Female reproductive competition within families in rural Gambia

Many studies show that the extended human family can be helpful in raising offspring, with maternal grandmothers, in particular, improving offspring survival. However, less attention has been given to competition between female kin and co-residents. It has been argued that reproductive conflict between generations explains the evolution of menopause in cooperatively breeding species where females disperse, and that older females are related to the offspring of younger females through their sons, whereas younger, incoming females are unrelated to older females. This means the pattern of help will be asymmetric, so older females lose in reproductive conflict and become 'sterile helpers'. Here, we seek evidence for female reproductive competition using longitudinal demographic data from a rural Gambian population, and examine when women are helping or harming each other's reproductive success. We find that older women benefit and younger women suffer costs of reproductive competition with women in their compound. But the opposite is found for mothers and daughters; if mother and daughter's reproductive spans overlap, the older woman reduces her reproduction if the younger woman (daughter) reproduces, whereas daughters' fertility is unaffected by their mothers' reproduction. Married daughters are not generally co-resident with their mothers, so we find not only competition effects with co-resident females, but also with daughters who have dispersed. Dispersal varies across human societies, but our results suggest reproductive conflict could be influencing reproductive scheduling whatever the dispersal pattern. A cultural norm of late male marriage reduces paternal grandmother/daughter-in-law reproductive overlap almost to zero in this population. We argue that cultural norms surrounding residence and marriage are themselves cultural adaptations to reduce reproductive conflict between generations in human families.     

Sperm competition risk generates phenotypic plasticity in ovum fertilizability

Theory predicts that sperm competition will generate sexual conflict that favours increased ovum defences against polyspermy. A recent study on house mice has shown that ovum resistance to fertilization coevolves in response to increased sperm fertilizing capacity. However, the capacity for the female gamete to adjust its fertilizability as a strategic response to sperm competition risk has never, to our knowledge, been studied. We sourced house mice (Mus domesticus) from natural populations that differ in the level of sperm competition and sperm fertilizing capacity, and manipulated the social experience of females during their sexual development to simulate conditions of either a future ‘risk’ or ‘no risk’ of sperm competition. Consistent with coevolutionary predictions, we found lower fertilization rates in ova produced by females from a high sperm competition population compared with ova from a low sperm competition population, indicating that these populations are divergent in the fertilizability of their ova. More importantly, females exposed to a ‘risk’ of sperm competition produced ova that had greater resistance to fertilization than ova produced by females reared in an environment with ‘no risk’. Consequently, we show that variation in sperm competition risk during development generates phenotypic plasticity in ova fertilizability, which allows females to prepare for prevailing conditions during their reproductive life.     

Rank relations among sisters in semi-free-ranging Barbary macaques (Macaca sylvanus)

Although semi-free-ranging Barbary macaque females are able to outrank older females from lower-ranking matrilines (matrilineal rank acquisition), they do not systematically outrank their older sisters, as is known to be the case for semi-free-ranging rhesus monkeys (Macaca mulatta) and Japanese macaques (Macaca fuscata). We test the hypothesis that differences in the support received by younger sisters against their older sisters and against older lower-ranking females might account for this interspecific difference. Thirty-one sister dyads, members of a group of 109 Barbary macaques living at La Montagne des Singes, France, were observed during 16 months. The results indicate that (1) all females were dominant to their younger sisters, and the latter were never observed to challenge their older sisters; (2) younger sisters received as much kin support against their older sisters as against older lower-ranking females; (3) only very young females received support from their kin against their older sisters; (4) younger sisters received much more support from nonkin females against lower-ranking females than against their older sisters; and (5) Barbary macaque females appear to be supported against their older sisters less frequently than rhesus macaque females are. We conclude that the lack of nonkin support is the main factor accounting for the failure of younger sisters to outrank their older sisters in Barbary macaques. Initially this might result from kin support not being sufficient to induce younger sisters to challenge and to solicit support against their older sisters.     

The evolution of matrilineal kinship organization

Matrilineal kinship organization is a human social system that emphasizes interactions between matrilineal kin, i.e. individuals related only through females. The ‘matrilineal puzzle’ refers to the potential for tension characteristic of this social system, owing to the conflict between the interests and responsibilities of men in their roles as brother/uncle versus husband/father. From an evolutionary perspective, matrilineal kinship organization is puzzling when it diverts investment of resources from the individuals who provide the potentially highest reproductive returns. I use a game-theoretic framework to investigate a particular form of matrilineal inheritance—the transfer of property from a maternal uncle to a sororal nephew. The analysis reveals two mechanisms that may make this strategy a stable evolutionary outcome. First, a polygynous male has multiple wives, and hence multiple brothers-in-law; with matrilineal inheritance, each additional brother-in-law may transfer resources to the male''s wife''s offspring, thus potentially contributing to the male''s inclusive fitness. Second, the husband of a polyandrous female is effectively ‘sharing’ paternity with other men; depending on the number of husbands, he may be better off investing in his sister''s offspring. I conclude by discussing how these results address the challenges posed by the occurrence of matrilineal kinship organization.     

