Questions terminology and underlying principles

Make Him a Monogamy Junkie

The Monogamy Method

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1.1 Introduction

Parasites are ubiquitous in the lives of primates, and infectious diseases can cause devastating mortality in wild populations, including recent deaths arising from Ebola hemorrhagic fever and anthrax infections in African apes (Walsh et al. 2003b; Leendertz 2004). An incredible diversity of parasites inhabits primate hosts, including sexually transmitted viruses, insect-borne protozoa that cause malaria, and helminths responsible for schistosomiasis and tapeworm infections. More than 50 different parasite species have been documented in some free-ranging primate species, such as olive and yellow baboons (Nunn et al. 2003a), and an individual primate may shed hundreds or thousands of parasite infectious stages over the course of a single day (Pitchford and Visser 1975; Müller-Graf et al. 1996; Nizeyi et al. 1999).

Many of these infectious agents, such as simian immunodeficiency viruses (SIVs), are relatively benign in their natural hosts, and thus have virtually undetectable effects on primate fitness. Others, such as Ebola, have caused alarming declines in primate populations and therefore play a major role in conservation efforts (Chapman et al. 2005a). Still other parasites, including intestinal worms and blood-borne protozoa, have more cryptic effects on primate survival or fecundity in the short term, but taken together their cumulative impacts could be enormous. Not to be overlooked are the myriad of ways that parasites affect patterns of primate behavior, including foraging decisions, behavioral defenses to insect vectors, and mating and social interactions.

Behavioral ecologists have highlighted a variety of ecological and social factors that underlie primate mating and social systems, including predation, resource competition, and inter-sexual conflict (Wrangham 1980; Dunbar 1988; van Schaik 1989, 1996; Smuts and Smuts 1993). Infectious disease represents another potential ecological force in primate social evolution, but the role of parasites in primate socioecology has received remarkably little attention compared to other factors. This omission is extraordinary given that social animals such as primates are expected to be at unusually high risk from infectious diseases, in part because greater contact rates among individuals in social networks should facilitate the spread of infectious disease (M0ller et al. 1993; Altizer et al. 2003b). Primates are an ideal group for investigating the links between parasites and socioecology because much is known about their basic biology, including life history traits, diet, habitat use, and mating patterns (Smuts et al. 1987; Lee 1999; Kappeler and Pereira 2003). This extensive knowledge base makes it possible to investigate the effects of parasites against the background of other ecological forces that influence social systems.

The goal of this book is to examine the links between parasitism and primate behavior, ecology and evolution. Although we focus on primates, many of the principles and approaches developed here apply to a wide range of animals, including other mammals, birds, and insects. A question central to this book is "what factors influence disease risk"? In other words, what intrinsic host characteristics and environmental parameters determine the number and types of parasites infecting wild animals at the individual, population, and species levels? A second and related question is "how can animals reduce this risk"? Data exist to test a broad range of hypotheses related to these two questions, although further research is needed to link many of these predictions with real-world data and to experimentally investigate key hypotheses. Given recent theoretical and empirical developments in wildlife epidemiology, this is an exciting and dynamic time to investigate these questions. We cannot yet hope to provide a definitive treatise; instead, we identify key hypotheses concerning the role of infectious disease in primate mating and social systems, synthesize existing evidence for these hypotheses, and identify future directions for testing predictions through field, comparative, and theoretical approaches.

We also explore the implications of infectious disease in nonhuman primates for both public health and conservation concerns. Humans are clearly the best studied of all primate species in terms of infectious diseases, and pathogens continue to impact human health around the world. The origins of multiple pathogens that crossed into humans both recently and thousands of years ago can be traced to nonhuman primates, with examples including malaria and several retroviral diseases, the best known of which is HIV/AIDS. Understanding the links between parasites and primate socioecology should provide new insights to human health in a broad ecological and evolutionary context, expanding the domain of Darwinian medicine (Ewald 1980; Nesse and Williams 1996; Stearns 1999; Trevathan et al. 1999), and generating new hypotheses to test across human societies at a global scale (Low 1987; Guegan et al. 2001; Guernier et al. 2004). Furthermore, epidemiological insights drawn from studies of infectious diseases in humans can advance our understanding of disease spread in nonhuman primates, which is critical for conserving endangered primates increasingly at risk from emerging pathogens and other anthropogenic threats (Wallis and Lee 1999; Walsh et al. 2003b).

