Fred B. Bercovitch

Behavioral masculinization is independent of genital masculinization in prenatally androgenized female rhesus macaques.

Genetic female fetuses were exposed transplacentally to testosterone propionate injected into their mothers either early (Days 40 through 64) or late (Days 115 through 139) in gestation. Early and late androgenized females (EAFs and LAFs, respectively) were raised with normal males and females that served as criteria for evaluating degree of behavioral masculinization induced by the prenatal androgen. EAFs were genitally virilized and LAFs were not. Males and untreated females differed reliably on five behavioral measures: males showed more mother-mounting, more peer-mounting, more rough play with peers, a preference for initiating play with male partners, and less grooming of mothers. Neither type of prenatally androgenized female showed masculinization of all five types of behavior. Compared with females, EAFs showed more mother-mounting, more peer-mounting, less mother-grooming, did not differ from females in rough play, and did not manifest a preference for male partners. LAFs, like females, groomed but did not mount their mothers, and did not show a preference for male partners; but unlike females they showed elevated rough play and mounting with peers. EAFs showed a statistically significant delay in puberty onset (menarche), but LAFs did not. Mothers inspected genitalia of their offspring more often if they were males than if they were females. Mothers of EAFs inspected their offsprings genitalia as often as mothers of males, but mothers of LAFs did not. No aspect of maternal behavior was associated with either the amount or kind of masculine behavior shown toward peers. We interpret the results to mean that genital virilization is independent of, and largely irrelevant to, the expression of those behavioral traits that characterize the juvenile male social role. Moreover, the individual behavior traits that are components of the juvenile male role are independently regulated by the organizing actions of androgen and have separable critical periods. Of the two major traits, mounting peers and rough play with peers, the latter has a greater requirement for androgenic stimulation late in prenatal life.

Coalitions, cooperation and reproductive tactics among adult male baboons

Male savanna baboons, Papio cynocephalus, form coalitions with each other as a technique for gaining access to a female in consort with another male. Reciprocal altruism has been invoked as the primary mechanism which underlies this reproductive tactic, but a 19-month field study of the reproductive behaviour of olive baboons, P. c. anubis, in Kenya contradicted this interpretation. Males who solicited others for coalition formation were not more likely to gain access to consort females than were their fellow coalition members. Males who refused to participate in a coalition at one time were still sought as coalition partners at other times by the same male. Coalitions were generally formed by older, middle- to lower-ranking males and targeted at younger, higher-ranking males. Coalitions are a low risk reproductive tactic and the benefits are not partitioned according to initiator/joiner status. Coalitions are likely to be an outcome of cooperation between males which results from the pursuit of self-interest.

A longitudinal analysis of reproductive skew in male rhesus macaques

One of the basic tenets of sexual selection is that male reproductive success should be large in polygynous species. Here, we analysed 6 years of molecular genetic data from a semi–free–ranging population of rhesus macaques (Macaca mulatta), using Nonacs B index, to assess the level of male reproductive skew in the study troop. On average, the top sire in each year produced 24% of the infants, while 71% of troop males sired no offspring at all. Consequently, 74% of infants had at least one paternal half–sibling in their own birth cohort. Reproductive success was greatest for high–ranking males, males who spent the whole mating season in the troop and males of 9–11 years of age. Heterozygosity for major histocompatibility complex (MHC) class II gene DQB1 was the strongest single predictor of male reproductive success. A negative relationship suggestive of female mate choice was noted between the B index and the proportion of extra–group paternities. Reproductive skew was not associated with relatedness among potential sires or with female cycle synchrony. We conclude that reproductive skew in male rhesus macaques is best accounted for by the ‘limited–control’ model, with multiple factors interacting to regulate individual reproductive output.

Reproductive strategies of rhesus macaques

Reproductive strategies incorporate a multitude of mechanisms that have evolved to promote the reproductive success of individuals. Evolutionary perspectives tend to emphasize the advantages of male-male competition and female choice as mediators of differential reproduction. Male rhesus macaques have not been observed to fight for access to sexually receptive females, although they suffer more wounds during the mating season. An increased likelihood of attacks appears to coincide with male troop entry. Males who spend more time in consort and mate with more females tend to sire more offspring. Genetic analysis of paternity has pinpointed age and endurance rivalry, rather than agonistic competition, as key variables associated with variation in progeny production. Female rhesus macaques often copulate with multiple males during their ovulatory period, and tend to conceive on the first cycle of the mating season. Female reproductive success is more likely to be a function of offspring survivorship than the identity of particular male partners. The role of female choice as a direct mediator of male reproductive success is unresolved, but female mate selection seems to indirectly affect male reproductive success because female preference for mating with novel males seems to foster male dispersal. Evaluating whether mating preferences for particular male phenotypes affectsfemale reproductive success is a task for the future. A common denominator to the reproductive strategies of both female and male rhesus macaques is that feeding patterns affect body condition which influences reproductive output and regulates relative reproductive success.

