Sexual behaviour and paternity in three captive groups of rhesus monkeys (Macaca mulatta)

Each offspring born into three captive groups of rhesus monkeys (Macaca mulatta) during the spring of 1981 was assigned (1) a most probable behavioural father and (2) a subset of all possible behavioural fathers, on the basis of intensive observations of sexual activity during the 1980 fall breeding season. These predictions were then compared with true paternity determined by electrophoretic and serological analyses of polymorphic blood proteins of mothers, infants, and all adult and subadult males. Coincidence between the assignments of paternity based upon behavioural and biochemical data occurred no more frequently than chance would allow. Furthermore, there were no significant relationships between biochemical and behavioural rankings of overall reproductive success. It was concluded that conventional estimates of sexual activity during the breeding season are not a reliable indicator of true paternity and relative reproductive success in rhesus macaques.     

A test of the randomness of paternity of members of maternal sibships in six captive groups of rhesus monkeys (Macaca mulatta)

Results of previous studies have shown that in captive groups of rhesus monkeys (Macaca mulatto)fathers associate more frequently with their own offspring than with those of other males and that mothers are most permissive of physical contact between their own infant and a juvenile when that juvenile shares the same father with her infant. These two observations suggest that the identity of offspring born in captive groups of rhesus monkeys is recognized by at least some adult members of the group. Consistent patterns of mating among mating seasons might explain this apparent recognition of offsprings’ paternity. Fathers, for example, might regularly associate with young who maintain a close relationship with females with whom they have previously mated, and mothers might selectively permit juveniles who maintain a close relationship with males with whom they have previously mated to associate with their infants. This hypothesis is tested in this paper by comparing the observed distribution of 70 maternal sibships, members of which were fathered by the same or by different adult males over a 4-year period in six captive groups of rhesus monkeys, with that distribution expected based on random mating from season to season. Seasonal mating patterns were found to be random. Preparations are now underway to test this hypothesis in several free-ranging groups.     

Social relations between fathers and offspring in a captive group of rhesus monkeys (Macaca mulatta)

Analysis of social relations between adult males and immatures of known paternity in a captive group of rhesus monkeys (Macaca mulatta) revealed that fathers and offspring associated significantly more than other male-immature dyads. This association was highly variable, however, and there was no evidence of active preference for or investment in offspring by fathers. The tendency of offspring to approach fathers more often than other males appeared to account for the pattern of selective association. Preferential father-offspring association occurred whether or not mothers were in proximity to fathers, but mothers' associations with males did predict their offspring's, especially for the younger juveniles and the infants. It is possible that long-term social relationships between mothers and fathers lead to father-offspring association, but a year-to-year pattern of shifting mating preferences in the group weakens this hypothesis.     

Effects of age, dominance, and seasonal changes on proximity relationships in female Japanese macaques (Macaca fuscata) in a free-ranging group at Katsuyama

The present study compares the behavior of old female Japanese macaques (Macaca fuscata) with that of their full adult daughters in a free-ranging group, with respect to dominance and seasonal changes. Old mothers (21 to 25 years old) spent more time resting and alone than did their middle-aged adult daughters (10 to 17 yr old). However, the number of skin-related animals in proximity to the subject females, did not differ between mothers and their adult daughters. Mothers maintained proximity to more non-kin-related immature animals in the mating season than did their adult daughters, perhaps to avoid sexual aggression from males and to reduce the loss of body temperature in the cold. Dominance rank clearly influenced the social interactions of old mothers: high-ranking mothers interacted with more non-related adult females and immature animals than did low-ranking mothers, indicating that old age does not decrease the attractiveness of high-ranking animals.     

