Reproductive promiscuity in the splendid fairy-wren: effects of group size and auxiliary reproduction

Extrapair fertilizations complicate our understanding of cooperativebreeding in a number of ways. For example, auxiliaries may reducethe costs of seeking extrapair fertilizations for breeding malesor females, and auxiliary males may themselves seek copulationswith the breeding female in their own group. We employed microsatellitemarkers to examine patterns of parentage in the cooperativelybreeding splendid fairy-wren (Malurus splendens melanotus).Our study population exhibited a relatively high level of extrapairpaternity (42% of 386 offspring) with considerable annual variation(range = 24–52%). Across years the proportion of offspringsired by extrapair males was significantly correlated with theaverage number of auxiliaries per group. Furthermore, the proportionof extrapair young within a brood was related to group composition;groups with multiple auxiliaries were twice as likely as groupswith zero or one auxiliary to contain extrapair young. Mostoffspring were sired by dominant breeding males, but auxiliarymales sired approximately 25% of all extrapair young (10% ofall offspring), and about half of these were cases in whichthe auxiliary male sired offspring in his own group. Within-groupsirings by auxiliary males were most common after replacementof the breeding female, and they also appeared to be more likelywhen the auxiliary was not related to the breeding male. Thus,the presence of auxiliary males increased the likelihood thatfemales would produce extrapair young, and although incest avoidancemechanisms usually prevent within-group copulations by auxiliarymales, a conflict of interest among group males arises whena new female joins the group.     

Multiple breeding females in free-ranging groups ofCallithrix jacchus

We present observations on the breeding patterns in a free-ranging population of common marmosets, Callithrix jacchusWe found evidence of the simultaneous presence of two reproductively active females in all three monitored groups. We recorded at least one full reproductive cycle (conception-birth) for two females in each group, but other adult females did not breed. An overview of data from other callitrichid field studies indicates that the observed pattern may be an additional characteristic of the flexibility of the social organization of common marmosets. Comparisons with data from other sites where callithrixhas been studied indicate that the presence of a second breeding female in a group may be related to high population density, though the underlying mechanisms remain unclear.     

Modeling Developmental Class Provides Insights into Individual Contributions to Infant Survival in Callitrichids

Cooperative breeders live in social groups in which individuals in an age–sex class vary in reproductive development due to reproductive dominance by a few individuals in each group. Among callitrichids, adult males have been implicated in driving group reproductive output, but uneven sampling efforts, the underlying effects of group size, and pseudoreplication at the group and species levels are confounding variables in these analyses. We examined the drivers of group reproductive output in callitrichids by 1) conducting a meta-analysis of published studies of callitrichid group composition; 2) assigning developmental class based on reproductive morphology; and 3) using multivariate modeling to test whether the proportion of individuals of each developmental class predicts the presence and the number of surviving offspring among free-ranging Weddell’s saddleback tamarins (Leontocebus weddelli) and emperor tamarins (Saguinus imperator) in Peru. The meta-analysis revealed that the number of adult females and group size, but not the number of adult males, are significantly correlated with group reproductive output. Statistical models of the new dataset revealed that the proportion of primary breeding males, primary breeding females, and group size predicted whether groups had surviving infants, and that only the proportion of primary breeding females and group size predicted the number of surviving infants. Thus, primary breeding males appear to be necessary for groups to raise any infants, but a higher proportion of primary breeding females and a larger group size increase group reproductive output overall.     

Social behaviour and infant carrying in a group of moustached tamarins,Saguinus mystax (primates: Platyrrhini: Callitrichidae), on Padre Isla,Peruvian Amazonia

The social behaviour of a group of eight moustached tamarins,Saguinus mystax, (five males, three females) was studied on Padre Isla in northeastern Peru. About 60% of all allogrooming was done by the two adult males in the group, and about 11% by a young adult female. All other group members groomed very little. The adult breeding female received more grooming than any other group member. After the death of the adult female (preyed upon by an anaconda) the amount of active allogrooming remained constant for all group members except for the young adult female, who increased her contribution to about 30%. Her preferred grooming partner was the subadult female, which generally screamed when being groomed by the young adult female and terminated grooming by going away. This kind of grooming relation is termed “forced grooming” and is interpreted as a possible social control mechanism. The young adult female groomed the adult males more often after the death of the adult female than before. This might have had the function of strengthening the social bond with the adult males and in obtaining the breeding position in the group. After the death of the adult female, the vulva of the young adult female grew to full adult size. Agonistic behaviour was less frequent than allogrooming. Most aggressive interactions (50%) originated from the subadult male of the group. The young adult female was the target of most of these aggressions. Extremely little aggression occurred between the three females. The young adult female was the only individual who tried to emigrate from the group during the study period. Her attempt to join a neighbour group failed due to rejection by all four members of this group. All group members participated in carrying an infant, but the adult males and the young adult female carried most frequently. Contribution to infant carrying varied with the infant's age.     

