Dominance rank,female reproductive synchrony,and male reproductive skew in wild Assamese macaques

In groups with multiple males, direct mate competition may select for the evolution of dominance hierarchies that sort males into a queue for access to fertile females. The priority-of-access (PoA) model proposed by Altmann in 1962 makes explicit predictions about the resulting paternity distribution based on an interaction between male dominance rank and the overlap of female receptive phases. Here, we investigated whether the logic of the PoA model predicted the distribution of paternity across ranks in a seasonal breeder with high reproductive synchrony over six consecutive mating seasons. We studied 18 males that resided in a group of wild Assamese macaques (Macaca assamensis) in their natural habitat at Phu Khieo Wildlife Sanctuary, Thailand, between 2006 and 2011 with 5 to 13 conceptions per season. We assessed whether mate guarding increased paternity success, described “short-term” deviations from predicted paternity distribution, and examined how these are related to the number of competitors and fertile females. We determined genetic paternity of 43 (93 %) offspring born into the study group and found reproductive skew to be relatively low with 29 % alpha male paternity in accordance with the high degree of female reproductive synchrony observed. Short-term deviations from expected paternity distribution over ranks were not explained by the number of resident males or the number of conceiving females or their interaction. Within the limits of this study, these results suggest that even if males cannot discern female fertile phases, if reproduction is seasonal, and if reproductive synchrony is high, males may also compete directly over access to females.     

Foraging responses of wild house mice to accumulations of conspecific odor as a predation risk

Many predators hunt using the social and waste odors of their prey. It is unknown, however, whether potential prey modify their behavior in response to the risks of predation associated with accumulations of conspecific odor. We examined this question by measuring foraging trade-offs of wild house mice (Mus domesticus) in the field where we increased both predation risk and conspecific odor at artificial food patches in a two-factor design. Mouse giving-up densities (GUDs) were significantly higher in open habitats than in closed habitats but did not differ with the addition of mouse odors. Fine-scale behavioral observations of captive mice confirmed their attraction to the conspecific odor in an enclosure experiment, without any change to the GUD. These results indicate that house mice continue to visit and forage at food patches despite accumulations of predator-attracting odors. This most likely occurs for the social benefits obtained from conspecific odor exploration; however, such behavior may cause mice to become vulnerable to considerable olfactory exploitation by their predators. Future work must therefore focus on how mice trade off the social benefits of investigating odors that also attract their enemies.     

Maternal investment, sex-differential prospects, and the sex ratio in wild house mice

In a population of first-generation offspring from wild-caught house mice (Mus musculus domesticus), previous evidence suggested that male fitness is more strongly affected by an increase in body weight than female fitness. This paper shows that in these mice the young are weaned at heavier weights the smaller the litter and the better the maternal body condition. These effects persisted into adulthood and were less pronounced in female young. However, contrary to expectation from conventional sex ratio theory, maternal condition and litter size had no detectable effect on sex ratios. Also, litter size did not affect sex ratios in two populations of laboratory-kept, wild-caught western (M. m. domesticus) and eastern house mice (M. m. musculus). Wild house mice, therefore, appear not to adaptively manipulate the sex ratio of offspring. It is argued that this absence of sex ratio trends might not be maladaptive, but rather that models currently used to predict sex ratio trends in rodents may not be valid. Received: 13 March 1997 / Accepted after revision: 9 August 1997     

Microsatellite length polymorphisms associated with dispersal-related agonistic onset in male wild house mice (Mus musculus domesticus)

Dispersal propensity, reflecting one of the most decisive mammalian life history traits, has been suggested to vary heritably and to locally adapt to prevailing dispersal conditions in wild house mouse populations. Because individual dispersal propensity highly significantly covaries with the developmental timing of the onset of agonistic interactions between littermate brothers, we used agonistic onset as an endophenotype to explore the potential genetic basis of dispersal-related behavioral variation in male house mice. We found significant covariation of microsatellite marker compositions with the probability of fraternal pairs to exhibit agonistic relationships before the age of 2 months. In particular, the presence of two alleles associated with a serotonin transporter protein gene (Slc6a4) and a testosterone dehydrogenase gene (Cyp3a11), respectively, strongly covaried with the probability of early agonistic onset. These results are congruent with recent findings of microsatellite length polymorphisms marking regulatory variation of gene expression that is relevant for social behavior, including dispersal propensity development, in other mammals. Genetic variability for ontogenetic timing of agonistic onset would be in agreement with genotypic differentiation of the dispersive behavioral syndrome in natural populations that could lead to local adaptation.     