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

SummaryTen 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.

Life history costs and consequences of rapid reproductive maturation in female rhesus macaques

SummaryLife history theory suggests that reproduction at one point in time involves costs in terms of energy, reduced survival, or probability of reproduction at a future point in time. ln long-lived iteroparous organisms, initiating reproduction at a relatively young age may exact a cost in terms of reduced survivorship, but an early age of first reproduction could be beneficial if it lengthens the breeding lifespan. Data collected over 30 years from one population of rhesus macaques, Macaca mulatta, were analyzed to determine the fertility and survivorship costs of initiating reproduction at a relatively young age. Low population density and high social status increased the chances of accelerating age at first parturition, but high dominance rank was not associated with greater lifetime reproductive success. Rapid reproductive maturation neither reduced short-term survivorship nor decreased lifespan. Fertility costs arose if young females reared a male, but not female, offspring. The fitness consequences of rapid reproductive maturation depend upon longevity, with age at death having a significantly greater impact on lifetime reproductive success than age at first parturition.

Male rank and reproductive activity in Savanna baboons

Access to sexually receptive baboon females has been linked to male dominance rank. An intensive 19-month field study of mate choice and mate competition among savanna baboons was undertaken in order to elucidate those factors influencing mating success. During this study, male agonistic rank was not correlated with male mating success among adult males. However, the inclusion of adolescent males into the analysis yielded significant correlations between rank and mating success. Examination of prior fieldwork revealed that no baboon field study has conclusively demonstrated a significant correlation between male rank and reproduction among adult males. Most studies reporting a correlation between male rank and reproduction have included subadult males in the analysis. It is concluded that male rank is an unreliable predictor of male reproductive activity among adult male baboons. A low agonistic rank need not reduce male mating success because adult male baboons utilize a variety of reproductive tactics in gaining access to consort females.

Dominance rank, cortisol concentrations, and reproductive maturation in male rhesus macaques

Among adolescent male rhesus macaques, Macaca mulatta, the highest ranking individual within a cohort has higher testosterone concentrations at a younger age, earlier in the mating season, and for a longer duration than his lower ranking conspecifics. We sought to determine whether such a rank-related pattern of reproductive maturation could be a function of differences in glucocorticoid levels. A 2-yr longitudinal study of a cohort of adolescent males living in a heterosexual group in a one acre outdoor enclosure revealed no differences in cortisol concentrations between high and low status males. Cortisol was not inversely correlated with testosterone in either adolescent or adult males. Young pubescent males had increases in cortisol levels coincident with maturation, while older adolescent males had cortisol concentrations comparable to those of adult males. Low ranking males tended to have more variable cortisol concentrations across time. We conclude that cortisol concentrations are not a function of dominance status and that the timing of reproductive maturation in male rhesus macaques is independent of cortisol concentrations.

Social stratification, social strategies, and reproductive success in primates

Abstract Social stratification characterizes primate societies, and the conventional assumption is that high rank should enable one to produce more offspring. But the data from primate studies offers conflicting evidence with respect to the actual reproductive consequences of high social status. Nonhuman primates are tactical opportunists who use multiple means for improving reproductive success. Social skills can circumvent social status as determinants of reproductive success. Social stratification probably evolved as a mechanism for reducing the probability of escalated aggressive encounters by providing a reasonable degree of predictability and stability to social relationships. Social cognition may have evolved as a mechanism enabling individuals to adopt alternative reproductive tactics for improving their reproductive success. The frequent nonassociation between rank and reproduction in primates can be attributed to the diversity of reproductive tactics used by primate in attempting to maximize their individual fitness.

Reproductive success in male savanna baboons

SummaryDifferent techniques have been utilized to ascertain male savanna baboon reproductive success based upon behavioral data. A 19 month field study of the reproductive behavior of savanna baboons in Kenya revealed a high degree of concordance among five different measures of male baboon reproductive success. The number of ejaculations showed the highest correlation with time spent in consort. Male reproductive success was not correlated with the number of females mated with because most males mated with most females. Female baboons regularly undergo multiple cycles prior to conception and the penultimate cycle showed no behavioral or physiological differences from the conception cycle. In nearly one-third of conception cycles a single consort partner was responsible for almost two-thirds of ejaculations during the four day optimal conception period. One may be able to reasonably infer paternity in these cases, but the available data are insufficient to support the idea that the variance in male baboon reproductive success is greater than the variance in female baboon reproductive success. The variance in male savanna baboon reproductive success will remain uncertain until genetic paternity studies are undertaken. It is suggested that mate selectivity, longevity, and stochastic factors are important components influencing male baboon reproductive success.