Testicular Volume and Reproductive Status of Wild <Emphasis Type="Italic">Callithrix jacchus</Emphasis>

The social relationship dynamic among callitrichid females is well known. Breeding exclusivity by dominant females involves female-female competition, usually resulting in the inhibition of subordinate reproduction. However, the strategies to maintain the male breeding position are still unclear. Researchers have observed no overt aggression between males, and differences in testosterone levels between dominant and subordinate individuals do not correlate with differences in reproductive success. In Callithrix monogamy is the predominant mating system, and testicular size is compatible with the absence of sperm competition. We analyzed testicular volume during development in 95 individuals at different ages (infant n = 12, juvenile n = 9, subadult n = 15, and adult n = 59). We also investigated if the ratio between testicular volume and body mass correlates with breeding position in the social group. The ratio was significantly higher in breeding males and a positive correlation between body mass and testicular volume is significant only for nonbreeding males. The findings suggest that testicular size varies with male reproductive status in the social group and that the enlargement of testicular volume in breeding common marmoset males seems to be a result of proximate causes and to depend on social and reproductive contexts acting together or separately.     

Social environment and morpho-physiological status of young males in the fall groups of great gerbil (Rhombomys opimus Licht). Effect of adults' presence

The dependence of stress and sex hormone levels, size of mid-ventral skin gland, and body mass of young males on the presence in social groups of adult gerbils (>1 year old) were studied during the fall of 1999 in the non-breeding high density population of the great gerbil (Rhombomys opimus Licht; Bukhara region, Uzbekistan). Contents of corticosterone and testosterone in fecal samples collected from young males in the field were analyzed by non-invasive radioimmunoassay. The fall gerbil groups with adults were of larger size than those without adults. The total number of individuals in a group is positively correlated with concentration of corticosterone in feces of young males. Presence of adult male and especially of adult female suppresses maturation of juvenile males indicated by size of the androgene-dependent mid-ventral gland, but accelerates their total growth. Thus, the social environment influences morpho-physiological characters of young males, effecting rate of their maturation directly or indirectly through the density dependent stress.     

Group size,composition, and reproductive success in wild common marmosets (Callithrix jacchus)

Data from published sources about size and composition of wild common marmoset groups (Callithrix jacchus) were analyzed to see if the number of juveniles in a group is closely related to the number of other group members. Mean group size was 8.7 members including 4.4 adults (1.8 females, 2.5 males), 2.9 subadults, and 1.4 juveniles. The number of juveniles was significantly positively correlated to the number of adult males. Groups with one or two adult males had significantly fewer juveniles (mean: 1:1 juveniles) than groups containing more than two adult males (mean: 2.0 juveniles). Apart from a different number of subadults, results showed obvious similarities between common marmosets and tamarins of the genus Saguinus in size and composition of subgroups of adults as well as the key role of adult males in mediating the reproductive success of a breeding female. Common marmoset females seem to gain direct fitness benefits in increased reproductive success from the presence of a larger number of adult males. Whether or not other group members get fitness benefits depends on the reproductive strategy of adult males (monogamy vs. polyandry), their kinship, and on the genetic relationship of nonbreeders to the offspring of the breeding female. © 1995 Wiley-Liss, Inc.     