Length polymorphism at the avpr1a locus is correlated with male reproductive behavior in a natural population of prairie voles (Microtus ochrogaster)

Laboratory studies have shown that vasopressin can influence sociosexual behavior through its action on the vasopressin 1a receptor (V1aR). There is substantial evidence that the length of a microsatellite in the gene (avpr1a) encoding for the V1aR can affect social attachment to females and paternal behavior in male prairie voles under laboratory conditions. However, previous field studies of prairie voles have failed to detect a strong effect of the length of a male’s avpr1a allele on their sociosexual behavior, but these studies are typically much shorter than the average prairie vole breeding lifespan. We examined the relationship between male avpr1a microsatellite allele length and sociosexual behavior in a natural population of prairie voles for 15 weeks, closer to the lifespan of prairie voles in nature. Contrary to predictions, we found that males with the longest avpr1a microsatellite alleles were significantly more likely to sire offspring with more than one female and to sire offspring that survived until trappable age than males with the shortest avpr1a microsatellite allele lengths. This relationship was the strongest for males with the longest tenure on the study site. As in previous field studies, we did not find evidence of a relationship between a male’s avpr1a genotype and any index of social behavior including male residency status or the number of females with which males associate. This is the first study to support the hypothesis that a male’s avpr1a genotype is a factor underlying variation in the genetic mating system of prairie voles under natural conditions.     

Kin-preferential cooperation,dominance-dependent reproductive skew,and competition for mates in communally nesting female house mice

Little is known about the behavioural mechanisms facilitating kin-preferential communal breeding in wild house mice (Mus domesticus). We evaluated the effect of kinship and male availability on aggression, social structure and reproductive skew in groups of female mice freely interacting and reproducing in semi-natural indoor enclosures. Triplets of either sisters or non-sisters were established in enclosures provided with either one or three littermate males, which were unrelated and unfamiliar to the females. Sisters were more spatially associated and less aggressive than non-sisters, leading to higher incidences of communal breeding and reproduction. This is in agreement with theoretical considerations on kin selection in house mice. Reproductive success was highly skewed in favour of dominant females due to subordinate infertility or complete loss of first litters, which might have been caused by dominant females. In spite of this, subordinates only rarely dispersed from the enclosures, suggesting that perceived dispersal risk generally outweighed relatively reduced reproductive potentials. Aggression levels among females were significantly higher when one male was available, compared to when three males were available. We suggest that this might result from higher female-female competition for mates, due to the risk of missing fertilisation when synchronously oestrous females encounter limited numbers of males in a deme. Our results indicate that, first, communal nursing in house mice might have evolved to make the best out of a bad job rather than to enhance offspring fitness; and, second, that female-female mate-competition might play an important role in shaping female social structure in this polygynous mammal.Electronic Supplementary Material Supplementary material is available in the online version of this article at Communicated by F. Trillmich     

Kinship and social tolerance among female and juvenile wild house mice: kin bias but not kin discrimination