A Novel Quantitative Approach to Women’s Reproductive Strategies

The patterned way in which individuals allocate finite resources to various components of reproduction (e.g. mating effort, reproductive timing and parental investment) is described as a reproductive strategy. As energy is limited, trade-offs between and within aspects of reproductive strategies are expected. The first aim of this study was to derive aspects of reproductive strategies using complete reproductive histories from 718 parous Western Australian women. Factor analysis using a subset of these participants resulted in six factors that represented ‘short-term mating strategy’, ‘early onset of sexual activity’, ‘reproductive output’, ‘timing of childbearing’, ‘breastfeeding’, and ‘child spacing’. This factor structure was internally validated by replication using a second independent subset of the data. The second aim of this study examined trade-offs between aspects of reproductive strategies derived from aim one. Factor scores calculated for each woman were incorporated in generalised linear models and interaction terms were employed to examine the effect of mating behaviour on the relationships between reproductive timing, parental investment and overall reproductive success. Early sexual activity correlates with early reproductive onset for women displaying more long-term mating strategies. Women with more short-term mating strategies exhibit a trade-off between child quantity and child quality not observed in women with a long-term mating strategy. However, women with a short-term mating strategy who delay reproductive timing exhibit levels of parental investment (measured as breastfeeding duration per child) similar to that of women with long-term mating strategies. Reproductive delay has fitness costs (fewer births) for women displaying more short-term mating strategies. We provide empirical evidence that reproductive histories of contemporary women reflect aspects of reproductive strategies, and associations between these strategic elements, as predicted from life history theory.     

Family and Fertility: Kin Influence on the Progression to a Second Birth in the British Household Panel Study

Particular features of human female life history, such as short birth intervals and the early cessation of female reproduction (menopause), are argued to be evidence that humans are ‘cooperative breeders’, with a reproductive strategy adapted to conditions where mothers receive substantial assistance in childraising. Evolutionary anthropologists have so far largely focussed on measuring the influence of kin on reproduction in natural fertility populations. Here we look at the effect in a present-day low-fertility population, by analysing whether kin affect parity progression in the British Household Panel Study. Two explanatory variables related to kin influence significantly increase the odds of a female having a second birth: i) having relatives who provide childcare and ii) having a larger number of frequently contacted and emotionally close relatives. Both effects were measured subject to numerous socio-economic controls and appear to be independent of one another. We therefore conclude that kin may influence the progression to a second birth. This influence is possibly due to two proximate mechanisms: kin priming through communication and kin assistance with childcare.     

The police are not the army: context-dependent aggressiveness in a clonal ant

Animals often exhibit particular ‘personalities’, i.e. their behaviour is correlated across different situations. Recent studies suggest that this limitation of behavioural plasticity may be adaptive, since continuous adjustment of one''s behaviour may be time-consuming and costly. In social insects, particularly aggressive workers might efficiently take over fighting in the contexts of both nest defence and ‘policing’, i.e. the regulation of kin conflict in the society. Here, we examine whether workers who engage in aggressive policing in the ant Platythyrea punctata play a prominent role also in nest defence against intruders. The participation of individuals in policing and nest defence was highly skewed and a minority of workers exhibited most of the aggression. Workers who attacked reproductives after experimental colony fusion were less active during nest defence and vice versa. This suggests that workers show situation-dependent behavioural plasticity rather than consistently aggressive personalities.     

Parental provisioning behaviour plays a key role in linking personality with reproductive success

Repeatable behavioural traits (‘personality’) have been shown to covary with fitness, but it remains poorly understood how such behaviour–fitness relationships come about. We applied a multivariate approach to reveal the mechanistic pathways by which variation in exploratory and aggressive behaviour is translated into variation in reproductive success in a natural population of blue tits, Cyanistes caeruleus. Using path analysis, we demonstrate a key role for provisioning behaviour in mediating the link between personality and reproductive success (number of fledged offspring). Aggressive males fed their nestlings at lower rates than less aggressive individuals. At the same time, their low parental investment was associated with increased female effort, thereby positively affecting fledgling production. Whereas male exploratory behaviour was unrelated to provisioning behaviour and reproductive success, fast-exploring females fed their offspring at higher rates and initiated breeding earlier, thus increasing reproductive success. Our findings provide strong support for specific mechanistic pathways linking components of behavioural syndromes to reproductive success. Importantly, relationships between behavioural phenotypes and reproductive success were obscured when considering simple bivariate relationships, underlining the importance of adopting multivariate views and statistical tools as path analysis to the study of behavioural evolution.     

