The dawn of primate social complexity: kin selection in asocial mammals
Since Hamilton's ground-breaking theory of inclusive fitness in 1964, kin-biased behavior has been theorized to have played a crucial role in the evolution of mammalian sociality (Hamilton, 1964; de Waal and Tyack, 2003; Chapais and Berman, 2004). Given the amount of attention given to the topic over the subsequent decades, it is surprising that while group-living and social complexity has evolved multiple times in mammals, we still know very little about how this process occurs (Waser and Jones, 1983; Müller and Thalmann, 2000; de Waal and Tyack, 2003). In this section we review what is known about ancestral mammals and how they were the foundation for the evolution of ancestral primates.
Ancestral mammals are believed to have been asocial, as are many extant mammal species (Waser and Jones, 1983; Müller and Thalmann, 2000). Asocial species forage alone and maintain no relationships outside of the mating and infant-rearing seasons (Charles-Dominique, 1974, 1978; Waser and Jones, 1983; Müller and Thalmann, 2000). Interactions between adults, including adult kin, are marked by avoidance and aggression (Charles-Dominique, 1974; Waser and Jones, 1983; Müller and Thalmann, 2000). This is note-worthy because in many species, females typically disperse shorter distances than males, leading to a spatial clustering of female kin (Waser and Jones, 1983; Stoen et al., 2005; Maher, 2009). For many scientists, it is this spatial clustering of kin which is the first step towards increasing sociality (Waser and Jones, 1983; Perrin and Lehmann, 2001; Kappeler et al., 2002; Lutermann et al., 2006; Meshriy et al., 2011; Messier et al., 2012). The transition to group-living is believed to have occurred through solitary foraging (Müller and Thalmann, 2000). Extant solitary foragers forage alone, but, in contrast to the asocial mammalian ancestors, maintain year-round social networks, communicating with conspecifics via scent-marks and vocalizations (Charles-Dominique, 1974, 1978; Zimmermann, 1990, 1995a, 1995b, 2010; Müller and Thalmann, 2000; Nash, 2004; see also Chapter 21). Individuals may interact affiliatively during their active periods and sometimes sleep in social groups, often consisting of matrilineal kin, during the inactive periods (e.g., Radespiel et al., 2001b; Eberle and Kappeler 2006; for review, see Müller and Thalmann, 2000).
Studies of parasite burden and transmission in wild non-human primates are important for combating emerging infectious diseases in humans, understanding processes of zoonosis, and managing and conserving endangered species (Gillespie et al., 2008). In a biodiversity hotspot facing extreme anthropogenic pressure, lemurs are a high conservation priority (Schwitzer et al., 2014) and the relationship between lemur health and human health is only beginning to be understood (Bublitz et al., 2015; Zohdy et al., 2015). Mouse lemurs (Microcebus spp.) are well positioned to become a very useful model for endoparasite studies in lemurs. As a highly specious genus with 21 recognized species, they are widespread across the island of Madagascar, occurring in diverse habitats including rainforests, dry deciduous forests, littoral forests, etc. (Radespiel, 2006; Sommer et al., 2014; Zimmermann and Radespiel, 2014). In addition, species vary (within and between species) in their diets, use of torpor, degree of sociality, and sympatry with congeneric species (Lahann et al., 2006; Radespiel, 2006; Sommer et al., 2014; Chapter 22). This variation, combined with the ease with which they can be trapped, examined, and sampled without anesthesia, thus yielding reasonable sample sizes, makes them attractive for asking a multitude of questions with implications for understanding host–parasite coevolution, transmission dynamics and zoonosis, conservation, and wildlife management.
Mouse lemurs harbor, in particular, vector-borne parasites and direct lifecycle parasites (Radespiel et al., 2015). They may become infected with vector-borne parasites when feeding on arthropods serving as intermediate hosts (Radespiel et al., 2015). In addition, they are vulnerable to parasites with direct lifecycles when feeding in contaminated vegetation or co-sleeping in tree holes/nests with infected individuals who may defecate in the sleeping sites (Sommer et al., 2014; Radespiel et al., 2015). The endoparasite studies conducted to date have included foci on relationships between parasites and seasonality (Raharivololona and Ganzhorn, 2010), forest fragmentation (Schad et al., 2005), the genetics of parasite resistance (Schad et al., 2005; Schwensow et al., 2010a, 2010b; Sommer et al., 2014), sympatry among host mouse lemur species (Sommer et al., 2014; Radespiel et al., 2015), and parasites with the potential to be zoonotic with human populations (Rasambainarivo et al., 2013; Bublitz et al., 2015; Zohdy et al., 2015). Many of these studies were conducted within the last five years and meeting abstracts suggest that several other studies are underway (e.g., Alldredge et al., 2013, 2014; Rodriguez et al., 2013).
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