Shared parentage and incest avoidance in the cooperatively breeding acorn woodpecker

Social groups of acorn woodpeckers (Melanerpes formicivorus) range in size from unaided pairs to 15 adults. Behavioural indicators of mate guarding, assumed incest avoidance and observations of egg-laying indicate that social organization ranges from monogamous pairs to groups with up to seven male and three female putative cobreeders plus up to 10 nonbreeding helpers. In addition, groups occasionally lack a putative breeder throughout the breeding season. Here we report results from multilocus DNA fingerprinting of 372 nestlings from 123 nests in groups with putative cobreeders of one or both sexes. No extra-group fertilizations were found. Putative cobreeding males within social groups shared paternity. However, the most reproductively successful male was, on average, almost three times as successful as the next most successful and additional males only occasionally sired offspring. In contrast, cobreeding females shared parentage equally. Helpers never bred incestuously when their opposite-sex parent (or another relative, such as their uncle) held breeding status in the group. However, during breeding male vacancies, 14 nestlings were produced when helper males bred incestuously with their mother. Both male and female helpers usually became successful cobreeders with their same-sex parent following replacement of the opposite-sex breeder(s) by unrelated individuals.     

Group unity of chimpanzees elucidated by comparison of sex differences in short-range interactions in Mahale Mountains National Park,Tanzania

Chimpanzees (Pan troglodytes) form multi-male and multi-female unit groups with fission–fusion grouping patterns. Short-range interaction (SRI) plays an important role in the unity of these groups and in maintaining social bonds among members. This study evaluated three models of chimpanzee social structure that differed according to the emphasis each placed on social bonds between the sexes, i.e., the male-only, the bisexual, and the male-bonded unit-group model. I investigated differences in SRI between the sexes among group members in well-habituated wild chimpanzees in Mahale Mountains National Park, Tanzania. I followed six focal adult males and six females, and quantified their respective SRI with other chimpanzees. Except between subordinate males and adult females, adults in general engaged in SRI with about 60–90% of the individuals with whom they made visual contact each day, whether in large or small parties. Although the number of social grooming (SGR) partners was limited, male–male SGR networks were wider than were either male–female or female–female SGR networks among adults. The number of contact-seeking behavior (CSB) partners was also limited, but dominant males had more CSB partners. Adult females mainly interacted by pant-grunt greeting (PGG) with adult males, but tended to do so mainly with the highest-ranking male(s) within visual contact. These results indicated that the social bonds among adult males were essential to group unity. Because of clear male dominance, adult females established peaceful coexistence with all group members despite less frequent SRI with subordinate males by maintaining affiliative social bonds with dominant males, thereby supporting the male-bonded unit-group model. Adult females had many female SRI partners, but these interactions did not involve performing conspicuous behaviors, suggesting that females maintain social bonds with other females in ways that differ from how such bonds are maintained with and between adult males.     

Changes in the size,composition, and reproductive condition of wild marmoset groups (Callithrix jacchus jacchus) in north east Brazil

Five groups ofCallithrix jacchus jacchus were studied in the field in north east Brazil. Group size and composition were similar to that described for other callitrichids, but changes in group membership occurred much more frequently than previously reported. There was a 50% turnover in group membership in a six month period, and adult males changed groups particularly often. Most groups contained only one reproductively active female, but there was evidence that one group contained two females that were reproductively active simultaneously. Some groups had several adult females, and the role of reproductive female switched from one individual to another with time. Individual marmosets are faced with an unusually wide range of alternative life history strategies involving different combinations of location and reproductive condition. We argue that marmoset social organization is best studied at the level of the whole population within an area, rather than at the level of the individual group.     

The reproductive status of nonbreeding group members in captive golden lion tamarin social groups

Reproductive activity is limited to only one female in many species of callitrichid primates (marmosets and tamarins): daughters and subordinate females do not produce offspring. A suppression of ovulatory cyclicity is responsible for the lack of reproductive activity in three species of callitrichids studied to date. This study evaluated the endocrine status of golden lion tamarins (Leontopithecus rosalia) housed as daughters or sons in family groups and of individuals housed in isosexual peer groups. Daughters 17 months of age and older and a subordinate female had high levels of estrogen excretion. Mean levels of estrogen excretion in these females were similar to those of nonpregnant, breeding adult females (17.14 ± 6.82 versus 11.93 ± 6.33 μg/mg creatinine, respectively). Estrogen profiles were similar to those of breeding adult females, with sinusoidal cycles in estrogen excretion. Younger daughters in family groups (10 and 12 months old) showed markedly lower levels of estrogen excretion (0.84 ± 0.58 μg/mg creatinine). Estrogen profiles lacked the sinusoidal nature of cycles in older daughters and breeding females, and elevations in estrogen excretion occurred frequently and remained elevated for 1 or 2 days. Plasma testosterone levels in males varied widely, but mean concentrations did not differ among males housed in different social conditions. These results suggest that older daughters and subordinate females may be capable of expressing normal ovarian function in the presence of a breeding adult female. This finding may account for two unusual observations in the lion tamarin: the high level of female-female aggression and the presence of groups in the wild with more than one actively breeding female.     