Does kin selection moderate sexual conflict in Drosophila?

Two recent studies provide provocative experimental findings about the potential influence of kin recognition and cooperation on the level of sexual conflict in Drosophila melanogaster. In both studies, male fruit flies apparently curbed their mate-harming behaviours in the presence of a few familiar or related males, suggesting some form of cooperation mediated by kin selection. In one study, the reduction in agonistic behaviour by brothers apparently rendered them vulnerable to dramatic loss of paternity share when competing with an unrelated male. If these results are robust and generalizable, fruit flies could be a major new focus for the experimental study of kin selection and social evolution. In our opinion, however, the restrictive conditions required for male cooperation to be adaptive in this species make it unlikely to evolve. We investigated these phenomena in two different populations of D. melanogaster using protocols very similar to those in the two previous studies. Our experiments show no evidence for a reduction in mate harm based upon either relatedness or familiarity between males, and no reduction in male reproductive success when two brothers are in the presence of an unfamiliar, unrelated, ‘foreign’ male. Thus, the reduction of sexual conflict owing to male cooperation does not appear to be a general feature of the species, at least under domestication, and these contrasting results call for further investigation: in new populations, in the field and in the laboratory populations in which these phenomena have been reported.     

A strategy of movement and resource utilization

A set of age-specific rates of birth and death implies expected numbers of kin. An individual girl or woman chosen at random out of a population whose birth and death rates are specified can be expected to have a certain number of older sisters, younger sisters, nieces, cousins; expressions for these values are provided for both total kin and kin who are still living. Included also are the probabilities of living mother, grandmother, and great grandmother for girls and women of various ages. The methods are applicable to the size of the nuclear and the extended family. All formulas have been programmed and specimen numerical values are given.     

Conjugative plasmids: vessels of the communal gene pool

Comparative whole-genome analyses have demonstrated that horizontal gene transfer (HGT) provides a significant contribution to prokaryotic genome innovation. The evolution of specific prokaryotes is therefore tightly linked to the environment in which they live and the communal pool of genes available within that environment. Here we use the term supergenome to describe the set of all genes that a prokaryotic ‘individual’ can draw on within a particular environmental setting. Conjugative plasmids can be considered particularly successful entities within the communal pool, which have enabled HGT over large taxonomic distances. These plasmids are collections of discrete regions of genes that function as ‘backbone modules’ to undertake different aspects of overall plasmid maintenance and propagation. Conjugative plasmids often carry suites of ‘accessory elements’ that contribute adaptive traits to the hosts and, potentially, other resident prokaryotes within specific environmental niches. Insight into the evolution of plasmid modules therefore contributes to our knowledge of gene dissemination and evolution within prokaryotic communities. This communal pool provides the prokaryotes with an important mechanistic framework for obtaining adaptability and functional diversity that alleviates the need for large genomes of specialized ‘private genes’.     

Sexual deception in a cannibalistic mating system? Testing the Femme Fatale hypothesis

Animal communication theory holds that in order to be evolutionarily stable, signals must be honest on average, but significant dishonesty (i.e. deception) by a subset of the population may also evolve. A typical praying mantid mating system involves active mate searching by males, which is guided by airborne sex pheromones in most species for which mate-searching cues have been studied. The Femme Fatale hypothesis suggests that female mantids may be selected to exploit conspecific males as prey if they benefit nutritionally from cannibalism. Such a benefit exists in the false garden mantid Pseudomantis albofimbriata—females use the resources gained from male consumption to significantly increase their body condition and reproductive output. This study aimed to examine the potential for chemical deception among the subset of females most likely to benefit from cannibalism (poorly fed females). Females were placed into one of four feeding treatments (‘Very Poor’, ‘Poor’, ‘Medium’ and ‘Good’), and males were given the opportunity to choose between visually obscured females in each of the treatments. Female body condition and fecundity varied linearly with food quantity; however, female attractiveness did not. That is, Very Poor females attracted significantly more males than any of the other female treatments, even though these females were in significantly poorer condition, less fecund (in this study) and more likely to cannibalise (in a previous study). In addition, there was a positive correlation between fecundity and attractiveness if Very Poor females were removed from the analysis, suggesting an inherently honest signalling system with a subset of dishonest individuals. This is the first empirical study to provide evidence of sexual deception via chemical cues, and the first to provide support for the Femme Fatale hypothesis.     

