Complete separation along matrilines in a social spider metapopulation inferred from hypervariable mitochondrial DNA region

The distribution and quantity of genetic diversity may be profoundly influenced by the emergence and dynamics of social groups. Permanent social living in spiders has resulted in the subdivision of their populations in more or less isolated colony lineages that grow, proliferate and become extinct without mixing with one another. A newly discovered hypervariable mitochondrial DNA region allowed us to examine the fine scale metapopulation structure in the social Anelosimus eximius. We sampled 39 colonies in Ecuador and French Guiana and identified 25 haplotypes. The majority of colonies contained one haplotype. Additional haplotypes occurred in approximately 15% of the colonies, and were always closely related to the common colony haplotype. Our findings confirm that colonies consist of single matrilines, with within‐colony variation explained by mutations within the matriline. We thus found no evidence of mixing of matrilines. Likewise, colonies in a cluster often shared a haplotype, implying common colony ancestry. In few cases, however, haplotypes were shared between more distant colonies, providing evidence for occasional longer distance dispersal and/or widespread colony lineages. The geographical localities of colonies were incongruent with phylogenetic trees and haplotype networks, showing that some areas contained two or more matrilines. Hence, females do not migrate into foreign colonies, but faithfully remain within their own colony lineage, even when they disperse into new areas. These results indicate that the fine scale metapopulation structure of pure matrilines is maintained over the long term and that colony turnover is not extensive or radical enough to homogenize entire geographical areas. Genetic diversity is thus preserved to some extent at the metapopulation level.     

Social rank and sex ratio of captive long-tailed macaque females (Macaca fascicularis)

Variation in birth sex ratios in primates can be accounted for by two hypotheses: the local resource competition hypothesis [Silk: American Naturalist 121:56–66, 1983] and the hypothesis of Trivers & Willard [Science 179:90–92, 1973] concerning the maternal effect on the quality of a male. We examined the effects of female dominance rank on aspects of reproduction in three well-established captive groups of long-tailed macaques (Macaca fascicularis). High-ranking females produced a higher proportion of sons than low-ranking females, and factors other than rank did not have significant effects on birth sex ratios. Interbirth intervals following daughters were longer than those following sons, but they were independent of the mother's rank. The sons of high-ranking mothers had better survival prospects than sons of low-ranking mothers in some of the groups; no such difference was found for daughters. Overall, there was no sex difference in survival up to 5 years of age. These results support the Trivers-Willard hypothesis rather than the local resource competition hypothesis. An analysis of interbirth intervals suggested that the deviation in birth sex ratio is already established at conception.     

Sex Allocation in a Colobine Monkey

In polygynous, sexual dimorphic species with higher variance in male reproductive success compared with females, females are expected to invest more heavily in sons than daughters within the constraints imposed by their physical condition (Science 1973; 179:90). Mothers in good condition, usually those of high rank, should produce more sons than females in poor condition or of low rank. We investigated sex allocation and sex‐biased maternal investment in a population of wild Hanuman langurs using rank and group size as approximations of female physical condition. Our results show that reproductive costs of sons were higher with both significantly longer interbirth intervals following male births and longer lactational periods for sons. Not in all groups did analyses of rank‐dependent sex allocation reveal the expected pattern of high‐ranking mothers producing more sons. However, sex ratio was significantly influenced by group size, with females from larger groups, i.e., in worse physical condition, producing a daughter‐biased sex ratio. In fact, only females of population‐wide superior physical condition can be expected to produce sons, because in Hanuman langurs males disperse and compete population‐wide. Thus, our results support the Trivers–Willard model and may explain the mixed evidence accruing from studies of single groups. We present a graphical model of how group size and dominance‐related differences in energy gain may influence sex allocation under different competitive regimes relative to overall resource availability. Tests of adaptive sex allocation models should consider whether reproductive competition of the preferred sex takes place primarily within a group or within the population.     

