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Mastozoología neotropical

versión impresa ISSN 0327-9383versión On-line ISSN 1666-0536

Mastozool. neotrop. v.12 n.1 Mendoza ene./jun. 2005


Social parasitism in mammals with particular reference to neotropical primates

Clara B. Jones

Department of Psychology, Fayetteville State University. Fayetteville, NC 28301, USA.

ABSTRACT: Organisms often respond in ways that appear to benefit others rather than themselves. This phenomenon is consistent with the views of Darwin (1859) and Dawkins (1999) that individuals may exploit the responses of others. This phenomenon, "social parasitism", has been extensively investigated in social insects, particularly, ants. Other empirical studies have demonstrated social parasitism in fish, birds, and mammals. This paper reviews several possible examples of mammalian social parasitism, with an emphasis upon intraspecific social parasitism (ISP) in Neotropical primates. Social parasitism is discussed as a life history feature of long-lived, social organisms such as many primates, including humans. A simple mathematical model, applied to social parasitism, is presented linking parasite transmission to a parasite's influence on its host. Phenotypic manipulation is assessed as a mechanism of social parasitism, and possible examples from the literature on Neotropical primates are provided. Social parasitism is discussed in relation to the evolution of higher grades of sociality (eusociality, cooperative breeding), manipulation success (infectivity), and the evolution of virulence (e.g., aggression, punishment). It is proposed that an understanding of variations in virulence and infectivity by social parasites is likely to reveal important evolutionary dynamics for an integrated view of social evolution.

Key words. Social parasitism. Phenotypic manipulation. Neotropical primates. Life history. Social evolution.


Dawkins (1999: 69) proposed that, "Any nervous system can be subverted if treated in the right way." Consistent with this view, group-living individuals often act in ways that appear to benefit others (altruism) instead of themselves (selfishness or cooperation). Several hypotheses have been advanced to explain ostensibly altruistic behavior in which the donor bears a (genotypic or phenotypic) cost and the recipient experiences a genotypic or phenotypic advantage over the donor or a third party. These hypotheses, kin selection (Hamilton, 1964; Bertram, 1983; West et al., 2002), reciprocal altruism (Trivers, 1971), manipulation (West-Eberhard, 1975; Ridley and Dawkins, 1981; Stuart, 2002), and/or "trait group" selection (DS Wilson, 1975), are fundamental schemas in most attempts to explain the evolution of social behavior in invertebrate and vertebrate societies. Students of social behavior have been particularly concerned with those interindividual interactions in which one individual's responses benefit the genotypic and/or phenotypic interests of another (West, 1967; EO Wilson, 1975; West-Eberhard, 1979) since these responses are not explained in a straightforward manner by classical evolutionary theory. Darwin (1859: 208) argued, for example, "[N]o instinct can be shown to have been produced for the good of other animals, though animals take advantage of the instincts of others."
     For mammals, the highest social grades are achieved among cooperatively breeding species such as the Latin American marmosets and tamarins (Tardif, 1997; Abbott et al., 1998; Saltzman, 2003; also see Andersson, 1984; Emlen, 1991, 1995; Solomon and French, 1997) and the eusocial naked mole rats of Africa (Sherman et al., 1991, 1995; Lacey and Sherman, 1997; Burland et al., 2004). In these groups, some individuals, generally females, more or less temporarily (marmosets and tamarins: Cebidae, Primates) or more or less permanently (naked mole rats: Bathyergidae, Rodentia) delay individual (selfish) reproduction to assist dominant group members rear one or more offspring who are usually the helper's kin. Altruistic behavior in these cases, then, is thought to arise via kin selection in combination with other factors (e.g., ecological effects such as habitat saturation: Andersson, 1984; Emlen, 1991, 1995; Faulkes, et al. 1997) and to be beneficial to the helper (host, victim). Helping behavior and consequent reproductive suppression may represent a "decision" by the helper or may be imposed by a dominant (reproductive parasite), often through mechanisms of behavioral "policing" or chemical communication.
     It is relatively straightforward to formulate sound Darwinian hypotheses explaining altruism when the actor's selfish interests appear to be served. It has proven difficult, however, to proffer credible evolutionary scenarios for numerous actions that appear counterintuitive within a Darwinian paradigm (e.g., same sex partner preference, homicide, suicide, delaying or foregoing reproduction, spite, dependency complexes, alloparenting: see, for example, Dawkins, 1999; Berdoy et al., 2000). This challenge has led some researchers to propose group-level (Wilson, 1980) or other controversial constructs (Fehr and Henrich, 2003) to explain altruism (Kerr et al., 2004). The evolutionary trap of altruism will exist when assisting another's reproductive (genotypic or phenotypic) interests is detrimental to one's own interests, a dilemma that is expected to arise wherever interindividual (genotypic and/or phenotypic) conflicts of interest exist (Reeve and Keller, 1996).
     While the ecology of social parasitism has not been studied thoroughly, Jamieson et al. (2000), studying parasitic birds, suggested that social parasitism is most likely to be expressed in temporally and spatially heterogeneous regimes. Furthermore, Savolainen and Vepsäläinen (2003) argued that polygyny is a prerequisite for intraspecific social parasitism and that social parasites are often related ("Emery's rule"). Neotropical primates are an excellent test for these propositions because of the extensive variability of their behavior and social organization (Fleagle, 1999). These studies have been initiated by O'Brien's (1988) investigations of parasitic nursing by infant Cebus olivaceus, Jones' (1997a) research on reproductive parasitism by female Alouatta palliata, and Treves' (2001) review of the role of conspecific threat and constraints on individual fitness imposed by conspecifics in Alouatta spp. The present paper explores the topic of intraspecific social parasitism (ISP) in mammals relying, in particular, upon examples from the literature on Neotropical primates (Platyrrhini: Groves, 2001).

Defining criteria for the classification of social parasitism

Mammalogists have probably not emphasized the role of social parasitism in the evolution of behavior and social organization among social mammals because the pertinent models have been associated with the insect literature, invertebrate constructs that are rarely employed for the investigation of mammals. Parasitism generally implies a non-fatal interspecific relationship whereby one actor benefits at the expense of another. The familiar parasite is a fungus, virus, bacteria, protozoan, arthropod or other small organism exploiting the tissues, blood, or other products of a host (the victim). This classical body of work on non-social parasitism is used in the present paper as a conceptual framework for the analysis of social parasitism, in particular, intraspecific social parasitism (ISP). Social parasitism, sometimes termed "involuntary altruism," implies associations characterized by an exploitative relationship (interspecific or intraspecific) whereby the parasite is wholly or partially dependent upon the social behavior and/or social organization of the host. As Poulin (2002) points out, all forms of parasitism reflect Dawkins' (1982) concept of the "extended phenotype" whereby exploitation by parasites of their hosts can be viewed as the former expressing his/her genes in the latter.
     Several patterns of social parasitism have been described. "Brood parasitism" is a type of social parasitism common among birds and entails one individual laying its egg(s) in the nest of the bird of another species who raises the parasitic egg(s) at the expense of its own young (Lack, 1968; Rothstein, 1990; Cichon, 1996). Some types of adoption in mammals may be similar to brood parasitism in birds (see, for example, Nicolson, 1987; Hrdy, 1979). "Kleptoparasitism," reported for mammals and common among birds (Bautista et al., 1998), is another type of social parasitism in which one species steals the prey of another species. Kleptoparasitism of the food supply of the African wild dog (Lycaon pictus) by the spotted hyaena (Crocuta crocuta), for example, was documented by Gorman et al. (1998). Each of these types of exploitative interspecific associations has analogies at the intraspecific level, such as reports of "manipulation by harassment" in primates [Stevens and Stephens, 2002; Stevens, 2004 (see below)]. Bronstein (2001, 2003) has pointed out that, like herbivory and predation, parasitism is defined primarily by its costs. Thus, students of social mammals need to develop confident measures or estimates of cost (to phenotypic and/or genotypic success) in order to distinguish social parasitism from other types of associations (e.g., spite, cooperation, mutualism, symbiosis, parasitoidism, inquilism).
     Ecologists define exploitation as a form of competition in which the interaction of two or more species or individuals indirectly reduces a limiting resource, yielding differential fitness benefits to the interactants (Begon and Mortimer, 1986). A necessary, but not sufficient, feature of a parasite is that it exist in close association, often, but not necessarily, obligate, with a host for some part, if not most, of its life (Begon and Mortimer, 1986). By definition, parasites obtain resources from and harm their hosts, and only experimental studies can determine whether or not these costs harm the inclusive fitness of hosts beyond critical threshold values (spite). Parasitism, then, implies dependency, a characteristic that may predispose its expression where individuals characterized by asymmetries live in groups and/or exhibit long lifespans, virtually ubiquitous conditions for primates.