Helpful Female Subordinate Cichlids Are More Likely to Reproduce

Background

In many cooperatively breeding vertebrates, subordinates assist a dominant pair to raise the dominants'' offspring. Previously, it has been suggested that subordinates may help in payment for continued residency on the territory (the ‘pay-to-stay hypothesis’), but payment might also be reciprocated or might allow subordinates access to reproductive opportunities.

Methodology/Principal Findings

We measured dominant and subordinate female alloparental brood care and reproductive success in four separate experiments and show that unrelated female dominant and subordinate cichlid fish care for each other''s broods (alloparental brood care), but that there is no evidence for reciprocal ‘altruism’ (no correlation between alloparental care received and given). Instead, subordinate females appear to pay with alloparental care for own direct reproduction.

Conclusions/Significance

Our results suggest subordinate females pay with alloparental care to ensure access to the breeding substrate and thereby increase their opportunities to lay their own clutches. Subordinates'' eggs are laid, on average, five days after the dominant female has produced her first brood. We suggest that immediate reproductive benefits need to be considered in tests of the pay-to-stay hypothesis.     

Size-dependent alternative male mating tactics in the yellow dung fly,Scathophaga stercoraria

Whenever males can monopolize females and/or resources used by females, the opportunity for sexual selection will be great. The greater the variation among males in reproductive success, the greater the intensity of selection on less competitive males to gain matings through alternative tactics. In the yellow dung fly, Scathophaga stercoraria, males aggressively compete for access to receptive, gravid females on fresh dung. Larger males are better able to acquire mates and to complete copulation successfully and guard the female throughout oviposition. Here we demonstrate that when an alternative resource is present where females aggregate (i.e. apple pomace, where both sexes come to feed), smaller males will redirect their searching for females from dung to the new substrate. In addition, we identify a class of particularly small males on the alternative substrate that appears never to be present searching for females on or around dung. Smaller males were found to have a mating ‘advantage’ on pomace, in striking contrast to the pattern observed on dung, providing further support for the existence of an alternative male reproductive tactic in this species.     

Female and male genetic contributions to post-mating immune defence in female Drosophila melanogaster

Post-mating reduction in immune defence is common in female insects, and a trade-off between mating and immunity could affect the evolution of immunity. In this work, we tested the capacity of virgin and mated female Drosophila melanogaster to defend against infection by four bacterial pathogens. We found that female D. melanogaster suffer post-mating immunosuppression in a pathogen-dependent manner. The effect of mating was seen after infection with two bacterial pathogens (Providencia rettgeri and Providencia alcalifaciens), though not after infection with two other bacteria (Enterococcus faecalis and Pseudomonas aeruginosa). We then asked whether the evolution of post-mating immunosuppression is primarily a ‘female’ or ‘male’ trait by assaying for genetic variation among females for the degree of post-mating immune suppression they experience and among males for the level of post-mating immunosuppression they elicit in their mates. We also assayed for an interaction between male and female genotypes to test the specific hypothesis that the evolution of a trade-off between mating and immune defence in females might be being driven by sexual conflict. We found that females, but not males, harbour significant genetic variation for post-mating immunosuppression, and we did not detect an interaction between female and male genotypes. We thus conclude that post-mating immune depression is predominantly a ‘female’ trait, and find no evidence that it is evolving under sexual conflict.     

Book notes

The costs and benefits of polygyny have been widely debated and vary according to local sociopolitical context, the level of female autonomy, and economic considerations such as the mode of production. This study aims to understand perceptions of polygyny as a function of household demography, particularly the number of female kin present in the household who can provide labor that is largely substitutable to that of a co-wife. The presence of these helpers is proposed to shift the cost-benefit structure of polygyny, in which having more female kin available is associated with a more negative view of the practice. Interview and census data from 106 Himba women, who are traditional, seminomadic pastoralists, were used to test this prediction. Among married women who reside patrilocally, the presence of more elder daughters was associated with a more negative view of polygyny. Among unmarried women, who reside in their natal homes, it is the total number of adult female kin that predicts perception of polygyny. In addition, unmarried women are significantly more likely to report fights over resources as a source of co-wife conflicts when they have more dependent children, but no such association was found among married women.     