To set the stage for the rest of the book, in this introductory chapter we begin by defining key terms and providing a historical overview of previous research on the interplay between ecological factors and primate sociality. To emphasize the ecological impacts of infectious diseases and their potential role as selective agents, we conclude the chapter by reviewing the effects of parasites on host fitness in wild primate populations.

1.2 Essential terminology: parasite, disease, and disease risk

1.2.1 What is a parasite?

The word parasite has different meanings depending on the discipline in which it is used and how it is applied. In this book, we use the ecological definition of a parasite as any organism that lives on and draws nutrients from another living organism (the host), usually to the host's detriment. Parasites not only drain material resources from their hosts, but can also exploit host metabolism and behavior. Combes (2001) refers to host-parasite relationships as "durable interactions", in contrast to predator-prey relationships that are of shorter duration and result in death of the prey. The definition of parasite we use excludes some groups of organisms that have a close association with primate hosts, such as symbiotic bacteria that aid digestion of leaves in colobines (Bauchop and Martucci 1968). This definition also excludes mosquitoes and other highly mobile arthropods that feed on blood or other host resources. As with predators, their associations with hosts tend to be ephemeral at the level of individual animals; hence, these biting insects are more accurately described as "micro-predators" (Bush et al. 2001). However, many blood-feeding arthropods play an important role as vectors for parasites that infect primate hosts, including vector-borne protozoa, nematodes, and viruses. As such, many behavioral defenses against parasitism target arthropod vectors that are responsible for the spread of these parasites.

An important distinction made by Anderson and May (1979, 1991) is that parasitic organisms can be categorized either as microparasites or as macroparasites. Microparasites are often referred to as pathogens or disease-causing microbes and include viruses, bacteria, protozoa, and fungi, whereas macroparasites typically include worms (helminths) and arthropods. The distinction between micro- and macroparasites is useful to ecologists and epidemiologists, as these groups differ in the degree of within-host replication, factors affecting their population dynamics, and how they are measured in natural populations. Later chapters address these fundamental differences in more detail, and also consider additional classifications of parasites, with special attention to parasite characteristics that govern their transmission within populations and between species.

1.2.2 Parasite and disease

The terms "parasite" and "disease" are often used interchangeably, yet it is incorrect to do so. Disease refers to the pathology caused by infection, including outward physical signs and internal or behavioral changes, whereas parasites are the disease-causing organisms. A related term is pathogen, which refers to any disease-causing agent, although this term is most commonly used for microbial parasites (viruses and bacteria). In this book, we primarily use the term parasite to refer to all infectious organisms that can potentially harm their hosts, but occasionally substitute related words when appropriate (e.g. pathogen, infectious agent).

Although not all infections are pathogenic, parasitic organisms can cause a staggering array of pathologies in primate hosts (e.g. Kuntz 1982). These manifestations might result directly from activities of the parasite, as in the painful migration of warble flies through the flesh of large mammals (Bush et al. 2001; Colwell 2001), or as diarrhea resulting from reduced intestinal water absorption caused by Giardia (Olson and Buret 2001). Physiological consequences of parasite infection in the host usually fall into one of three categories—those that benefit the parasite, those that benefit the host, and those that are byproducts of infection and benefit neither host nor parasite (Ewald 1980; Dawkins 1982; Holmes and Zohar 1994; Thompson 1994b). For example, several arthropod-borne parasites clog the insect vector's digestive systems and impair their ability to obtain a full blood meal, thereby increasing the biting rate of these vectors to the parasites' advantage (and to the detriment of the host, Koella et al. 1998). On the other hand, a rise in host body temperature (fever) following infection can interfere with the growth of some parasites and facilitate a more intense immune response, in this case to the host's advantage (Ewald 1994a).