Analogies between social parasitism in insects and in Neotropical primates

Social parasitism is particularly common among ants (Hölldobler and Wilson, 1990; Bourke and Franks, 1995) and has been extensively studied in these and other social insects (Stuart, 2002). Several patterns of (interspecific) social parasitism have been described for social insects, classified from least (e.g., temporary kleptoparasitism) to most "intimate" associations whereby the whole life cycle of the social parasite is completed within that of the host (see Stuart, 2002: 318-324). Stuart points out that these associations may be temporary and facultative or obligate and relatively permanent, and the insect classification system has utility as a representative schema for social mammals. Strier (2000: 307), for example, described two examples of temporary polyspecific associations among Neotropical primates in the Atlantic forest of Brazil that may involve interspecific social parasitism because the associations appear to be costly for one of the species. In these cases, one species may initially assist another in predator or food detection (see, for example, Eckardt and Zuberbühler, 2004), providing an opportunity for subsequent exploitation.
     Stuart's (2002: 318-324) discussion highlights patterns of "intimacy," dependence, and exploitation, and it is likely that initial stages of research on social parasitism in social mammals will rely heavily upon the rich literature existing on this topic for social insects. Caveats are required for these comparisons, however, since social mammals and insects may differ significantly in their genetics, anatomy and morphology, behavior, social organization, and in other traits. Studies of social parasitism in insects (Hölldobler and Wilson, 1990; Bourke and Franks, 1995) and other taxa are fundamental because within-species local competition for limiting resources is believed to drive social evolution (Perez-Tomé and Toro, 1982; West et al., 2002; Dybdahl and Storfer, 2003). Only additional theoretical and empirical, including experimental, research can determine which features of invertebrate social parasitism will apply to vertebrates. For example, several researchers have found that social insect parasites lose many traits characteristic of higher grades of sociality (e.g., worker castes: Parker and Rissing, 2002; multiple mating by females: Sumner et al., 2004). By analogy, research on primates and other social mammals may find that social parasites are more likely to demonstrate infantilized behavior such as the paedomorphic vocalizations exhibited by a subordinate male mantled howler competing with a dominant for a female in estrus (Jones, 1985, 1995a).
     Several conditions can be proposed for the delimitation of social parasitism in social mammals and, perhaps, other social vertebrates, based upon the discussion of Lewis et al. (2002): (1) social parasitism is a one- or two-trophic level interaction in which the social parasite receives a (genotypic and/or phenotypic) benefit at the expense of the host (victim, involuntary altruist); (2) the social parasite must exhibit some degree of dependence upon or "intimacy" with the host; and, (3) social parasites demonstrate tactics and strategies for the expression and proliferation (transmission) of their phenotypes. Condition (2) implies that organisms may benefit from dependency and/or host status under some conditions (e.g., immatures or nursing female mammals). Condition (3) suggests that social parasitism is beneficial to the actor, setting the (evolutionary) stage for parasite virulence (e.g., aggression and/or punishment). Stuart (2002) has argued that a social parasite's host might be one or more than one organism.
     Poulin (2002) has pointed out that the methods of behavioral ecology are powerful tools for the analysis of "parasites of all kinds." This author discusses the application of optimality models, game theory, and inclusive fitness theory to a study of parasitism in order to demonstrate the ways in which Tinbergen's (1951) program for answering questions in behavioral ecology might be realized. Tinbergen's emphasis upon function, proximate and ultimate causation, and development remains the conceptual framework for work in animal behavior and behavioral ecology (Alcock, 1993; Strier, 2000; Jones, 2003a), providing the context for studies of social parasitism, most of which have investigated only the proximate level of analysis (Poulin, 2002; but see Taborsky, 2001).
     An integrated approach to social parasitism requires a careful assessment of differential costs and benefits of social parasitism to both parasite and host for an understanding of its adaptive significance, although Poulin (2002) has pointed out that, in some conditions, parasitism may not be costly to the parasite (see above). Moore (2002) argued that parasitism might benefit the parasite, benefit the host, benefit both parasite and host, or benefit neither, a range of possibilities revising original definition(s) of parasitism given above whereby parasitism is necessarily deleterious to the host. A resolution of this potential inconsistency may lie with an understanding that the value of cost is relative to costs of alternative responses and with an investigation of thresholds of costs and benefits. Research on the evolutionary history of dependent and exploitative associations, including experimental manipulations, are required in order to understand not only the initial conditions favoring social parasitism but also the counteradaptations that may be adopted by hosts in some conditions which may decrease the costs of parasitism to them, all other things being equal.

The costs and benefits of intraspecific social parasitism (ISP)

In general, it is expected that ISP will be favored where the fitness benefits to parasites and hosts outweigh the costs. Benefits to the host will parallel those addressed in the literature for the advantages of all social responses, such as improved predator or competitor detection, improved foraging efficiency, increased access to mates, access to information centers, increased defense of limiting resources, and increased survivorship of the host and/or her/his offspring. Costs to the host may entail increased competition for limiting resources, increased risk of phenotypic manipulation (see below), increased risk of exploitation of offspring, increased interference with parenting, vulnerability to spite, or increased mortality (e.g., by predation). Moore (2002) has discussed many of these effects in detail.
     Following May and Anderson (1990, cited in Moore, 2002), Moore points out that the fitness of the parasite can be measured as reproductive rate (R0), a density-dependent value. May and Anderson's equation linking parasite transmission to a parasite's influence on its host (Moore, 2002: 6) is related to virulence by way of a measure of cost to host fitness [e.g., increased inter-birth intervals (IBI) among social mammals or decreased litter size]. May and Anderson's equation can be modified for social parasitism such that

R0 = y(N)/(a+b+v)

where y is transmission (infectivity, manipulation success), N is host population density, a is rate of host cost (e.g., rate of decrease in IBI) from virulence (aggression), b is rate of host cost from all but virulence, and v is recovery rate (the host's ability to completely or partially escape the deleterious effects of social parasitism). For example, in the case described by Jones (1997a), Alouatta palliata females may parasitize males (hosts) reproductively by leading males to a feeding source which males defend. Females feed before "deciding" to copulate or not to copulate. Reproductive parasitism by these females may increase a female parasite's reproductive rate by decreasing her interbirth interval (IBI). Following May and Anderson's equation, decreased IBI (increased R0) is a function of manipulation success which might be measured as energy obtained by females for conversion into offspring. Virulence (host cost) might be measured as decreased male IBI resulting from "punishment" by females (e.g., time expended to guard a female who does not copulate after feeding: see Jones, 2002d). Rate of host cost (b) might be measured as time expended by males in following and guarding females who deceive them or who extract more time for feeding than they, in fact, require to produce a viable offspring. Finally, v, the host's ability to escape or avoid parasitic females ("negative reinforcement") might be measured as the standard deviation of a male's "persistence" in guarding parasitic females. As Moore (2002) points out, R0 increases as a decreases when virulence, transmission, and recovery rate are independent. Under these conditions, the parasite should evolve towards a harmless state since the costs of social parasitism would not outweigh its benefits. In such conditions, the potential for female manipulation of males should be minimized (Brachyteles ?). Where virulence, transmission, and/or recovery rate are related, however, social parasitism should be favored, and the degree of virulence should be determined by the relative degree of benefit to the social parasite, all other things being equal (Alouatta).