Parental rank and reproductive success of natal rhesus males

In primates, the relationship between the ranks of parents and those of their sons has not been studied systematically, yet it has important implications for sociobiological theories. The influence of parents' ranks upon the ranks and reproductive success of their sons who remain and breed within their natal group was tested in two captive groups of rhesus macaques, Macaca mulatta. Paternity exclusion analyses revealed that both the rank and reproductive success of natal males were strongly associated with their mothers', but not their fathers', ranks. The ranks of natal males were also significantly correlated with their own reproductive success. However, this correlation was not nearly as strong as the correlation between the ranks and reproductive success of the fathers of these natal males. This difference was associated with a decline in reproductive success, but not in rank, of some founding males after natal males reached sexual maturity, and might result from an age bias in mating and/or the increase in the ratio of adult males to females. Although the reproductive advantage enjoyed by sons of high-ranking mothers prior to dispersal from their natal groups might be of evolutionary significance, it is important to determine whether or not this advantage persists after dispersal.     

Relationships of vervet mothers with sons and daughters from one through three years of age

Social relationships between mothers and juvenile offspring were examined in captive, socially-living vervet monkeys (Cercopithecus aethiops sabaeus) to assess the effects of offspring age and sex, and the mother's dominance rank on behavioural interactions. The results indicate that both high-and low-ranking mothers approach and groom their daughters more than they approach and groom their sons. The frequency of both aggressive behaviour toward offspring and support of offspring in agonistic encounters with other group members is influenced by the mother's dominance rank, but not by offsprin sex. Compared to sons, daughters (particularly daughters of high-ranking females) approach and groom their mothers more often, and support their mothers more often in intra-group aggression. The results are discussed in terms of several predictions from parental investment theory and the concept of mutualism.     

Queen-worker conflicts over male production and sex allocation in a primitively eusocial wasp

Abstract In a colony headed by a single monandrous foundress, theories predict that conflicts between a queen and her workers over both sex ratio and male production should be intense. If production of males by workers is a function of colony size, this should affect sex ratios, but few studies have examined how queens and workers resolve both conflicts simultaneously. We conducted field and laboratory studies to test whether sex-ratio variation can be explained by conflict over male production between queen and workers in the primitively eusocial wasp Polistes chinensis antennalis.
Worker oviposition rate increased more rapidly with colony size than did queen oviposition. Allozyme and micro-satellite markers revealed that the mean frequency of workers' sons among male adults in queen-right colonies was 0.39 ± 0.08 SE (n = 22). Genetic relatedness among female nestmates was high (0.654–0.796), showing that colonies usually had a single, monandrous queen. The mean sex allocation ratio (male investment/male and gyne investments) of 46 queen-right colonies was 0.47 ± 0.02, and for 25 orphaned colonies was 0.86 ± 0.04. The observed sex allocation ratio was likely to be under queen control. For queen-right colonies, the larger colonies invested more in males and produced reproductives protandrously and/or simultaneously, whereas the smaller colonies invested more in females and produced reproductives protogynously. Instead of positive relationships between colony size and worker oviposition rate, the frequency of workers' sons within queen-right colonies did not increase with colony size. These results suggest that queens control colony investment, even though they allow worker oviposition in queen-right colonies. Eggs laid by workers may be policed by the queen and/or fellow workers. Worker oviposition did not influence the outcome of sex allocation ratio as a straightforward function of colony size.     

In poor families, mothers' milk is richer for daughters than sons: A test of Trivers-Willard hypothesis in agropastoral settlements in Northern Kenya