In some situations, pathology produced by the host's body in the context of infection actually can be harmful to host survival and reproductive success. Consider, for example, the famous images of elephantiasis of the lower extremities (lymphatic filariasis; Fig. 1.1). These horrifying pathologies are the result of complex, long-term immune responses to the mosquito-transmitted nematodes Brugia malayi and Wuchereria bancrofti (Bush et al. 2001). Interestingly, B. malayi is documented to occur in free-living Southeast Asian monkeys (Laing et al. 1960; Mak et al. 1982), but in these species the parasite does not cause the striking pathology found in humans (Orihel and Seibold 1972).

Parasites that induce detrimental pathology in hosts are more likely to regulate populations than those with weaker effects on host fitness (Scott and Dobson 1989). But it is important to keep two caveats in mind. First, when parasites affect host survival alone, standard host-parasite models (Anderson and May 1979, 1991) predict that parasites with low or intermediate effects on hosts will depress host density to a greater extent than parasites that cause high host mortality. This occurs because extremely harmful parasites are likely to kill their hosts before new transmission events occur, highlighting the kinds of insights that emerge when questions are addressed from a rigorous epidemiological modeling perspective—an approach described in later chapters. Thus, an important point to emerge from models is that parasites with low or moderate effects on hosts should not be overlooked when assessing sources of disease risk and potential causes of wildlife declines (McCallum 1994; McCallum and Dobson 1995). This point especially applies to parasites that affect host fecundity (or, in extreme cases sterilize their hosts), as theory predicts that such parasites can limit host recruitment and cause extreme reductions in host population size.

Second, counter to conventional wisdom, the most frequently observed parasites are not necessarily the ones most responsible for population declines (Anderson

Fig. 1.1 Woman in Ghana exhibits elephantiasis of the right leg and oedema of the left leg. Reprinted from the World Health Organization (WHO/TDR/Crump, image 9902944).

and Gordon 1982). Mathematical models predict that highly transmissible micro- or macroparasites with little or no fitness effects should be relatively common at the population level. In this case, the general host population will show relatively high levels of infection, and the parasite will be found incidentally among a large number of animals that die. Thus, high rates of parasitism in morbid or dead hosts do not necessarily indicate that the parasite in question is having a major impact on the population (McCallum and Dobson 1995). Later in this chapter and subsequent chapters, we discuss more appropriate ways to measure population-level impacts of parasites (Gulland 1992; Hudson et al. 1998b).

1.2.3 What is disease risk and how is it measured?

Throughout this book we refer to "disease risk" as the probability of acquiring an infectious disease. In using this term, we are approaching questions from the host's perspective, as the parasite would view this as an opportunity rather than a risk.

In most cases, we consider disease risk without factoring in the effects of parasites on individual host fitness or population size, in large part because these impacts are presently unknown for the vast majority of parasites in wild primates. In future studies, infectious disease risk could be quantified as some combination of the probability of acquiring an infectious disease and its fitness impact on the host.

At least two questions related to disease risk are of fundamental importance. First, what factors influence the risk of acquiring an infectious disease at the individual, population, and species levels, and second, how does this risk influence the evolution of host behavioral or immune defenses? Biologists have addressed components of these questions in primates (Freeland 1976; Nunn et al. 2000; Tutin 2000), and in other vertebrates (M0ller et al. 1993; Altizer et al. 2003b) and invertebrates (Schmid-Hempel 1998; Wilson et al. 2003). In reviewing past work and developing new hypotheses, we distinguish between two measures of disease risk. Intrinsic disease risk refers to the probability that an individual host encounters or acquires an infectious disease, whereas observed patterns of infection involve the presence and severity of infection at the individual level, or rates of occurrence at the population level. This distinction between intrinsic risk and infection rate should be familiar to primatologists, as it follows similar distinctions in the literature on intrinsic risk versus observed rates of predation in primates (Cowlishaw 1997; Hill and Dunbar 1998; Janson 1998; Nunn and van Schaik 2000).

Different questions sometimes require different measures of disease risk. In this book we refer to three ways of quantifying disease risk.