Intraspecific social parasitism (ISP) and life history theory

May and Anderson's (1990, cited in Moore, 2002) treatment links the topic of parasitism, and, by extension, social parasitism, to life history theory since R0 is a life history expression (Stearns, 1992; Jones, 1997b; Alberts and Altmann, 2003). Discussing social parasitism in ants, Stuart (2002) provides a robust schema for the preliminary analysis of social parasitism in social mammals and other social vertebrates. This author classifies systems of social parasitism in a binary manner, with one class representing breeding systems that raise young more or less selfishly (without helpers) and the other class representing breeding systems raising young more or less cooperatively or communally. Both of these systems are represented in Neotropical primates.
     Female social spiders, Stegodyphus dumicola, rear their own cocoons in an attempt to avoid ISP (Kürpick, 2000). Similarly, female mantled howlers (A. palliata) rear their single offspring with little or no assistance from relatives, unrelated females, or males (Jones, 1978, 2005; Clarke and Glander, 1984; Clarke, 1990; Calegaro-Marques and Bicca-Marques, 1993; Clarke et al., 1998), a reproductive tactic that may have evolved in response to the costs of ISP. Alloparenting and other behaviors characteristic of more gregarious systems (e.g., grooming) are rare in this and other species of Alouatta (Jones, 1979; Brockett et al., 2000). Altmann (1959) noted that weaning in mantled howlers is harsh, suggesting that these mothers' tolerance for infant dependence is limited. Since Galef, (1981; also see O'Brien, 1988) has suggested that immature mammals are "ultimate subordinates" because of their tendency to employ deceptive tactics and strategies to achieve their selfish ends (Trivers, 1974, 1985; Crespi and Semeniuk, 2004), mantled howlers may be an excellent model for the investigation of the genetic, ecological, and other factors limiting social parasitism by this age group. If developmental costs are sufficiently high for young mantled howlers and if the potential for offspring parasitism of mothers is restricted by maternal behaviors, selection may favor infants who parasitize the responses of group members other than their mother (Fig. 1).


Fig. 1. Juvenile mantled howler monkey (Alouatta palliata) carrying unrelated conspecific infant across a space between trees impassable to the infant. Distress vocalizations emitted by the infant may have functioned to induce the juvenile's helping behavior. Photo by © Clara B. Jones.

     At the other extreme, some callitrichids are cooperative breeders, and mothers receive assistance from putative fathers and other group members who are often infants' older siblings (Mitani and Watts, 1997; Porter, 2001; Saltzman, 2003). Porter (2001) reports that the reproductive output of female Goeldi's marmosets (Callimico goeldii: Fig. 2) is increased by assistance from other group members as well as the presence of biannual birth seasons. In addition to some callitrichids, the socially monogamous Aotus and Callicebus as well as polygynous Saimiri and Cebus are the only Neotropical taxa exhibiting extensive allocare (Hrdy, 1976; Nicolson, 1987; Tardif, 1997). These taxa belong to the Neotropical primate family Cebidae. Charnov's (1978; Mousseau and Fox, 1998) mathematical result that maternal parasitism is more likely to be found in species with low levels of multiple mating by females can be tested for this rearing guild, as well as Savolainen and Vepsäläinen's (2003) argument that polygyny is a prerequisite for ISP. The pattern of rearing identified for Neotropical primates whereby members of the family Atelidae, folivorous primates, exhibit little maternal parasitism or allocare may indicate that the potential costs (to fitness) from ISP are prohibitively high in some ecological regimes, a possibility deserving investigation.

Fig. 2. Adult male Goeldi's marmoset (Callimico goeldii) helper. Photo taken at San Sebastian, Bolivia by © Edilio Nacimento B.

     Stuart's (2002; van Schaik and Kappeler, 1997) binary system based upon female rearing strategies is consistent with a life history approach whereby female "decisions" ultimately determine a population's profile. Emlen and Oring (1977) and others (Trivers, 1972; Wittenberger, 1980; Wrangham, 1980, 1987; Shuster and Wade, 2003; Lindenfors et al., 2004) have shown that the abundance of fertilizeable females limits male fitness and that male reproductive strategies depend upon females' choices. It is important to recall, however, that, since the interests of the sexes will often differ, males and females may be engaged in a coevolutionary race to minimize the deleterious effects of one sex upon the other (Rice, 2000). Nonetheless, because higher grades of sociality are expected to evolve in response to energetic savings, as suggested by Heinze and Keller (2000), and because females are expected to be more sensitive than are males to energetic costs (Schoener, 1971), females are expected to be more social than males where sociality delivers an energetic gain benefiting inclusive fitness, all other things being equal (Queller, 1997). These hypothesized relationships are depicted in a graphical manner in Fig. 3.

Fig. 3. A graphical model describing the costs (C) or benefits (B) to female inclusive fitness (lifetime reproductive success) of relative degree of sociality as a function of differential energy-savings, from low (—) to high (++) (see Heinze and Keller 2000; Jones and Agoramoorthy, 2003: 124-124). Benefits will increase and then level off as the costs increase linearly (because resources are limiting), and the maximum net benefit (benefit minus cost) to females should occur at "x". The location of "x" will depend upon the position and shape of the benefit and cost curves, a function of environmental unpredictability over the short and long terms.

Phenotypic manipulation in primates

In 1997, Byrne and Whiten stated: "For each individual primate, [group living] sets up an environment favouring the use of social manipulation to achieve individual benefits at the expense of other group members...." (p. 2, emphasis in original). This statement reflects not only the neo-Darwinian view that an individual's actions are expected to be selfish rather than altruistic but also the view that some individuals may manipulate others against the latters' interests. As pointed out above, numerous hypotheses have been proposed to explain this apparent inconsistency. The type of animal discussed by Byrne and Whiten (1997; also see Frith and Frith, 1999) is one with a plastic or flexible phenotype vulnerable to a range of manipulations.
     The view that primate, including human, phenotypes are modifiable to a greater degree than those of other organisms has a long history, extending at least to the early psychologists such as Baldwin (1902; West-Eberhard, 2003, Chapter 1; Jones, 2005; see Smuts et al., 1987; Dunbar, 1997). These views no doubt account for the radical behaviorism representative of the early stages of American Psychology and its emphasis upon exogenous stimulation and the mechanisms of learning. Currently, however, psychologists are more likely to advance cognitive rather than behavioral explanations for the responses observed in primates and other animals showing "complex adaptations" (Byrne and Whiten, 1988; Whiten and Byrne, 1997; Dunbar, 2003).
     The chapters in Byrne and Whiten's volumes cited previously pertain specifically to the ways that organisms use intellectual processes (e.g., "theory of mind") to deceive others ("social intelligence"). The topic of intraspecific deceit has a long history in evolutionary biology, including primatology (Otte, 1975; Byrne and Whiten, 1985); however, scientists have recognized that a variety of mechanisms may explain the various forms of signaling and communication. Indeed, any sensory modality may be employed by the sender of a deceptive signal to manipulate the phenotype of a receiver (Eberhard, 2000; Lenoir et al., 2001; Double and Cockburn, 2002; Heiling et al., 2003; Mizutani et al., 2003; Pennisi, 2003). Costa Rican mantled howler monkeys, for example, demonstrate a broad array of behaviors suggesting that olfactory (Jones, 2002a, 2003b) and visual (Jones, 2002b, c), in addition to vocal (Jones, 1985, 2000) communication are important in intraspecific communication and in the coordination and control of conspecifics, patterns of response that may involve phenotypic manipulation, defined as a social parasite's ability to alter the phenotype of a host in a manner beneficial to the manipulator but costly to the host (Lobue and Bell, 1993; Poulin, 2003). Some mammalian studies have documented intraspecific phenotypic manipulation (e.g., maternal behavior: Meaney, 2001; Crabbe and Phillips, 2003; group foraging: Held et al., 2002; mate choice: Jones, 1997a; alloparental behavior: Hrdy, 1976; Jones, 1986). However, none of these studies unequivocally measures costs to the putative host.
     Deception may be employed by parasites as a social tool to effect phenotypic manipulation. Although students of animal, including human, communication continue to debate the extent to which signals are reliable ("honest"), there seems to be general agreement that deception may occur where its benefits (to inclusive fitness) outweigh its costs (Otte, 1975; Bradbury and Vehrencamp, 1998; Royle et al., 2002). Importantly, recent theoretical and empirical treatments (Reeve 2000; Stevens and Stephens, 2002; Stevens, 2004) stress "the selfish nature of generosity" (Stevens and Stephens, 2002), providing an alternative interpretation of sharing and cooperation based upon self-interest (also see Johnstone and Bshary, 2002). Like foraging common cranes, Grus grus, the primates studied by Stevens and his colleagues may be sharing to prevent "intraspecific kleptoparasitism" (Bautista et al., 1998). Variations of these interpretations might be applied to numerous observations of ostensibly altruistic or cooperative behavior such as grooming, the most common social behavior among primates, especially females (Silk et al., 2003). In order to understand phenotypic manipulation and its relationship to ISP in mammals, it will be necessary to explore the costs as well as the benefits of associations and to measure the differential effect of costs in determining patterns of interindividual response. Table 1 presents possible examples of parasitic phenotypic manipulation in Neotropical primates based upon documented cases from the literature on other taxa. Empirical research, including laboratory and field experiments, are required to determine the utility of the social parasitism paradigm for primates and other social mammals.