The Trivers–Willard hypothesis predicts the unequal parental investment between daughters and sons, depending on maternal condition and offspring reproductive potential. Specifically, in polygynous populations where males have higher reproductive variance than females, it predicts that mothers in good condition will invest more in sons, whereas mothers in poor condition will invest more in daughters. Previous studies testing this hypothesis focused on behavioral investment, whereas few examined biological investment. This study investigates the Trivers–Willard hypothesis on both behavioral and biological parental investment by examining breastfeeding frequencies and breast milk fat concentrations. Data from exclusively breastfeeding mothers in Northern Kenya were used to test hypotheses: Economically sufficient mothers will breastfeed sons more frequently than daughters, whereas poor mothers will breastfeed daughters more frequently than sons, and economically sufficient mothers will produce breast milk with higher fat concentration for sons than daughters, whereas poor mothers will produce breast milk with higher fat concentration for daughters than sons. Linear regression models were applied, using breastfeeding frequency or log‐transformed milk fat as the dependent variable, and offspring's sex (son = 1/daughter = 0), socioeconomic status (higher = 1/lower = 0), and the sex‐wealth interaction as the predictors, controlling for covariates. Our results only supported the milk fat hypothesis: infant's sex and socioeconomic status interacted (P = 0.014, n = 72) in their relation with milk fat concentration. The model estimated that economically sufficient mothers produced richer milk for sons than daughters (2.8 vs. 0.6 gm/dl) while poor mothers produced richer milk for daughters than sons (2.6 vs. 2.3 gm/dl). Further research on milk constituents in relation to offspring's sex is warranted. Am J Phys Anthropol , 2012. © 2012 Wiley Periodicals, Inc.     

Unrelated queens coexist in colonies of the termite Macrotermes michaelseni

Relatedness increases the likelihood of cooperation within colonies of social insects. Polygyny, the coexistence of numerous reproductive females (queens) in a colony, is common in mature colonies of the termite Macrotermes michaelseni. In this species, polygyny results from pleometrosis and from several female alates that jointly found a new colony. To explain this phenomenon, it was suggested that only related females cooperate and survive during maturation of colonies. Using multilocus fingerprints as well as microsatellites, we showed that nestmate queens in mature colonies are unrelated. Furthermore, we found that all nestmate queens contributed to the production of steriles. Even in mature colonies, several matrilines of steriles coexist within a colony. Although genetic diversity within colonies may increase the likelihood of conflicts, high genetic diversity may be important for foraging, colony growth, and resistance to disease and parasites.     

Reproductive conflicts in polyandrous and polygynous ant Formica sanguinea

The occurrence of multiple reproductives within an ant colony changes the balance between indirect fitness benefits and reproductive competition. We test whether the number of matings by an ant queen (polyandry) correlates negatively with the number of reproductive queens in the colony (polygyny), whether the patrilines and matrilines differ in their contribution to the sexual and worker progeny and whether there is an overall reproductive skew. For these aims, we genotyped both worker and sexual offspring from colonies of the ant Formica sanguinea in three populations. Most colonies were monogynous, but eight (11%) were polygynous with closely related queens. Most queens in the monogynous colonies (86%) had mated with multiple males. The effective paternity was lower than the actual number of mates, and the paternity skew was significant. Furthermore, in some monogynous colonies, the patrilines were differently represented in the worker pupae and sexual pupae produced at the same time. Likewise, the matrilines in polygynous colonies were differently present in worker pupae and male offspring. The effective number of matings by a queen was significantly lower in polygynous colonies (mean m_e = 1.68) than in monogynous colonies (means 2.06–2.61). The results give support to the hypotheses that polyandry and polygyny are alternative breeding strategies and that reproductive competition can lead to different representation of patrilines and matrilines among the sexual and worker broods.     

Status change during adulthood: life-history by-product or kin selection based on reproductive value?

When dominance status predicts fitness, most adaptive models of dominance relationships among cercopithecine primate females predict lifetime maintenance of status. These models and alternative ones positing rank decline as a non-adaptive by-product have remained largely untested, however, because lifetime status of older adults has been virtually unknown for natural populations. In a 25-year study of adult female savannah baboons (Papio cynocephalus), in each of three social groups, rank losses were common among the 66 females that lived past median adult age. These losses were not accounted for by loss in relative rank from group growth or by loss in absolute rank from reversals in rank between members of different maternal families or between sisters. Rather, females that had mature daughters experienced loss of dominance status to these offspring, a characteristic of all but the top-ranking matriline of each group. Among proposed hypotheses for rank reversals between adults, that of kin selection based on relative reproductive value is most clearly supported by these data. In contrast, observed patterns of rank loss are not consistent with alternative models that postulate that changes during adult lifespan are a product of accumulated risk, physical decline during ageing, or coalitionary support among females within or between matrilines.     