Resolving the evolution of sterile worker castes: a window on the advantages and disadvantages of monogamy

Many social Hymenoptera species have morphologically sterile worker castes. It is proposed that the evolutionary routes to this obligate sterility must pass through a ‘monogamy window’, because inclusive fitness favours individuals retaining their reproductive totipotency unless they can rear full siblings. Simulated evolution of sterility, however, finds that ‘point of view’ is critically important. Monogamy is facilitating if sterility is expressed altruistically (i.e. workers defer reproduction to queens), but if sterility results from manipulation by mothers or siblings, monogamy may have no effect or lessen the likelihood of sterility. Overall, the model and data from facultatively eusocial bees suggest that eusociality and sterility are more likely to originate through manipulation than by altruism, casting doubt on a mandatory role for monogamy. Simple kin selection paradigms, such as Hamilton''s rule, can also fail to account for significant evolutionary dynamics created by factors, such as population structure, group-level effects or non-random mating patterns. The easy remedy is to always validate apparently insightful predictions from Hamiltonian equations with life-history appropriate genetic models.     

Cooperation and the common good

In this paper, we draw the attention of biologists to a result from the economic literature, which suggests that when individuals are engaged in a communal activity of benefit to all, selection may favour cooperative sharing of resources even among non-relatives. Provided that group members all invest some resources in the public good, they should refrain from conflict over the division of these resources. The reason is that, given diminishing returns on investment in public and private goods, claiming (or ceding) a greater share of total resources only leads to the actor (or its competitors) investing more in the public good, such that the marginal costs and benefits of investment remain in balance. This cancels out any individual benefits of resource competition. We illustrate how this idea may be applied in the context of biparental care, using a sequential game in which parents first compete with one another over resources, and then choose how to allocate the resources they each obtain to care of their joint young (public good) versus their own survival and future reproductive success (private good). We show that when the two parents both invest in care to some extent, they should refrain from any conflict over the division of resources. The same effect can also support asymmetric outcomes in which one parent competes for resources and invests in care, whereas the other does not invest but refrains from competition. The fact that the caring parent gains higher fitness pay-offs at these equilibria suggests that abandoning a partner is not always to the latter''s detriment, when the potential for resource competition is taken into account, but may instead be of benefit to the ‘abandoned’ mate.     

Influences on communication about reproduction: the cultural evolution of low fertility

The cultural norms of traditional societies encourage behavior that is consistent with maximizing reproductive success but those of modern post-demographic transition societies do not. Newson et al (2005) proposed that this might be because interaction between kin is relatively less frequent in modern social networks. Assuming that people's evaluations of reproductive decisions are influenced by a desire to increase their inclusive fitness, they will be inclined to prefer their kin to make fitness-enhancing choices. Such a preference will encourage the emergence of pronatal cultural norms if social networks are dense with kin. Less pronatal norms will emerge if contact between kin makes up a small proportion of social interactions. This article reports evidence based on role-play studies that supports the assumption of the kin influence hypothesis that evaluations of reproductive decisions are influenced by a desire to increase inclusive fitness. It also presents a cultural evolutionary model demonstrating the long-term effect of declining kin interaction if people are more likely to encourage fitness-enhancing choices when interacting with their kin than with nonrelatives.     

Supply and Demand Determine the Market Value of Access to Infants in the Golden Snub-Nosed Monkey (Rhinopithecus roxellana)

According to a biological market paradigm, trading decisions between partners will be influenced by the current ‘exchange rate’ of commodities (good and services), which is affected by supply and demand, and the trader’s ability to outbid competitors. In several species of nonhuman primates, newborn infants are attractive to female group members and may become a desired commodity that can be traded for grooming within a biological market place. We investigated whether grooming was interchanged for infant handling in female golden snub-nosed monkeys (Rhinopithecus roxellana) inhabiting the Qinling Mountains of central China. R. roxellana exhibit a multilevel social organization characterized by over 100 troop members organized into 6–11 one-male units each composed one adult male and several adult females and their offspring. Behavioral data were collected over the course of 28 months on grooming patterns between mothers with infants less than 6 months old (N = 36) and other adult female troop members. Our results provide strong evidence for the interchange of grooming for access to infants. Grooming for infant access was more likely to be initiated by potential handlers (nonmothers) and less likely reciprocated by mothers. Moreover, grooming bout duration was inversely related to the number of infants per female present in each one-male unit indicating the possibility of a supply and demand market effect. The rank difference between mothers and handlers was negatively correlated with grooming duration. With increasing infant age, the duration of grooming provided by handlers was shorter suggesting that the ‘value’ of older infants had decreased. Finally, frequent grooming partners were allowed to handle and maintain access to infants longer than infrequent groomers. These results support the contention that grooming and infant handling may be traded in R. roxellana and that the price individuals paid for access to infants fluctuated with supply and demand.