Male Reproductive Skew Is Higher in Bonobos Than Chimpanzees
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Current Biology Magazine Correspondence receptivity and attractiveness are 2007 and 2013, the time period more extended in bonobos [2], males for which we sampled all potential Male reproductive compete less intensely for each mating sires, in the Bompusa community of opportunity. This would reduce the bonobos at LuiKotale, Democratic skew is higher strength of selection for traits that lead Republic of the Congo. Skew was to success in direct contest competition calculated from published paternity in bonobos than between males and in sexual coercion data from 41 temporally overlapping chimpanzees of females, thus increasing the potential 7-year time periods in fi ve chimpanzee for female choice [3]. Accordingly, it communities, which represented a total has been predicted that the infl uence of of 191 paternities occurring over 70 Martin Surbeck1,6,*, male dominance rank on reproductive independent chimpanzee community- 2,3,6, Kevin E. Langergraber *, success and the extent of male years (Table 1). Nonac’s binomial skew Barbara Fruth4,5, Linda Vigilant1 reproductive skew should be lower (B) index [6], where –1 indicates an equal and Gottfried Hohmann1 in bonobos than in chimpanzees [1]. distribution of reproduction, 0 a random Although relevant for understanding distribution, and 1 total monopolization The two closest living relatives of the evolution of the unusual levels of by one individual, was higher in bonobos humans, bonobos (Pan paniscus) and egalitarianism and cooperation found in (0.22) than in any chimpanzee period chimpanzees (Pan troglodytes), share human hunter-gatherers [4], comparative (range: –0.03–0.14, mean: 0.03; Table 1). many traits that are common in humans analyses in the genus Pan have been The percentage of paternities achieved but rare in other mammals, including limited by the scanty paternity data by the most reproductively successful societies with high fi ssion–fusion available for wild bonobos [5]. Here, male was also higher in bonobos (62%) dynamics, male philopatry, female we show using the largest sample of than in any chimpanzee 7-year period dispersal and extensive social bonding paternity data available that, contrary (range: 7–56%, mean = 26%; Table 1). among unrelated individuals [1]. The to expectation, male bonobos have a We also calculated skew in bonobos major difference between these two higher reproductive skew and a stronger after extending the analysis to a 12-year species is that male aggression is more relationship between dominance period (2002–2013) where we had a frequent and intense in male-dominated rank and reproductive success than larger sample of genotyped offspring chimpanzees than in bonobos, where chimpanzees. (n = 24) but lacked genotypes from the highest-ranking individuals are We compared skew in bonobos an estimated one to three candidate female [1]. One potential explanation is using paternities for 13 offspring sire males present at the beginning that because periods of female sexual conceived in the seven years between (2002 – 2006). Even if we assume Table 1. Overview of male reproductive competition in one bonobo (bold) and fi ve chimpanzee communities over 7-year and 12-year time periods. Average Most Number Average rank Time number of Number of Nonac’s B successful Species Community of time of sires period males per paternitiesa indexa sire’s sharea periods (95% C.I.) conceptiona [%] 2007– 0.81 Bonobos Bompusa 1 7.4 13 0.22 62 2013 (0.63–0.95) 1987– 6.3 10.5 0.09 51 0.77 Chimpanzees Taï North 2 1994 (6.1–6.5) (10–11) (0.07–0.11) (45–56) (0.60–0.91) 1985– 11.6 12 0.05 31 0.65 Chimpanzees Kasakela 21 7-year 2011 (11.3–12.3) (8–16) (-0.03–0.14) (13–45) (0.53–0.76) periods 1999– 0.91 Chimpanzees M group 1 11.6 11 0.06 36 2005 (0.84–0.97) 1993– 16.0 11 0.01 34 0.80 Chimpanzees Sonso 4 2002 (15.7–16.2) (11–11) (0.01–0.02) (27–36) (0.66–0.91) 1996– 41.8 42 0.01 11 0.66 Chimpanzees Ngogo 13 2014 (40.2–43.9) (30–54) (0–0.02) (7–13) (0.62–0.71) 2002– Bonobos Bompusa 1 - 23 0.08 39 - 2013 12-year 1996– 72.3 0.01 7 Chimpanzees Ngogo 8- - periods 2014 (62–80) (0.00–0.01) (6–8) 1985– 20.7 0.04 27 Chimpanzees Kasakela 16 - - 2011 (15–25) (-0.01–0.12) (16–41) avalues represent the average across all time periods for each group and the values in brackets indicate the range of values of all time periods for each group. R640 Current Biology 27, R623–R641, July 10, 2017 © 2017 Elsevier Ltd. Current Biology Magazine that all 3 offspring with unassigned lower estrous synchrony among females ACKNOWLEDGEMENTS paternity were sired by different does not appear to explain the stronger ungenotyped males, the B-index was infl uence of dominance rank on male Thanks to C. Rowney and A. Nicklisch for still higher in bonobos (0.083) than in reproductive success in bonobos than in performing genetics lab work, to R. Mundry all but two of 24 12-year periods in chimpanzees. for statistical advice, to P. L. Hooper and two chimpanzees (range = -0.010–0.123, If not an effect of the numbers of reviewers for helpful comments. The Congolese wildlife authority (ICCN) gave permission to mean = 0.028; Table 1). Additionally, competing males or simultaneously conduct fi eld research and export fecal samples the most successful male’s share of receptive females, how did high- for genotyping. Funding for bonobo fi eld and reproduction, which is unaffected by the ranking males more effectively genetics research was provided by the Max presence of ungenotyped males, was monopolize reproduction in bonobos Planck Society, the National Geographic Society higher in bonobos (39%) than in all but than chimpanzees? One possibility is and the Wenner-Gren Foundation. M.S. was 1 of 24 chimpanzee 12-year periods that higher levels of male aggression partially supported by SNF. K.E.L. is supported by (range = 6–41%, mean = 20%; Table 1). in chimpanzees actually decrease NIH RO1AG049395 and Arizona State University Comparative research in group- reproductive skew. Although rank and President’s Strategic Initiative Fund. The authors living primates indicates that male sexual coercion are positively correlated have no fi nancial confl icts of interest that reproductive skew is high when the in male chimpanzees, coercion by infl uence the results or interpretations contained number of competing males is low low-ranking males may also result in this paper. [7]. However, this does not appear in paternities that are unavailable for to explain why skew was higher in low-ranking bonobos [9]. Within-group REFERENCES bonobos than chimpanzees. Although infanticide also appears to be absent in 1. Hare, B., Wobber, V., and Wrangham, R. (2012). The we found that the chimpanzee periods bonobos. The need to confuse paternity self-domestication hypothesis: Evolution of bonobo with skew values most similar to those through promiscuous mating may thus psychology is due to selection against aggression. of bonobos also had a small average lower for female bonobos. Rather, the Anim. Behav. 83, 573–585. 2. 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