Effects of allocare-givers on fitness of infants and parents in callitrichid primates

The effects of callitrichid primate helpers (allocare-givers other than an infant's father) on the survival, reproduction or behavior of infants and parents are reviewed, using both published studies and data from free-ranging golden lion tamarins (Leontopithecus rosalia). Three lines of evidence suggest that helpers may increase their own inclusive fitness: (1) The number of adult males acting as helpers in free-ranging groups is correlated with the number of surviving infants in 3 callitrichid species. However, the lack of a negative correlation with number of infants dying suggests that activities other than direct infant care (e.g. territory defense) may be more important, especially in newly formed groups. (2) In 2 species, captive groups with helpers carry infants for longer periods of time than do groups without helpers. Whether such differences would translate into meaningful survival differences in free-ranging groups is unclear. (3) Helpers reduce the energetic burden of parents by reducing the amount of time they spend transporting or provisioning infants in at least 4 species. Reproductive males are more likely than reproductive females to benefit from the presence of helpers, reducing their investment in infant care activities as the number of helpers in the group increases. In free-ranging golden lion tamarins, the reproductive tenure of males, but not females, increases with the number of helpers in the group, suggesting that a reduction in energetic investment may translate into increased survival. 'Decisions' made by helpers to participate in infant transport are weighed against competing needs for foraging, vigilance, territory defense and, in some cases, prospecting for breeding opportunities. Given this complexity, a sophisticated model may be required to answer the question of how helpers 'decide' to participate in infant care versus other activities.     

One for all and breeding for one: Cooperation and competition as a tamarin reproductive strategy

In this paper I examine behavioral strategies used by male and female tamarins to increase individual reproductive opportunities while continuing to maintain a high level of group cohesion and social cooperation. Tamarins of the genus Saguinus are characterized by social groups generally composed of more than one adult of each sex, but a breeding system in which only a single female in each group gives birth. The breeding sovereignty of a single dominant female limits the reproductive opportunities of subordinate females as well as the reproductive opportunities of resident adult males.^1-3 Despite extreme variability in year-to-year reproductive success among members of the same social group, field studies indicate that within-group intrasexual aggression and fighting are rare, and that both breeding and nonbreeding individuals expend time and energy cooperatively caring for young, defending productive feeding sites, and assisting in food harvesting activities.^4-11 In fact, Caine¹² has argued that “co-operation, tolerance, and flexibility” are the primary themes of tamarin social interactions (p. 218). A major question that remains unanswered, however, is how such high levels of cooperation could have evolved in a social system characterized by emigration of both adult males and females from the natal group, polyandrous mating, and intense reproductive competition.     

Social organization of the Alaotran gentle lemur (Hapalemur griseus alaotrensis)

Knowledge of the social organization of lemurs is still limited for most species. Where there is sufficient information, it has been shown that lemur social organization differs in essential points from that of other primates. In the field study reported here, demographic structure and life-history processes were investigated in order to characterize the social organization of the Alaotran gentle lemur (Hapalemur griseus alaotrensis). Data were obtained through captures and observations. Alaotran gentle lemurs were found in small groups of up to nine individuals. Although most groups contained just one breeding female, a substantial proportion of groups (35%) had two breeding females. Therefore, Alaotran gentle lemurs cannot be classed as being organized in monogamous family groups. An extended birth season was found, and groups with two breeding females had significantly higher breeding output per adult than groups with a single adult female. Limited data suggest that females emigrate from their natal group while still subadult, whereas males can stay in the natal group until they are fully grown and disperse as adults. Variability in group composition, significantly higher reproductive output per adult in groups with two breeding females, and delayed dispersal of males suggest that Alaotran gentle lemurs pursue a resource-defense mating strategy, rather than a female-defense mating strategy. The suggestion that extant social lemurs may have evolved from a monogamous system, could explain the differences between lemur social systems and those of other primates.     

