Max-Planck-Institut für demogra sche Forschung Max Planck Institute for Demographic Research Konrad-Zuse-Strasse 1 · D-18057 Rostock · GERMANY Tel +49 (0) 3 81 20 81 - 0; Fax +49 (0) 3 81 20 81 - 202; http://www.demogr.mpg.de MPIDR WORKING PAPER WP 2010-032 NOVEMBER 2010 To care or to fi ght: must primate males choose? Daniel A. Levitis ([email protected]) Laurie Bingaman Lackey This working paper has been approved for release by: Alexander Scheuerlein ([email protected]), Deputy Head of the Laboratory of Evolutionary Biodemography. © Copyright is held by the authors. Working papers of the Max Planck Institute for Demographic Research receive only limited review. Views or opinions expressed in working papers are attributable to the authors and do not necessarily re ect those of the Institute. 1 To care or to fight: must primate males choose? 2 3 Daniel A. Levitis1,2 and Laurie Bingaman Lackey3 4 1Max Planck Institute for Demographic Research 5 Laboratory of Evolutionary Biodemography 6 Konrad-Zuse-Straße 1 7 18057 Rostock Germany 8 Email: [email protected] 9 10 2Museum of Vertebrate Zoology 11 University of California, Berkeley 12 3101 Valley Life Sciences Building 13 Berkeley, CA 94720-3160 USA 14 15 3International Species Information System 16 2600 Eagan Woods Drive, Suite 50 17 Eagan, MN 55121-1170 USA 1 18 Females in all mammalian species care for their offspring, while most mammalian males 19 do not. This failure of paternal investment is generally explained in terms of a trade-off 20 between paternal care and mating competition. While there has been great interest in the 21 optimal pattern of investment in paternal care versus mating effort, comparative evidence 22 that such a trade-off exists has not been published for any large group of mammal 23 species. We employ comparative data on primates to test for such a trade-off. Across 24 primate species, the degree to which males engage in direct care of young is inversely 25 related to levels of overt male-male conflict, and to canine dimorphism, a morphological 26 measure associated with male-male conflict. When phylogeny is taken into account, there 27 is no significant relationship between sex-biased longevity and whether males engage in 28 care, implying that investment in care and investment in competition are functional 29 alternatives to each other. Males of most primate species engage in either intensive direct 30 care, or intense or frequent intrasexual competition, but not both. The hypothesis that 31 investment in care and in intrasexual conflict are alternative strategies is strongly 32 supported. 33 34 Keywords: paternal care, primates, tradeoffs, reproductive strategies 2 35 36 37 1. Introduction 38 39 It is frequently argued (e.g., Clutton-Brock 1989; Gubernick & Teferi 2000; Trivers 40 1972) that the high prevalence of males who do not care for their young is driven by the 41 need to partition limited resources. Males of many species may gain higher fitness by 42 investing their reproductive effort in competing with other males for access to females 43 rather than caring for existing young. Similarly, an existing tendency toward paternal care 44 may limit the resources males can dedicate to fighting with each other. However a trade- 45 off between paternal care and male-male conflict has been demonstrated for few groups 46 of species (Tanganyikan cichlid fishes (Gonzalez-Voyer et al. 2008) and shorebirds 47 (Thomas & Székely 2005)), and across no large group of mammals. It is particularly 48 surprising that such a relationship has not been demonstrated in primates, both because 49 there has been considerable interest in the evolution of paternal care in primates (Buchan 50 et al. 2003; Charpentier et al. 2008; Kleiman 1985; Tardif 1994; Wright 1990) and 51 because there is a large and fruitful comparative literature on primate life-history 52 evolution (e.g., Bronikowski et al. 2002; Kappeler & Pereira 2003; Lee 1999; Thoren et 53 al. 2006). We present comparative evidence bearing on the question of whether the males 54 of a primate species must choose to help raise young or to fight with each other for access 55 to mates, but cannot do both. We further examine whether this choice influences sexual 56 dimorphism in longevity, complicating the structure of the tradeoff. 3 57 A casual survey of primate species reveals a negative correlation between two 58 important aspects of male reproductive effort: paternal care and male intrasexual conflict. 59 In large groups of primates, particularly the Aotidae and Callitrichidae (Kleiman 1985; 60 Nowak et al. 1999), males provide extensive care to young and overt conflict between 61 males is rare. In others, such as the Cercopithecids, paternal care is absent or minimal, 62 male-male conflict is intense, and morphological dimorphism in size and dentition 63 (correlates of intrasexual conflict Leutenegger & Kelly 1977; Mitani et al. 1996; Plavcan 64 2004) are generally large (Plavcan & van Schaik 1992; Plavcan & van Schaik 1997). We 65 focus on these two aspects, although other forms of competition and investment (e.g. in 66 sperm competition or influencing female choice) may also be important. 