SEX-RATIO SELECTION IN A BIVOLTINE THRIPS. I. CONDITIONAL SEX-RATIO MANIPULATION AND FITNESS VARIATION

Females of the bivoltine thrips Elaphrothrips tuberculatus (Hood) (Insecta: Thysanoptera) produce broods of either all males (by viviparity) or all females (by oviparity). Measurements of the sex-allocation ratio, ecological and physiological conditions affecting male and female offspring body size, and correlates of the relative fitnesses of adult males and females in relation to size indicate that female parents tend to be viviparous (produce males) if their offspring will become relatively large adults, and that males gain more in fitness from large size than do females. However, the conditions that link sex allocation with offspring fitness differ between the spring and summer generations. In spring, when breeding is synchronous, 1) oviparous and viviparous females do not differ in body size, 2) females tend to be viviparous where the fungus upon which they feed is relatively dense and where their offspring will become relatively large adults, and 3) fungus density is highly correlated with male and female offspring size. In summer, when breeding is relatively asynchronous, 1) viviparous females are much larger than oviparous females early (but not late) in the season, 2) large viviparous females begin breeding earlier than smaller ones, 3) offspring developing earlier in the season become larger adults, and 4) a higher proportion of females are viviparous earlier than later. Field experiments and field collections show that the covariation among sex allocation, conditions, and fitness is not caused by differential mortality by size or sex. Differences between the spring and summer generations in the cues used by females to adjust offspring sex ratio may be caused by seasonal variation in the factors that affect offspring size. However, in both generations, females tend to produce sons only when their offspring will become relatively large adults, whereas daughters are produced regardless of offspring size. These data suggest that females of E. tuberculatus avoid production of males (the sex with higher variance in expected fitness) when the size of their offspring is relatively uncertain.     

Inbreeding avoidance in rhesus macaques: Whose choice?

Whether nonhuman primates avoid copulating with close kin living in their social group is controversial. If sexual aversion to relatives occurs, it should be stronger in females than in males because of females' greater investment in each offspring and hence greater costs resulting from less viable offspring. Data presented here show that adult male rhesus macaques breeding in their natal groups at Cayo Santiago experienced high copulatory success, but copulated less with females of their own matrilineages than with females of other matrilineages. Adult females were never observed to copulate with males of their own matrilineage during their fertile periods. Although natal males sometimes courted their relatives, examination of two measures of female mate choice showed that females chose unrelated natal males over male kin. Female aversion to male kin was specific to the sexual context; during the birth season, females did not discriminate against their male relatives in distributing grooming. Evolved inbreeding avoidance mechanisms probably produce different outcomes at Cayo Santiago than in wild rhesus macaque populations. Gender differences in sexual aversion to relatives may be partly responsible for differences between studies in reported frequency of copulations by related pairs. © 1993 Wiley-Liss, Inc.     

Adaptive significance of environmental sex determination in an amphipod

Environmental sex determination (ESD) permits adaptive sex choice under patchy environmental conditions, where the environment affects sex-specific fitness and where offspring can predict their likely adult status by monitoring an appropriate environmental cue. For Gammarus duebeni, an amphipod with ESD, it has been proposed that this flexible sex determination system is adaptive because males gain more from large size. Under ESD, young which are born earlier in the season become mostly males and, experiencing longer to grow, are therefore larger at breeding than females which are born later in the season. In order to test the hypothesis that ESD is adaptive for this species we investigated the relationship between size and fitness for both males and females, in a population of G. duebeni known to have ESD. We measured size related pairing success and fecundity, and used these two measures to calculate the relative fitness gains achieved through an increase in size for either sex. The fitness of both males and females increased with size, but males gained more from an increase in size than did females, throughout the breeding season. The data support the adaptive explanation for the evolution and maintenance of ESD in this species.     

Sex differences in infant rhesus macaque separation-rejection vocalizations and effects of prenatal androgens

Infant and juvenile rhesus macaques exhibit many sexually dimorphic behaviors, including rough and tumble play, mounting, and time spent with nonmother females. This study investigated sex differences in infant rhesus monkey separation-rejection vocalizations (SRVs), and the effects of altering the prenatal hormone environment on these differences. Pregnant females received exogenous androgen (testosterone enanthate), an androgen antagonist (flutamide), or vehicle injections for 30 or 35 days during the second (early) or third (late) trimester of pregnancy. Control females used a greater percentage of coos and arched screams than did control males. In contrast, males used a greater percentage of geckers and noisy screams than did females. Females also had longer SRV bouts, used more calls, and used more types of vocalizations than did males. Mothers were more likely to respond to the SRVs of male infants than to the SRVs of female infants. Prenatal flutamide treatment early in gestation reduced the likelihood that mothers would respond to their male offspring, but prenatal androgen treatment had no effect on response rates of mothers to female offspring. Early, but not late, androgen treatment produced females who vocalized in a male-typical manner. Similarly, early flutamide treatment produced males who displayed more female-typical SRVs. Late flutamide treatments of females produced as much masculinization of SRVs as did early androgen treatment in females. These results demonstrate sex differences in highly emotional vocalizations in infant rhesus macaques and provide evidence that the timing and form of prenatal hormonal exposure influence such vocalizations.     