Kin-biased social tolerance among house mice has been interpreted in terms of kin discrimination. However, several lines of evidence suggest it may instead be an incidental artifact of group member discrimination. This leads to very different predictions about the social consequences of relatedness within and between social groups. Social interactions between wild-stock adult female and juvenile house mice (Mus domesticus) established in neighbouring territorial groups within enclosures reveal relatedness to dominant males within groups as the major factor determining social tolerance of juveniles by females. Relatedness to the female herself had no significant independent effect on responses indicating tolerance. Females were generally more aggressive toward neighbouring-group juveniles (all unrelated to females) compared with those from their own group (all related to females), but were most aggressive toward neighbouring juveniles sired by the neighbouring dominant male. They were also more aggressive toward their own-group juveniles that had been sired by the neighbouring dominant but only when encountered in the neighbouring territory and with a greater bias against female juveniles. Females were least aggressive toward own-group juveniles sired by their own-group dominant male. The sire-bias in tolerance among females is similar to that reported among the dominant males themselves in an earlier study. As a result of the combined sire-bias in tolerance by adult males and females, juveniles sired by their own-group dominant males become less likely to intrude into a neighbouring territory with time. Overall, the results suggest that differences in social tolerance reflect discrimination on the basis of social group membership rather than relatedness between interactants and thus provide strong experimental evidence in support of incidental kin bias rather than kin discrimination.     

Optimality of parental investment: The influence of nursing on reproductive success of mother and female young house mice

Summary The amount of parental milk investment determines not only the number of young the parent can produce, but also affects the offspring's fitness. The antagonism between quantity and quality of offspring was investigated in laboratory mice.In nursing first litters containing 2,4, ..., 14 pups, mothers invested increasing amounts of milk. This mainly extended the intervals between their first and second litters and slightly increased the size of their second litters, whilst third litters were not affected. In the female young, the decreasing amount each individual received as a result of increasing litter size led to delayed birth and reduced the size of their first litters. The intervals between their first and second litters and the size of the second litters were also affected, although to a lesser extent.Taking these results into consideration on a standard lifetime pattern of reproduction, the effects were calculated on net reproductive rates as an expression of fitness. Death rates were assumed that referred to population equilibrium or population growth. In both situations, the fitness curves of mothers and young showed that the actual level of milk investment and the level yielding optimal reproduction were in agreement. There was no significant deviation towards increased investment, as might result from parent-offspring conflict.     

Dominance rank,resource availability,and reproductive maturation in female savanna baboons

Summary Ten years of data collected from a population of savanna baboons, Papio cynocephalus anubis, residing near Gilgil, Kenya were analyzed to ascertain the extent to which social and ecological factors influence reproductive maturation in females. First sexual swelling occurred at an average age of 4.79 years and first birth occurred at an average age of 6.92 years. Age at first menses was significantly correlated with age at first sexual swelling, but age at first sexual swelling was not a good predictor of age at first birth. The amount of rainfall in the 6 months preceding first sexual swelling and resource availability were significantly correlated with age at first sexual swelling. When ecological factors were taken into account, dominant females had an earlier age at onset of puberty, but not an earlier age at first birth, than did subordinate females. We suggest that nutritional and social stress operate at the same physiological level to disrupt GnRH pulsatility and retard reproductive maturation in some females. Given that socioecological variables modify the timing of life history events related to fitness in female baboons, the task for the future is to unravel how socioecological factors influence different life history components and generate variation in lifetime reproductive success. Correspondence to: F.B. Bercovitch     

Gene flow in house mice: Behavior in a population cage

Summary The social behavior of house mice captured from natural populations was studied in an enclosure. Six replicate experiments with observations totalling 344 h were done to contrast the behavior of outbreeders, individuals that have progeny by interdemic reproduction; inbreeders, individuals that have progeny by intrademic reproduction; and nonbreeders. The frequency of outbreeding was also determined.In each replicate, two male and three female commensal house mice, Mus musculus, homozygous for the same allele at the hemoglobin locus, Hbb ^s , were put in half of a population cage. A barrier separated this deme from another deme homozygous for the alternative allele, Hbb^d. The barrier was removed after a month and each experiment continued for a further two months with daily observations.In five of six experiments, the mice from both demes formed one social group and in the sixth experiment, the mice remained in their original demes. In two experiments, outbreeding occurred: females from one deme produced offspring by males from the other deme. In three experiments, inbreeding occurred: females produced offspring by males from the same deme. Soon after the demes had formed one social group in these three experiments, the remaining male in a deme was killed and the experiment terminated; females without a male readily join other demes. The pattern of breeding resulted in a genetically effective size, N _e , that was approximately half of the maximum N _e obtainable with random mating. The social organization of house mice, although structured and characterized by male territoriality, presents no major barrier to gene flow within populations.Affiliative (mount, allogroom, follow) and agonistic (fight, chase, attack) behavior occurring when the barrier was present had no predictive value in determining which mice would be outbreeders. With the barrier absent, outbreeders were the recipients of more affiliative behavior than inbreeders. Male outbreeders initiated more agonistic behavior than inbreeders. Outbreeders engaged in more interdemic affiliative behavior than inbreeders.Contribution no. 362 from the Department of Ecology and Evolution at SUNY, Stony Brook     