Table 1
Documented examples of parasitic phenotypic manipulation (virus, insects, fish, birds, mammals) including empirical evidence and possible analogies in Neotropical primates. See text for further explanation.

Avoidance of intraspecific social parasitism (ISP) within and between the sexes

Several apparent cases of escape from or avoidance of social parasitism have been documented for mammals and other taxa, and the growing theoretical literature treating parasitism as a form of punishment is an important development (e.g., Gardner and West, 2004; Skubic et al., 2004; also see Jones, 2002d). Studying foraging pigs (Sus scrofa), Held et al. (2002) showed that exploited individuals altered their food-finding behavior in order to increase their time spent foraging. These authors argued that such a counterstrategy is most likely to occur where parasitized individuals are not able to disperse or to become producers or scroungers themselves. This study is particularly pertinent to species in which some individuals locate food that is, over time, parasitized by conspecifics, especially other group members (e.g., Jones, 1996) and may, as well, assist in the interpretation of some mixed-species feeding groups (Terborgh, 1983; Jones, 1995b). Held and her colleagues also suggested that the counterstrategy they describe for foraging pigs represents learned behavior and that exploited individuals exhibited greater behavioral flexibility than less exploited or unexploited pigs. Several papers have discussed the relationship between parasitic exploitation and the evolution of diversity, including components of phenotypic plasticity (Poulin and Thomas, 1999; Summers et al., 2003). Although the primary emphasis of these papers is non-social parasitism, this topic is in need of investigation for ISP in primates and other social mammals.
     Mimicry may represent another category of responses to escape or avoid social parasitism and/or phenotypic manipulation (Holen et al., 2001; Neumann, 2002). Possible examples in Neotropical primates may include pseudopregnancy by females of some taxa, pseudofemale morphology by sub-adult male mantled howlers, and paedomorphic vocalizations (Jones, 1995c). Multiple mating by females, a pattern of response that is probably ubiquitous among mammals (e.g., Jones and Cortés-Ortiz, 1998), including primates, may also represent a countertactic to avoid parasitic males. This view supports Wolff and Macdonald's (2004: 127) conclusion that multi-male mating by female mammals "functions to confuse paternity, which, in turn, deters infanticide," a hypothesis originally proposed by Hrdy (1979). Multi-male mating by females may represent female parasitism of males, an interpretation supported by some avian studies (Richardson and Burke, 1999; Hughes et al., 2003) and may indicate antagonistic coevolution between the sexes (Rice, 2000; Nunn, 2003; also see Rice and Holland, 1997; Holland and Rice, 1999).


The main conclusion of the present paper holds that individuals may exhibit responses serving a social parasite's self-interests rather than those of the host or victim and that the study of intraspecific social parasitism has the potential to explain many responses that appear inconsistent with Darwinian principles. Analogies from non-social parasitism suggest that intraspecific social parasitism may result in the manipulation of hosts' phenotypes, possibly because it is in the interests of the host to be parasitized (Dawkins, 1999), particularly over the short-term. Possible examples might be parental manipulation of offspring or some forms of manipulation by individuals of their mates. Theoretical and empirical, including experimental, research must be conducted to determine the extent to which it may benefit individuals to become hosts. For example, individuals with little or no opportunity for future reproduction (e.g., individuals whose reproductive costs are very high or whose benefits are very low) may gain from settling for host status (e.g., helpers) imposed by a dominant. In addition, in some environmental regimes, it may benefit parents (or dominants) to resist offspring's (or other subordinates') independence and/or autonomy through phenotypic manipulation.
     Intraspecific social parasitism, in particular, phenotypic manipulation, will bias an association for high levels of reproductive skew (apportionment of reproduction within groups) because some individuals (parasites) are expected to reproduce much more than others (hosts). Intraspecific social parasitism is related to reproductive skew because the social parasite (subordinate: see Taborsky, 2001) harnesses the labor and/or resources of his/her host to the detriment of the latter's inclusive fitness, possibly marking a major evolutionary transition (see Wahl, 2002; Crespi et al., 2004). These harmful responses may increase reproductive skew, creating a division of labor within groups. Intraspecific social parasitism, then, is related to the evolution of complex social behavior, a topic of interest to all students of social vertebrates. Andersson (1984) reviewed the literature for the evolution of eusociality in insects and vertebrates, noting that several traits, including parental manipulation, appear to be preconditions for advanced sociality in both of these groups. The treatment by Andersson and others (e.g., Emlen, 1995; Dawkins, 1999) supports the view that general principles of social evolution may be identified, and papers by Reeve and others (2001; Reeve and Emlen, 2000; Shellman-Reeve and Reeve, 2000; also see Hager, 2003a, b; Jones and Agoramoorthy, 2003) link reproductive skew models with the identification of these general causes and effects.
     Finally, the study of intraspecific social parasitism is also likely to reveal important information about the evolution of virulence (e.g., aggression, punishment) since the costs and benefits of direct or indirect damage to the host are expected to vary as a function of their differential costs and benefits to the parasite's inclusive fitness, environmental heterogeneity, and the potential for antagonistic coevolution. Discussing Grafen's (1979) game theoretical analysis of evolutionary stable queen and worker strategies, Dawkins (1999: 77) emphasized the importance of division of power within groups (see Jones, 2000; Hager, 2003b). It will be instructive for students of social mammals and other social vertebrates to identify the abiotic and biotic, including social, conditions favoring low, moderate, or high levels of virulence by social parasites. In addition to studies of infectivity or manipulation success by social parasites, then, research on virulence by social parasites can be employed as a measure of parasite fitness, as suggested by Dybdahl and Storfer (2003). An understanding of variations in virulence and infectivity by social parasites, as defined above, is likely to reveal important evolutionary dynamics for an integrated view of social evolution.


I am grateful to William C. Dilger for encouraging me to study the topic of mimicry in primates and to the late Jasper Loftus-Hills for stimulating my interest in social parasitism. Bernard Crespi, Bruce Patterson, and two anonymous reviewers generously provided constructive criticism on a prior version of this paper, significantly improving the manuscript. The Werner Hagnauer family kindly offered hospitality and logistical support from 1973-1980 when I studied mantled howlers on their ranch, Hacienda La Pacífica, Cañas, Guanacaste, Costa Rica. I thank Leila M. Porter and Juan Carlos Serio Silva for sharing photographs of their target species and Jim Moore for responding to a query about dispersal. I am indebted to the many students of social parasitism in invertebrates, especially social insects, and vertebrates, particularly fish and birds, who generated the important theoretical and empirical work informing my own studies.


ABBOTT DH, W SALTZMAN, NJ SCHULTZ-DARKEN, and PL TANNENBAUM. 1998. Adaptations to subordinate status in female marmoset monkeys. Comparative Biochemistry and Physiology Part C 119:261-274.         [ Links ]

AGORAMOORTHY G and R. Rudran. 1992. Adoption in free-ranging red howler monkeys, Alouatta seniculus, of Venezuela. Primates 33:551-555.         [ Links ]

ALBERTS SC and J. ALTMANN. 2003. Matrix models for primate life history analysis. Pp. 66-102, in: Primate life histories and socioecology (PM Kappeler and ME Pereira, eds.). The University of Chicago Press, Chicago, USA.         [ Links ]

ALCOCK J. 1993. Animal Behavior: an evolutionary approach (5th ed.). Sinauer Associates, Inc., Publishers, Sunderland, MA, USA.         [ Links ]

ALEXANDER RD, DC MARSHALL, and JR COOLEY. 1997. Evolutionary perspectives on insect mating. Pp. 4-31, in: The evolution of mating systems in insects and arachnids (JC Choe and BJ Crespi, eds.). Cambridge University Press, Cambridge, UK.         [ Links ]

ALTMANN S. 1959. Field observations of a howling monkey society. Journal of Mammalogy 40:317-330.         [ Links ]

ANDERSSON M. 1984. The evolution of eusociality. Annual Review of Ecology and Systematics 15:165-189.         [ Links ]

BALDWIN JM. 1902. Modification. Pg. 94 In: Dictionary of philosophy and psychology (JM Baldwin, ed.) The Macmillan Company, New York, USA.         [ Links ]

BAUTISTA LM, JC ALONSO, and JA ALONSO. 1998. Foraging site displacement in common crane flocks. Animal Behaviour 56:1237-1243.         [ Links ]