Sex Differences in Infant Rhesus Macaque Separation–Rejection Vocalizations and Effects of Prenatal Androgens

Infant and juvenile rhesus macaques exhibit many sexually dimorphic behaviors, including rough and tumble play, mounting, and time spent with nonmother females. This study investigated sex differences in infant rhesus monkey separation–rejection vocalizations (SRVs), and the effects of altering the prenatal hormone environment on these differences. Pregnant females received exogenous androgen (testosterone enanthate), an androgen antagonist (flutamide), or vehicle injections for 30 or 35 days during the second (early) or third (late) trimester of pregnancy. Control females used a greater percentage of coos and arched screams than did control males. In contrast, males used a greater percentage of geckers and noisy screams than did females. Females also had longer SRV bouts, used more calls, and used more types of vocalizations than did males. Mothers were more likely to respond to the SRVs of male infants than to the SRVs of female infants. Prenatal flutamide treatment early in gestation reduced the likelihood that mothers would respond to their male offspring, but prenatal androgen treatment had no effect on response rates of mothers to female offspring. Early, but not late, androgen treatment produced females who vocalized in a male-typical manner. Similarly, early flutamide treatment produced males who displayed more female-typical SRVs. Late flutamide treatments of females produced as much masculinization of SRVs as did early androgen treatment in females. These results demonstrate sex differences in highly emotional vocalizations in infant rhesus macaques and provide evidence that the timing and form of prenatal hormonal exposure influence such vocalizations.     

Sexual activity of male rhesus monkeys introduced into a heterosexual group.

Unfamiliar males were introduced during the breeding season to a stable heterosexual group of rhesus monkeys to determine how the presence of more dominant resident males affected their mating activity and how their entry was received by resident females. Initially, new males were allowed access to females under controlled conditions both in the presence and absence of resident males, simulating situations which may occur under natural conditions. Results indicated that the sexual activity, including ejaculation rate, of the new males was initially inhibited by the presence of more dominant, resident males, but these inhibiting properties did not carry over to periods when the resident males were absent and were diminished with time. Group females preferentially directed their behavior towards the new males throughout the study. These data suggest that although entry of new males into a stable group is at low rank, their subsequent reproductive success may not be reduced and that the association with resident females may facilitate male rhesus transfer between groups observed during the breeding season.     

Immunogenetic studies of rhesus monkeys

To assay for transplacental immunization in rhesus monkeys, sera from 253 postpartum females, 31 virgin females, and 40 males were tested for erythrocyte agglutinins. Nineteen percent of the mothers exhibited antibodies, but less than three percent of the virgin females or males did so. Antibodies were detected in 26 percent of the mothers who bore blood group-incompatible infants, in contrast to only eight percent of the mothers with compatible offspring. Thus, blood group incompatibility may lead to transplacental alloimmunization of the rhesus female. Unlike the situation in humans, hemolytic disease was not observed, even when the erythrocytes of the newborn rhesus were coated with maternal antibodies.     

Birth-season interactions of adult female Japanese Macaques(Macaca fuscata) without newborn infants

The affiliative interactions of 11 adult female Japanese macaques that did not deliver an infant during the 1981 birth season of the Arashiyama West troop were examined. Consideration was given to the effects of kinship as a structuring element in these birth-season interactions and to the degree of association with various categories of troop members based on age, sex, and (in the case of adult females) whether or not the females were new mothers. Females without infants interacted predominantly with their yearling off-spring, although it was the behavior of the offspring that precipitated the interaction. These females were active in soliciting affiliation with nonkin new mothers, whereas female matrilineal relatives with new infants approached and remained in proximity to them more than did nonrelated new mothers. Females without newborns groomed and approached nonkin infants more than infants within their own matriline, and these infants were predominantly those of females in the highest-ranking matriline of the troop. Adult males were responsible for 40% of all grooming received from nonkin by the females without newborns, and these males approached them significantly more than did other adult females without infants. These patterns demonstrate that the structure of social relationships is influenced by the particular dynamics of troop contexts such as birth seasons, as well as by enduring, broad-based affinities which are less affected by cyclic changes in troop context.     

