accumulates, the assumption that females should not mate multiply because they cannot increase offspring numbers by doing so appears questionable. Importantly, since females have greater potential than males to influence the quality of their offspring, and investment in current reproduction has consequences for future reproductive attempts, they should be expected to optimise offspring numbers rather than maximise numbers produced in any given reproductive attempt (Roff, 1992; Stearns, 1992). Moreover, the relationship between female lifetime reproductive success and offspring numbers and/or size may not be as straightforward as is generally assumed (e.g. Madsen and Shine, 1998; Stockley and Macdonald, 1998). To suggest that females should not mate multiply simply because they cannot increase offspring numbers in a given reproductive attempt by doing so is therefore to confuse the currency of male and female fitness, and thereby to considerably under-estimate the complexity of female reproductive strategies.

The Genetic Basis of Inbreeding Avoidance in House Mice

Summary Animals might be able to use highly polymorphic genetic markers to recognize very close relatives and avoid inbreeding [1, 2]. The major histocompatibility complex (MHC) is thought to provide such a marker [1, 3–6] because it influences individual scent in a broad range of vertebrates [6–10]. However, direct evidence is very limited [1, 6, 10, 11]. In house mice (Mus musculus domesticus), the major urinary protein (MUP) gene cluster provides another highly polymorphic scent signal of genetic identity [8, 12–15] that could underlie kin recognition. We demonstrate that wild mice breeding freely in seminatural enclosures show no avoidance of mates with the same MHC genotype when genome-wide similarity is controlled. Instead, inbreeding avoidance is fully explained by a strong deficit in successful matings between mice sharing both MUP haplotypes. Single haplotype sharing is not a good guide to the identification of full sibs, and there was no evidence of behavioral imprinting on maternal MHC or MUP haplotypes. This study, the first to examine wild animals with normal variation in MHC, MUP, and genetic background, demonstrates that mice use self-referent matching of a species-specific [16, 17] polymorphic signal to avoid inbreeding. Recognition of close kin as unsuitable mates might be more variable across species than a generic vertebrate-wide ability to avoid inbreeding based on MHC.

Sperm competition and the evolution of male reproductive anatomy in rodents

Sperm competition is a pervasive selective force in evolution, shaping reproductive anatomy, physiology and behaviour. Here, we present comparative evidence that varying sperm competition levels account for variation in the male reproductive anatomy of rodents, the largest and most diverse mammalian order. We focus on the sperm-producing testes and the accessory reproductive glands, which produce the seminal fluid fraction of the ejaculate. We demonstrate a positive association between relative testis size and the prevalence of within-litter multiple paternity, consistent with previous analyses in which relative testis size has been found to correlate with sperm competition levels inferred from social organization and mating systems. We further demonstrate an association between sperm competition level and the relative size of at least two accessory reproductive glands: the seminal vesicles and anterior prostate. The size of the major product of these glands—the copulatory plug—is also found to vary with sperm competition level. Our findings thus suggest that selection for larger plugs under sperm competition may explain variation in accessory gland size, and highlight the need to consider both sperm and non-sperm components of the male ejaculate in the context of post-copulatory sexual selection.

Sperm competition or sperm selection: no evidence for female influence over paternity in yellow dung flies Scatophaga stercoraria

Abstract Recent studies of non-random paternity have suggested that sperm selection by females may influence male fertilization success. Here we argue that the problems originally encountered in partitioning variation in non-random mating between male competition and female choice are even more pertinent to interpreting patterns of non-random paternity because of intense sperm competition between males. We describe an experiment with the yellow dung fly, Scatophaga stercoraria, designed to partition variance in the proportion of offspring sired by the second male, P2, between males and females, and to control for sperm competition. Large males were shown to have a higher P2 than small males but P2 was independent of the size of the female’s first mate. This result might suggest an absolute female preference for large males via sperm selection. However, large males have a higher constant rate of sperm transfer and displacement. After controlling for this effect of sperm competition, large males did not achieve higher paternity than small males. We argue that a knowledge of the mechanism of sperm competition is essential so that male effects can be controlled before conclusions are made regarding the influence of sperm selection by females in generating non-random paternity.

Sperm Displacement in the Yellow Dung Fly, Scatophaga stercoraria: An Investigation of Male and Female Processes

Despite the ubiquity with which patterns of sperm utilization have been studied, the mechanisms underlying fertilization in insects are far from clear. One well‐studied system is the yellow dung fly, in which the last males ejaculate is thought to displace rival sperm from the females sperm stores. Here we follow the movement of the copulating males ejaculate through the females reproductive tract using males labeled with different radioisotopes. We find that males ejaculate into the bursa copulatrix and that male‐1 sperm are displaced from the spermathecae during copulation. The increase in male‐2 ejaculate in the spermathecae matches the pattern of male‐2 fertilization gain, indicating that only spermathecal sperm are utilized at fertilization. Previously we have analyzed this system with a direct model of sperm displacement in which the male displaces rival sperm from the spermathecae. The data, and morphology of the female, clearly preclude such a mechanism. Here we contrast this model with a new indirect model, in which the female facilitates displacement by exchange of sperm from the bursa copulatrix to the spermathecae. The two models give equivalent fits to the observed sperm utilization patterns because the rate of sperm transfer into the bursa copulatrix greatly exceeds the rate of sperm exchange with the spermathecae so that the concentration of the first males sperm in the bursa remains considerably lower than that of the second male. These analyses provide a quantitative attempt to incorporate female processes into the analysis of sperm utilization patterns in insects.