1. Quantitative measures of immune and behavioral defenses can be used to assay levels of risk, based on the reasoning that increased disease risk should select for increased expression and mobilization of host defenses (Harvey et al. 1991; M0ller and Saino 1994). These defenses can include behavioral avoidance or physical removal of parasites by preening or grooming, innate or generalized immune defenses, and the adaptive arm of the immune system, including antigen-specific responses (Roitt et al. 1998). For example, Fig. 1.2 shows results from a study that used counts of circulating white blood cells to assay disease risk across a large number of primate species. This figure shows that more promiscuous primate species have higher white blood cell counts, consistent with the hypothesis that risk of acquiring sexually transmitted diseases (STDs) increases when individuals have more mating partners (Nunn et al. 2000; Nunn 2002a; Anderson et al. 2004). Because immune response was not measured directly, these counts are more likely to reflect variation in innate or baseline defenses.

2. Another gauge of risk concerns the number of parasite species to which a host is exposed. Empirical measures include observed parasite community diversity within single host populations, or parasite species richness at the level of host species or broader taxonomic scales (e.g. Morand and Poulin 2000; Nunn et al. 2003a). A related measure acknowledges that pathogens might "spillover" from one host species to individuals of another species (Daszak et al. 2000; Cleaveland et al. 2001; Haydon et al. 2002a; Fenton and Pedersen 2005). Such risk can be quantified using

Contrasts in relative testes mass

Fig. 1.2 Variation in overall white blood cell counts in relation to mating promiscuity in primates. Mating promiscuity was measured as testes mass after controlling for body mass; as a measure of sperm competition, relative testes mass quantifies female mating promiscuity. Data points represent independent contrasts based on the phylogeny of Purvis (1995). Altered slightly from figure 5 in Nunn, C. L. 2002. A comparative study of leukocyte countsand disease risk in primates. Evolution 56:177-190. Reproduced with permission from the Society for the Study of Evolution.

Contrasts in relative testes mass

Fig. 1.2 Variation in overall white blood cell counts in relation to mating promiscuity in primates. Mating promiscuity was measured as testes mass after controlling for body mass; as a measure of sperm competition, relative testes mass quantifies female mating promiscuity. Data points represent independent contrasts based on the phylogeny of Purvis (1995). Altered slightly from figure 5 in Nunn, C. L. 2002. A comparative study of leukocyte countsand disease risk in primates. Evolution 56:177-190. Reproduced with permission from the Society for the Study of Evolution.

information on the parasites known to occur across multiple host species within a focal host's habitat or geographic range, such as those found in geographically overlapping (sympatric) host populations.

3. Finally, it is possible to quantify observed levels of infection in a population based on the prevalence, intensity, and abundance of parasites. Prevalence refers to the proportion of individuals in a population or sub-group that are infected with a parasite. A related term, incidence, refers to the rate at which new cases occur, or the change in prevalence over a specified time interval. An individual's infection status can be determined based on direct isolation of the parasite itself, physical signs of infection, or using serum antibodies produced by the host in response to infection, also called seroprevalence. Estimates of seroprevalence should be interpreted cautiously, however, because these antibodies could indicate past exposure rather than current levels of infection. Intensity of infection refers to the number of parasites (i.e. parasite load) within infected hosts only, and abundance measures the mean parasite load of the entire host population. As such, these latter two measures might indicate the total population size of parasites themselves and their quantitative impacts in draining host resources and damaging host tissues.

1.3 Ecological drivers of primate sociality

Socioecologists investigate the ecological basis of social and mating systems, largely through field and comparative studies (Struhsaker 1969; Crook 1970; Sterck et al. 1997; Lee 1999; Harcourt 2001). In terms of primate socioecology, models for ecological determinants of primate mating and social systems initially grew from the pioneering work of Crook and Gartlan (1966). These authors proposed that the environment and sexual selection determined "grades" of primate sociality. Under this scenario, grades were identified as discrete transitions from nocturnal, solitary primates that consume insects, to diurnal species living in socially structured groups in more open environments. The emergence of sociobiology in the 1970s (Wilson 1975; Trivers 1985; Segerstrale 2000) pointed to a larger number of factors influencing primate socioecology, including infanticide as a male reproductive tactic that is costly to females (Hrdy 1974; Hausfater and Hrdy 1984).

