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Sexual selection theory predicts that males will compete actively for access to females and fertilizations, as females are usually a limited resource [Clarke et al., 2009; Paul, 2002; Smuts & Smuts, 1993; Trivers, 1972]. This may result in male–male relationships characterized by competition, intolerance, and dominance hierarchies [Cowlishaw & Dunbar, 1991; Kappeler & van Schaik, 2002; van Hooff, 2000; Wang & Milton, 2003]. Although fertilizations cannot be shared among males, increasing social tolerance among resident males is possibly related to benefits derived from indirect inclusive fitness and/or male–male negotiation of favors (i.e., reproductive benefits for support given during intergroup encounters or collective defense of resident males) [Garber & Kowalewksi, 2011; Silk, 2006]. In general, kin relationships may influence the degree of agonistic behavior between individuals [Chapais et al., 2001].
In Alouatta caraya, as in many New World primate species, several adult males may co-reside in the same social group (A. caraya [Kowalewski & Garber, 2010], Brachyteles hypoxanthus [Strier et al., 2002]; Ateles paniscus [Symington, 1990]; Alouatta palliata [Wang & Milton, 2003]). However, Alouatta males usually engage in inter- and intragroup competition for resident females especially during female fertile periods [Di Fiore et al., 2011; van Belle et al., 2008]. In the present study, we analyze male social structure and genetic relatedness in one population of A. caraya. Specifically, we investigate the relationship between male dominance hierarchies, mating success and reproductive success in multimale groups of black and gold howler monkeys.
In most multimale/multifemale primate groups, promiscuous copulation occurs, with a pronounced skew in male mating success as a function of dominance rank or central position [Cowlishaw & Dunbar, 1991; Paul, 1997; Pope, 1990; van Belle et al., 2009]. Therefore, the maintenance of social dominance hierarchies and/or central positions is expected to play an important role in the access to fertile females [Altmann, 1962; Boesch et al., 2006; Constable et al., 2001; De Ruiter & van Hooff, 1993; Dixson, 1998; Jones, 1985; Ryan et al., 2008]. Although mating success is often correlated with dominance in multimale groups, mating success is not necessarily translated directly into male reproductive success or paternity success [Altmann et al., 1996; Constable et al., 2001]. Therefore, to test hypotheses on reproductive skew, the relationship between social dominance hierarchies/male centrality and paternity success, it is necessary to combine behavioral and genetic studies. These types of studies have been successful in several primate species and, in general, have demonstrated a positive correlation between high male rank and paternity (e.g., Papio cynocephalus [Altmann et al., 1996], Pan troglodytes [Constable et al., 2001], Pan paniscus [Gerloff et al., 1999], Cercocebus torquatus [Gust et al., 1998], Semnopithecus entellus [Launhardt et al., 2001], Alouatta arctoidea [Pope, 1990]). However, studies in macaques suggest that there is no direct relationship between dominance and paternity and it may be greatly diminished in species with weak hierarchies or centrality [Paul, 2004].
Both sexes of Alouatta typically disperse from their natal social groups but often at different ages [Crockett & Pope, 1993; Glander, 1980; Oklander et al., 2010; Rumiz, 1990]. In this regard, many individuals are likely to spend a large portion of their adult lives in groups without close kin [Di Fiore et al., 2011]. Previous studies showed that most adult individuals of the study population that belong to the same group are not closely related (average r within groups r = 0.118), but in some groups females related as sisters or half-sisters and males related as brothers or half-brothers were found [Oklander et al., 2010].
In Argentina, A. caraya shows differences in density and social organization in different types of habitat such as fragmented, gallery, and flooded forests. Multimale groups are present at higher frequencies in flooded and continuous forests than in fragmented and gallery forests [Kowalewski & Zunino, 2004; Rumiz, 1990]. In our study population, the average number of adult males per group was 2.1 ± 0.7 (range 1–3), and the average number of adult females was 3.1 ± 0.9 (range 2–4) [Oklander et al., 2010]. These groups frequently engaged in intergroup encounters (almost twice a day), making the support of other resident males a potentially important benefit to trade for access to females [Garber & Kowalewksi, 2011; Kowalewski, 2007]. Black and gold howler male tenure in this species is relatively short (4 ± 1 years [Kowalewski & Garber, 2010]). Solitary males or male coalitions may try to enter in a group by confronting the resident central male who can defend the group with the support of other resident males [Kowalewski, 2007; Oklander, 2007]. If a new male enters in a group, the event is usually followed by infanticide [Pavé et al., 2012]. We also witnessed, in one occasion, a resident male taking over the group displacing the central male [Kowalewski, 2007; Oklander, 2007]. Alouatta caraya females at our study site engage in fertile (during ovulation) and non-fertile copulations (e.g., during gestation and lactation) with resident and non-resident males [Kowalewski & Garber, 2010] and births occurred throughout the year [Kowalewski & Zunino, 2004]. Conspicuous behavior during females' fertile periods, such as mate guarding, characterize short periods of high within-group male–male interference (e.g., persistent following of a female at close range for 2–3 days [Kowalewski & Garber, 2010]).
The present study combines behavioral studies over 14 months and genetic analyses in multimale–multifemale groups of black and gold howler monkeys in order to determine male (1) dominance hierarchies (2) relatedness within groups (3) mating success, and (4) paternity success. Based on previous observations of mate guarding and asynchronous births within groups [Kowalewski, 2007; Kowalewski & Garber, 2010; Kowalewski & Zunino, 2004; Oklander, 2007], we predict that there will be a male dominance hierarchy in which higher ranked/central males will father most of the offspring in their resident group. We expect that higher ranked/central males will obtain most of the matings, however we also predict that alpha males will not monopolize copulations because: (1) dominant males allow lower ranking males to copulate in order to gain support during intergroup encounters and male incursion attempts and/or (2) risk of infanticide, and the fact that females copulate during gestation and lactation, suggests that females might choose to mate with subordinate males in order to confuse paternity [Garber & Kowalewksi, 2011; Kowalewski & Garber, 2010; Oklander et al., 2010]. We also expect that closely related males will have lower levels of male–male agonistic interactions indicating greater male–male tolerance within groups.