Spatial clumping of sexually receptive females induces space sharing among male voles

The spatial organization of individuals in populations (their spacing system) can be highly variable even among populations of the same species. As spacing systems have important consequences for ecological processes such as population regulation, competition and mating systems, there have been many attempts to explore factors that may cause this variation. For mammals, it has been argued that the spatial distribution of sexually receptive females is the most important factor determining the spacing system of males, whereas habitat characteristics are most important to females. This has been difficult to test experimentally as it requires manipulations of the spatial distribution of the opposite sex without changing other properties of the environment. Here, I present a novel experimental procedure that can achieve this and demonstrate that the spatial distribution of the opposite sex in a population of voles is indeed an important determinant of the spacing system of males, but not of females. However, the effects on males are different from those predicted by many theoretical studies.     

Female mate-choice drives the evolution of male-biased dispersal in a social mammal

Dispersal has a significant impact on lifetime reproductive success, and is often more prevalent in one sex than the other. In group-living mammals, dispersal is normally male-biased and in theory this sexual bias could be a response by males to female mate preferences, competition for access to females or resources, or the result of males avoiding inbreeding. There is a lack of studies on social mammals that simultaneously assess these factors and measure the fitness consequences of male dispersal decisions. Here we show that male-biased dispersal in the spotted hyaena (Crocuta crocuta) most probably results from an adaptive response by males to simple female mate-choice rules that have evolved to avoid inbreeding. Microsatellite profiling revealed that females preferred sires that were born into or immigrated into the female's group after the female was born. Furthermore, young females preferred short-tenured sires and older females preferred longer-tenured sires. Males responded to these female mate preferences by initiating their reproductive careers in groups containing the highest number of young females. As a consequence, 11% of males started their reproductive career in their natal group and 89% of males dispersed. Males that started reproduction in groups containing the highest number of young females had a higher long-term reproductive success than males that did not. The female mate-choice rules ensured that females effectively avoided inbreeding without the need to discriminate directly against close kin or males born in their own group, or to favour immigrant males. The extent of male dispersal as a response to such female mate preferences depends on the demographic structure of breeding groups, rather than the genetic relatedness between females and males.     

Sexual swellings advertise female quality in wild baboons

The females of many Old World primate species produce prominent and conspicuous swellings of the perineal skin around the time of ovulation. These sexual swellings have been proposed to increase competition among males for females or to increase the likelihood of a female getting fertilized, by signalling either a female's general reproductive status, or the timing of her ovulation. Here we show that sexual swellings in wild baboons reliably advertise a female's reproductive value over her lifetime, in accordance with a theoretical model of honest signalling. Females with larger swellings attained sexual maturity earlier, produced both more offspring and more surviving offspring per year than females with smaller swellings, and had a higher overall proportion of their offspring survive. Male baboons use the size of the sexual swelling to determine their mating effort, fighting more aggressively to consort females with larger swellings, and spending more time grooming these females. Our results document an unusual case of a sexually selected ornament in females, and show how males, by mating selectively on the basis of the size of the sexual swelling, increase their probability of mating with females more likely to produce surviving offspring.     

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.     

Mate guarding as paternity insurance in Idaho ground squirrels

Following a copulation, males in many species of vertebrates (particularly birds) and invertebrates remain near the inseminated female and repel other suitors with displays or force. Guarding males must delay resumption of competitive mate searching, but they may insure their paternity by reducing possibilities for secondary matings and sperm competition. Among mammals, post-copulatory mate guarding has been reported in rodents, mongooses, ungulates and primates, including humans, but the effects of such behaviour on male reproductive success have not been determined genetically. I report here that mate guarding by male Idaho ground squirrels (Spermophilus brunneus) enhances a male's probability of paternity. Furthermore, an analysis based on game theory shows that mate guarding is an evolutionarily stable strategy for male S. brunneus, but not male Belding's ground squirrels (S. beldingi), which resume searching once copulation is completed.     

Unusually dynamic sex roles in a fish

Sex roles are typically thought of as being fixed for a given species. In most animals males compete for females, whereas the females are more reluctant to mate. Therefore sexual selection usually acts most strongly on males. This is explained by males having a higher potential reproductive rate than females, leading to more males being sexually active (a male-biased operational sex ratio). However, what determines sex roles and the strength of sexual selection is a controversial and much debated question. In this large-scale field study, we show a striking temporal plasticity in the mating competition of a fish (two-spotted goby, Gobiusculus flavescens). Over the short breeding season fierce male-male competition and intensive courtship behaviour in males were replaced by female-female competition and actively courting females. Hence, sex role reversal occurred rapidly. This is the first time that a shift in sex roles has been shown in a vertebrate. The shift might be explained by a large decline in male abundance, strongly skewing the sex ratio towards females. Notably, the sex role reversal did not occur at an equal operational sex ratio, contrary to established sex role theory.     