The colony structure and dominance hierarchy of the Damaraland mole-rat, Cryptomys damarensis (Rodentia: Bathyergidae), from Namibia

Cryptomys damarensis is one of the few subterranean rodents which is social. This species is found in the semi-arid regions of southwestern and central Africa. The Damaraland mole-rat occurs in coloniesof up to 25 individuals, in which reproduction is limited to one or two of the largest males and the largest female in the colony.
The mean colony size is 18 mole-rats ( n =6 colonies). The mean colony biomass is 2.32 kg and the sex ratio is female biased (0.71–0.78). The number of mole-rats in each colony, the mean body mass and the sex ratio are described for six field-captured colonies, three of which were captured in their entirety.
The dominance hierarchy of two colonies of C. damarensis was found to be linear with a value of between 0.94 and 1.00 calculated from Landau's linearity index. Dominance was found to be related to gender, with the males more dominant than females. The reproductive individuals are the dominant animals within each respective gender. The non-reproductive females rank lowest in the hierarchy.     

Life history in male mandrills (Mandrillus sphinx): physical development, dominance rank, and group association

We assess life history from birth to death in male mandrills (Mandrillus sphinx) living in a semifree-ranging colony in Gabon, using data collected for 82 males that attained at least the age of puberty, including 33 that reached adulthood and 25 that died, yielding data for their entire lifespan. We describe patterns of mortality and injuries, dominance rank, group association, growth and stature, and secondary sexual character expression across the male lifespan. We examine relationships among these variables and investigate potential influences on male life history, including differences in the social environment (maternal rank and group demography) and early development, with the aim of identifying characteristics of successful males. Sons of higher-ranking females were more likely to survive to adulthood than sons of low-ranking females. Adolescent males varied consistently in the rate at which they developed, and this variation was related to a male's own dominance rank. Males with fewer peers and sons of higher-ranking and heavier mothers also matured faster. However, maternal variables were not significantly related to dominance rank during adolescence, the age at which males attained adult dominance rank, or whether a male became alpha male. Among adult males, behavior and morphological development were related to a male's own dominance rank, and sons of high-ranking females were larger than sons of low-ranking females. Alpha males were always the most social, and the most brightly colored males, but were not necessarily the largest males present. Finally, alpha male tenure was related to group demography, with larger numbers of rival adult males and maturing adolescent males reducing the time a male spent as alpha male. Tenure did not appear to be related to characteristics of the alpha male himself.     

Dominance and queen succession in captive colonies of the eusocial naked mole-rat,Heterocephalus glaber.

Naked mole-rat colonies exhibit a high reproductive skew, breeding being typically restricted to one female (the ''queen'') and one to three males. Other colony members are reproductively suppressed, although this suppression can be reversed following the removal or death of the queen. We examined dominance and queen succession within captive colonies to investigate the relationship between urinary testosterone and cortisol, dominance rank and reproductive status; and to determine if behavioural and/or physiological parameters can be used as predictors of queen succession. Social structure was characterized by a linear dominance hierarchy before and after queen removal. Prior to queen removal, dominance rank was negatively correlated with body weight and urinary testosterone and cortisol titres in males and females. Queen removal results in social instability and aggression between high ranking individuals. Dominance rank appears to be a good predictor of reproductive status: queens are the highest ranking colony females and are succeeded by the next highest ranking females. The intense dominance-related aggression that accompanies reproductive succession in naked mole-rats provides empirical support for optimal skew theory.     

