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Reproductive Skew in Vertebrates (eds. Hager and Jones)
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The Causes and Consequences of Reproductive Skew in Male Primates
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Nobuyuki Kutsukake (1, 2) and Charles L Nunn (3, 4)
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(1) Department of Biological Sciences, Graduate School of Sciences, The University of Tokyo
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(2) Laboratory for Biolinguistics, RIKEN Brain Science Institute
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(3) Max Planck Institute for Evolutionary Anthropology, Leipzig, Germany
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(4) Department of Integrative Biology, University of California, Berkeley
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Address: Nobuyuki Kutsukake - Laboratory for Biolinguistics, Brain Science Institute, RIKEN, 2-1 Hirosawa, Wako-shi, Saitama, 351-0198, JAPAN Tel: +81-48-462-1111-6823, fax: +81-48-467-7503
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E-mail:
[email protected]
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INTRODUCTION
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Reproductive skew theory attempts to explain the uneven distribution of
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reproductive success among same-sexed group members by multiple social, ecological,
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and genetic factors (Fig. 1; reviewed in Johnstone 2000). Reproductive skew theory has
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often been divided into two broad categories known as transactional and compromise
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frameworks.
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make. In a version of the transactional framework known as the concession model, the
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dominant individual controls the reproduction of subordinates and allows them to
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reproduce in return for the subordinate staying in the group (i.e., the dominant offers a
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“staying incentive”; Vehrencamp 1983a, b; Keller and Reeve 1994; Clutton-Brock
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1998; Johnstone 2000). Retaining the subordinate is assumed to increase group
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productivity (i.e., total reproductive output of a group) and fitness benefits of a
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dominant, relative to the alternative of the subordinate leaving the group. In contrast, the
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tug-of-war model, which is part of the compromise framework, suggests that the
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dominant individual is unable to control the reproduction of subordinates completely
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(Reeve et al. 1998; Cant 1998; Clutton-Brock 1998); the division of reproduction is
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therefore determined by competition between a dominant and subordinate (Reeve et al.
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1998; Cant 1998; Clutton-Brock 1998), which is assumed to decrease group
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productivity. These models can be expanded into systems with more than two
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individuals competing for reproduction (Johnstone et al 1999; Reeve and Emlen 2000),
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including queuing systems (i.e., a subordinate acquiring a higher dominance position in
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the future: Kokko & Johnstone, 1999; Ragsdale 1999; Mesterton-Gibbons et al. 2006).
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These frameworks differ according to the assumptions that each of them
In this chapter, we consider the causes and the consequences of skew in male
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primates.
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frameworks into single conceptual models (Johnstone 2000; Reeve and Shen 2006), the
Although recent research has synthesized the transactional and compromise
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classic dichotomy of the transactional (concession model) and compromise frameworks
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(tug-of-war model) provides a useful starting point for investigating reproductive skew
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in primates and will therefore be used here.
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social groups.
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to which reproduction or matings are skewed (Cowlishaw and Dunbar 1991; Bulger
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1993; Kutsukake and Nunn 2006). Although inter-individual variation in male
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reproductive success has been a central topic in primate research (e.g., Cowlishaw &
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Dunbar 1991; Bulger 1993; Alberts et al. 2003; van Noordwijk and van Schaik, 2004),
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only recently have researchers applied the theoretical frameworks of reproductive skew
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to investigate patterns of mating and reproduction in male primates (Hager 2003;
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Widdig et al. 2004; Bradley et al. 2005; Kutsukake and Nunn 2006).
Social primates live in relatively stable
In these groups, males can exhibit considerable variation in the degree
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Figure 1 provides an overview of the topics covered in this chapter. First we
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focus on the causes of skew, starting with an explanation of the POA model and how
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this model corresponds to the newer theoretical frameworks for understanding
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reproductive skew.
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predictions of the tug-of-war and concession models, we review four case studies that
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have explicitly introduced and used paternity data to investigate predictions of skew
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models in primates, and we discuss a new research direction to examine predictions
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from skew theory using phylogenetic comparative methods (Kutsukake and Nunn
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2006).
In this first section, we also discuss the assumptions and
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In the second part of this chapter, we discuss another new research direction:
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investigating the consequences of reproductive skew on other biological traits (Fig. 1).
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We focus on two examples.
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within groups, and the other considers how patterns of skew might influence the spread
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of sexually transmitted diseases. We conclude by identifying several areas for future
The first involves the effects of skew on relatedness
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research, including comparative studies.
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THE CAUSES OF REPRODUCTIVE SKEW
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The priority-of-access (POA) model
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The POA model (Altmann, 1962) has been the most influential framework
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used to explain variation in reproduction among male primates (Altmann, 1962;
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Altmann et al. 1996; Boesch et al. 2006). The model predicts that the dominant male
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monopolizes reproduction within a group. However, the degree to which the dominant
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male succeeds in this goal is affected by the number of oestrous females in the group.
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When two or more females are in oestrus at the same time, the dominant male is unable
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to mate guard all of them effectively, thus providing an opportunity for subordinate
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males to mate. The model therefore makes predictions for the distribution of matings
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within groups, with the dominant male obtaining the largest share, and subordinates
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obtaining lesser amounts in proportion to their ranks.
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Empirical studies provide evidence for the dominant male’s advantages in both
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mating (Cowlishaw and Dunbar, 1991; Bulger, 1993; Ellis 1995; Alberts et al., 2003;
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Kutsukake and Nunn 2006) and paternity success (van Noordwijk and van Schaik 2004).
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In addition, some studies have investigated the effect of oestrous synchrony on the
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distribution of matings, reproductive success and the number of males in a group (e.g.,
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Bulger, 1993; Paul 1997; Nunn 1999a; Soltis et al. 2001; Takahashi 2004; van
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Noordwijk and van Schaik 2004; Boesch et al 2006; Alberts et al 2006). In general,
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these studies have shown that when more females are in oestrus, the ability of a
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dominant male to control access to females is more limited. The effect of oestrous
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synchrony has also been demonstrated in studies of non-primates (e.g., domestic cats,
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Felis catus: Say et al. 2001).
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The POA model has contributed greatly to primate research, but studies on
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primates have produced variable results (Dunbar 1988; Cowlishaw and Dunbar 1991;
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Bulger 1993; van Noordwijk and van Schaik 2004; Kutsukake and Nunn 2006).