Fine-scale genetic structuring on Manacus manacus leks

Leks have traditionally been considered as arenas where males compete to attract females and secure matings. Thus, direct fitness benefits mediated through competition between males to fertilize females have been considered to be the primary force driving the evolution of lekking behaviour. Inclusive fitness benefits mediated through kin selection may also be involved in lek formation and evolution, but to date this theory has been largely ignored. According to kin-selection theory, both reproducing and non-reproducing males may gain indirect inclusive fitness benefits. If females are attracted to larger leks, non-reproducing males add attractiveness to a lek, and therefore, in a genetically structured population, boost the reproductive success of kin. Theory predicts that the attractiveness of leks is plastic, and that males establish themselves on a lek in which the top male, in terms of reproductive success, is a close relative. Here we show that in white-bearded manakins (Manacus manacus), for which larger leks are more attractive to females and so secure the maximum number of matings, there is extraordinary fine-scale genetic structure, with leks being composed of clusters of related kin. We propose that males establish themselves where they find relatives to such an extent that they form groups within leks, and that such behaviour is consistent with kin-selection theory to maximize reproductive success of the group.     

Sperm competition between Drosophila males involves both displacement and incapacitation.

Females in almost all animal groups copulate with multiple males. This behaviour allows different males to compete for fertilization and gives females the opportunity to mediate this competition. In many animals and most insects, the second male to copulate with a female typically sires most of her offspring. In Drosophila melanogaster, this second-male sperm precedence has long been studied but, as in most species, its mechanism has remained unknown. Here we show, using labelled sperm in doubly mated females, that males can both physically displace and incapacitate stored sperm from earlier-mating males. Displacement occurs only if the second male transfers sperm to the female, and in only one of her three sperm-storage organs. Incapacitation can be caused by either fertile or spermless second males, but requires extended intervals between matings. Sperm from different males are not 'stratified' in the storage organs but mix freely. Many animal species may have multiple mechanisms of sperm competition like those observed here, and revealing these mechanisms is necessary to understand the genetic and evolutionary basis of second-male sperm precedence in animals.     

Variation in regulation of steroid sulphatase locus in mammals

Inactivation (lyonization) of one of the two copies of X-linked genes occurs in female mammals, thereby reducing the number of active copies to that of the male. It has been suggested that genes subject to lyonization would be expected to be preserved as a linkage group during mammalian evolution. A short region of the human X chromosome containing several genes, including that necessary for the expression of steroid sulphatase (STS), is exceptional in that it apparently escapes X-inactivation. As it is not apparent why the linkage of genes not subject to X-inactivation should be conserved, we have examined the expression of the STS gene in mice (it has been shown recently that this gene is X-linked). Enzyme levels were determined in normal males and females and in the progeny of crosses in which the sex reversing factor, Sxr, was segregating to produce XX males. We report here that in contrast to the situation in humans, the STS gene in mice is subject to the normal pattern of X-inactivation.     

Intrasexual competition and sexual selection in cooperative mammals

In most animals, the sex that invests least in its offspring competes more intensely for access to the opposite sex and shows greater development of secondary sexual characters than the sex that invests most. However, in some mammals where females are the primary care-givers, females compete more frequently or intensely with each other than males. A possible explanation is that, in these species, the resources necessary for successful female reproduction are heavily concentrated and intrasexual competition for breeding opportunities is more intense among females than among males. Intrasexual competition between females is likely to be particularly intense in cooperative breeders where a single female monopolizes reproduction in each group. Here, we use data from a twelve-year study of wild meerkats (Suricata suricatta), where females show high levels of reproductive skew, to show that females gain greater benefits from acquiring dominant status than males and traits that increase competitive ability exert a stronger influence on their breeding success. Females that acquire dominant status also develop a suite of morphological, physiological and behavioural characteristics that help them to control other group members. Our results show that sex differences in parental investment are not the only mechanism capable of generating sex differences in reproductive competition and emphasize the extent to which competition for breeding opportunities between females can affect the evolution of sex differences and the operation of sexual selection.     