Sexual selection favors female-biased sex ratios: the balance between the opposing forces of sex-ratio selection and sexual selection

In a verbal model, Trivers and Willard proposed that, whenever there is sexual selection among males, natural selection should favor mothers that produce sons when in good condition but daughters when in poor condition. The predictions of this model have been the subject of recent debate. We present an explicit population genetic model for the evolution of a maternal-effect gene that biases offspring sex ratio. We show that, like local mate competition, sexual selection favors female-biased sex ratios whenever maternal condition affects the reproductive competitive ability of sons. However, Fisherian sex-ratio selection, which favors a balanced sex ratio, is an opposing force. We show that the evolution of maternal sex-ratio biasing by these opposing selection forces requires a positive covariance across environments between the sex-ratio bias toward sons (b) and the mating success of sons (r). This covariance alone is not a sufficient condition for the evolution of maternal sex-ratio biasing; it must be sufficiently positive to outweigh the opposing sex-ratio selection. To identify the necessary and sufficient conditions, we partition total evolutionary change into three components: (1) maternal sex-ratio bias, (2) sexual selection on sons, and (3) sex-ratio selection. Because the magnitude of the first component asymmetrically affects the strength of the second, biasing broods toward females in a poor environment evolves faster than the same degree of bias toward males in a good environment. Consequently, female-biased sex ratios, rather than male-biased sex ratios, are more likely to evolve. We discuss our findings in the context of the primary sex-ratio biases observed in strongly sexually selected species and indicate how this perspective can assist the experimental study of sex ratio evolution.     

Patterns of variation in female-biased colony sex ratios in a social spider

Colonies of a social spider Achaearanea wau (Theridiidae) from Papua, New Guinea have adult and juvenile sex ratios that are biased towards females, and this probably represents a primary bias at the egg stage. Adult sex ratios are less female-biased than are juvenile sex ratios, and both vary significantly among colonies. Adult sex ratios covary with colony size: small colonies have a larger proportion of males than large ones. The pattern of variation in adult sex ratio may be due to greater mortality of females than of males during maturation. Juvenile sex ratios do not covary with colony size, nor do they differ among populations. Colony size, however, does have a significant effect on survival and dispersal in colonies. I conclude, therefore, that a conditional sex ratio strategy, in which the primary sex ratio of the colony is adjusted to changing demographic patterns, does not occur in A. wau. I suggest that environmental heterogeneity acting on individual reproductive output may be responsible for the observed variation among colonies in juvenile sex ratios.     

Secondary sex ratio variation in the Cayo Santiago macaque population

Secondary sex ratios (SSR) were calculated from 1,385 offspring delivered by 372 females in the Cayo Santiago population of free-ranging rhesus monkeys (Macaca mulatta) from 1976 through 1984. The SSR for the entire colony ranged from 0.86 to 1.46 males per female (combined total: 1.08), but no significant difference was observed (P > .05). SSR values were compared among the troops for each year. The SSR differed significantly among the six social groups (P < .05) only in 1978. The annual SSR of each troop was compared over 9 years. Significant variation was found only in group O. The annual SSR was significantly skewed (P < .05, males > females) for three troops in 3 separate years. The SSR did not vary according to troop rank. No significant difference was found among the 17 matrilines of the population, but comparison of matrilines within each social group revealed a significant difference in the SSR (P < .02) for the three matrilines in group I. This was due to the significantly skewed SSR (P = .0080, females > males) of the DM genealogy in that troop. SSR values were not related to matrilineal rank. Individual dominance rank did not bias the SSR. Complete reproductive histories for 266 females showed no evidence of significantly skewed SSR values. Age-related effects on the SSR were examined by using cross-sectional and cohort-based analyses. The SSR did not vary significantly (P > .05) with maternal age, but it was significantly skewed (P < .05) toward males at the ages of 5 and 9 years. Parity had no significant effect (P > .05) on SSR values. Wide variation occurred in the SSR of the Cayo Santiago population. Rank-related adjustment of the SSR at the level of the troop, matriline, or individual, as reported in short-term studies of other primate social groups, may reflect normal annual variation in the SSR evident only from longitudinal observations of large multigroup primate populations.     

