The reproductive consequences of male cooperation in the red howler monkey: paternity exclusion in multi-male and single-male troops using genetic markers

Abstract

Variance in male reproductive success in single and multi-male red howler (Alouatta seniculus) troops was examined through paternity exclusion using genetic markers. Coalitions of relatives were compared to coalitions of non-relatives with regard to duration, stability, and number of offspring expected for each participant based on paternity exclusion results. No evidence of paternity by males living outside of the troop was found. In multi-male troops, only the dominant male was found to father offspring conceived during his tenure. This was the only male observed to mount females. In both troops examined genetically wherein a status change had occurred, paternity changed with status. Coalitions of relatives and potential relatives lasted significantly longer than coalitions of non-relatives, and experienced fewer status changes between males. A direct advantage of forming a coalition for both dominant and subordinate red howler males resulted from the superior competitive ability of coalitions over single males in establishing and maintaining tenure in the limited number of female troops in the population. Although the mating success of a subordinate male in a coalition appears to be extremely low, his chances of achieving membership in a bisexual troop as a single male may be even lower. Since the majority of troops in the population during any given year were multi-male or age-graded male (85%-96%), the number of troops that a single male would be able to invade unaided was very small. A subordinate male may be able to assume dominance, particularly if he is a subadult. In coalitions in which males are related, the subordinate male will further benefit from inclusive fitness. A dominant male that forms a coalition with a relative can expect to have longer reproductive tenure than in a troop with a non-relative, thereby producing more offspring and directly enhancing his fitness. Anecdotal evidence suggests that males choose relatives over non-relatives as coalition partners when possible.

Factors influencing male affiliation and coalitions in a species with male dispersal and intense male–male competition, Colobus vellerosus

“…In this situation, it was predicted and observed that within-group male coalitions would be directed towards extra-group males and function to reduce male group size (Pope, 1990;Dias et al, 2010;Berghänel et al, 2010). However, data from one of our groups shows high reproductive skew in favor of the alpha male.…”

“…Groups with more females and species where female receptivity is temporally concentrated are more likely to show multi-male groupings because a single male cannot monopolize many females (Nunn, 1999;Cords, 2000). In a typical uni-male, multi-female system, multi-male groups may form due to male influxes, attempted takeovers by single males where the resident male remains in the group, takeovers by coalitions of extra-group males, or when males remain in their natal group past maturity creating age-graded groups (Dunbar, 1984;Pope, 1990;Sicotte, 1993;Cords, 2000;Sterck & van Hooff, 2000;Watts, 2000b;Dias et al, 2010). When males are able to co-reside in these types of multimale groups, male relationships may vary from simple mutual tolerance to the formation of strong affiliative bonds, which may include within-group coalitions against conspecifics, potentially with a preference for certain partners over others (Mitchell, 1994;van Hooff & van Schaik, 1994;Olson & Blumstein, 2009).…”

“…When male reproductive competition within-group is mainly scramble (when females show synchronous estrus, engage in polyandrous mating, or show a long period of receptivity around ovulation), one expects within-group male coalitions to be directed towards reducing male group size, as male reproductive success will be influenced primarily by the number of male co-residents (Berghänel et al, 2010). In this competitive situation, most male coalitions are directed towards extra-group males to prevent male immigration (Pope, 1990;Dias et al, 2010).…”

“…Population density and local demography are certainly factors influencing the frequency and duration of multi-male groups and hence the possibility of male-male affiliation and male coalitions (Pope, 1990;Hill, 1994;van Schaik et al, 2006;Higham & Maestripieri, 2010). There are also costs that may prevent the expression of male coalitions, such as the risk of injury if a coalition partner withdraws prior to the resolution of the conflict.…”

“…We also predicted that when males engaged in within-group coalitions, it would be mostly during post-takeover situations when attempting to expel one another (Sterck & van Hooff, 2000). We expected that coalitions would be formed most often between males that were kin, of high dominance rank, long-term co-residents, that had engaged in parallel transfer, that had affiliative relationships, and that rarely showed aggression towards each other (Pusey & Packer, 1982;Pope, 1990;van Hooff & van Schaik, 1992;Higham & Mastrieprieri, 2010). We have observed affiliation among subadult males more often than between adults so we predicted that we would see an effect of age on male affiliation.…”