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some cases, researchers have uncovered the biological reasons for departures from the
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POA model. For example, mate choice by females also can impact the distribution of
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reproduction in ways that differ from predictions of POA (Dunbar 1988; Soltis 2004).
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Females may confuse paternity by mating promiscuously and concealing ovulation –
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both of which should decrease skew – or females may increase skew by copulating with
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the dominant male during periods in which the probability of fertilization is high (van
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Schaik et al. 1999, 2000; Nunn 1999b; van Noordwijk and van Schaik 2004).
In
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Some researchers have incorporated the effect of the number of males in
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evaluating the POA model (e.g., Alberts et al. 2003; 2006; Boesch et al. 2006), based on
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the reasoning that it should be more difficult for a dominant male to monopolize
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females when there are more males in the group who are competing for females
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(Cowlishaw and Dunbar 1991). Our comparative work – discussed below – provides
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evidence for this effect in analyses that control for phylogeny, suggesting that male
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number is the primary factor that affects skew in social primates.
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of males was not explicitly considered by Altmann (1962), here we call this framework
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the extended-POA model, in order to separate it from the original POA model.
Because the number
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The POA and skew models are not fundamentally different in their goals of
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explaining the distribution of reproduction within groups. Relative to the POA model,
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however, the reproductive skew framework provides a richer set of variables to consider,
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potentially explaining more variation in male mating success. For example, skew
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models take into account the possibilities for males to leave the group and either attempt
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to breed on their own or join another group where their fitness would be greater, and
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thus also the need for dominant males to provide staying incentives. The concession
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model from the transactional framework also makes explicit assumptions about the
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degree of control that dominant males have over reproduction, with the tug-of-war
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models explicitly challenging the assumption of the dominant’s complete control of
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subordinate reproduction. Skew models make use of data on relationships among
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males, with greater skew predicted under the concession model when males are more
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closely related. In addition to male reproductive success, they can be applied to
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investigate female reproductive success.
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Testing the reproductive skew frameworks
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Evaluating whether a particular skew model applies to a species requires
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information on multiple parameters. Quantification of these parameters is difficult in
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any species, including primates.
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studies of skew, such as in Hymenoptera, are difficult or unethical to attempt in primates,
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in part because most primates have long lifespans and many are highly threatened. Here
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we discuss two approaches: first to investigate the assumptions of different skew models
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(Johnstone 2000; Magrath et al 2004), and second to test specific predictions in
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observational and comparative studies.
Moreover, experiments common in other empirical
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Testing assumptions of different skew models
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The first assumption of the transactional framework is that the presence of
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subordinates increases productivity and the fitness benefits of the dominant individual.
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Positive relationships between male number and group productivity (or efficiency of
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defense against extra-group males) have been reported in male primates (Wrangham
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1999; Treves 2001). In wild chimpanzees, for example, intergroup aggression is mainly
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conducted by males (Wrangham 1999), and the number of offspring and probability of
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infant survival increases with the number of males (Boesch et al. 2006). This pattern
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could occur through the combined effects of attracting females to the group and better
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defense of the territory or offspring.
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documented that a decrease in the number of males in a small group, possibly caused by
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intergroup killing by the larger neighboring group, resulted in the transfer of females to
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the larger group (Nishida et al., 1985). Thus, this assumption that subordinates provide
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fitness benefits and higher group productivity could be met in species where males
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defend a territory or a group of females, and in other situations in which dominant
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males benefit from membership in multimale groups.
In another population, at Mahale, researchers
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A key assumption of the concession model within the transactional framework
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is that the dominant individual has complete control over reproduction by subordinates.
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Field studies provide weak support for this assumption. In most species of social
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primates, for example, the presence of a dominant individual does not suppress the
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reproductive states of subordinates (see Carlson and Young, this volume), and complete
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control must be difficult if there are too many rivals in a group. A dominant male can
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often interrupt mating by subordinates, but in many cases he is ineffective in completely
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preventing copulations by subordinate males (Soltis 2004). Various studies have further
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shown that the degree to which the alpha male succeeds in reproduction decreases as the
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number of rivals increases (van Noordwijk and van Schaik 2004). Finally, complete
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control should be especially difficult in species living in fission-fusion societies
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(Dunbar 1988), where subdivision of the group into foraging parties should make it
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more difficult for males to monitor mating attempts by other males. These species
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include chimpanzees (Pan troglodytes), bonobos (Pan paniscus) and spider monkeys
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(Ateles spp.).
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An important assumption of the compromise framework is that group
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productivity decreases as a result of competition between the dominant and subordinate.
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Infanticide by males is widely observed in primates (van Schaik and Janson 2001) and
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reduces group productivity. Correlational studies showed that groups with multiple
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males are less productive than single-male groups (black-and-white colobus, Colobus
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guereza: Dunbar 1987; Hanuman langurs, Semnopithecus entellus: Srivastava and
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Dunbar, 1996), although the behavioral mechanism for how the presence of multiple
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males affects male-male competition – and ultimately group productivity – is largely
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unknown. Moreover, some studies reported positive effects of subordinate males on
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group productivity (red howler monkeys, Alouatta seniculus: Crockett & Janson 2000;
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mountain gorillas, Gorilla gorilla: Watts 2000). These results suggest that the links
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between the number of subordinate males in a group and competition among males or
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group productivity is not universal. Future studies should test this assumption more
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broadly across species, including species living in multimale groups.
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This brief summary suggests that males are unlikely to have complete control
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over reproduction (as assumed in the concession model), and that group productivity
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can either increase or decrease with the number of males and the intensity of
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competitions among dominant and subordinate males (as predicted by transactional and
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compromise frameworks, respectively).
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appropriate for some species but not others, and quantitative testing of the assumptions
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could help to disentangle which models should be investigated in different species.
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Other models (and extensions of these models, such as social queuing or models that
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incorporate multiple individuals) make additional assumptions (Kokko & Johnstone,
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1999; Johnstone et al 1999; Reeve and Emlen 2000) that would be worth investigating
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as skew frameworks are applied to primate mating systems.
