Female control of paternity

Of the two components of sexual selection, female choice is much less obvious than male-male competition, and hence has always been considered to be of secondary importance. However, recent field observations and new theory have brought about a radical change of emphasis. It now appears that although a female's choice of who fathers her offspring often occurs in a subtle manner, it may be widespread and take place through a variety of behavioural and physiological mechanisms, including the manipulation of male behaviour and the selection of sperm within the female reproductive tract.     

Infanticide and control of reproduction in cooperative and communal breeders

Many communal breeders are characterized by a conflict over who gets to reproduce, with dominant individuals often claiming the largest share of reproduction in the group. How do dominants control breeding in these species? Although infanticide has often been invoked as a means of control, previous theoretical work on indiscriminate killing of young did not support this idea. There is, however, increasing evidence from field studies in both vertebrates and insects that infanticidal individuals can discriminate between their own offspring and those of other group members, and thus avoid the risk of accidentally killing their own progeny. In a simple game-theoretical model we demonstrate that the capacity for discriminate infanticide can promote high reproductive skew even though few or no offspring are actually killed. When discrimination is good and offspring are cheap to produce, the threat of infanticide prevents the subordinate cobreeder from adding many young to the joint brood, and no killing need occur. High levels of infanticide tend to occur only when discrimination is poor, costs of offspring production are low and/or relatedness is low.     

Female control of paternity in the sexually cannibalistic spider Argiope keyserlingi

Sexual conflict theory predicts an antagonistic coevolution, with each sex evolving adaptations and counter-adaptations to overcome a temporary dominance of the other sex over the control of paternity. Polyandry allows sexual selection to operate after mating has commenced, with male and female interests competing for control of fertilization. There are numerous examples of male control of paternity, but few studies have unambiguously revealed female control. Attributing variance in paternity to females is often difficult since male and female influences cannot be separated unambiguously. However, we show that polyandrous female orb-web spiders Argiope keserlingi (Arancidae) control the paternity of their offspring by adjusting the timing of sexual cannibalism. Our experiments reveal that females copulating with relatively smaller males delay sexual cannibalism, thereby prolonging the duration of copulation, and that these males consequently fertilize relatively more eggs.     

Behavioural tactics of breeders in cooperative meerkats

In eusocial invertebrates, queens commonly show morphological and behavioural modifications to their role as the principal breeders in their colonies. With the exception of naked mole-rats, Heterocephalus glaber, morphological modification of breeders has yet to be shown in cooperative vertebrates, but the behaviour of dominant individuals may be modified so as to maximize reproductive success. We studied the cooperative behaviour of dominant and subordinate adults in meerkats, Suricata suricatta, and found that the decision rules governing the contributions of dominant breeders differed from those of subordinate helpers. Dominant breeders contributed less than adult helpers to babysitting and pup feeding, but raised their individual contributions to pup care to a greater extent when helper:pup ratios were low. In contrast to subordinates, dominant breeders did not increase their contributions when they foraged successfully. Finally, while subordinates of both sexes assisted in rearing the young when dominants bred, dominant females contributed little when subordinates attempted to breed, and male helpers (but not females) reduced their contributions to the care of pups. Our results suggest that the division of labour between breeders and helpers in meerkats is intermediate between that of facultatively cooperative species, where parents are principally responsible for rearing young, and that of specialized eusocial species, which show a well-defined division of labour between breeders and workers.     

Female control in yellow-legged gulls: trading paternity assurance for food

Females in many socially monogamous birds copulate hundreds of times more than necessary for fertilization, although little is known about the benefits of this excess. Females may not directly benefit from high copulation rates, but instead may exploit male interest in copulating to obtain benefits. In species with courtship feeding, females may trade copulations for food (immediate benefits hypothesis). I tested this hypothesis by analysing female behaviour during courtship in yellow-legged gulls, Larus cachinnans. Female gulls to some extent controlled sperm transfer, because they moved during copulation bouts, and this behaviour influenced the number of cloacal contacts per mounting that the male achieved. Female control was related to previous feeding by the male, and hence the male courtship feeding rate correlated with the cloacal contact rate. Males that give more food probably enhance their chances of fathering offspring. By analysing within-individual female behaviour, I also found that the number of cloacal contacts was higher when the male fed the female than when he did not, which indicates that female gulls followed a decision rule to resist copulation when food is not given. Overall, these results support the hypothesis that female gulls manipulate their mates to obtain food.     