BEGON M and M MORTIMER. 1986. Population ecology: a unified study of animals and plants. Sinauer Associates, Inc., Sunderland, MA, USA.         [ Links ]

BERDOY M, JP WEBSTER, and DW MAC DONALD. 2000. Fatal attraction in rats infected with Toxoplasma gondii. Proceedings of the Royal Society of London B 267:1591-1594.         [ Links ]

BERTRAM B. 1983. Kin selection and altruism. Pp. 727-729 In: Advances in the study of mammalian behavior (JF Eisenberg and DG Kleiman, eds.). The American Society of Mammalogists, Pittsburgh, PA, USA.         [ Links ]

BICCA-MARQUES JC. 2003. Sexual selection and foraging behavior in male and female tamarins and marmosets. Pp. 455-475, in: Sexual selection and reproductive competition in primates: new perspectives and directions (CB Jones, ed.). American Society of Primatologists, Norman, OK, USA.         [ Links ]

BIEDZICKI de MARQUES AA and C ADES. 2000. Male care in a group of wild Alouatta fusca climitans in southern Brazil. Folia Primatologica 71:409-412.         [ Links ]

BIZE P, A ROULIN, and H RICHNER. 2003. Adoption as an offspring strategy to reduce ecotparasite exposure. Proceedings of the Royal Society of London B 270:S114-S116.         [ Links ]

BOURKE AFG and NR FRANKS. 1995. Social evolution in ants. Princeton University Press, Princeton, USA.         [ Links ]

BRADBURY JW and SL VEHRENCAMP. 1998. Principles of animal communication. Sinauer Associates, Inc., Sunderland, MA, USA.         [ Links ]

BROCKETT RC, RH HORWICH, and CB JONES. 2000. A model for the interpretation of grooming patterns applied to the Belizean black howling monkey (Alouatta pigra). Primate Report 56:23-32.         [ Links ]

BRONSTEIN JL. 2001. The costs of mutualism. American Zoologist 41:825-839.         [ Links ]

BRONSTEIN JL. 2003. The scope for exploitation within mutualistic interactions. Pp. 185-202, in: Genetic and cultural evolution of cooperation (P Hammerstein, ed.). The MIT Press, Cambridge, MA, USA.         [ Links ]

BROWN WD, C LIAUTARD, and L KELLER. 2003. Sex-ratio dependent execution of queens in polygynous colonies of the ant Formica exsecta. Oecologia 134:12-17.         [ Links ]

BURLAND TM, NC BENNETT, JU JARVIS, and CG FAULKES. 2004. Colony structure and parentage in wild colonies of co-operatively breeding Damaraland mole-rats suggest incest avoidance alone may not maintain reproductive skew. Molecular Ecolology 13:2371-2379.         [ Links ]

BYRNE RW and A WHITEN. 1985. Tactical deception of familiar individuals in baboons. Animal Behaviour 33:669-673.         [ Links ]

BYRNE RW and A WHITEN. 1988. Machiavellian intelligence: social expertise and the evolution of intellect in monkeys, apes, and humans. Clarendon Press, Oxford, UK.         [ Links ]

BYRNE RW and A WHITEN. 1997. Machiavellian intelligence, Pp. 1-23, in: Machiavellian intelligence II: extensions and evaluations (Whiten A and RW Byrne). Cambridge University Press, Cambridge, UK.         [ Links ]

CALEGARO-MARQUES C and JC BICCA-MARQUES. 1993. Allomaternal care in the black howler monkey (Alouatta caraya). Folia Primatologica 61:104-109.         [ Links ]

CHARNOV EL. 1978. Evolution of eusocial behavior: Offspring choice or parental parasitism? Journal of Theoretical Biology 75:451-465.         [ Links ]

CICHON M. 1996. The evolution of brood parasitism: the role of facultative parasitism. Behavioral Ecology 7:137-139.         [ Links ]

CLARKE MR. 1990. Behavioral development and socialization of infants in a free-ranging group of howling monkeys (Alouatta palliata). Folia Primatologica 54:1-15.         [ Links ]

CLARKE MR and KE GLANDER. 1981. Adoption of infant howling monkeys (Alouatta palliata). American Journal of Primatology 1:469-472.         [ Links ]

CLARKE MR and KE GLANDER. 1984. Female reproductive success in a group of free-ranging howling monkeys (Alouatta palliata) in Costa Rica. Pp. 111-126, in: Female primates: studies by women primatologists (MF Small, ed.). Alan R. Liss, New York, USA.         [ Links ]

CLARKE MR, KE GLANDER, and EL ZUCKER. 1998. Infant-nonmother interactions of free-ranging mantled howlers (Alouatta palliata) in Costa Rica. International Journal of Primatology 19:451-472.         [ Links ]

CRABBE JC and TJ PHILLIPS. 2003. Mother nature meets mother nurture. Nature Neuroscience 6:440-442.         [ Links ]

CRESPI B and C SEMENIUK. 2004. Parent-offspring conflict in the evolution of vertebrate reproductive mode. American Naturalist 163:635-653.         [ Links ]

CRESPI BJ, DC MORRIS, and LA MOUND. 2004. Evolution of ecological and behavioural diversity: Australian acacia thrips as model organisms. Biological Resources Study & CSIRO Entomology, Canberra, Australia.         [ Links ]

CROCKETT CM and CH JANSON. 2000. Infanticide in red howlers: female group size, male membership, and a possible link to folivory. Pp. 75-98, in: Infanticide by males and its implications (CP van Schaik and CH Janson, eds.). Cambridge University Press, Cambridge, UK.         [ Links ]

DARWIN C. 1859. The origin of species. Random House, Modern Library Edition, New York, USA.         [ Links ]

DAWKINS R. 1982. The extended phenotype. Oxford University Press, Oxford, UK.         [ Links ]

DAWKINS R. 1999. The extended phenotype (Revised edition). Oxford University Press, Oxford, UK.         [ Links ]

DIXSON AF. 1998. Primate sexuality: comparative studies of the prosimians, monkeys, apes, and human beings. Cambridge University Press, Cambridge, UK.         [ Links ]

DOUBLE MC and A COCKBURN. 2002. Subordinate superb fairy-wrens (Malurus cyaneus) parasitize the reproductive success of attractive dominant males. Proceedings of the Royal Society of London B. Retrieved February 15, 2004, from doi:10.1098/rspb.2002.2261.         [ Links ]

DUNBAR RIM. 1997. Grooming, gossip, and the evolution of language. Harvard University Press, Cambridge, MA, USA.         [ Links ]

DUNBAR RIM. 2003. Psychology: evolution of the social brain. Science 302:1160-1161.         [ Links ]

DYBDAHL MF and A STORFER. 2003. Parasite local adaptation: Red Queen versus Suicide King. Trends in Ecology and Evolution 18:523-530.         [ Links ]

EBERHARD WG. 1985. Sexual selection and animal genitalia. Harvard University Press, Cambridge, MA, USA.         [ Links ]

EBERHARD WG. 1996. Female control: sexual selection by cryptic female choice. Princeton (NJ): Princeton University Press.         [ Links ]

EBERHARD WG. 2000. Spider manipulation by a wasp larva. Nature 406:255-256.         [ Links ]

ECKHARDT W and K ZUBERBUHLER. 2004. Cooperation and competition in two forest monkeys. Behavioral Ecology 15:400-411.         [ Links ]

EMLEN ST. 1991. Evolution of cooperative breeding in birds and mammals. Pp. 301-337, in: Behavioural ecology: an evolutionary approach (JR Krebs and NB Davies, eds.). Blackwell Scientific Publications, London, UK.         [ Links ]

EMLEN ST. 1995. An evolutionary theory of the family. Proceedings of the National Academy of Sciences of the United States of America 92:8092-8099.         [ Links ]

EMLEN ST and LW ORING. 1977. Ecology, sexual selection and the evolution of mating systems. Science 197:215-223.         [ Links ]

ESTRADA A. 1982. A case of adoption of a howler monkey infant (Alouatta villosa) by a female spider monkey. Primates 23:135-137.         [ Links ]

ESTRADA A and JD PATERSON. 1980. A case of adoption in a captive group of Mexican spider monkey (Ateles geoffroyi). Primates 21:128-129.         [ Links ]

FAULKES CB, NC BENNETT, MW BRUFORD, HP O'BRIEN, GH AGUILAR, and JU JARVIS. 1997. Ecological constraints drive social evolution in the African mole-rats. Proceedings of the Royal Society of London B 264:1619-1627.         [ Links ]