Thus, a particular skew model could be
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Testing specific predictions of skew models
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Reproductive skew models also make different predictions for the effects of
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demographic variables (number of males and females), female reproductive traits
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(oestrous synchrony), and relatedness among males on patterns of reproductive skew
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(Table 1). The tug-of-war model and the extended POA model predict that skew
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decreases as the number of males in a group increases, based on the reasoning that it
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will be difficult for a dominant male to control or monitor reproductive attempts by
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other males when more rivals are present (Cowlishaw and Dunbar 1991; van Noordwijk
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and van Schaik 2004). Similarly, increases in the number of females in a group should
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decrease skew if this provides more mating opportunities for subordinate males
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(Altmann 1962; Cowlishaw and Dunbar 1991; Bulger 1993; van Noordwijk and van
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Schaik 2004).
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Another prediction from the tug-of-war model and the POA model involve
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female oestrous overlap (Table 1). Increased oestrous overlap, which results from a
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long mating season, a long oestrous duration, or socially mediated synchrony, should
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make it more difficult for a dominant male to monopolize a receptive female, thus
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decreasing skew among males (Ridley 1986; Cowlishaw and Dunbar 1991; Paul 1997;
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Shuster and Wade 2003).
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causing dominant males to guard females over only part of their cycles (Packer 1979;
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Bercovitch 1983; Alberts et al. 1996). Few mathematical or empirical models of
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reproductive skew among males have considered the influence of female reproduction
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and behavior; exceptions include the female control model, developed by Cant and
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Reeve (2002), and studies of acorn woodpeckers (Melanerpes formicivorus, Haydock
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and Koenig 2002), brown jays (Cyanocorax morio, Williams 2004), and some studies of
Similar effects can arise if the costs of guarding are high,
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primates (e.g., Soltis et al. 2001; Charpentier et al 2005a; Boesch et al. 2006).
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of these exceptions involve female effects on male monopolization, and therefore
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address assumptions of the tug-of-war model. Because the primate socioecological
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model focuses explicitly on female reproductive strategies as influencing male
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behaviour (Dunbar 1988; Nunn 1999a; van Schaik et al. 1999), this is an area where
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primatology has the potential to contribute to further development of skew models.
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Many
Finally, the tug-of-war model predicts no relationship between male
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relatedness and skew (Table 1).
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circumstances in which males exert weaker control over close relatives (Reeve et al.
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1998). In some circumstances, for example, dominants could increase their inclusive
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fitness by exerting fewer restrictions on mating by related subordinates, thus generating
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a negative association between relatedness and skew.
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This relationship could even be negative in
The concession model predicts no association between demographic factors or
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oestrous synchrony and skew (Table 1).
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will impact patterns of skew, with high relatedness associated with high skew, due to the
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expectation that related subordinate males can receive their “staying incentive” in the
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form of inclusive fitness benefits (Keller and Reeve 1994; Johnstone 2000).
Instead, this model predicts that relatedness
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Case studies of the causes of reproductive skew
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Data on patterns of reproductive success are steadily growing in primates (van
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Noordwijk and van Schaik 2004), offering potential for investigating whether
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compromise or transactional frameworks are more appropriate for studying skew in
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male primates (Widdig et al. 2004; Setchell et al. 2005; Charpentier et al. 2005a;
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Bradley et al. 2005; Boesch et al. 2006).
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framework appears to offer a better fit for primate males, and the extended POA model
As reviewed below, the compromise
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may be equally powerful in explaining patterns of reproductive skew among male
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primates. Even so, we should not let this blind us to the possibility that transactional
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frameworks could account for additional variation in male skew, particularly when
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males defend territories, as this is one way that group productivity can increase with the
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number of males (see above).
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In what follows, we review four case studies of male skew in
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multimale-multifemale primate groups (Table 2).
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exhaustive; rather we use selected examples to reveal how skew theory provides new
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insights to variation in male reproductive success in primates.
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section with a summary, and then present comparative evidence in the following
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section.
These examples are not meant to be
We conclude this
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Rhesus macaques
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In rhesus macaques, males disperse from their natal groups, while females
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remain in the group in which they were born. Widdig et al (2004) investigated
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reproductive skew in a population on Cayo Santiago and found that the top-sire fathered
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between 19 and 30% of the offspring per year over a six-year period, while 69 to 79%
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of males sired no infants at all. In terms of specific tests, the authors showed that (1)
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males exhibited significant variation in skew, with a measure of skew (the B-index,
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Nonacs 2000) significantly different from zero in most tests; (2) the B index was not
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significantly associated with either average pairwise relatedness among males nor
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female synchrony (estimated indirectly from births); (3) heterozygosity of MHC genes
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predicted male reproductive success, highlighting the potential role of female choice.
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The authors concluded that their results support the compromise framework, as the
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concession model would predict few effects of female choice, a lower level of
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relatedness among breeders, and stronger control of group reproduction by resident
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(dominant) males.
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Mandrill In the wild, mandrills (Mandrillus sphinx) live in groups of up to several
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hundred individuals (Abernethy et al 2002). Behaviour in these groups has not been
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investigated, largely due to the difficulties of habituating and observing behavior of
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mandrills in their natural habitat. Important information on this species has been
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provided by research from a semi-free-ranging captive colony (CIRMF Mandrill
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Colony, Gabon). In this population, only the alpha male exhibits the distinctive
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secondary sexual traits (e.g., bright colour of the face) characteristic of this extremely
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sexually dimorphic species. Although multiple males are present in the colony,
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paternity analyses have shown that the alpha male fathers 69% of offspring, indicating
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extreme reproductive skew among males (Setchell et al 2005).
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Two studies have investigated different aspects of reproductive skew in this
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colony. Although these authors studied the same groups, some results differed between
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the studies, in part due to differences in the specific aims of each study, in samples
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collected and variables that were analyzed, and in statistical approaches. In one of these
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studies, Setchell et al (2005) investigated deviations in the alpha male’s reproductive
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success from the expected value based on the POA model. The authors showed that
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departures from the POA model increased as the number of males in a group increased
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(Table 2), which fits predictions from the extended POA and the tug-of-war models. By
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comparison, Charpentier et al. (2005a) studied factors affecting the failure of alpha
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males to sire offspring.
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oestrous synchrony, relatedness between the dominant male and females, and the
These authors reported that relatedness among males, female
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number of males affected paternity of the dominant male. Specifically, (1) the dominant
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male’s reproduction decreased as relatedness among males increased; (2) oestrous
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overlap decreased reproduction by the dominant male; (3) relatedness between the
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dominant male and females negatively affected reproduction by the alpha male.