Dominance relationship in the establishment of reproductive division of labour in a primitively eusocial wasp (Ropalidia marginata)

In mature post-emergence colonies of the tropical primitively eusocial polistine wasp Ropalidia marginata, the queen is not a behaviourally dominant individual. Nevertheless, she completely suppresses reproduction by the workers and becomes the sole egg-layer in the colony. Mechanisms by which a female is able to establish her exclusive reproductive status in the colony can be investigated by examining dominance-submission relationships and hierarchy formation at particular stages of the colony cycle when reproductive competition is behaviourally manifest. Observations on the behaviour of R. marginata females (1) during early stages of colony-founding, (2) when potential queens challenge the existing queen, and (3) immediately after queen replacement show that these wasps use highly aggressive dominance interactions to establish their reproductive status. Both the frequency and the intensity of dominance behaviours are significantly higher at these stages than those observed at phases of the colony when there is no apparent reproductive strife. Once her position as the only egg-layer of the colony has been established, the levels of dominance interactions initiated by the queen decrease and the nature of these interactions also becomes comparatively milder. Thus, the mechanisms by which a queen establishes her social status in her colony and those by which she continues to suppress reproduction of her nestmates in the absence of overt physical dominance may be quite different. Received: 17 November 1995/Accepted after revision: 20 April 1996     

Contest behavior and other reproductive efforts in aging breeders: a test of residual reproductive value and state-dependent models

Two models have been proposed to explain age-related changes in reproductive performance. State-dependent models predict that reproductive effort depends on the magnitude of surplus energy reserves, which often varies with age. Contrary to this prediction, there was no significant effect of starvation on the outcome of contests for carcasses by female Nicrophorus orbicollis despite weight loss by starved females relative to controls. The residual reproductive value (RRV) model predicts that individuals adjust their current reproductive effort based on potential for future reproduction. Younger adults are predicted to restrain reproductive effort because they are less willing to risk their potentially longer reproductive careers. This model was tested empirically for several components of reproduction. Age was found to be strongly correlated with dominance when two similarly sized females discovered a carcass on the same day. Age also had a small positive effect on egg mass and was positively correlated with ovipositing at least one egg. Age did not affect nesting performance (the degree of carcass burial or the value of a prepared carcass for another female). Age also had no effect on fecundity when a female bred alone but was an important factor when two females were in direct competition. Changing RRV related to aging appears to be a robust determinant of contest outcomes in burying beetles, but effects on other components of reproductive effort in the present and previous studies are more variable, perhaps because of effects of changing state.     

Prospecting at conspecific nests and exploration in a novel environment are associated with reproductive success in the jackdaw

Consistent behavioural differences between individuals of the same population (“personality” variation) might arise if individuals follow different life-history strategies. Thus, it would be important to determine how personality variation relates to behaviours potentially associated with life-history strategies, such as those related to the use of information about the state of the environment. Little is, however, known about how personality is associated with information use and reproductive success. We tested whether wild social jackdaws, Corvus monedula, show consistent behavioural differences in their exploratory behaviour (in a novel environment in the lab and in their reaction towards a novel object in the wild) and prospecting behaviour (number of visits to conspecific nests). We furthermore examined whether these behavioural traits are linked with each other and predictors of reproductive success. Breeding jackdaws were consistent in their exploratory behaviour within, and in their prospecting behaviour between, years. Exploratory behaviour in the novel environment was correlated with the latency to approach a novel object in the wild but not with the frequency of prospecting at conspecific nests. Highly exploratory males and females and frequently prospecting males produced fewer fledglings than less exploratory individuals or less prospecting males, respectively. We discuss the importance of consistent individual differences in exploration and information sampling on individual fitness.     

