Social monogamy in gibbons: the male perspective

Behavioral Ecology and Sociobiology, 1998

We report observations on reproduction, natal dispersal, pair formation, and group structure based on longitudinal observations of several white-handed gibbon (Hylobates lar) groups spanning 18 years. Our observations are at odds with the traditional view that gibbons live in nuclear family groups consisting of a pair of adults and their ospring, and that parents exclude young from the family territory when they reach adult size. In the relatively dense Khao Yai study population, dispersing young usually obtain mates by replacing adults in existing territories, which creates non-nuclear families. Six subadults, ®ve males and one female, matured and dispersed at an average age of 10 years, or about 2 years after reaching adult size. Average natal dispersal distance was 710 m, or between one and two territories away. At least two dispersing males replaced adults in neighboring groups. In one case, forcible displacement of the resident male resulted in a group which included a young juvenile presumably fathered by the previous male, two younger juveniles (probably brothers) from the new male's original group, and (later) ospring of the new pair. Social relations within this heterogeneous group remained harmonious: the adults groomed all the young and play occurred between all preadult members. In only two out of a total of seven cases of dispersal seen did two subadults pair and disperse into new territorial space. Nonreproducing subadults which delay dispersal may be tolerated by the adults provided that they contribute bene®ts to the adults or their ospring. Possible bene®ts include behaviors such as grooming, social play with juveniles, and support of the adult male in defending the territory. Delayed dispersal is probably advantageous in a saturated environment where there is no room for¯oaters, but subadults may also gain indirect ®tness bene®ts by aiding siblings and other relatives.

American Journal of Physical Anthropology, 2005

Animal Behaviour, 2008

White-handed gibbons usually live in monogamous pairs, but at Khao Yai National Park, Thailand groups often contain two adult males. We studied mating and sexual behaviour (i.e. proceptivity, receptivity and attractivity) of 12 females in relation to the females' fertile phases as assessed by faecal progestogen analysis. Females' mating activity, in pairs and multimale groups, exceeded the fertile phase and extended well into gestation and, in one exceptional case, into lactation. Whereas copulation frequency was skewed towards one male and peaked during the periovulatory period, no significant difference between fertile and nonfertile phases of the menstrual cycle was detected. Similarly, frequencies of female sexual behaviours, such as proceptivity and receptivity, did not differ across menstrual cycle phases and were common during pregnancy but absent during lactation. However, female attractivity in the form of sexual swellings directly affected copulation frequency, in that copulations were concentrated in the period when females were maximally swollen. Our data suggest that female sexual behaviours do not provide reliable information on the precise timing of the fertile phase to males. Because copulation frequencies were closely associated to sexual swelling stage during both ovarian cycles and pregnancy, we advocate that gibbon females display such visual signals to manipulate male mating behaviour. The results suggest that sexual swellings enable females to mate with multiple males during times when they are not fertile, perhaps to benefit from paternity confusion or to bias copulations towards preferred males when highly fertile to acquire 'good genes'.

Animal Behaviour, 2000

Social monogamy, which does not necessarily imply mating or genetic monogamy, is important in the formation of male-female pair associations. We operationally define social monogamy as occurring when two heterosexual adults, exclusive of kin-directed behaviour, direct significantly less aggression and significantly more submission towards each other, and/or spend significantly more time associating with each other relative to other adult heterosexual conspecifics. Long-term pair associations (i.e. those lasting through a lengthy breeding season) that are characteristic of social monogamy are common in some taxa but are virtually unknown in amphibians. Recent studies, however, have suggested that red-backed salamanders, Plethodon cinereus, have complex (for amphibians) social systems. Our laboratory experiments tested the hypothesis that red-backed salamanders found in pairs in the forest display behaviours consistent with social monogamy. During the summer noncourtship season, newly collected malefemales pairs showed no preference to associate with their partners more than with a novel conspecific of the opposite sex. However, during the autumn courtship season, paired males and females significantly directed preferential behaviours towards their partners rather than towards a surrogate or a novel paired salamander. Focal animals showed no significant preferences when presented with their partner and a novel single salamander, but they never directed preferential behaviours towards a novel salamander (whether paired or single) or a surrogate. These results are the first to suggest that a salamander species engages in social monogamy. Furthermore, our results suggest that social monogamy may not inhibit paired males and females from displaying alternative strategies: preferring partners when extrapair associations may be disadvantageous (i.e. the extrapair animal is already paired) but not preferring partners when extrapair associations may be advantageous (i.e. the extrapair animal is single).