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Although the behavioural mechanism for this result is unknown, incest avoidance may
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have played a role because the degree of heterozygosity correlated positively with
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individual reproductive success (Charpentier et al. 2005b). (4) Counter to predictions
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from the tug of war model and patterns found by Setchell et al. (2005) and more
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generally in primates (van Noordwijk and van Schaik 2004; Kutsukake and Nunn 2006),
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the number of males correlated positively with the proportion of offspring that the alpha
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male sires (Charpentier et al, 2005a). To explain this result, Charpentier et al. (2005a)
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suggested that competition among subordinates increased as the number of males
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increases, deflecting competition away from the dominant male.
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Although the effect of male number differed between the studies, both Setchell
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et al. (2005) and Charpentier et al (2005a) concluded that the limited control model best
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characterized this species; predictions of the concession model were never supported.
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Setchell et al. (2005) also noted that conditions in wild mandrills might produce weaker
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patterns of control than those found in the colony studied by these authors.
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Mountain gorilla
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There is variation in the number of males in groups of mountain gorillas
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(Gorilla gorilla) in the Virunga mountains, with multimale groups representing 40% of
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the groups in the population (Robbins et al 2001). Female reproductive cycles are short
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and it is rare that the receptive periods of two or more females overlap.
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overlap should tend to enable the dominant male to monopolize reproduction within a
The lack of
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group. However, paternity analyses have shown that subordinates also reproduce to
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some extent (about 15%), suggesting that the reproductive skew (estimated by the B
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index) is high but not complete (Bradley et al 2005).
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In another study, Robbins and Robbins (2005) used an individual-based
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simulation model with demographic parameters from the same population studied by
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Bradley et al. (2005) to investigate the expected reproductive success of subordinates
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that remain in their group.
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subordinate more than dispersing. However, the model revealed that the dominant
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does not benefit from retention of subordinates, suggesting that dominant males do not
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concede reproduction. Thus, both Bradley et al. (2005) and Robbins and Robbins (2005)
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concluded that reproductive skew in this population corresponds better to predictions
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from the tug-of-war model than the concession model.
The model revealed that remaining in a group benefits a
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Chimpanzees
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In chimpanzees, males remain in their natal group and exhibit a high degree of
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a fission-fusion sociality. Females develop sexual swellings when they are in oestrus,
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with synchronous oestrous relatively common. The dominant male has higher
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reproductive success, but subordinate males also reproduce (Constable et al. 2001).
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Boesch et al (2006) investigated paternity in chimpanzees of Taï National Park in Cote
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d’Ivoire using long-term records.
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the alpha male decreased as the number of males increased and when female oestrous
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overlap increased.
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extended POA model and the tug-of-war model.
These results therefore agree with predictions from both the
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They found that the proportion of reproduction by
Summary of Case Studies
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Overall, these studies suggest that limited control is a characteristic of male
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behaviour in primates (Table 2) and that the tug-of-war model or the extended POA
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model can explain variation in skew among male primates. However, these studies do
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not completely reject the concession model for the following reasons. First, empirical
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studies mainly tested predictions from mathematical models that were designed for
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systems other than primates, often assuming that the group contains only two
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individuals – a dominant and a subordinate. In contrast, mathematical models that
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incorporate more realistic parameters, such as three or more group members or the
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possibility of social queuing by subordinates, predict a reduced necessity of offering
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incentives by a dominant individual to a subordinate (in particular to a unrelated
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subordinate) relative to the two-player models (Kokko & Johnstone, 1999; Ragsdale
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1999; Johnstone et al 1999; Reeve and Emlen 2000; Reeve and Shen, 2006). This makes
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it difficult to draw firm predictions for how relatedness should correlate with patterns of
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skew. Second, no studies in primates have succeeded in accurately quantifying
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parameters that are necessary to test the skew model, in large part because it is difficult
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to conduct experimental manipulations in primates. Crucially, these parameters include
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the probability of solitary reproduction by subordinates, fitness benefit of the dominant
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male when there are no subordinate males, and the effects of subordinate males’
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presence on group productivity. Finally, the concession and tug-of-war models are not
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mutually exclusive, and can in fact coexist within a single framework (Johnstone 2000;
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Reeve and Shen, 2006).
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Phylogenetic comparative analyses
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Skew models have been regarded as a unifying framework for understanding
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the diversity of social systems seen in animals (Keller and Reeve 1994; Sherman et al.
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1995), but surprisingly few studies have examined broad evolutionary patterns of skew
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within one clade of either vertebrates or invertebrates (Boomsma and Sundström 1998;
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Duffy et al. 2000; Faulkes et al. 1997). Such comparative perspectives are important in
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reproductive skew research for at least four reasons.
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a means to understand the factors generating broad evolutionary patterns of skew
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(Nonacs 2000) and therefore can assess the generality of a pattern across species,
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leading to greater unification of models of social evolution. Second, comparative
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approaches offer an opportunity to test assumptions and predictions of skew models
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from an evolutionary perspective, and they can be used to test assumptions or
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predictions of skew models. Third, by identifying differences among species,
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comparative results can point to new variables to investigate in future field or laboratory
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research. Finally, comparative research can be used to generate new hypotheses, which
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can then be tested in the field or laboratory, or refined through theoretical models.
First, comparative studies provide
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In previous primate research, cross-species comparisons have been conducted
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to examine the effects of seasonality on variance in mating or reproductive success
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(Cowlishaw and Dunbar 1991; Paul 1997). We conducted a phylogenetic comparative
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analysis on the determinants of “mating” skew in male primates, based on a database of
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species in multimale primate groups (in total from 84 studies representing 31 species in
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17 genera, Kutsukake and Nunn 2006). Since few studies have investigated the
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distribution of paternity for a sufficient number of primate species, we investigated
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mating distribution. While many studies have shown that mating frequency predicts
391
reproductive success (e.g., Smith 1981; Pope 1990; Ohsawa et al. 1993; de Ruiter et al.
392
1994; Paul and Kuester 1996; Soltis et al. 1997; Alberts et al. 2006), other studies failed
393
to find such links (e.g., Curie-Cohen et al. 1983; Shively and Smith 1985; Inoue et al.