Determinants of breeding dispersal in the sand lizard, Lacerta agilis, (Reptilia, Squamata)

We studied determinants of breeding dispersal (the distance that an animal shifts its mean home range co-ordinate between reproductive events) in an individually marked population of sand lizards (Lacerta agilis) in south west Sweden during 1987–1991. Female breeding dispersal was not determined by age, size, body condition, or number of partners, and females and males that dispersed further did not experience a higher mortality. However, females with a low reproductive output dispersed further than females that reproduced more successfully, and males that lost in bodily condition dispersed further than males that better maintained body condition. We also looked for relationships between age-differences and band-sharing similarity (DNA fingerprinting = DFP) in three categories of lizards — all females, all males, and males and females — to establish whether males would be likely to mate with close kin. Age-difference was strongly correlated with band-sharing in only one category, males and females. When males were older than females this relationship was not significant. However, when females were older than males, age-difference was strongly correlated with band-sharing. Furthermore, females that were old enough to be the mothers of the courting males shared significantly more bands with these males than did the younger females, including the females of the same age as the males. Although parental-specific DFP bands necessary for establishing paternity among our adult lizards were inaccessible to us, we suggest that our circumstantial evidence strongly suggests that some males mate with their mothers. Males that were more closely related with their neighbours also moved further when we controlled statistically for age and mating success. We suggest that by mating with many partners males not only increase their mating success, but also increase the probability of mating with females with ‘good genes’: mean heterozygosity of parents (as revealed by micro-satellites) were strongly correlated with offspring survival.     

Plumage redness predicts breeding onset and reproductive success in the House Finch: a validation of Darwin's theory

Darwin (1871) and later Fisher (1958) suggested that sexual selection can drive the evolution of ornamental traits in monogamous species when female preferences for these traits allow well-ornamented males to begin breeding earlier in a season and, as a result, gain reproductive advantages over poorly ornamented males. However, few studies have been conducted to test this fundamental concept upon which much of the sexual selection theory for monogamous species has been based. In this study, we examined the relationship between breeding onset, reproductive success, and male ornamentation in the House Finch Carpodacus mexicanus , a species in which males display bright carotenoid-based plumage pigmentation. In previous work, it has been shown that bright male House Finches are preferred as social mates by females and, as a result, begin nesting earlier in the season than do drab orange and yellow males. Here we show that, by initiating breeding earlier in the season, brightly colored males fledge more offspring in a season than do drab males. Thus, differential timing of breeding generates considerable variance in reproductive success among male House Finches and contributes to sexual selection for male plumage ornamentation in this species.     

Phenotypic variability in nesting success among Osmia lignaria propinqua females in a glasshouse environment: (Hymenoptera: Megachilidae)

Abstract. 1. The phenotypic variability of several estimates of fitness among seventeen nesting female O.lignaria Cresson was examined in a glasshouse provided with abundant resources.
2. Females exhibited wide variation in: (a) number of nests and cells made and in their rate of construction, (b) the incidence of mortality of offspring, and (c) the percentage of male offspring produced (52–100%).
3. In confirmation of earlier field studies: (a) more offspring of both sexes were produced during the first half of the nesting season, (b) most female offspring were produced early in the nesting season, (c) most parental investment during the last half of the flight season was made in male offspring, (d) there was a decrease in offspring size with season, with females decreasing more than males, and (e) the ratio of female/male body weight was = 1.8. These results appear to be due to ageing rather than to a reduction in resource availability.
4. No relation between female size and fecundity was evident.
5. There was no evidence that small females tended to produce a greater proportion of the smaller sex (males) than did large females.
6. Smaller offspring of both sexes had a much greater probability of dying overwinter than did large offspring. However, where the sexes overlapped in size (large males, small females), almost all females died and almost all males survived. We hypothesize that as size of offspring produced declines with season, a greater proportion of males are produced because they have a much greater probability of surviving at small body sizes.     

Effects of age,lactation, and repeated cycles on rhesus monkey copulatory intervals

Young, sexually mature female rhesus monkeys copulate on more days prior to conception than do older females, and this prolonged discrete mating period is associated with an earlier rise in serum estradiol prior to the first ovulation of the breeding season. The influence of repeated ovulatory cycles and the presence of a suckling infant on the copulatory patterns were examined in two separate analyses. Extending previous work, young, nulliparous females copulated on more days at the first ovulation of the breeding season than did older, multiparous females. However, the duration of the copulatory period at the second ovulation of the breeding season was similar and significantly shorter for both age groups. Furthermore, the presence of a suckling infant did not influence the duration of the mating periods in adult, multiparous females. The onset of copulatory behavior for all females was associated with serum estradiol concentrations of approximately 90 pg/ml, indicating that the age and cycle differences in the duration of the copulatory periods are due to the time course of serum estradiol prior to ovulation. A separate, longitudinal analysis of the duration of the mating period associated with the first ovulation of three successive breeding seasons indicated that females copulated on more days during their first ovulatory cycle of their first breeding season. These data indicate that the copulatory interval is longer for females during the first ovulation of the breeding season, and this pattern is accentuated in young, sexually mature animals.     