Throughout the 1960s and 1970s, long-term field studies of baboons, chimpanzees, gorillas, and langurs provided further insights to primate sociality and ecology (e.g. Altmann and Altmann 1970; Hrdy 1977; Fossey 1983; Goodall 1986), including the role of communication, resource acquisition, predation, and infanticide. Pioneering comparative studies of trait evolution focused on the functional basis of variation across species, including studies by Clutton-Brock et al. (1976,1977,1980), Milton and May (1976), and Mitani and Rodman (1979). These studies identified the primary axes of variation in primate socioecology, namely body size, sex ratio, home range size, diet, group size, and life history features. Results of these studies revealed some of our core knowledge of the traits that vary among primate species, including that sexual dimorphism increases when male intrasexual competition for mates increases; that ranging patterns correlate with diet, group size, defense of the home range, and body mass; and that life history traits correlate with body mass (see also Nunn and van Schaik 2001).

This book uses several terms to describe broad aspects of primate sociality. Social organization is commonly used to describe the size, composition, and spatial distribution of groups; it specifies how individuals in a population are organized into social units (Kappeler and van Schaik 2002). Key dimensions of social organization in primates include group size, number of adult males and females, age structure, and measures of territoriality (e.g. the defensibility index, Mitani and Rodman 1979). Social structure addresses how individuals interact within primate groups, focusing on patterns of individual behavior and the type and frequency of interactions, such as aggression, grooming, cooperative breeding, and food sharing (Kappeler and van Schaik 2002). Mating system describes patterns of mating contact among individuals, with categories that include monogamy, polygyny (one male mating with multiple females), polygnyandry (both sexes having multiple partners), and polyandry (one female mating with multiple males, see Clutton-Brock 1989 for an overview). Finally, the social system combines both social organization and social structure to describe overall patterns of interaction in the context of group size and composition. Embedded within this framework is the important issue of dispersal, with one or both sexes typically emigrating (Moore 1984; Pusey and Packer 1987).

Modern views of primate socioecology focus on factors that influence different components of social systems, particularly the size and composition of groups, relationships among individuals, and intergroup dispersal. Four main ecological forces have been proposed as key drivers of primate social evolution: resource competition, predation, inter-sexual conflict, and infectious disease. In what follows, we briefly review the major conceptual models that were built around these ecological factors. Further details are available in Smuts et al. (1987), Dunbar (1988), Janson (1992, 2000), Sterck et al. (1997), Isbell and Young (2002), and Nunn and van Schaik (2000).

1.3.1 Between-group resource competition

Wrangham (1980) first proposed that females living in social groups experience a major advantage in competing with other groups for resources. This early and influential model of primate social systems proposed that larger groups of females dominated smaller groups at preferred feeding sites, thus obtaining greater food rewards. Wrangham's model was used to explain the evolution of "female-bonded" kin groups in which related individuals remained in differentiated networks of social relationships rather than living alone. Although between-group competition might provide an advantage to larger groups when population densities are high, more recent studies suggest that resource competition probably does not represent a primary selective force driving the formation of female social relationships (Cheney 1992; Cowlishaw 1995; Sterck et al. 1997; Matsumura 1999). Instead, predation and competition among females within groups, as discussed next, probably play a larger role.

1.3.2 Predation and within-group competition

In response to Wrangham's (1980) model of primate socioecology, van Schaik (1983, 1989) proposed that female primates form groups to reduce their risk of predation (following on previous researchers, for example, Alexander 1974). Several studies supported this general hypothesis (Krause and Ruxton 2002). For example, van Schaik et al. (1983) found a significant association between group size and the ease with which animals detected a (human) predator. Similarly, in a comparative study of cercopithecoid primates, Hill and Lee (1998) found that group size increased in populations that experienced greater predation risk.