Endocrine Monitoring of Wild Dominant and Subordinate Female Leontopithecus rosalia

In captive callitrichid primates, female reproductive function tends to vary with social status. However, little is known about the interplay between these factors in wild groups. We report observations on normative ovarian function in dominant and subordinate female golden lion tamarins (Leontopithecus rosalia) living in wild groups. We monitored ovarian status by measuring, via enzyme immunoassay, concentrations of excreted pregnanediol glucuronide (PdG) and estrone conjugates (E₁C) in fecal samples collected noninvasively from individuals in social groups in the Poço das Antas Biological Reserve, Rio de Janeiro State, Brazil. Dominant breeding females demonstrated steroid levels similar to those previously reported for wild cotton-top tamarin females, with statistically significant rises during pregnancy. The duration of elevation of fecal steroids in breeding females was ca. 4 mo, which corresponds with estimates of gestation from captive studies. Low steroid concentrations from December to June suggest a seasonally-related period of infertility in female golden lion tamarins. Dominant and subordinate females demonstrated several differences in endocrine function. In general, younger females living in intact natal family groups showed no evidence of ovarian cyclicity. We noted endocrine profiles consistent with ovulation and subsequent pregnancy for behaviorally subordinate females living in groups with unrelated males or in which a reversal in female dominance status occurred. Results suggest that in addition to changes in female reproductive endocrinology associated with puberty, the regulation of reproduction in females in wild callitrichid groups can be sensitive to status and relatedness to breeding males.     

Secondary transfer of adult mantled howlers (<Emphasis Type="Italic">Alouatta palliata</Emphasis>) on Hacienda La Pacifica,Costa Rica: 1975–2009

Natal emigration by male and female mantled howlers (Alouatta palliata), and subsequent immigration into breeding groups, is well documented for the free-ranging population on Hacienda La Pacifica, Costa Rica, but secondary transfer was considered rare (Glander in Int J Primatol 3:415–436, 1992). Population surveys in 1998 and 2006 caused us to question our assumptions and to re-evaluate our long-term data set from a post hoc perspective. We first identified all animals observed or captured as adults in more than one non-natal group anywhere in the population. We then systematically analyzed joining or leaving by adults in seven groups tracked for various times from 1975 to 2005 for patterns suggesting secondary transfer. Fourteen adults (nine females, five males) were found in two different non-natal groups as adults. In addition, one male and one female that became dominant and reproduced in their natal group later transferred to a second group, and one female was known to be a tertiary transfer. Data from the seven tracked social groups indicate that 35% of all the males and 29% of all the females were potential secondary transfers. In these groups, males leaving or joining was not associated with group size or absolute number of females. Females leaving or joining was not associated with group size or absolute number of males, but females left groups with more females and joined groups with fewer females. Both sexes left groups with unfavorable sex ratios for their sex and joined groups with sex ratios more favorable for their sex. Since a favorable sex ratio is associated with reproductive success in other howler populations, this suggests secondary transfer as a reproductive strategy. Other factors could also influence secondary transfer.     

Group structure,within-group conflict and reproductive tactics in cooperatively breeding Galápagos mockingbirds,Nesomimus parvulus

Reproductive conflict within groups can be an important feature of cooperative breeding systems, especially when more than one individual of a sex breeds within a social group. Relationships between group structure, dominance, within-group conflict and reproductive tactics of cooperatively breeding Galápagos mockingbirds were examined on Isla Genovesa. Territorial groups of 2–24 adults included up to three breeding females, with 42% of the groups containing more than one (plural groups); females in most plural groups nested separately. Territory size increased with group size, but the area available per pair in plural groups was smaller than in singular groups (groups with only one breeding pair). Most pairings were monogamous, and males usually outnumbered females; high-ranking males obtained mates more frequently than subordinate males. In 3 relatively dry years, but not in a wet El Niño year, subordinate pairs in plural groups fledged fewer young than dominant pairs or pairs breeding in singular groups. Interference by dominant breeders, often leading to abandonment of nests by subordinate pairs, appears to account for these differences: through nest disruption in drier years, dominant individuals may reduce the cost of sharing their territories and increase the chances of recruiting helpers. Dominant males in plural groups may also father young through extra-pair copulations with subordinate females. Despite costs imposed by within-group conflict, subordinate breeders have higher long-term reproductive success than birds that defer breeding. Plural group structure is maintained because unpredictable climatic variation favours opportunistic breeding by subordinates.     