67 The choice of whether to dedicate one’s time to fighting or to caring potentially 68 conflates two of the most central life-history trade-offs: the balance between reproductive 69 rate and mortality risk reduction (Cichon 1997; Partridge 1987; Williams 1957; Williams 70 1966), and between offspring quantity and offspring quality (Clutton-Brock 1991; Lack 71 1954; Smith & Fretwell 1974; Walker et al. 2008). In primates intrasexual mating 72 conflict bears considerable mortality costs (Smith & Jungers 1997). Therefore the 73 outcome of the trade-off between male care and mating competition may be influenced 74 by the fact that one choice (care) allows for greater longevity than the other. 75 Allman et al. (1998) argue that in primate species where paternal care is 76 prevalent, the ratio of female to male longevity is lower than in other primates. 77 Caretakers may live longer because they experience more intense selection against 78 premature mortality (Plavcan et al. 1995). A caretaker who dies loses not only the ability 79 to produce future offspring, but also some portion of the fitness prospects of extant 4 80 offspring, who are deprived of the resources which otherwise would have been 81 transferred to them (Chu et al. 2008; Lee 2003). In such a situation, males would need to 82 balance increased production of offspring on the one hand against the combination of 83 higher offspring quality and higher longevity on the other, complicating the selective 84 calculus. 85 In models of this decision making process (e.g., Kokko & Jennions 2008; Webb et 86 al. 2002), mated individuals face the choice to continue investing in the fitness of current 87 offspring (bearing fitness costs in the form of time, individual quality and mortality risk), 88 or abandoning mate and young to seek new mating opportunities (also incurring costs and 89 risks). The likely payoff in each scenario may depend on several variables, many of 90 which are rarely measured in wild populations. These include the social system, the 91 Operational and Adult Sex Ratios, the need for biparental care, the non-random variance 92 in lifetime mating success and reproductive success for each sex, the certainty of 93 parentage and the relative mortality risks of the two activities. The interactions of these 94 many variables and multiple individuals can lead to strongly counter-intuitive results. For 95 example, Kokko and Jennions (2008), in a recent formal model and detailed discussion of 96 the co-evolution of parental investment and mating competition, found that when 97 multiple traits are allowed to co-vary, increasing the mortality risk associated with a 98 strategy can lead to an increased optimal investment in that strategy, not the decreased 99 investment intuition would tend to point to. They also clarify that where mate 100 competition and parental care consist of the same activity (e.g., where females are more 101 likely to mate with males whom they have observed to be involved fathers) the two goals 102 may cease to be in competition. Due to these complexities, and the possible failure of 5 103 intuition, we argue it is necessary to test for, rather than assume, the trade-off between 104 investment in intrasexual mating conflict and investment in parental care in taxa for 105 which we think this trade-off important. 106 In the current paper we conduct a phylogenetically controlled comparative 107 analysis, focusing on primate males. Approximately 60% of primate genera display no 108 male care, according to an older and probably somewhat high estimate (Kleiman et al. 109 1981), allowing for a robust set of contrasts between caring males and non-caring males. 110 We employ these phylogenetic contrasts to examine the co-evolution of paternal care, 111 male-male conflict and sex-biased longevity in primates. We test the assumption that they 112 are traded-off against each other by examining the predictions that males of each species 113 will tend to invest heavily in care or competition, but not both, or neither; that the 114 correlation between these two types of reproductive effort is stronger than the 115 relationship of either to longevity and that these relationships are phylogenetically robust. 116 117 2. Methods 118 119 For 63 primate species for which longevity dimorphism (see below) and mass 120 dimorphism data (Smith & Jungers 1997) were available, we searched for data on the 121 remaining variables (paternal care, male-male conflict and canine dimorphism). We 122 included in this sample 54 anthropoid primates and 10 strepsirrhines (lemurs, galagos and 123 lorises).