FEHR E and J HENRICH. 2003. Is strong reciprocity a maladaptation? On the evolutionary foundations of human altruism. Pp. 55-82, in: Genetic and cultural evolution of cooperation (P Hammerstein, ed.). The MIT Press, Cambridge, MA, USA.         [ Links ]

FLEAGLE JG. 1999. Primate adaptation and evolution (2nd ed.). Academic Press, San Diego, CA, USA.         [ Links ]

FRITH CD and U FRITH. 1999. Interacting minds-a biological basis. Science 286:1692-1695.         [ Links ]

GALEF BG. 1981. The ecology of weaning: parasitism and the achievement of independence by altricial mammals. Pp. 211-241, in: Parental care in mammals (I Gubernick and DJH Klopfer, eds.). Plenum, New York, USA.         [ Links ]

GARDNER A and SA WEST. 2004. Cooperation and punishment, especially in humans. American Naturalist 164:753-764.         [ Links ]

GORMAN ML, MG MILLS, JP RAATH, and JR SPEAKMAN JR. 1998. High hunting costs make African wild dogs vulnerable to kleptoparasitism by hyaenas. Nature 391:479-481.         [ Links ]

GRAFEN A. 1979. The hawk-dove game played between relatives. Animal Behaviour 27:905-907.         [ Links ]

GROVES CP. 2001. Primate taxonomy. Smithsonian Institution Press, Washington, DC, USA.         [ Links ]

HAGER R. 2003a. Models of reproductive skew applied to primates. Pp. 65-101, in: Sexual selection and reproductive competition in primates: new perspectives and directions (CB Jones, ed.). American Society of Primatologists, Norman, OK, USA.         [ Links ]

HAGER R. 2003b. The effects of dispersal costs on reproductive skew and within-group aggression in primate groups. Primate Report 67:85-98.         [ Links ]

HAMILTON WD. 1964. The evolution of social behavior. Journal of Theoretical Biology 7:1-52.         [ Links ]

HARE JF and TM ALLOWAY. 2001. Prudent Protomognathus and despotic Leptothorax duloticus: differential costs of ant slavery. Proceedings of the National Academy of Sciences of the United States of America 98:12093-12096.         [ Links ]

HAWKES K. 2004. The grandmother effect. Nature 428:128-129.         [ Links ]

HEILING AM, ME HERBERSTEIN, and L CHITTKA. 2003. Crab-spiders manipulate flower signals. Nature 421:334-335.         [ Links ]

HEINZE J and L Keller. 2000. Alternative reproductive strategies: a queen perspective in ants. Trends in Ecology and Evolution 15:508-512.         [ Links ]

HELD S, M MENDL, C DEVEREUX, and RW BYRNE. 2002. Foraging pigs alter their behaviour in response to exploitation. Animal Behaviour 64:157-166.         [ Links ]

HOLEN OH, GP SAETRE, T SLAGSVOLD, and NC STENSETH. 2001. Parasites and supernormal manipulation. Proceedings of the Royal Society of London B 268:2551-2558.         [ Links ]

HOLLAND B and WR RICE. 1999. Experimental removal of sexual selection reverses inter-sexual antagonistic coevolution and removes a reproductive. Proceedings of the National Academy of Sciences of the United States of America 96:5083-5088.         [ Links ]

HOLLDOBLER B and EO WILSON. 1990. The Ants. Belknap/Harvard, Cambridge, MA, USA.         [ Links ]

HRDY SB. 1976. The care and exploitation of nonhuman primate infants by conspecifics other than the mother. Advances in the Study of Behavior 6:101-158.         [ Links ]

HRDY SB. 1979. Infanticide among animals: a review, classification, and examination of the implications for the reproductive strategies of females. Ethology and Sociobiology 1:13-40.         [ Links ]

HUGHES JM, PB MATHER, A TOON, J MA, J ROWLEY, and E RUSSELL. 2003. High levels of extra-group paternity in a population of Australian magpies Gymnorhina tibicen: evidence from microsatellite analysis. Molecular Ecology 12:3441-3450.         [ Links ]

JAMIESON IG, SB MC RAE, M TREWBY, and RE SIMMONS. 2000. High rates of conspecific brood parasitism and egg rejection in coots and moorhens in ephemeral wetlands in Namibia. Auk 117, 250-252.         [ Links ]

JOHNSTONE RA and R BSHARY. 2002. From parasitism to mutualism: partner control in asymmetric interactions. Ecology Letters 5:634-639.         [ Links ]

JONES CB. 1978. Aspects of reproduction in the mantled howler monkey (Alouatta palliata Gray). Unpublished Ph.D. dissertation, Cornell University, Ithaca, NY, USA.         [ Links ]

JONES CB. 1979. Grooming in the mantled howler monkey (Alouatta palliata Gray). Primates 20:289-292.         [ Links ]

JONES CB. 1983. Do howler monkeys feed upon legume flowers preferentially at flower opening time? Brenesia 21:41-46.         [ Links ]

JONES CB. 1985. Reproductive patterns in mantled howler monkeys: estrus, mate choice, and copulation. Primates 26:130-142.         [ Links ]

JONES CB. 1986. Infant transfer behavior in humans: a note on the exploitation of young. Aggressive Behavior 12:167-173.         [ Links ]

JONES CB. 1995a. Alternative reproductive behaviors in the mantled howler monkey (Alouatta palliata Gray): testing Carpenter's hypothesis. Boletin Primatologico Latinoamericano 5:1-5.         [ Links ]

JONES CB. 1995b. The potential for metacommunity effects upon howler monkeys. Neotropical Primates 3:43-45.         [ Links ]

JONES CB. 1995c. Mimicry in primates: implications for heterogeneous conditions. Neotropical Primates 3:69-72.         [ Links ]

JONES CB. 1996. Temporal division of labor in a primate: age-dependent foraging behavior. Neotropical Primates 4:50-53.         [ Links ]

JONES CB. 1997a. Social parasitism in the mantled howler monkey, Alouatta palliata Gray (Primates: Cebidae): Involuntary altruism in a mammal? Sociobiology 30:51-61.         [ Links ]

JONES CB. 1997b. Life history patterns of howler monkeys in a time-varying environment. Boletin Primatologico Latinoamericano 6:1-8.         [ Links ]

JONES CB. 1997c. Subspecific differences in vulva size between Alouatta palliata palliata and A. p. mexicana: implications for assessment of female receptivity. Neotropical Primates 5:46-48.         [ Links ]

JONES CB. 1999. Testis symmetry in the mantled howling monkey. Neotropical Primates 7:117-119.         [ Links ]

JONES CB. 2000. Alouatta palliata politics: empirical and theoretical aspects of power. Primate Report 56:3-21.         [ Links ]

JONES CB. 2002a. How important are urinary signals in Alouatta? Laboratory Primate Newsletter 41:15-17.         [ Links ]

JONES CB. 2002b. Genital displays by adult male and female mantled howling monkeys, Alouatta palliata (Atelidae): evidence for condition-dependent compound displays. Neotropical Primates 10:144-147.         [ Links ]

JONES CB. 2002c. A possible example of coercive mating in mantled howling monkeys (Alouatta palliata) related to sperm competition. Neotropical Primates 10:95-96.         [ Links ]

JONES CB. 2002d. Negative reinforcement in primate societies related to aggressive restraint. Folia Primatologica 73:140-143.         [ Links ]

JONES CB (Ed.). 2003a. Sexual selection and reproductive competition in primates: new perspectives and directions. American Society of Primatologists, Norman, OK, USA.         [ Links ]

JONES CB. 2003b. Urine-washing behaviors as condition-dependent signals of quality by adult mantled howler monkeys (Alouatta palliata). Laboratory Primate Newsletter 42:12-14.         [ Links ]

JONES CB. 2004. The number of adult females in groups of polygynous howling monkeys (Alouatta spp.): theoretical inferences. Primate Report 68:7-25.         [ Links ]

JONES CB. 2005. Behavioral flexibility in primates: causes and consequences. Springer, New York, USA.         [ Links ]

JONES CB and G AGORAMOORTHY. 2003. Alternative reproductive behaviors in primates: towards general principles. Pp. 103-139, in: Sexual selection and reproductive competition in primates: new perspectives and directions (CB Jones, ed.). American Society of Primatologists, Norman, OK, USA.         [ Links ]

JONES CB and L CORTES-ORTIZ. 1998. Facultative polyandry in the howling monkey (Alouatta palliata): Carpenter was correct. Boletín Primatológico Latinoamericano 7:1-7.         [ Links ]

