Like other animals, primates employ an impressive battery of defenses to prevent or respond to attacks from disease-causing organisms. These anti-parasite strategies include immune defenses to combat infections and behavioral defenses to avoid parasites in the environment. Some host defenses have a strong genetic basis, as illustrated by the importance of diverse genes at the major histocompatibility complex (MHC) in the ability of vertebrate animals to recognize and respond to diverse pathogens (Hedrick and Kim 2000; Knapp 2005). Other defenses are phenotypically plastic or learned, such as when primates use medicinal plants to eliminate gastrointestinal helminths (Huffman et al. 1996), or when they avoid parasites spread through fecal contamination of the environment (Freeland 1980; Hausfater and Meade 1982). In many cases, resistance-conferring traits are costly in terms of time or energy that could otherwise be spent foraging, reproducing, or defending territories (Webster and Woolhouse 1999). Inducible immune or behavioral defenses activated upon infection might be less costly and relatively effective in responding to rare or unpredictable risks of infection (Harvell 1990).
Disease-causing organisms enter their hosts using a variety of mechanisms, and these entry points act as selective pressures on immune and behavioral defenses. Some parasites gain access through portals provided by cuts and skin abrasions. Vector-borne parasites like malaria enter when biting arthropods pierce the skin and effectively inject the parasite, potentially favoring behavioral strategies to avoid contact with the vectors. Similarly, cercariae (free-swimming intermediate stages of schistosomes) and hookworm larvae burrow directly into the skin of vertebrate hosts (Schmidt et al. 2000), possibly leading to selection on animals to avoid prolonged contact with water and moist soil. Parasites can also enter their hosts through mucous membranes at epithelial sites in the respiratory, gastrointestinal, and urogenital tracts. Once inside a host, parasites move to the blood, lungs, digestive tract, or other host tissues to initiate growth and replication.
In this chapter we examine the incredible array of defenses employed by free-living primates to prevent initial infection and limit subsequent parasite replication. We begin by considering strategies for parasite removal, including immune responses, self-medication, and grooming behavior. In the second section, we review behavioral strategies that primates use to limit the risk of encountering parasites. Finally, we investigate the links between sexual selection and parasites, focusing on mate choice related to parasite avoidance, selection of healthy caregivers, and the indirect benefits of "good genes." This chapter focuses primarily on individual-level strategies, such as the immune system and behavioral defenses. Chapter 6 builds on these ideas by considering properties of mating and social systems that serve as defenses to infectious disease.
When reading this chapter, it is essential to remember that host behavioral and immune defenses are part of a coevolutionary "arms race" that takes place between hosts and parasites (Hamilton 1982; Hart 1994; Frank 2002). Parasites influence host immunity and other host defenses, which exerts reciprocal selection pressure on the parasite, including selection for alternative transmission strategies, manipulation of host behavior, and changes in virulence (Knell 1999; Mackinnon and Read 2004). Another crucial aspect of behavioral and immune defenses is that they are often costly to implement in terms of energy expenditure, life history tradeoffs, and opportunity costs (Hart 1994; Sheldon and Verhulst 1996; Moret and Schmid-Hempel 2000). Moreover, defenses employed against one parasite could increase vulnerability to other parasites, and an important area for future research involves developing a better understanding of costs of resistance and tradeoffs in host-parasite interactions. Such investigations require means of reliably measuring both immune and behavioral defenses in the wild and their correlations with other fitness-related traits (Norris and Evans 2000).
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