Mastozoología Neotropical ISSN: 0327-9383 [email protected] Sociedad Argentina para el Estudio de los Mamíferos Argentina Jones, Clara B. Social parasitism in mammals with particular reference to Neotropical primates Mastozoología Neotropical, vol. 12, núm. 1, enero-junio, 2005, pp. 19-35 Sociedad Argentina para el Estudio de los Mamíferos Tucumán, Argentina Available in: http://www.redalyc.org/articulo.oa?id=45712103 How to cite Complete issue Scientific Information System More information about this article Network of Scientific Journals from Latin America, the Caribbean, Spain and Portugal Journal's homepage in redalyc.org Non-profit academic project, developed under the open access initiative Mastozoología Neotropical, 12(1):19-35, Mendoza, 2005 ISSN 0327-9383 ©SAREM, 2005 Versión on-line ISSN 1666-0536 SOCIAL PARASITISM IN MAMMALS WITH PARTICULAR REFERENCE TO NEOTROPICAL PRIMATES Clara B. Jones Department of Psychology, Fayetteville State University. Fayetteville, NC 28301, USA. [email protected] 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 para- sitism”, 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 intraspe- cific 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 trans- mission 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 understand- ing 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. INTRODUCTION 2002), reciprocal altruism (Trivers, 1971), manipulation (West-Eberhard, 1975; Ridley and Dawkins (1999: 69) proposed that, “Any ner- Dawkins, 1981; Stuart, 2002), and/or “trait vous system can be subverted if treated in the group” selection (DS Wilson, 1975), are fun- right way.” Consistent with this view, group- damental schemas in most attempts to explain living individuals often act in ways that appear the evolution of social behavior in invertebrate to benefit others (altruism) instead of them- and vertebrate societies. Students of social selves (selfishness or cooperation). Several behavior have been particularly concerned with hypotheses have been advanced to explain those interindividual interactions in which one ostensibly altruistic behavior in which the do- individual’s responses benefit the genotypic nor bears a (genotypic or phenotypic) cost and and/or phenotypic interests of another (West, the recipient experiences a genotypic or phe- 1967; EO Wilson, 1975; West-Eberhard, 1979) notypic advantage over the donor or a third since these responses are not explained in a party. These hypotheses, kin selection straightforward manner by classical evolution- (Hamilton, 1964; Bertram, 1983; West et al., ary theory. Darwin (1859: 208) argued, for Recibido 23 junio 2004. Aceptación final 18 marzo 2005. 20 Mastozoología Neotropical, 12(1):19-35, Mendoza, 2005 C. B. Jones www.cricyt.edu.ar/mn.htm example, “[N]o instinct can be shown to have one’s own interests, a dilemma that is expected been produced for the good of other animals, to arise wherever interindividual (genotypic though animals take advantage of the instincts and/or phenotypic) conflicts of interest exist of others.” (Reeve and Keller, 1996). For mammals, the highest social grades are While the ecology of social parasitism has achieved among cooperatively breeding spe- not been studied thoroughly, Jamieson et al. cies such as the Latin American marmosets and (2000), studying parasitic birds, suggested that tamarins (Tardif, 1997; Abbott et al., 1998; social parasitism is most likely to be expressed Saltzman, 2003; also see Andersson, 1984; in temporally and spatially heterogeneous re- Emlen, 1991, 1995; Solomon and French, gimes. Furthermore, Savolainen and 1997) and the eusocial naked mole rats of Vepsäläinen (2003) argued that polygyny is a Africa (Sherman et al., 1991, 1995; Lacey and prerequisite for intraspecific social parasitism Sherman, 1997; Burland et al., 2004). In these and that social parasites are often related groups, some individuals, generally females, (“Emery’s rule”). Neotropical primates are an more or less temporarily (marmosets and tama- excellent test for these propositions because of rins: Cebidae, Primates) or more or less per- the extensive variability of their behavior and manently (naked mole rats: Bathyergidae, Ro- social organization (Fleagle, 1999). These stud- dentia) delay individual (selfish) reproduction ies have been initiated by O’Brien’s (1988) to assist dominant group members rear one or investigations of parasitic nursing by infant more offspring who are usually the helper’s Cebus olivaceus, Jones’ (1997a) research on kin. Altruistic behavior in these cases, then, is reproductive parasitism by female Alouatta thought to arise via kin selection in combina- palliata, and Treves’ (2001) review of the role tion with other factors (e.g., ecological effects of conspecific threat and constraints on indi- such as habitat saturation: Andersson, 1984; vidual fitness imposed by conspecifics in Emlen, 1991, 1995; Faulkes, et al. 1997) and Alouatta spp. The present paper explores the to be beneficial to the helper (host, victim). topic of intraspecific social parasitism (ISP) in Helping behavior and consequent reproductive mammals relying, in particular, upon examples suppression may represent a “decision” by the from the literature on Neotropical primates helper or may be imposed by a dominant (re- (Platyrrhini: Groves, 2001). productive parasite), often through mechanisms of behavioral “policing” or chemical commu- Defining criteria for the classification nication. of social parasitism It is relatively straightforward to formulate Mammalogists have probably not emphasized sound Darwinian hypotheses explaining altru- the role of social parasitism in the evolution of ism when the actor’s selfish interests appear to behavior and social organization among social be served. It has proven difficult, however, to mammals because the pertinent models have proffer credible evolutionary scenarios for been associated with the insect literature, in- numerous actions that appear counterintuitive vertebrate constructs that are rarely employed within a Darwinian paradigm (e.g., same sex for the investigation of mammals. Parasitism partner preference, homicide, suicide, delay- generally implies a non-fatal interspecific rela- ing or foregoing reproduction, spite, depen- tionship whereby one actor benefits at the ex- dency complexes, alloparenting: see, for ex- pense of another. The familiar parasite is a ample, Dawkins, 1999; Berdoy et al., 2000). fungus, virus, bacteria, protozoan, arthropod This challenge has led some researchers to or other small organism exploiting the tissues, propose group-level (Wilson, 1980) or other blood, or other products of a host (the victim). controversial constructs (Fehr and Henrich, This classical body of work on non-social 2003) to explain altruism (Kerr et al., 2004). parasitism is used in the present paper as a The evolutionary trap of altruism will exist conceptual framework for the analysis of so- when assisting another’s reproductive (geno- cial parasitism, in particular, intraspecific so- typic or phenotypic) interests is detrimental to cial parasitism (ISP). Social parasitism, some- SOCIAL PARASITISM IN MAMMALS 21 times termed “involuntary altruism,” implies close association, often, but not necessarily, associations characterized by an exploitative obligate, with a host for some part, if not most, relationship (interspecific or intraspecific) of its life (Begon and Mortimer, 1986). By whereby the parasite is wholly or partially definition, parasites obtain resources from and dependent upon the social behavior and/or harm their hosts, and only experimental stud- social organization of the host. As Poulin ies can determine whether or not these costs (2002) points out, all forms of parasitism re- harm the inclusive fitness of hosts beyond criti- flect Dawkins’ (1982) concept of the “extended cal threshold values (spite). Parasitism, then, phenotype” whereby exploitation by parasites implies dependency, a characteristic that may of their hosts can be viewed as the former predispose its expression where individuals expressing his/her genes in the latter. characterized by asymmetries live in groups Several patterns of social parasitism have and/or exhibit long lifespans, virtually ubiqui- been described. “Brood parasitism” is a type tous conditions for primates. of social