394
1991, 1993), possibly because many matings in primates are likely to be
Kutsukake and Nunn: reproductive skew in male primates
17
395
non-reproductive (Soltis 2004). To deal with this problem, we used data that are most
396
tightly linked to male reproductive success whenever possible; specifically, we
397
preferred data on ejaculation frequency more than copulation frequencies, and
398
copulation data at times when conception was most likely to take place (Kutsukake and
399
Nunn 2006). Genetic information on actual reproduction in groups would clarify these
400
issues and allow skew to be examined more directly, but such data are not yet
401
sufficiently available to test the predictions in a comparative context.
402
In quantifying the magnitude of mating skew, we focus here on results using
403
the “maximum mating proportion” (Bulger 1993), which is the proportion of mating by
404
the most successful male.
405
(Nonacs, 2000) and lambda (Kokko and Lindström, 1997). We investigated the effects
406
of three variables: demographic factors (the number of males or females in a group),
407
female reproductive factors that are related to the difficulties of monopolizing oestrous
408
females (i.e., duration of the breeding season, duration of oestrus, and measures of
409
oestrous overlap), and male dispersal pattern (categorized as male philopatry or male
410
dispersal). Regarding male dispersal pattern, the concession model predicts high skew
411
in male philopatric species relative to species in which males disperse because there is
412
(1) a high probability that a dominant male has a brother within a group and (2) a lower
413
probability that subordinates will disperse. Taken together, these factors reduce the
414
need for the dominant male to provide a staying incentive.
We also examined other skew indices, including the B index
415
The main results of our study (Kutsukake and Nunn 2006) can be summarized
416
as follows. First, based on Nonac’s B, mating was significantly skewed among males in
417
75.4% of cases (43 / 57 cases), and the alpha male or resident male tended to mate more
418
frequently. Second, using the independent contrasts method (Felsenstein 1985) and
419
stepwise multiple regression, we found that only male number correlated with mating
Kutsukake and Nunn: reproductive skew in male primates
18
420
skew (P<0.001), with the proportion of mating by the most successful male falling as
421
the number of males in a group increases (Fig. 2). Finally, neither female reproductive
422
proxies nor male dispersal pattern affected mating skew. Overall, these results are most
423
consistent with the tug-of-war model and partially consistent with the extended POA
424
model (in the sense that the number of males negatively affected skew).
425
This result raises the possibility that the effects of oestrous synchrony are not
426
universal to all primate species, its effects are weak, or synchrony is difficult to quantify,
427
all of which would limit our ability to detect a significant association in comparative
428
analyses given existing data. Although the intensity of the correlation between
429
dominance rank and reproductive success was affected by seasonality (Paul 1997), up to
430
now, few studies have investigated paternity among males in relation to oestrous
431
synchrony (Setchell et al 2005; Charpentier et al, 2005a; Boesch et al 2006).
432
One could argue that the concession model also predicts that mating skew
433
should decrease as the number of males increases, specifically if the dominant male
434
needs to pay staying incentives to each subordinate male. However, we also found a
435
similar negative relationship in an intraspecific analysis of wild chimpanzees
436
(Kutsukake and Nunn 2006). The negative relationship is not expected in a male
437
philopatric species, such as the chimpanzee, because subordinate males have few
438
opportunities for reproduction outside of their natal communities, and therefore do not
439
need an incentive to stay.
440
Even with this intraspecific analysis, however, we cannot firmly reject the
441
concession model.
442
and mating skew can also be explained by the concession model because reproductive
443
skew may decrease when the power difference between a dominant and subordinate is
444
small (e.g., in a group with many males; Cowlishaw and Dunbar 1991); therefore, the
For example, a negative relationship between the number of males
19
Kutsukake and Nunn: reproductive skew in male primates
445
dominant may concede the reproduction as a ‘peaceful’ incentive to avoid a risky fight
446
with powerful rival males (Reeve and Ratnieks 1993). Indeed, the power differences
447
may be smaller in a group with a large number of males because one would expect that
448
males are, on average, more similar in age (and therefore competitive ability). This idea
449
needs further testing, but this example highlights the difficulty of testing between the
450
different skew models, even in well-studied mammalian species.
451
In addition, our comparative study does not reject the possibility that the
452
concession model applies to particular primate species, even if it is not a general
453
explanation for patterns of skew across primates. As is shown by a recent synthetic
454
model, the transactional framework and compromise framework are not mutually
455
exclusive (Johnstone 2000; Reeve and Shen 2006). So, one model may fit one species
456
but not others, or in certain demographic or ecological situations but not in others within
457
a species. For example, even within a species, the dominant male may be able to exert
458
complete control in a small group in which there is only one subordinate, but not in a
459
large group with multiple subordinates. This possibility can be tested by investigating
460
how the effects of relatedness on reproductive skew vary according to the number of
461
subordinate males in groups.
462
Although our approach focused on males in short time intervals, such as a
463
single breeding season, this approach can be used to examine complex life history
464
trajectories (patterns of lifetime reproductive success).
465
could be applied to both sexes.
466
primates can be estimated using long-term data. Finally, it would be interesting to apply
467
this approach to other clades in which data on reproduction and phylogeny are widely
468
available, such as birds, social insects, and in other well-studied mammalian groups,
469
such as rodents, ungulates and carnivores.
In addition, this approach
For example, reproductive success among female
20
Kutsukake and Nunn: reproductive skew in male primates
470 471
Applying comparative approaches to other biological systems
472
Comparative tests can focus on either the predictions or the assumptions of
473
skew models, and testing is possible if researchers have quantitative data for the
474
distribution of reproduction or mating among group males.
475
stimulate further comparative research in other clades of animals, we list several
476
methodological practices for conducting comparative tests of predictions related to
477
reproductive skew models.
Here, in an attempt to
478
1) Carefully choose the hypotheses, predictions or assumptions to be tested.
479
Within the framework of the models and the biology of the organisms, the researcher
480
needs to consider alternative explanations and how different parameters might influence
481
the predictions of a skew model.
482
that are specific to the study animals because some parameters are difficult to quantify
483
in some clades.