Consortships and conceptions in captive rhesus macaques (Macaca mulatta)

A captive group of rhesus macaques (Macaca mulatta) was observed during the breeding season to determine if consortship behavior, rather than promiscuous matings, resulted in higher reproductive success for either partner. The 38 adult females in this group were observed “in consort” with the 5 adult or 4 subadult males on 179 occasions. Most of these consortships were short-term, lasting less than one day. Six females engaged in consortships with one male that spanned more than three days, but the majority of these long-term associations did not result in a pregnancy with that male. The term “consortship” has been traditionally accepted as a specific nonhuman primate mating pattern, but the exact nature of this behavioral pattern and its evolutionary importance have been less clearly understood. Consort behavior could be considered a precursor to a monogamous mating system if long-term exclusive sexual associations resulted in higher reproductive success for the participants. But this study demonstrates that for rhesus macaques, who exhibit both consort behavior and more promiscuous matings, there is no clear reproductive advantage to long-term consortships. In light of the inconsistent use of the term consortship, the possible adaptive significance of an exclusive male-female sexual association for the evolution of human mating patterns needs to be reevaluated.     

Reconstruction of Parentage in a Band of Captive Hamadryas Baboons

The male leaders of free-ranging harem groups of hamadryas baboons are believed to mate exclusively with the female members of their harems, which typically contain no more than 2–3 females. Using no-parent parentage exclusion analysis (PEA) we identified the paternity of 25 offspring born in a captive band of hamadryas baboons (Papio hamadryas hamadryas) containing five adult males, each with a stable harem of about five females. Nine of 13 microsatellite (SSR) loci known to be highly polymorphic in rhesus macaques (Macaca mulatta) were successful in identifying the sires of all but two offspring without knowledge of the dams' genotypes, and we were able to determine the sires of all offspring when the dams' genotypes were considered. Mating success of the males ranged between 2 and 7 offspring and bore no clear relationship to the males' ages, ranks or the number of females in their harems. The males sired 7 of the 25 offspring with females outside their own harems, with higher-ranking males exhibiting greater success monopolizing access to females in their harem than lower-ranking males did. More surprisingly, the females assigned as the dams of 14 of the 25 offspring could be unequivocally excluded from parentage. The identity of the true dam could be determined for each of these 14 offspring using single-parent PEA and was uncorrelated with the ranks of these offsprings' sires and whether the offspring were born to dams outside the sires' harem groups. The combined effect of this extraharem mating and kidnapping was that only 12 of the 25 offspring were raised within their sires' harem groups. A second group of hamadryas baboons of identical structure exhibited the same high incidences of infant kidnapping and mating outside the harem group. It is unclear whether these behaviors provide an adaptive advantage or represent aberrant behavior resulting from captivity or other circumstances.     

Prolonged lactational infertility in adolescent rhesus monkeys

The present study examined the effects of first pregnancy and nursing behavior on postpartum infertility in seasonally breeding rhesus monkeys to assess whether prolonged lactational infertility observed in adolescent mothers is due to a particular pattern of nursing or to decrements in body growth rates. After a successful first pregnancy, a significant percentage of the lactating adolescent mothers (57.1%; n = 8) failed to exhibit an ovulation with normal luteal phase during the subsequent breeding season. In contrast, the remaining lactating adolescents (42.9%, n = 6) and all of the adult mothers (100%, n = 6) exhibited ovulations with a normal luteal phase. Age alone was not the critical variable, since all nonlactating adolescents exhibited ovulations with normal luteal phase parameters in the subsequent breeding season. The luteal phase abnormalities exhibited by the subset of lactating adolescent females were characterized by an inadequate luteal phase (ILP) and by significantly lower serum levels of progesterone, estradiol, and bioactive luteinizing hormone. The occurrence of these ILP ovulations was associated with more frequent nursing bouts prior to ovulation and during the subsequent luteal phase. In contrast, nursing patterns for adult females who had ovulations with normal luteal phases were more similar to those of the infertile lactating adolescents exhibiting significantly longer and more frequent nursing bouts, suggesting that fully adult females may be less sensitive to the inhibitory aspects of a suckling stimulus. Differences in luteal phase function among lactating adolescents were not related to differential rates of ponderal or skeletal growth. A still-developing neuroendocrine system may thus render a significant proportion of adolescent females more sensitive to suckling-induced suppression of gonadotropin secretion.