Forebrain peptides modulate sexually polymorphic vocal circuitry

The peptide arginine-vasopressin (mammals) and its evolutionary precursor arginine-vasotocin (non-mammals) modulate reproductive physiology and numerous related social behaviours, as do oxytocin (mammals) and its homologues mesotocin and isotocin (fish). The distributions in the brain and/or the behavioural functions of these peptides often differ between the sexes, and between species with divergent social structures. Here we present neurophysiological evidence that males with vocal characteristics typical of females share a pattern of neuropeptide function with females rather than conspecific males. The plainfin midshipman fish (Porichthys notatus) has two male morphs with different reproductive tactics and vocalizations (a key species-typical behaviour which varies in its physical attributes and contextual usage, depending on the morph's social strategy). Forebrain-evoked, rhythmic vocal-motor activity that precisely mimics natural vocalizations was modulated by arginine-vasotocin, isotocin and their antagonists delivered to the preoptic area-anterior hypothalamus, a primary site for behavioural integration in all vertebrates. Peptides had different effects in males that acoustically court females (arginine-vasotocin-sensitive) than in females and sneak-spawning males (isotocin-sensitive), showing that the neuromodulatory mechanisms that establish reproduction-related behaviour can be dissociated from gonadal sex.     

Female transfer and inbreeding avoidance in social mammals

In most social mammals, males leave their natal group to breed in other groups whereas females commonly remain in the same group throughout their lives. In a few species however, females usually transfer between groups during adolescence. The functional significance of sex differences in dispersal and their connection, if any, to the avoidance of inbreeding is disputed. Here I show that in polygynous mammals where females commonly remain to breed in their natal group, their average age at first conception typically exceeds the average period of residence of adult males in breeding groups. In contrast, where females usually transfer to breed in other groups, the average residence of breeding males or of resident male kin groups typically exceeds the average age of females at first conception. These results support the suggestion that female mammals commonly transfer to avoid inbreeding with their father or other close relatives, although female dispersal may also occur for other reasons.     

Mutual mate choice in the Asiatic toad, Bufo gargarizans, exerts stabilizing selection on body size

Sexual selection is critical to both reproduction and evolution.The effects of male–male competition and female choice regarding body size have been examined in a large number of taxa,including toad species.Males and females have different optimal reproductive strategies,achieving breeding advantages in discrepant ways.Further,the relative contributions of intra-and inter-sexual size selection vary among species.Thus,to understand the mechanisms affecting mating success,it is important to consider both male–male and male–female interactions simultaneously and elucidate their interrelationship.In this study,we measured body sizes of all mated and unmated individuals in a population of Asiatic toad(Bufo gargarizans)and counted fertilized eggs of several clutches.Based on correlation and regression techniques,we tested for female choice and intra-sexual competition among males relative to body size gradients,and we compared the relative importance of these two processes for mating success.Our results reveal that male–male competition and female choice simultaneously contribute to sexual selection in toads.Furthermore,both interactions are most intense among smaller toads.The synergistic trends of male–male competition and female choice support the mutual mate choice hypothesis and works to stabilize body size in B.gargarizans.Normal distributions of breeding success relative to body size were detected for both sexes,suggesting that medium-sized individuals enjoy a reproductive advantage in the population studied.     

Sperm death and dumping in Drosophila

Mating with more than one male is the norm for females of many species. In addition to generating competition between the ejaculates of different males, multiple mating may allow females to bias sperm use. In Drosophila melanogaster, the last male to inseminate a female sires approximately 80% of subsequent progeny. Both sperm displacement, where resident sperm are removed from storage by the incoming ejaculate of the copulating male, and sperm incapacitation, where incoming seminal fluids supposedly interfere with resident sperm, have been implicated in this pattern of sperm use. But the idea of incapacitation is problematic because there are no known mechanisms by which an individual could damage rival sperm and not their own. Females also influence the process of sperm use, but exactly how is unclear. Here we show that seminal fluids do not kill rival sperm and that any 'incapacitation' is probably due to sperm ageing during sperm storage. We also show that females release stored sperm from the reproductive tract (sperm dumping) after copulation with a second male and that this requires neither incoming sperm nor seminal fluids. Instead, males may cause stored sperm to be dumped or females may differentially eject sperm from the previous mating.     