It is also important to incorporate the characteristics
484
2) Collect data on mating or reproductive skew and other important variables
485
such as group composition (e.g., number of males and females), relatedness, female
486
behaviors, and reproductive biology. Data on reproduction are available in many
487
non-primates (e.g., Ellis 1995), which could be used for comparative analyses. It is also
488
important to obtain a phylogeny for the group of species being studied. “Supertrees”
489
and other large-scale, dated phylogenies are now available for many species
490
(Bininda-Emonds 2004), making this process easier than in the past.
491
3) Quantify the distribution of reproduction using several skew proxies
492
(Nonacs 2003). Many studies will not provide these measures directly, and may not
493
even provide information for the comparative biologist to calculate the measures.
494
Thus, it might be necessary to use a simple index that maximizes sample size (in terms
Kutsukake and Nunn: reproductive skew in male primates
495
21
of the number of species).
496
4) Test the hypotheses using phylogenetic comparative methods, such as
497
independent contrasts (Felsenstein 1985; Harvey and Pagel 1991; Nunn and Barton
498
2001).
499
and Garland 2002), to test the statistical and evolutionary assumptions, and to determine
500
whether the results are robust to alternative assumptions.
It is important to check whether the data show phylogenetic signal (Blomberg
501 502
CONSEQUENCES OF REPORDUCTIVE SKEW
503
Previous studies mainly investigated the causes of the skew and tested specific
504
models. An important new direction in skew research is to consider the consequences of
505
reproductive skew on other biological traits, including social structure and individual
506
social strategies (Fig. 1; Heinze 1995; Widdig et al. 2001; Cant & English 2006). For
507
example, in some systems, the number of breeders and characteristics of the breeding
508
queue could influence optimal group size (Cant and English 2006). With the goal of
509
developing new questions for future studies, we briefly discuss two consequences of
510
reproductive skew in male primates: effects on within-group relatedness and the spread
511
of disease.
512 513
Reproductive skew and within-group relatedness
514
In species characterized by high skew, infants born in a short period are more
515
likely to be paternally related. For example, Widdig et al. (2004) found that in a
516
high-skew rhesus macaque troop at Cayo Santiago, 74% of the infants had at least one
517
paternal sibling in the group, and individuals had almost four times as many paternal as
518
maternal siblings.
519
fathered by different males, thus tending to reduce the level of relatedness at the group
In contrast, infants in low skew societies are more likely to be
Kutsukake and Nunn: reproductive skew in male primates
22
520
level. The paternal relatedness among group members should have a major impact on a
521
wide range of social behaviours, including affiliation, cooperation, competition and
522
mate choice (Hamilton 1964, Chapais and Berman, 2003).
523
Several studies have suggested that individuals recognize paternal relationships
524
and adjust their behaviour accordingly. For example, skew is high in male western
525
gorillas, and the silverbacks of different groups are closely related (Bradley et al. 2004).
526
This result may explain the occurrence of non-agonistic encounters between groups
527
observed in this species, which might be unexpected in such a sexually dimorphic
528
species in which male-male competition is likely to be especially intense. Paternal
529
half-siblings are more affiliative with one another than unrelated individuals in rhesus
530
macaques (Widdig et al. 2001) and in savanna baboons (Smith et al. 2003; see also Silk
531
et al. 2006). Also in baboons, paternal half-siblings showed less affiliative and sexual
532
behaviour during consortships than did unrelated pairs (Alberts 1999). As a final
533
example, infants were supported by a biological father (Buchan et al. 2003) or were not
534
the target of infanticide by the biological father in species living in multimale groups
535
(Borris et al 1999a,b; Soltis et al. 2000).
536
When reproductive skew is high and the dominant male’s tenure is long enough
537
for his female offspring to mature sexually, it could be adaptive for the dominant male
538
to discriminate the paternity of the offspring and avoid mating with his daughters. In
539
wild white-faced capuchin monkeys (Cebus capucinus), for example, the probability of
540
reproduction by the alpha male varied with whether or not a female was a daughter of
541
the alpha male, with a lower probability of reproduction between the alpha male and his
542
daughter (Muniz et al. 2006). It would be interesting to investigate whether such incest
543
avoidance mechanisms are common in primates, because some studies have found
544
evidence for incest avoidance (Table 2), while others have not (Constable et al. 2001). If
Kutsukake and Nunn: reproductive skew in male primates
23
545
incest avoidance is an important selective force, strong skew combined with long male
546
tenures could reduce future opportunity for the alpha male to reproduce within a group,
547
thus creating an incentive for secondary dispersal.
548
As discussed above, the degree to which paternal relatedness affects individual
549
behaviour and social structure represent important areas for future research. In addition,
550
it will be important to uncover the proximate mechanisms responsible for identifying
551
paternal kin (Rendall 2004).
552
of their information on the monopolization of receptive females as a proximate cue to
553
assess the probability that they are fathers of the offspring. Similarly, for human
554
observers, it may be possible to estimate the magnitude of reproductive skew a
555
posteriori from the genetic relatedness among infants and juveniles in a group.
It is possible, for example, that dominant males make use
556 557
Reproductive skew and the spread of infectious disease
558
Reproductive skew also can have consequences for patterns of social contact
559
within social units, thus impacting the spread of disease within primate groups (Nunn
560
and Altizer 2006).
561
example, one or a few males will gain access to the vast majority of mating
562
opportunities.
563
fight to improve or maintain their dominance ranks. This fighting causes wounds for
564
males by biting and scratching and can result in the spread of disease, as demonstrated
565
in the case of retroviruses (SIV and STLV) in a semi-free-ranging colony of mandrills
566
(Nerrienet et al. 1998). In addition to being involved in male intrasexual competition,
567
a high-ranking male in a high skew society also has better access to mates, resulting in
568
higher rates of sexual contact.
569
sexually transmitted diseases (STDs; Graves and Duvall 1995), potentially even
In a high skew primate group under the tug-of-war model, for
Thus, there is likely to be intense competition among males as they
Thus, such a male can act as a contact point for
24
Kutsukake and Nunn: reproductive skew in male primates
570
selecting for reduced skew (Thrall et al. 2000; Kokko et al. 2002). If a female is
571
already infected with an STD at the time that a new male rises in rank, this male is
572
likely to become infected shortly after he attains high rank; he can thus serve as the
573
source of infection for the many females that he mates with during his tenure as the
574
alpha male.
575
A number of models have investigated the epidemiology of STDs in both human
576
(Anderson and May 1991) and non-human systems (Thrall et al. 1997; Boots and Knell
577
2002; Kokko et al. 2002).