The evolution of delayed dispersal in cooperative breeders.

Why do the young of cooperative breeders--species in which more than two individuals help raise offspring at a single nest--delay dispersal and live in groups? Answering this deceptively simple question involves examining the costs and benefits of three alternative strategies: (1) dispersal and attempting to breed, (2) dispersal and floating, and (3) delayed dispersal and helping. If, all other things being equal, the fitness of individuals that delay dispersal is greater than the fitness of individuals that disperse and breed on their own, intrinsic benefits are paramount to the current maintenance of delayed dispersal. Intrinsic benefits are directly due to living with others and may include enhanced foraging efficiency and reduced susceptibility to predation. However, if individuals that disperse and attempt to breed in high-quality habitat achieve the highest fitness, extrinsic constraints on the ability of offspring to obtain such high-quality breeding opportunities force offspring to either delay dispersal or float. The relevant constraint to independent reproduction has frequently been termed habitat saturation. This concept, of itself, fails to explain the evolution of delayed dispersal. Instead, we propose the delayed-dispersal threshold model as a guide for organizing and evaluating the ecological factors potentially responsible for this phenomenon. We identify five parameters critical to the probability of delayed dispersal: relative population density, the fitness differential between early dispersal/breeding and delayed dispersal, the observed or hypothetical fitness of floaters, the distribution of territory quality, and spatiotemporal environmental variability. A key conclusion from the model is that no one factor by itself causes delayed dispersal and cooperative breeding. However, a difference in the dispersal patterns between two closely related species or populations (or between individuals in the same population in different years) may be attributable to one or a small set of factors. Much remains to be done to pinpoint the relative importance of different ecological factors in promoting delayed dispersal. This is underscored by our current inability to explain satisfactorily several patterns including the relative significance of floating, geographic biases in the incidence of cooperative breeding, sexual asymmetries in delayed dispersal, the relationship between delayed dispersal leading to helping behavior and cooperative polygamy, and the rarity of the co-occurrence of helpers and floaters within the same population. Advances in this field remain to be made along several fronts.(ABSTRACT TRUNCATED AT 400 WORDS)     

Impact of natural enemies on obligately cooperative breeders

Obligately cooperative breeders (cooperators) display a negative growth rate once they fall below a minimum density. Constraints imposed by natural enemies, such as predators or competitors, may push cooperator groups closer to this threshold, thus increasing the risk that stochastic fluctuations will drive them below it. This may indirectly drive these groups to extinction, thereby increasing the risk of population extinction. In this paper, we construct mathematical models of the dynamics of groups of cooperators and non-cooperators in the presence of two types of enemies: enemies whose dynamics do not depend on the dynamics of their victim (e.g., amensal competitor, generalist predator) and those whose dynamics do. In the latter case, we distinguish positive (e.g., specialist predator) and negative (e.g., bilateral competitor) reciprocal effects. These models correspond to the classical amensal, predation and competition models, in the presence of an Allee effect. We then develop the models to study consequences at the population level. By comparing models with or without an Allee effect, we show that enemies decrease the group size of cooperators more than that of non-cooperators, and this increases their group extinction risk. We also demonstrate how an Allee effect at a lower dynamical level can have consequences at a higher level: inverse density dependence at the group level generated lower population sizes and higher risks of population extinction. Our results also suggest that demographic compensation can be achieved by cooperators through an increased intrinsic growth rate, or by decreasing the enemy constraint. Both of these types of compensation have been observed in empirical studies of cooperators.     

Stable group size in cooperative breeders: the role of inheritance and reproductive skew

Recent studies of reproductive skew have revealed great variationin the distribution of direct fitness among group members, yetthere have been surprisingly few attempts to explore the consequencesof such variation for stable group size, and none that takeinto account the future benefits of group membership to nonbreeders.This means that the existing theory is not suited to explainthe group size of most cooperatively breeding vertebrates andprimitively social insects in which group membership involvessubstantial future benefits. Here we model the group size ofsuch species as social queues in which nonbreeders can inherita breeding position if they outlive those ahead of them in thequeue. We demonstrate, however, that the results can be generalizedto systems in which inheritance occurs via scramble competition,rather than via a strict queue. The model predicts that stablegroup size will depend on the number of breeding positions inthe group and the mortality rates of breeders and nonbreeders,but not on the distribution of reproduction among the pool ofbreeders. This is because deaths occur at random, so that eachindividual has the same chance of surviving to reach each breedingposition. We tested a specific prediction of the model usingdata on ovarian development in the paper wasp, Polistes dominulus.We found a positive correlation between group size and the proportionof females with fully developed eggs, as predicted. Our resultsclarify the interaction between the dominance structure andsize of animal groups and add to the growing recognition ofthe potential for inheritance as a major determinant of bothindividual behavior and group-level characteristics of animalsocieties.     