KERR B, PG GODFREY-SMITH, and MW FELDMAN. 2004. What is altruism? Trends in Ecology and Evolution 19:135-140.         [ Links ]

KHROMOVA SV. 1995. The behavioral phenomenon of "parasitism" in rats. Zh. Vyssh. Nerv. Deiat. Im. I.P. Pavlova 45:479-489 (English Abstract, article in Russian). Retrieved March 5, 2004 from        [ Links ]

KURPICK SM. 2000. Cocoon care in the social spider Stegodyphus dumicola (Eresidae). Pp. 39-44, in: European arachnology 2002 (S Toft and N Scharff, eds.). Aarhus University Press, Aarhus, DK.         [ Links ]

LACEY EA and PW SHERMAN. 1997. Cooperative breeding in naked mole-rats: implications for vertebrate and invertebrate sociality. Pp. 267-301, in: Cooperative breeding in mammals(NG Solomon and JA French, eds.). Cambridge University Press, Cambridge, UK.         [ Links ]

LACK D. 1968. Ecological adaptations for breeding in birds. Methuen, London, UK.         [ Links ]

LENOIR A, P D'ETTORE, C ERRARD, and A HEFETZ. 2001. Chemical ecology and social parasitism in ants. Annual Review of Entomology 46:573-599.         [ Links ]

LEWIS EE, JF CAMPBELL, and MVK SUKHDEO. 2002. Parasite behavioural ecology in a field of diverse perspectives. Pp. 337-346, in: The behavioural ecology of parasites (EE Lewis, JF Campbell, and MVK Sukhdeo, eds.). CABI Publishing, New York, USA.         [ Links ]

LEWIS SE and AE PUSEY. 1997. Factors influencing the occurrence of communal care in plural breeding mammals. Pp. 335-363, in: Cooperative breeding in mammals (NG Solomon and JA French, eds.). Cambridge University Press, Cambridge, UK.         [ Links ]

LINDENFORS P, L FROBERG, and CL NUNN. 2004. Females drive primate social evolution. Biology Letters 271 (S3):S101-S103 (DOI:10.1098/rsbl.2003.0114).         [ Links ]

LINKLATER WL and EZ CAMERON. 2000. Tests for cooperative behaviour between stallions. Animal Behaviour 60:731-743.         [ Links ]

LOBUE CP and MA BELL. 1993. Phenotypic manipulation by the cestode parasite Schistocephalus solidus of its intermediate host, Gasterosteus aculeatus, the threespine stickleback. The American Naturalist 142:725-735.         [ Links ]

MEANEY MJ. 2001. Maternal care, gene expression, and the transmission of individual differences in stress reactivity across generations. Annual Review of Neuroscience 24:1161-1192.         [ Links ]

MITANI JC and D WATTS. 1997. The evolution of non-maternal caretaking among anthropoid primates: Do helpers help? Behavioral Ecology and Sociobiology 40:213-220.         [ Links ]

MIZUTANI A, JS CHAHL, and MV SRINIVASAN. 2003. Motion camouflage in dragonflies. Nature 423:604.         [ Links ]

MOORE J. 2002. Parasites and the behavior of animals. Oxford University Press, Oxford, UK.         [ Links ]

MOUSSEAU TA and CW FOX. 1998. The adaptive significance of maternal effects. Trends in Ecology and Evolution 13:403-407.         [ Links ]

NEUMANN P. 2002. Social parasitism. Retrieved May 17, 2004 from        [ Links ]

NEUMANN PL, SE RADLOFF, RFA. MORITZ, HR HEPBURN, and SL REECE. 2001. Social parasitism by honeybee workers (Apis mellifera capensis Escholtz): host finding and resistance of hybrid host colonies. Behavioral Ecology 12:419-428.         [ Links ]

NEUMANN P, CWW PIRK, HR HEPBURN, and RFA MORITZ. 2003. Spatial differences in worker policing facilitate social parasitism of Cape honeybee workers (Apis mellifera capensis Esch.) in queenright host colonies. Insectes Sociale 50:109-112.         [ Links ]

NICOLSON NA. 1987. Infants, mothers, and other females. Pp. 330-342, in: Primate societies (BB Smuts, DL Cheney, RM Seyfarth, RW Wrangham, and TT Struhsaker, eds.). The University of Chicago Press, Chicago, IL, USA.         [ Links ]

NUNN CL. 2000. Collective benefits, free-riders, and male extra-group conflict. Pp. 192-204, in: Primate males: causes and consequences of variation in group composition (PM Kappeler, ed.). Cambridge University Press, Cambridge, UK.         [ Links ]

NUNN CL. 2003. Comparative and theoretical approaches to studying sexual selection in primates. Pp. 539-613, in: Sexual selection and reproductive competition in primates: new perspectives and directions (CB Jones, ed.). American Society of Primatologists, Norman, OK, USA.         [ Links ]

O'BRIEN TG. 1988. Parasitic nursing in the wedge-capped capuchin monkey (Cebus olivaceus). American Journal of Primatology 16:341-344.         [ Links ]

OTTE D. 1975. On the role of intraspecific deception. The American Naturalist 109:239-242.         [ Links ]

PARKER JD and SW RISSING. 2002. Molecular evidence for the origin of workerless social parasites in the ant genus Pogonomyrmex. Evolution 56:2017-2028.         [ Links ]

PENNISI E. 2003. Outside agitators alter wasp behavior. Science 302:372.         [ Links ]

PEREZ-TOME JM and MA TORO. 1982. Competition of similar and non-similar genotypes. Science 299:153-154.         [ Links ]

PORTER LM. 2001. Social organization, reproduction and rearing strategies of Callimico goeldii: new clues from the wild. Folia Primatologica 72:69-79.         [ Links ]

POULIN R. 2002. Parasite manipulation of host behaviour. Pp. 243-257, in: The behavioural ecology of parasites(EE Lewis, JF Campbell, and MVK Sukhedeo, eds.). CABI Publishing, New York, USA.         [ Links ]

POULIN R. 2003. Phenotypic manipulation and parasite-mediated host evolution. Pp. 205-212, in: The new panorama of animal evolution: proceedings of the 18th International Congress of Zoology (A Legakis, S Sfenthourakis, R Polymeni, and M Thessalou-Legaki, eds.). Penshoft Publishers, Sofia, Bulgaria.         [ Links ]

POULIN R and F THOMAS. 1999. Phenotypic variability induced by parasites: extent and evolutionary implications. Parasitology Today 15:28-32.         [ Links ]

QUELLER DC. 1997. Why do females care more than males? Proceedings of the Royal Society of London B 264:1555-1557.         [ Links ]

REEVE HK. 2000. A transactional theory of within-group conflict. The American Naturalist 155:365-382.         [ Links ]

REEVE HK. 2001. In search of unified theories in sociobiology: help from social wasps. Pp. 57-71, in: Model systems in behavioral ecology: integrating conceptual, theoretical, and empirical approaches (LA Dugatkin, ed.). Princeton University Press, Princeton, USA.         [ Links ]

REEVE HK and ST EMLEN. 2000. Reproductive skew and group size: an N-person staying incentive model. Behavioral Ecology 11:640-647.         [ Links ]

REEVE HK and L KELLER. 1996. Relatedness asymmetry and reproductive sharing in animal societies. The American Naturalist 148:764-769.         [ Links ]

RICE WR. 2000. Dangerous liaisons. Proceedings of the National Academy of Sciences of the United States of America 97:12953-12955.         [ Links ]

RICE WR and B HOLLAND. 1997. The enemies within: intergenomic conflict, interlocus contest evolution (ICE), and the intraspecific Red Queen. Behavioural Ecology and Sociobiology 41:1-10.         [ Links ]

RICHARDSON DS and T BURKE. 1999. Extra-pair paternity in relation to male age in Bullock's orioles. Molecular Ecology 8:2115-2126.         [ Links ]

RIDLEY M and R DAWKINS. 1981. The natural selection of altruism. Pp. 19-39, in: Altruism and helping behavior (JP Rushton and RM Sorrentino). Erlbaum, Hillsdale, NJ, USA.         [ Links ]

ROTHSTEIN SI. 1990. A model system for coevolution: avian brood parasitism. Annual Review of Ecology and Systematics 21:481-508.         [ Links ]

ROYLE NJ, IR HARTLEY, and GA PARKER. 2002. Begging for control: When are offspring solicitation behaviours honest? Trends in Ecology and Evolution 17:434-440.         [ Links ]