Once individuals form groups to counter predation risk, the effects of within-group feeding competition were hypothesized to influence female relationships within groups (van Schaik 1989; Janson 1992). The intensity of competition will increase when food patches are small, distributed patchily, or when female spatial clumping is high for other reasons (Janson 1988b). Where the potential for within-group contest competition is high, female-bonded groups show decided dominance relationships, alliances with relatives, and female philopatry (van Schaik 1989; Isbell 1991; Sterck et al. 1997), as supported by cumulative evidence from detailed behavioral studies (e.g. Mitchell et al. 1991; Barton et al. 1996; Isbell and Pruetz 1998; Koenig et al. 1998).

1.3.3 Inter-sexual conflict

Recent attention has focused on male behavior as a selective force affecting female sociality, although it has long been recognized that the social context might be as important as ecological factors in influencing primate mating and social systems (Clutton-Brock and Harvey 1976; Wrangham 1979). Males can use sexual coercion, involving actual or threatened force, to increase their access to mates and to reduce the probability that females mate with other males (see also Clutton-Brock and Parker 1995). Sexual coercion by male primates includes forced copulation, infanticide to shorten the time to fertility, and herding behavior (a form of mate-guarding) to prevent females from copulating with other males. Infanticide in particular has been proposed as a major force on primate behavior (Hrdy 1974; Hausfater and Hrdy 1984; van Schaik and Janson 2000). Females can counter male coercion by forming special relationships with "protector" males and other females (Smuts 1985; Palombit et al. 1997). Thus, female counterstrategies to infanticide can generate variation in mating and social systems, including patterns of male-female associations (van Schaik and Kappeler 1997), female coalitions (Treves and Chapman 1996), and possibly even the evolution of monogamy (van Schaik and Dunbar 1990; cf. Palombit 2000).

1.3.4 Infectious disease

In a series of pioneering papers in the late 1970s, Freeland proposed that primate social interactions and behavior have evolved in ways that reduce the risks of acquiring infectious diseases (Freeland 1976, 1977, 1979, 1980). As one example, Freeland (1977) hypothesized that multi-species associations, in which individuals from different primate species aggregate together, reduce individual rates of attack by blood-sucking flies (Fig. 1.3) in a process analogous to the encounter-dilution effect used by animals to reduce predation by living in groups (see Mooring and Hart 1992; Krause and Ruxton 2002). He even used himself as a human "guinea pig" by sitting on a platform 20 m above the forest floor from dawn until dark, recording the number of bites to his bare arms and legs throughout the day. Freeland was interested in a wide variety of links between primate socioecology and disease risk, proposing, for example, that variation in rates of exchange of individuals between groups was influenced by variation in disease risk (Freeland 1979), and that primate arboreal ranging patterns were linked to avoidance of fecal-contaminated pathways (Freeland 1980). More recently, Loehle (1995) reinvigorated discussion about disease and social barriers to transmission across a wide variety of animals (including primates), with hypotheses linked directly to modes of parasite transmission.

Freeland's proposals remain provocative and interesting, but largely untested. Many of his hypotheses require careful consideration of alternative ideas, because

Time of day

Fig. 1.3 One of the earliest studies of primate social behavior in relation to infectious disease risk. Plot shows polyspecific associations and biting fly attacks in Kibale, Uganda (data from Freeland 1977). Open circles show the occurrence of polyspecific associations by a group of mangabeys (Cercocebus albigena), with associations defined as the presence of an individual of another species within 20 m of the nearest mangabey. Closed circles are the occurrence of biting fly attacks (mosquitoes and other insects) measured on humans at the site. Spearman rank correlation=0.63, which is significant (P < 0.05) in a one-tailed test.