Female influence over offspring paternity in the red flour beetle Tribolium castaneum

In animals having internal fertilization, both sexes can potentially influence the post-copulatory processes of sperm transfer, sperm storage and sperm use for fertilization. In this experiment, we investigated whether Tribolium castaneum females can influence male paternity success following consecutive matings with two different males. We compared second male paternity success (P2) between females exposed to carbon dioxide (CO2) and control females kept in air, in both cases for 30 min between two matings. CO2 exposure inhibits muscular activity and has previously been shown to decrease sperm storage by T. castaneum females. Females exposed to CO2 after their first mating showed significantly higher P2 than control females during the later portion of a one-month oviposition period. These results are consistent with reduced storage of first male sperm by CO2-exposed females. Also, T. castaneum females showed considerable variation in spermathecal morphology, and P2 decreased with increasing spermathecal tubule volume. These results demonstrate that T. castaneum females can influence male paternity success, and suggest that differential sperm storage may be an important mechanism of post-copulatory female choice.     

Female choice and extra-pair paternity in a traditional human population

Seeking out extra-pair paternity (EPP) is a viable reproductive strategy for females in many pair-bonded species. Across human societies, women commonly engage in extra-marital affairs, suggesting this strategy may also be an important part of women's reproductive decision-making. Here, I show that among the Himba 17 per cent of all recorded marital births are attributed by women to EPP, and EPP is associated with significant increases in women's reproductive success. In contrast, there are no cases of EPP among children born into 'love match' marriages. This rate of EPP is higher than has been recorded in any other small-scale society. These results illustrate the importance of seeking EPP as a mechanism of female choice in humans, while simultaneously showing it to be highly variable and context-dependent.     

Female aggression predicts mode of paternity acquisition in a social lizard

Individual differences in behaviour are ubiquitous in nature. Despite the likely role of selection in maintaining these differences, there are few demonstrations of their fitness consequences in wild populations and, consequently, the mechanisms that link behavioural variation to variation in fitness are poorly understood. Specifically, the consequences of consistent individual differences in behaviour for the evolution of social and mating strategies have rarely been considered. We examined the functional links between variation in female aggression and her social and mating strategies in a wild population of the social lizard Egernia whitii. We show that female Egernia exhibit temporally consistent aggressive phenotypes, which are unrelated to body size, territory size or social density. A female''s aggressive phenotype, however, has strong links to her mode of paternity acquisition (within- versus extra-pair paternity), with more aggressive females having more offspring sired by extra-pair males than less aggressive females. We discuss the potential mechanisms by which female aggression could underpin mating strategies, such as the pursuit/acceptance of extra-pair copulations. We propose that a deeper understanding of the evolution and maintenance of social and mating systems may result from an explicit focus on individual-level female behavioural phenotypes and their relationship with key reproductive strategies.     

Female mate choice predicts paternity success in the absence of additive genetic variance for other female paternity bias mechanisms in Drosophila serrata

After choosing a first mate, polyandrous females have access to a range of opportunities to bias paternity, such as repeating matings with the preferred male, facilitating fertilization from the best sperm or differentially investing in offspring according to their sire. Female ability to bias paternity after a first mating has been demonstrated in a few species, but unambiguous evidence remains limited by the access to complex behaviours, sperm storage organs and fertilization processes within females. Even when found at the phenotypic level, the potential evolution of any mechanism allowing females to bias paternity other than mate choice remains little explored. Using a large population of pedigreed females, we developed a simple test to determine whether there is additive genetic variation in female ability to bias paternity after a first, chosen, mating. We applied this method in the highly polyandrous Drosophila serrata, giving females the opportunity to successively mate with two males ad libitum. We found that despite high levels of polyandry (females mated more than once per day), the first mate choice was a significant predictor of male total reproductive success. Importantly, there was no detectable genetic variance in female ability to bias paternity beyond mate choice. Therefore, whether or not females can bias paternity before or after copulation, their role on the evolution of sexual male traits is likely to be limited to their first mate choice in D. serrata.     