The Cooperative Breeding System of the Red-cockaded Woodpecker

The breeding system of the red-cockaded woodpecker is described based on data collected over six years from a population of 500 marked individuals in the Sandhills of North Carolina. Male-female pairs were the most common social unit (59%), but 30% of social units contained one or more adult helpers, and 11% consisted of solitary males. Helpers were almost exclusively male: 27% of males remained in their natal group as helpers for at least one year, whereas only four (1%) females did. Most breeding females remained as breeders in the same group from one year to the next (56%), but a surprising number (12%) moved to another group. Many movements were related to incest avoidance or mate death, but 39% involved deserting a mate, usually following successful reproduction. We suggest that females sometimes are forced from groups by immigrants or other group members. The median distance of movements by adult females was only 1.3 km. In contrast to females, no breeding males switched groups. Survival of both breeding (76%) and helper (80%) males was higher than that of breeding females (69%). Males exhibited two distinct life-history strategies. Some remained as helpers on their natal territory for one or more years, and became breeders by inheriting breeding status in the natal group (17% per year) or by replacing a deceased breeder in a nearby group (13% per year, median distance moved 1.0 km). Other males dispersed from their natal group permanently during their first year. Some of these males were floaters at age one year, others were solitary, and a few became helpers in a non-natal group, but many were breeders. In contrast to males that first functioned as helpers, those that dispersed after fledging moved long distances (median dispersal distance 4.5 km), longer even than dispersing female fledglings moved (median distance 3.2 km). The habitat saturation model of the evolution of cooperative breeding is based on selection between the two life-history strategies exhibited by male red-cockaded woodpeckers. The model therefore may be tested directly with this species. Another indication that this model is appropriate for this species is the existence of a resource (cavity trees) that might provide an ecological basis for habitat saturation.     

Infant Carrying Behavior in Callitrichid Primates: Callithrix and Leontopithecus

Care of offspring by individuals other than the mother is ubiquitous in callitrichid primates. In spite of its widespread occurrence, however, there is considerable taxonomic variation in the timing and intensity of parental effort by breeding males and nonbreeding juvenile group members. These differences may be attributable to generic and specifies differences in the costs of reproduction for females or in ecological constraints on travel and foraging. We present data on patterns of infant carrying in social groups of two taxa of callitrichid primates (Callithrix and Leontopithecus) throughout the first 3 months of infant life. We evaluated patterns of care in small groups (two or fewer juvenile or subadult helpers) and in large groups (three or more helpers in addition to the breeding adult male and female). Group size had little effect on levels of maternal carrying effort in either marmosets or lion tamarins, and mothers ceased carrying infants by 3 months of age. Carrying efforts by fathers were significantly reduced in groups with many helpers relative to small groups. Helpers carried at consistent rates during the second and third months of infant life in Leontopithecus, while in Callithrix, carrying by helpers peaked during the second month. These results suggest that if helpers reduce energetic demands on lactating females, the mechanism by which helpers reduce these burdens is independent of maternal carrying effort.     

Reproductive success and survivorship of the Galapagos Hawk Buteo galapagoensis: potential costs and benefits of cooperative polyandry

The Galapagos Hawk Buteo galapagoensis is one of few species showing cooperative polyandry. As many as four males may mate with one female and share a territory and nest, Such groups, on average, produce more young than monogamous pairs, but on a per male basis (assuming that each male of a group has an equal chance to fertilize each young) polyandrous males produce fewer young per year than monogamous males. Territorial breeding birds show higher yearly survivorship (90%) than non-territorial, non-breeding birds (50% or less). All territorial birds seem to remain on their territories for life, and monogamous pairs actually constitute the remnants of polyandrous groups. Some potential factors producing such an unusual system are discussed. Limited breeding space and high mortality among non-territorial birds seem to work in favour of group breeding in this and other cooperative species. Polyandry may be favoured because of the reduced value of extra females in hawk breeding behaviour. Equal-status males may occur because of the lack of kinship among cooperating males and the high potential genetic cost of being a helper in a long-lived, low fecundity species. Other possible factors favouring group breeding are territory acquisition and the variable nature of the Galapagos climate.