SALTZMAN W. 2003. Reproductive competition among female common marmosets (Callithrix jacchus): proximate and ultimate causes. Pp. 197-229, in: Sexual selection and reproductive competition in primates: new perspectives and directions (CB Jones, ed.). American Society of Primatologists, Norman, OK, USA.         [ Links ]

SAVOLAINEN R and K VEPSALAINEN. 2003. Sympatric speciation through intraspecific social parasitism. Proceedings of the National Academy of Sciences of the United States of America 100:7169-7174.         [ Links ]

SCHOENER TW. 1971. Theory of feeding strategies. Annual Review of Ecology and Systematics 2:369-404.         [ Links ]

SCOLLAY PA. 1978. The kidnapping of a neonate squirrel monkey Saimiri sciureus (peruviano). Laboratory Primate Newsletter 17:11-13.         [ Links ]

SHELLMAN-REEVE JS and HK REEVE. 2000. Extra-pair paternity as the result of reproductive transactions between paired mates. Proceedings of the Royal Society of London B 267:2543-2546.         [ Links ]

SHERMAN PW, JU Jarvis, and RD Alexander (Editors). 1991. The biology of the naked mole-rat. Princeton University Press, Princeton, NJ, USA.         [ Links ]

SHERMAN PW, EA LACEY, HK REEVE, and L KELLER. 1995. The eusociality continuum. Behavioral Ecology 6:102-108.         [ Links ]

SHUSTER SM and MJ WADE. 2003. Mating systems and strategies. Princeton University Press, Princeton, NJ, USA.         [ Links ]

SILK JB, SC ALBERTS, and J ALTMANN. 2003. Social bonds of female baboons enhance infant survival. Science 302:1231-1234.         [ Links ]

SKUBIK E, M TABORSKY, JM MC NAMARA, and AI HOUSTON. 2004. When to parasitize? A dynamic optimization model of reproductive strategies in a cooperative breeder. Journal of Theoretical Biology 227:487-501.         [ Links ]

SMUTS BB, DL CHENEY, RM SEYFARTH, RW WRANGHAM, and TT STRUHSAKER (eds.). 1987. Primate societies. The University of Chicago Press, Chicago, IL, USA.         [ Links ]

SOLOMON NG and JA FRENCH. (Editors). 1997. Cooperative breeding in mammals. Cambridge University Press, Cambridge, UK.         [ Links ]

STEARNS SC. 1992. The evolution of life histories. Oxford University Press, Oxford, UK.         [ Links ]

STEVENS JR. 2004. The selfish nature of generosity: harassment and food sharing in primates. Proceedings of the Royal Society of London B DOI: 10.1098/rspb.2003.2625.         [ Links ]

STEVENS JR and DW STEPHENS. 2002. Food sharing: a model of manipulation by harassment. Behavioral Ecology 13:393-400.         [ Links ]

STRIER KB. 2000. Primate behavioral ecology. Allyn and Bacon, Boston, USA.         [ Links ]

STUART RJ. 2002. The behavioural ecology of social parasitism in ants. Pp. 315-336, in: The behavioural ecology of parasites (EE Lewis, JF Campbell, and MVK Sukhdeo, eds.). CABI Publishing, New York, USA.         [ Links ]

SUMMERS K, S MC KEON, J SELLARS, M KEUSENKOTHEN, J MORRIS, D GLOECKNER, D PRESSLEY, B PRICE, and H SNOW. 2003. Parasitic exploitation as an engine of diversity. Biological Reviews 78:639-675.         [ Links ]

SUMNER S, WOH Hughes, JS PEDERSEN, and J BOOMSMA. 2004. Ant parasite queens revert to mating singly. Nature 428:35-36.         [ Links ]

TABORSKY M. 1998. Sperm competition in fish: "bourgeois" males and parasitic spawning. Trends in Ecology and Evolution 13:222-227.         [ Links ]

TABORSKY M. 2001. The evolution of bourgeois, parasitic, and cooperative reproductive behaviors in fishes. Journal of Heredity 92:100-110.         [ Links ]

TARDIF SD. 1997. The bioenergetics of parental behavior and the evolution of alloparental care in marmosets and tamarins. Pp. 2-33, in: Cooperative breeding in mammals (NG Solomon and JA French, eds.). Cambridge University Press, Cambridge, UK.         [ Links ]

TAUB D and P MEHLMAN. 1991. Primate paternalistic investment: a cross-species view. Pp. 51-89, in: Understanding behavior: what primate studies can tell us about human behavior(JD Loy and CB Peters, eds.). Oxford University Press, Oxford, UK.         [ Links ]

TAUB DM, NDM LEHNER, MR ADAMS. 1977. Enforced adoption and successful raising of a neonate squirrel monkey Saimiri sciureus (Brazilian). Laboratory Primate Newsletter 16:8-10.         [ Links ]

TERBORGH J. 1983. Five New World primates: a study in comparative ecology. Princeton University Press, Princeton, NJ, USA.         [ Links ]

TINBERGEN N. 1951. The study of enstinct. Oxford University Press, Oxford, UK.         [ Links ]

TREVES A. 2001. Reproductive consequences of variation in the composition of howler monkey (Alouatta spp.) groups. Behavioral Ecology and Sociobiology 50:61-71.         [ Links ]

TRIVERS RL. 1971. The evolution of reciprocal altruism. Quarterly Review of Biology 46:35-57.         [ Links ]

TRIVERS RL. 1972. Parental investment and sexual selection. Pp. 136-179, in: Sexual selection and the descent of man, 1871-1971 (B Campbell, ed.). Aldine, New York, USA.         [ Links ]

TRIVERS RL. 1974. Parent-offspring conflict. American Zoologist 14:249-264.         [ Links ]

TRIVERS RL. 1985. Social evolution. Menlo Park (CA): Benjamin/Cummings.         [ Links ]

VAN SCHAIK CP and PM KAPPELER. 1997. Infanticide risk and the evolution of male-female association in primates. Proceedings of the Royal Society of London B 264:1687-1694.         [ Links ]

VARALDI J, P FOUILLET, M RAVALLEC, M LOPEZ-FERBER, M BOULETREAU, and F FLEURY. 2003. Behavior in a parasitoid. Retrieved February 15, 2004, from        [ Links ]

WAHL LM. 2002. Evolving the division of labour: generalists, specialists and task allocation. Journal of Theoretical Biology 219:371-388.         [ Links ]

WEST MJ. 1967. Foundress associations in polistine wasps: dominance hierarchies and the evolution of social behavior. Science 157:1584-1585.         [ Links ]

WEST SA, I PEN, and AS GRIFFIN. 2002. Cooperation and competition between relatives. Science 296:72-75.         [ Links ]

WEST-EBERJARD MJ. 1975. The evolution of social behavior by kin selection. Quarterly Review of Biology 50:1-33.         [ Links ]

WEST-EBERHARD MJ. 1979. Sexual selection, social competition, and evolution. Proceedings of the American Philosophical Society 123:222-234.         [ Links ]

WEST-EBERHARD MJ. 2003. Developmental plasticity and evolution. Oxford University Press, Oxford, UK.         [ Links ]

WHITEN A and RW BYRNE. 1997. Machiavellian intelligence II: extensions and evaluations. Cambridge University Press, Cambridge, UK.         [ Links ]

WILSON DS. 1975. A theory of group selection. Proceedings of the National Academy of Sciences of the United States of America 72:143-146.         [ Links ]

WILSON DS. 1980. The natural selection of populations and communities. The Benjamin/Cummings Publishing Company, Inc., Menlo Park, CA, USA.         [ Links ]

WILSON EO. 1975. Sociobiology: a new synthesis. Belknap, Cambridge, MA, USA.         [ Links ]

WITTENBERGER JF. 1980. Group size and polygamy in social mammals. The American Naturalist 115:197-222.         [ Links ]

WOLFF JO and DW MAC DONALD. 2004. Promiscuous females protect their offspring. Trends in Ecology and Evolution 19:127-134.         [ Links ]

WRANGHAM RW. 1980. An ecological model of female-bonded primate groups. Behaviour 75:262-300.         [ Links ]

WRANGHAM RW. 1987. Evolution of social structure. Pp. 282-296 In Primate societies (BB Smuts, DL Cheney, RM Seyfarth, RW Wrangham, and TT Struhsaker, Eds.), The University of Chicago Press, Chicago        [ Links ]

Recibido 23 junio 2004.
Aceptación final 18 marzo 2005.

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