578
Thrall et al. (2000) developed an individual based model to explore how variance in
579
mating success, patterns of female dispersal and mortality rates of both sexes influence
580
the spread of STDs.
581
males and females, every male would have one female if there was no skew (equivalent
582
to monogamy); each additional female assigned to a male means one less female for
583
another male, resulting in increased reproductive skew.
584
the prevalence of STDs is higher as the degree of polygyny (reproductive skew)
585
increases.
In the context of variance in male mating skew, for example,
Given that the simulated population had an equal number of
The simulations revealed that
586
A challenge in applying these concepts to generate testable predictions is that
587
low skew in multimale-multifemale primates groups can also favour the spread of an
588
STD.
589
higher rate of mating with more males throughout the female’s cycle, possibly as a
590
strategy to reduce the risk of infanticide (Hrdy and Whitten 1987; van Schaik et al.
591
1999).
592
(Anderson and May 1991).
593
even higher levels than revealed by models of STD spread under skew, such as the
594
Thrall et al. (2000) study, especially if most subordinates have some mating success.
Thus, if males have relatively equal access to females, this could result in a
And of course, increased promiscuity should increase the spread of an STD This promiscuity is likely to increase the prevalence to
Kutsukake and Nunn: reproductive skew in male primates
25
595
Thrall et al.’s (2000) STD model provides a way out of this conundrum, however,
596
because output from the model also predicts a higher prevalence of infection in females
597
than in males as reproductive skew increases, i.e., a sex difference is predicted. Kokko
598
et al. (2002), in a different modeling approach, confirmed that female choice for a
599
particular (presumably high-ranking) male can also lead to higher prevalence of
600
infection in females.
601
only high prevalence (relative to, say, monogamy); increasing skew should also produce
602
a sex difference in the prevalence of an STD, with higher prevalence in females than in
603
males.
604
(Nunn and Altizer 2004).
605
correlate with skew and other variables that influence the establishment of an STD,
606
including mortality rates, dispersal, and differences in transmission probabilities
607
between the sexes (e.g., with females potentially being more susceptible to an STD).
608
In addition, it will be important to bring queuing or life history (age dependency) into
609
the STD models, because if most individual males have some mating opportunities over
610
their lifetimes, the difference in STD exposure between the sexes may become more
611
narrow.
Thus, a critical prediction is that higher skew will produce not
This prediction has been tested and supported using data on STDs in primates A next step is to examine whether sex-differences also
612 613
CONCLUSIONS
614
This chapter discussed the causes and consequences of reproductive skew in
615
male primates. Several studies have investigated the assumptions of the transactional
616
framework in primates in order to test skew theory. Empirical studies showed that the
617
tug-of-war model may explain the pattern of skew among males better than the
618
concession model. Our comparative studies revealed a negative association between the
619
number of males in a group and skew, which agrees with previous findings in primates
Kutsukake and Nunn: reproductive skew in male primates
26
620
(Setchell et al. 2005; Boesch et al. 2006; reviewed in van Noordwijk and van Schaik
621
2004) and also agrees with predictions from the tug-of-war model. Therefore, we
622
tentatively conclude that incomplete control is a general characteristic of male primates,
623
but more studies are needed to test the assumptions or predictions of the concession
624
model.
625
The priority-of-access (POA) model (Altmann 1962) has had a major impact in
626
studies of male reproductive success in primates.
627
oestrous overlap on the distribution of reproduction among males in multi-male
628
multi-female groups, including non-primates. A major conclusion of our chapter is
629
that the POA model – especially an extended version that incorporates the number of
630
males – is almost indistinguishable from the compromise framework.
631
particularly true with regard to the predictions, where only one prediction differs (Table
632
1).
633
bottle.” This would be misleading, however, as the skew framework is actually much
634
broader than the previous POA model. For example, it builds significantly on POA by
635
encapsulating factors involving relatedness, breeding opportunities and costs of
636
dispersal.
This model highlighted the effect of
This is
It might therefore seem that the skew framework represents “new wine in an old
637
Several challenges remain for the future. First, the present mathematical
638
models of reproductive skew are not designed to apply to primate social systems. In
639
particular, it would be worthwhile to develop skew models that incorporate three or
640
more players (Johnstone et al 1999; Reeve and Emlen 2000), social queuing (Kokko &
641
Johnstone, 1999; Ragsdale 1999; Mesterton-Gibbons et al. 2006), female influences
642
such as incest avoidance (Cant & Reeve, 2002; Johnstone, 2000), and female choice for
643
males with particular biological traits (“good genes” or high dominance rank). Recent
644
mathematical models in which one individual adjusts behaviour in response to the
Kutsukake and Nunn: reproductive skew in male primates
27
645
behaviour of the other individual (negotiation game: McNamara et al. 1999; Cant and
646
Shen 2006) may be more appropriate in primates, because social interactions in
647
primates change temporally according to the strategy of opponents. Also, an
648
individual-based model based on empirical demographic parameters would be a useful
649
tool for generating more refined predictions for patterns of skew in primates (e.g.,
650
Robbins and Robbins 2005).
651
Second, no empirical studies of primates have successfully estimated the
652
parameters that are needed to distinguish among the different skew models. These
653
parameters include the links between competition within groups and group productivity
654
and ecological constraint that determines the probability of solitary reproduction. This
655
may represent a limitation of skew theory, with very few predictions distinguishing the
656
different models.
657
composition, would help to more formally test skew theory in primates.
658
could be conducted in semi-free-ranging groups.
Nonetheless, experimental studies, including manipulating group Such tests
659
Third, most of the studies in primates estimate skew in a relatively short time
660
period. Thus, it is unknown how short-term skew is associated with long-term (i.e.,
661
lifespan) reproductive success (Altmann et al. 1996).
662
The consequences of reproductive skew have been largely unexplored, yet
663
these topics offer great opportunities for future research in primates. Irrespective of
664
causes of skew, how a given magnitude of skew affects social structure, individual
665
decision-making, and other biological traits that relate to reproduction is a promising
666
area for both empirical and theoretical research. For example, investigating the
667
relationship between skew and the prevalence of STDs could have important
668
implications for conservation biology, given that STDs often cause sterility (Canfield et
669
al. 1991; Lockhart et al. 1996).