Maternal Investment of the Virunga Mountain Gorillas

The Trivers & Willard hypothesis (TWH) predicts that females with more resources should bias their maternal investment toward offspring of the sex that is most likely to benefit from those additional resources. This paper examines the sex allocation of 61 female mountain gorillas (Gorilla beringei beringei) of the Virunga volcanoes, Rwanda from 1967 to 2004. Like most highly dimorphic, polygynous mammals, mountain gorillas are expected to show greater variance in reproductive success among males than females, so mothers in good condition should bias their investment toward sons. Using dominance rank as the indicator of maternal condition, the TWH was tentatively supported by our results with interbirth intervals (IBI). Dominant mothers had longer IBI following the birth of sons, relative to the longer IBI that subordinate mothers had with daughters. In contrast, maternal condition did not have a significant effect on birth sex ratios. We also found no significant relationships with other variables that might influence birth sex ratios (e.g., maternal age, parity, or group size), and the overall birth sex ratio was not significantly different from a 50:50 split. Collectively, our results suggest that female mountain gorillas do not control the sex ratio of their offspring at birth, but they may adjust their subsequent maternal investment. This conclusion is consistent with recurring questions about whether any adjustments in birth sex ratios occur in primates.     

Problems with primate sex ratios

Birth sex ratios of baboons in Gombe National Park, Tanzania, show an overall male bias of ca. 20%, but there is no obvious explanation for this trend. Individual females did not alter their sex ratios according to persistent levels of local resource competition. Sex ratios showed an unexpected relationship between age and rank: subordinate females had more sons when they were young; dominant females had more sons when they were old. The sex ratio of low-ranking females also varied with the severity of environmental conditions during pregnancy. Our findings suggest that mammalian sex ratios might be the product of more complex processes than is generally recognized or that sex-determining mechanisms impose sufficient constraints to prevent adaptive variation in all contexts.     

Hormonal and behavioural correlates of male dominance and reproductive status in captive colonies of the naked mole-rat,Heterocephalus glaber.

Naked mole-rat colonies are societies with a high reproductive skew, breeding being restricted to one dominant female (the ''queen'') and 1-3 males. Other colony members of both sexes are reproductively suppressed. Experimental removal of breeding males allowed us to investigate the relationship between urinary testosterone and cortisol, dominance rank, and male reproductive status. Dominance rank was strongly correlated with body weight, age, and urinary testosterone titres in males. No relationship between urinary cortisol levels and male reproductive status or dominance was found. Breeding males were among the highest-ranking, heaviest and oldest males in their respective colonies, and were succeeded by other high-ranking, large, old colony males. In contrast to females, no evidence of competition over breeding status was observed among males. Male-male agonism was low both before and after removal of breeders and mate guarding was not observed. The lower reproductive skew for males compared with female skew or queen control over male reproduction may explain why males compete less strongly than females over breeding status after removal of same-sexed breeders.     

REPRODUCTIVE SKEW AND SPLIT SEX RATIOS IN SOCIAL HYMENOPTERA

Abstract I present a model demonstrating that, in social Hymenoptera, split sex allocation can influence the evolution of reproductive partitioning (skew). In a facultatively polygynous population (with one to several queens per colony), workers vary in their relative relatedness to females (relatedness asymmetry). Split sex‐ratio theory predicts that workers in monogynous (single‐queen) colonies should concentrate on female production, as their relatedness asymmetry is relatively high, whereas workers in the polygynous colonies should concentrate on male production, as their relatedness asymmetry is relatively low. By contrast, queens in all colonies value males more highly per capita than they value females, because the worker‐controlled population sex ratio is too female‐biased from the queens' standpoint. Consider a polygynous colony in a facultatively polygynous population of perennial, social Hymenoptera with split sex ratios. A mutant queen achieving reproductive monopoly would gain from increasing her share of offspring but, because the workers would assess her colony as monogynous, would lose from the workers rearing a greater proportion of less‐valuable females from the colony's brood. This sets an upper limit on skew. Therefore, in social Hymenoptera, skew evolution is potentially affected by queen‐worker conflict over sex allocation.