Time of day

Fig. 1.3 One of the earliest studies of primate social behavior in relation to infectious disease risk. Plot shows polyspecific associations and biting fly attacks in Kibale, Uganda (data from Freeland 1977). Open circles show the occurrence of polyspecific associations by a group of mangabeys (Cercocebus albigena), with associations defined as the presence of an individual of another species within 20 m of the nearest mangabey. Closed circles are the occurrence of biting fly attacks (mosquitoes and other insects) measured on humans at the site. Spearman rank correlation=0.63, which is significant (P < 0.05) in a one-tailed test.

other ecological and social factors make predictions similar to those involving disease risk. The case of dispersal between groups provides an intuitive and accessible example of how alternative hypotheses could also account for behavioral patterns that might be linked with disease. Thus, Freeland (1976) noted that in many primate species, animals must endure a lengthy process to disperse from one group and assimilate into a new one. As an explanation, he proposed that individuals are forced to undergo a period of harassment prior to successfully transferring into a new group, during which time any latent infections might be expressed (with stressful challenges used to identify infectious immigrants). But an alternative hypothesis asserts that primates exclude potential immigrants to reduce competition for mates (among males) or resources (among both sexes)—and this might even be a more plausible explanation for resistance by group members to potential immigrants.

At one level, the consequences of sociality and group living for infectious disease seem relatively straightforward, in that animals living in close proximity or with high contact rates should experience higher rates of parasite transmission. Thus, more social primate species should have higher parasite prevalence and more diverse parasite communities relative to species that are solitary or live at low density, and they should also experience more intense selection for behavioral or immune defenses (M0ller et al. 1993, 2001). This link between population density and greater disease risk emerges from models of directly-transmitted micro- and macroparasites (Anderson and May 1979, 1991). In fact, the relationship between disease risk and group size was noted by Alexander (1974) in an early review of the evolution of social behavior.

Several researchers of primate socioecology have tested hypotheses concerning disease risk and primate social systems. For example, Hausfater and Watson (1976) investigated the parasite loads of individual baboons based on social rank, finding that higher-ranking males exhibited increased levels of parasitism with intestinal helminths. In another influential paper, Hausfater and Meade (1982) investigated patterns of habitat use and parasitism in baboons. They proposed that risks from fecal-borne parasites that accumulate in the soil influence baboon ranging patterns and movement between sleeping sites. These and other papers represent some of the first attempts to formulate and test hypotheses for the links between infectious disease and the behavior and demography of free-living primates.

Compared to the rapid proliferation of studies addressing the socioecological consequences of predation, resource competition, and inter-sexual conflict, studies of parasites in relation to group living in primates have proceeded at a slow trickle. In many cases, authors offered lip service to the possibility that parasites influence primate socioecology, often citing one of Freeland's publications, but then moved on to examine another ecological factor in greater depth. This tendency to focus on other ecological factors probably reflects the challenges of quantifying parasitism or disease risk. As we show in the chapters that follow, tests of hypotheses involving infectious diseases are now more feasible (see also Heymann 1999; Janson 2000).

A brief history of infectious disease in primate socioecology would be incomplete without mentioning medicinal plant use as a way that primates can lower their parasite loads or alleviate the symptoms of disease (Chapter 5). Following a provocative paper by Janzen (1978), Wrangham and Nishida (1983) proposed that chimpanzees (Pan troglodytes) consume the leaves of Aspilia spp. for their pharmacological effects. Similarly, Phillips-Conroy (1986) proposed that baboons consume the leaves and berries of Balanites aegyptiaca to eliminate infection with schistosomes, based on evidence that consumption of the plant was more common in areas where schis-tosomiasis was most likely to occur (although a follow-up study in captive mice failed to support the proposed mechanism; Phillips-Conroy and Knopf 1986). A large number of studies in the late 1980s and 1990s have investigated the use of medicinal plants and consumption of soil in chimpanzees and other primates (Huffman 1997, 2006).

Finally, a publication by two evolutionary ecologists produced reverberations in a wide range of fields, including primatology. Hamilton and Zuk (1982) proposed that parasites are important in female mate choice, and that secondary sexual traits in males signal their infection loads or ability to resist parasites. This hypothesis predicted that within species, the brightest males should have the lowest parasite loads, but across species, those in which males have the most exaggerated traits should experience the greatest disease risk. In primate males, expression of good health could involve color signals, such as the bright faces of mandrills (Mandrillus

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