Dominance and reproduction in a parthenogenetic lizard

Summary In most vertebrates, males and females are believed to differ in terms of their investment in offspring. Dominance theory suggests that one way individuals of the sex with lower parental investment can increase reproductive success would be to dominate others of the same sex. The dominant competitors are thought to achieve preferred access to mates, and thus, have greater reproductive success than subordinates.Reproduction in parthenogenetic Cnemidophorus uniparens normally proceeds without males, but individuals exhibit mounting behaviors in captivity that are typical of closely related Cnemidophorus species that reproduce sexually. Thus, these animals provide an unusual opportunity to study the effects of behavior on reproduction apart from copulation and fertilization. In this study relationships between dominance and reproduction were investigated in the unisexual lizard species, C. uniparens. Dominance hierarchies were rapidly established and maintained in the laboratory by agonistic encounters among individuals. The number of times an individual charged its cagemates was positively correlated with the number of clutches and eggs laid. Also, dominant animals who charged their cagemates were likely to win agonistic encounters; recipients of charges usually fled. Hierarchies based on different behaviors were not all related to reproduction. Charges as a predictor of dominance was unrelated to body length, percent increase in body length and time spent in the basking site. However, individuals with a high percent increase in body length spent more time basking. This is likely a result of the increased energy demands of growth in addition to reproduction. Physiological stress as measured by plasma corticosterone titers was unrelated to dominance. We suggest that dominance is an important factor affecting reproduction in C. uniparens.     

Culturally correct song dialects are correlated with male age and female song preferences in wild populations of brown-headed cowbirds

Variation in vocal behavior among local populations of songbirds may be significant to females in mate choice. In a study of dialect populations of brown-headed cowbirds, estradiol-implanted females from two dialects held the pre-copulatory lordosis posture longer in response to playback of the local flight whistle song than to foreign whistle types from adjacent and more distant dialects. Females were held in captivity for a relatively brief period prior to testing and received no tutoring so discrimination was based solely on experience in the wild. This is the first study to show evidence of discrimination by female cowbirds based on flight whistle type. Evidence is presented from one of the study dialects that the majority of yearling male cowbirds are vocally distinct from resident adults in having either foreign or incomplete local whistles. Although these yearlings are fully mature sexually, they have little or no mating success. The correlation between female whistle preference and male mating success suggests that the ability to give the correct local whistle type may be a characteristic used by females to assess age and quality of a potential mate. A learned female preference for the predominant local song type may be a factor in the stability of these dialects by making it adaptive for males to conform to the local dialect.     

Heterogeneous population growth, parental effects and genotype–environment interactions of a marine oligochaete

Cultures of asexually reproducing populations of the oligochaete Paranaislitoralis (Müller) collected from six different patches (3 to 50 m apart) on an intertidal mud flat in Flax Pond, New York, on two occasions, June and October 1993, showed significant differences among lines in life span, number of offspring produced, and in finite rate of increase (λ). Although growth rates were significantly lower in October than in June, they were always positive (λ > 1) in the laboratory cultures reared in field-collected sediment, while field data show that the densities of P. litoralis decreased sharply in summer and autumn from a seasonal high in early June. Cultures of worms reared at high densities without renewal of sediment crashed, and effects on individuals were irreversible: worms from late (declining) stages of population growth had a significantly higher mortality and lower reproduction than worms from earlier stages, also when transferred to high-quality food. Genetical analysis using RAPDs (random amplified polymorphic DNA) confirmed the existence of several clones of P. litoralis in our cultures. Experiments where parent and offspring were cultured in sediments of different qualities showed clone–environment interactions in the number of asexual offspring produced, but not in age at first reproduction. Clones also differed in that some showed significant parental effects of sediment quality on life-history characteristics while other clones did not. Our results indicate that P.litoralis populations in Flax Pond are not an example of a population subdivided into a set of permanent source and sink subpopulations, but rather an example of a continuously shifting mosaic of local growth conditions. Received: 21 April 1997 / Accepted: 3 September 1997