Kutsukake and Nunn: reproductive skew in male primates
28
670
In conclusion, bringing the skew paradigm to primatology may yield new
671
perspectives for understanding primate behaviour, specifically by integrating more
672
diverse factors that are relevant to male and female decisions on group formation,
673
interactions within groups, and reproductive strategies. Thus, skew models could play a
674
major role in developing an integrative model of primate socioecology. Key future
675
directions will involve developing skew models that are more appropriate for primates,
676
collecting data to test the assumptions and predictions of these models, and
677
investigating the consequences of reproductive skew for primate behavior. Moreover, a
678
primate perspective on reproductive skew should help to ground models of skew more
679
firmly, specifically in the context of multiple competitors and queuing within groups.
680 681
SUMMARY
682
In this chapter, we considered the causes and consequences of skew in male
683
primates. Although our understanding of the causes of skew is still in its infancy,
684
empirical studies thus far support the compromise framework (tug-of-war model) rather
685
than the concession model.
686
the priority of access (POA) model makes predictions that are very similar to the
687
compromise framework, but that skew models expand significantly on the POA model
688
by including additional factors that relate to patterns of reproduction within groups. Our
689
phylogenetic comparative analyses on mating skew in male primates also provided
690
supporting data for the tug-of-war model because mating skew decreased as the number
691
of males increased, suggesting that monopolization of females becomes more difficult
692
when there are more rivals. However, there have been no studies that represent strong
693
tests of skew models, possibly because of difficulties in estimating parameters that are
694
necessary for quantitative analyses. Future research could help to clarify the causes of
Our assessment of the different models also suggests that
Kutsukake and Nunn: reproductive skew in male primates
29
695
skew, including development of mathematical models that are more suitable to primate
696
societies, empirical studies based on paternity tests, and comparative approaches to
697
investigate interspecific patterns of skew in other biological systems.
698
Previous studies commonly investigated the causes of skew, but fewer have
699
considered the consequences of skew on other physiological and social parameters. We
700
discussed two examples of how the magnitude of reproductive skew affects other
701
biological traits of interest to behavioral ecologists, focusing on within-group
702
relatedness and sexual transmitted diseases. Of these, it appears that effects on
703
within-group relatedness could have the largest effects on patterns of primate sociality.
704
The introduction of reproductive skew models into primate research is likely to provide
705
new insights to primate social and reproductive behaviour in the future, while a primate
706
perspective is likely to stimulate new skew models.
707 708
ACKNOWLEDGEMENTS
709
We thank Reinmar Hager and Clara Jones for their invitation to contribute this
710
chapter, and we thank Mike Cant, Sarah Hodge, Kavita Isvaran, Jo Setchell and two
711
anonymous reviewers for helpful comments and discussion. This study was supported
712
by JSPS Research Fellowships, RIKEN Special Post-Doctoral Researchers Program,
713
financed by JSPS core-to-core program HOPE (to NK) and the Max Planck Society (to
714
CN).
715 716
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Kutsukake and Nunn: reproductive skew in male primates
1 2
Table 1. Predicted relationships between the reproductive skew and the number of males and females, oestrous overlap, and relatedness among males from three models Effects on reproductive skew The
The ‘extended’
priority-of-access
priority-of-access
model
model
The tug-of-war model
model
Number of males in group
No prediction
-
-
No prediction
Number of females in group
No prediction
No prediction
-
No prediction
-
-
-
No prediction
No prediction
No prediction
No prediction or -
+
Oestrous overlap Relatedness among males 3
Models
The concession
+: positive relationship between variable and degree of skew; -: negative relationship with skew.
44
Kutsukake and Nunn: reproductive skew in male primates
4
Table 2. Summary of empirical studies investigating reproductive skew in male primates Model
The
The
of
priority of
tug-of-
conces
Other
oestrous
access
access
war
sion
important
male
female
among males
overlap
model
model
model
model
factors
ns
Yes
No
Hetero-
Cayo Sandiago,
ns
Macaca mulatta
Puerto Rico
(but two most
(free-ranging
successful
provisioned)
males were related in two of five years)
colony, Gabon;
‘extended’
Relatedness
Rhesus macaque a
Mandrillus sphinx
priority
#
Study site, group
CIRMF mandrill
The
# Species
Mandrill b, c
The
zygosity
45
Kutsukake and Nunn: reproductive skew in male primates
(semi-free-ranging provisioned) Setchell et al. 2005
-
Charpentier et al.
+
-
-b
Yes
Yes
Yes
No
-
Yes
Partially
Yes
No
Yes f
2005a mountain gorilla c
Karisoke, Virunga,
Gorilla gorilla
Volcanoes National
ns
ns
+ in one (of
not
four) group
investigated,
Park, Rwanda
but overlap
(wild)
is unlikely
Chimpanzee d
Taï National Park in -
-
Pan troglodytes
Cote d’Ivoire (wild)
Comparative
-
ns
ns
analyses e (31 species) 5
+: positive relationship; -: negative relationship; ns: uncorrelated
ns
Yes
avoidance Yes
No
Yes
Yes
No
Partially
Yes
No
Yes f
Incest
Kutsukake and Nunn: reproductive skew in male primates
6
a: Widdig et al. 2004; b: controlled for the effect of oestrous overlap by calculating the deviance of observed data from expected value
7
from the priority-of-access model; c: Bradley et al. 2005; d: Boesch et al. 2006; e: Kutsukake and Nunn, 2006; f: “partial”
8
because the effect of oestrous overlap was not confirmed.
46
Kutsukake and Nunn: reproductive skew in male primates
47
1
Figure legends
2
Fig. 1. Scheme of the causes and consequences of reproductive skew discussed in this
3
chapter. Black arrows indicate the effects predicted from the compromise framework
4
(i.e., tug-of-war model), and the dashed arrows indicate the effects predicted from the
5
transactional framework (i.e., concession model).
6 7
Fig. 2. Phylogenetic comparative analyses on the relationship between male number in
8
a group and the maximum mating proportion (the proportion of mating by the most
9
successful male). For further details on these analyses, see Kutsukake and Nunn (2006).
10 11
Kutsukake and Nunn: reproductive skew in male primates
12
13
(Figure 1)
48
Kutsukake and Nunn: reproductive skew in male primates
14
15 16
(Figure 2)
49