Behavioral Ecology, 2008

Monogamy within social groups where there exists a high potential for polygyny poses a challenge to our understanding of mating system evolution. Specifically, the traditional explanation that monogamy evolves due to wide female dispersion, affording males little opportunity to defend multiple females, cannot apply. Instead, monogamy in groups potentially arises because females compete for breeding resources such as breeding sites, food, and paternal care. We conducted manipulative experiments to determine whether females compete over limiting resources within groups of the obligate coral-dwelling goby, Paragobiodon xanthosomus (Gobiidae). Breeding females behaved aggressively toward individuals of their own sex and evicted subordinate females that were large and mature from the group. Experimental removal of nest sites caused breeding partners to breed in alternative nest sites, demonstrating that nest site limitation was not the cause of female competition. Supplemental feeding resulted in an increase in the fecundity of breeding females but no maturation of subordinate females, demonstrating that foodlimited female fecundity was a likely cause of female competition. Finally, supplemental feeding of breeding pairs demonstrated that the difference in eggs hatched by fed versus unfed males was less than the difference in eggs laid by fed versus unfed females, suggesting that paternal care limitation might also drive female competition. These results suggest that competition over food and possibly paternal care selects for dominant, breeding females to suppress the maturation of subordinate females to minimize competition. Monogamy in association with group living is therefore likely to have evolved because female competition prevents males from utilizing the potential for polygyny.

American Journal of Physical Anthropology, 2000

Social organization involving pair bonding and two-adult groups is rare in mammals. Current sociobiological theory suggests that this grouping and behavior pattern is somewhat anomalous. The gibbons (genus Hylobates) are the only hominoids to exhibit pair bonds and two-adult groups. In this article I present an overview of the current issues in monogamy and pair-bond theory, and review traditional conceptualizations and the accumulated data relevant to gibbon social organization. The significance of hominoid behavioral phylogeny and population-wide studies is also considered. Recent findings indicate that pair-bonding and two-adult groups are not ubiquitous among the hylobatids. Many aspects of gibbon behavior and ecology do not conform to expectations of the conditions under which twoadult groups and/or pair-bonding patterns should evolve. A review of the information available from long-term and short-term studies of gibbons suggests an alternative way of viewing their socioecology. I propose that gibbons currently exist in variable communities that have arisen via ecological pressures and specific behavioral patterns from an ancestral multimale/multifemale grouping pattern. This social organization is not best characterized as "monogamous." This review also suggests that hominoid grouping patterns can be viewed as occurring along a continuum rather than as being discretely different units.

Biotropica, 2009

Although members of the family Hylobatidae are known to be monogamous, adult white-handed gibbons (Hylobates lar) at Khao Yai National Park, Thailand, also show multimale groups and polyandry. A need for more than one male to successfully raise offspring cannot explain the occurrence of polyandry in these territorial primates, because direct paternal care is absent in this species. We hypothesize that polyandry is primarily related to costs/benefits for males of cooperatively defending a female and/or resources; our prediction was that polyandry would become more frequent with increasing costs of female/resource defense. We measured the ecological quality of seven gibbon home ranges over a 3-yr period (2001)(2002)(2003) to investigate how resource availability affected the probability of polyandry, and found a significant negative relationship between home range quality and home range size. Larger home ranges were of lower quality. As predicted, groups living on larger, poorer home ranges also experienced longer periods of polyandry. In forest areas of comparatively low quality, acquiring and maintaining a large home range that includes enough resources for a female to reproduce steadily may surpass a single male's capacity. Our model of cooperative male polyandry was supported by preliminary data of shared territorial defense and access to the female. However, interaction proportions were strongly skewed, and female's primary male partners monopolized grooming and mating. Nevertheless, a primary male on a large territory may benefit from the presence of a secondary male with aid in territorial/female defense, whereas a secondary male may gain by avoiding high dispersal costs.

Behavioral Ecology and Sociobiology, 2004

In a recent review, compiled evidence that extra-pair paternity results from a three-player interaction in which sexual conflict is a potent force. Sequentially polyandrous species of birds appear to fit this idea well. Earlier breeding males may attempt to use sperm storage by females to obtain paternity in their mate's subsequent clutches. Later-breeding males may consequently attempt to avoid sperm competition by preferring to pair with previously unmated females. Females may bias events one way or the other. We examined the applicability of these hypotheses by studying mating behavior and paternity in red-necked phalaropes (Phalaropus lobatus), a sex-role reversed, socially polyandrous shorebird. Male red-necked phalaropes guarded mates more strongly than other shorebirds. Males increased within-pair copulation attempts during their mate's fertile period, and maintained or further increased attempts towards the end of laying, suggesting an attempt to fertilize the female's next clutch; these at-tempts were usually thwarted by the female. Paired males sought extra-pair copulations with females about to reenter the breeding pool. Multilocus DNA fingerprinting showed that 6% of clutches (4/63) each contained one chick sired by a male other than the incubator, producing a population rate of these events of 1.7% (n=226 chicks). Male mates had full paternity in all first clutches (n=25) and 15 of 16 monogamous replacement clutches. In contrast, 3 of 6 clutches of second males contained extra-pair young likely fathered by the female's previous mate. Previously mated female phalaropes may employ counterstrategies that prevent later mating males from discriminating against them. The stability of this polyandrous system, in which males provide all parental care, ultimately may depend on females providing males with eggs containing primarily genes of the incubating male, and not a previous mate.

Journal of Evolutionary Biology, 2004

J Evolution Biol, 2004