Behavioural ecology: transient sexual mimicry leads to fertilization

Sexual mimicry among animals is widespread, but does it impart a fertilization advantage in the widely accepted 'sneak-guard' model of sperm competition? Here we describe field results in which a dramatic facultative switch in sexual phenotype by sneaker-male cuttlefish leads to immediate fertilization success, even in the presence of the consort male. These results are surprising, given the high rate at which females reject copulation attempts by males, the strong mate-guarding behaviour of consort males, and the high level of sperm competition in this complex mating system.     

True paternal care in a multi-male primate society

Although male parental care is rare among mammals, adult males of many cercopithecine primate species provide care for infants and juveniles. This care is often in the form of grooming, carrying, support in agonistic interactions, and protection against infanticide. For these behaviours to be interpreted as true parental care, males must selectively direct care towards their own offspring and this care must result in fitness benefits. With the exception of males defending probable offspring from infanticide, male primates living in multi-male, multi-female social groups have not been shown to selectively direct care towards their own offspring. We determined paternity for 75 juveniles in a population of wild savannah baboons (Papio cynocephalus) and collected data on interventions in agonistic disputes by adult males on behalf of juveniles as a form of male care. Here we show that adult males differentiate their offspring from unrelated juveniles and selectively support their offspring in agonistic disputes. As support in agonistic disputes is likely to contribute to rank acquisition and protect juveniles from injury and stress, this can be considered true parental care.     

Outbred embryos rescue inbred half-siblings in mixed-paternity broods of live-bearing females

Females commonly mate with more than one male, and polyandry has been shown to increase reproductive success in many species. Insemination by multiple males shifts the arena for sexual selection from the external environment to the female reproductive tract, where sperm competition or female choice of sperm could bias fertilization against sperm from genetically inferior or genetically incompatible males. Evidence that polyandry can be a strategy for avoiding incompatibility comes from studies showing that inbreeding cost is reduced in some egg-laying species by postcopulatory mechanisms that favour fertilization by sperm from unrelated males. In viviparous (live-bearing) species, inbreeding not only reduces offspring genetic quality but might also disrupt feto-maternal interactions that are crucial for normal embryonic development. Here we show that polyandry in viviparous pseudoscorpions reduces inbreeding cost not through paternity-biasing mechanisms favouring outbred offspring, but rather because outbred embryos exert a rescuing effect on inbred half-siblings in mixed-paternity broods. The benefits of polyandry may thus be more complex for live-bearing females than for females that lay eggs.     

Directional postcopulatory sexual selection revealed by artificial insemination

Postcopulatory sexual selection comprises both sperm competition, where the sperm from different males compete for fertilization, and cryptic female choice, where females bias sperm use in favour of particular males. Despite intense current interest in both processes as potential agents of directional sexual selection, few studies have attributed the success of attractive males to events that occur exclusively after insemination. This is because the interactions between pre- and post-insemination episodes of sexual selection can be important sources of variation in paternity. The use of artificial insemination overcomes this difficulty because it controls for variation in male fertilization success attributable to the female's perception of male quality, as well as effects due to mating order and the relative contribution of sperm from competing males. Here, we adopt this technique and show that in guppies, when equal numbers of sperm from two males compete for fertilization, relatively colourful individuals achieve greater parentage than their less ornamented counterparts. This finding indicates that precopulatory female mating preferences can be reinforced exclusively through postcopulatory processes occurring at a physiological level. Our analysis also revealed that relatively small individuals were advantaged in sperm competition, suggesting a possible trade-off between sperm competitive ability and body growth.     

Egg investment is influenced by male attractiveness in the mallard

Why females prefer to copulate with particular males is a contentious issue. Attention is currently focused on whether females choose males on the basis of their genetic quality, in order to produce more viable offspring. Support for this hypothesis in birds has come from studies showing that preferred males tend to father offspring of better condition or with increased survivorship. Before attributing greater offspring viability to a male's heritable genetic quality, however, it is important to discount effects arising from confounding sources, including maternal effects. This has generally been addressed by comparing offspring viability from two different breeding attempts by the same female: one when offspring are sired by a preferred male, and one when offspring are sired by a less preferred male. However, here we show that individual female mallard (Anas platyrhynchos) lay larger eggs after copulating with preferred males and smaller eggs after copulating with less preferred males. As a result, females produced offspring of better body condition when paired with preferred males. After controlling for these differences in maternal investment, we found no effect of paternity on offspring condition. This shows that differences between half-sibs cannot always be attributed to paternal or maternal genetic effects.