Parentage assignment and extra-group paternity in a cooperative breeder: the Seychelles warbler (Acrocephalus sechellensis)

We describe the development and initial application of a semiautomated parentage testing system in the Seychelles warbler (Acrocephalus sechellensis). This system used fluorescently labelled primers for 14 polymorphic microsatellite loci in two multiplex loading groups to genotype efficiently over 96% of the warbler population on Cousin island. When used in conjunction with the program CERVUS, this system provided sufficient power to assign maternity and paternity within the Seychelles warbler, despite the complications associated with its cooperative breeding system and a relatively low level of genetic variation. Parentage analyses showed that subordinate 'helper' females as well as the dominant 'primary' females laid eggs in communal nests, indicating that the Seychelles warbler has an intermediate level of female reproductive skew, in between the alternative extremes of helper-at-the-nest and joint nesting systems. Forty-four per cent of helpers bred successfully, accounting for 15% of all offspring. Forty per cent of young resulted from extra-group paternity.     

Female reproductive strategies, paternity and community structure in wild West African chimpanzees

Although the variability and complexity of chimpanzee behaviour frustrates generalization, it is widely believed that social evolution in this species occurs in the context of the recognizable social group or community. We used a combination of field observations and noninvasive genotyping to study the genetic structure of a habituated community of 55 wild chimpanzees, Pan troglodytes verus, in the Ta? Forest, C?te d'Ivoire. Pedigree relationships in that community show that female mate choice strategies are more variable than previously supposed and that the observed social groups are not the exclusive reproductive units. Genetic evidence based on nuclear microsatellite markers and behavioural obser-vations reveal that females in the Ta? forest actively seek mating partners outside their social unit; noncommunity males accounted for half the paternities over 5 years. This female mating strategy increases male gene flow between communities despite male philopatry, and negates the predicted higher relatedness among community males. Kin selection seems unlikely to explain the frequent cooperation and sharing observed among group males in this population. Similarly, inbreeding avoidance is probably not the sole cause of permanent adolescent female dispersal as a combination of extragroup mating and avoidance of incest with home group males would allow females to avoid inbreeding without the hazards associated with immigration into a new community. Extragroup mating as part of chimpanzee females' reproductive strategy may allow them to choose from a wider variety and number of males, without losing the resources and support provided by their male social group partners. Copyright 1999 The Association for the Study of Animal Behaviour.     

Female effects,but no intrinsic male effects on paternity outcome in crickets

Competitive fertilization success can depend on the relative abilities of competing males to fertilize available ova, and on mechanisms of cryptic female choice that moderate paternity. Competitive fertilization success is thus an emergent property of competing male genotypes, female genotype and their interactions. Accurate estimates of intrinsic male effects on competitive fertilization success are therefore problematic. We used a cross‐classified nonbreeding design in which rival male family background was standardized to partition variation in competitive fertilization success among male and female family backgrounds in the field cricket Teleogryllus oceanicus. Male effects were close to zero, supporting previous quantitative genetic designs in which male competitors were assigned at random. In contrast, some 22% of the variance in competitive fertilization success was explained by female effects, suggesting that paternity in this species is influenced strongly by cryptic female choice.     

Subordinate male meerkats prospect for extra-group paternity: alternative reproductive tactics in a cooperative mammal

In cooperatively breeding species, subordinates typically suffer strong constraints on within-group reproduction. While numerous studies have highlighted the additional fitness benefits that subordinates might accrue through helping, few have considered the possibility that subordinates may also seek extra-group matings to improve their chances of actually breeding. Here, we show that subordinate males in cooperative meerkat, Suricata suricatta, societies conduct frequent extraterritorial forays, during periods of peak female fertility, which give rise to matings with females in other groups. Genetic analyses reveal that extra-group paternity (EGP) accrued while prospecting contributes substantially to the reproductive success of subordinates: yielding the majority of their offspring (approx. 70%); significantly reducing their age at first reproduction and allowing them to breed without dispersing. We estimate that prospecting subordinates sire 20-25% of all young in the population. While recent studies on cooperative birds indicate that dominant males accrue the majority of EGP, our findings reveal that EGP can also arise from alternative reproductive tactics employed exclusively by subordinates. It is important, therefore, that future attempts to estimate the fitness of subordinate males in animal societies quantify the distribution of extra-group as well as within-group paternity, because a substantial proportion of the reproductive success of subordinates may otherwise go undetected.