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).

Introduction

A central question in life history research is the extent of variation and potential constraints of life history traits within a species and between closely related species. The life history of any species is determined by developmental and reproductive rates as well as reproductive effort spent over its lifetime (Stearns, 1992). These traits are usually assessed by gestation length, number and size of offspring at birth, body mass and age at weaning, patterns of postnatal growth, age at first reproduction, interbirth interval, and lifespan. Intraspecific variation in life history pattern has been found in non-human primate species in the wild, and is often attributed to different socioecological factors such as social status, group size, predation risk, diet, and abiotic environmental conditions (Kappeler and Perreira, 2003; Jones, 2011). Thus, for example, in baboons, it was described that some life history patterns such as age at first reproduction or longevity are affected by rank and the quality of social bonds, matriline, nutritive condition and parasite load (e.g. Altmann and Alberts, 2003; Altmann et al., 2010, 2012; Silk et al., 2010; Gesquière et al., 2011). In a controlled laboratory setting, experimentally induced caloric restriction has been found to affect life history patterns such as longevity in rhesus macaques (Colman et al., 2009; but see Mattison et al., 2012 for contrary results in another colony). In mouse lemurs caloric restriction does not generally seem to affect aging (Dal-Pan et al., 2011), but lifespan was extended under caloric restriction when food was supplemented with resveratrol (Marchal et al., 2013). Interspecific life history variation is common between species of different primate lineages and forms the basis for life history theory (e.g. Stearns, 1992; Kappeler and Perreira, 2003; Zimmermann and Radespiel, 2007, 2014). It is postulated that life history trait variation between closely related species should be minor, due to a long common history in the past and the same phylogenetic constraints shaping life history (Harvey and Clutton-Brock, 1985; Kamilar and Cooper, 2013). Thus, it is important to understand which determinants modify the variation of life history patterns in a species to get insight into environmental and phylogenetic plasticity.

Introduction

How and why species emerge, persist, and become extinct is a central and controversially debated topic in evolutionary biology (Martin, 1990; Meyer, 1993; Masters, 1999; Mayr, 1999; see also Chapter 1). Acoustic signaling systems are known to mediate discrimination within and between species and play a major role in speciation and evolution (Wilkins et al., 2013). However, empirical research on this topic for primates is currently in its infancy.

Most research related to this topic comes from various non-mammalian animal groups, such as birds (e.g. Irwin et al., 2008; Podos, 2010), frogs (e.g. Amézquita et al., 2011; Willink et al., 2014), and insects (e.g. McNett and Cocroft, 2008), although singing mice present a rare exception for mammals (Campbell et al., 2010). Current comparative bioacoustic research suggests that three major selective forces drive acoustic divergence within and among species, favoring speciation and evolution (see Figure 21.1): adaptive mechanisms such as ecological and sexual selection as well as neutral mechanisms such as drift. For instance, in Darwin finches (Geospiza ssp.), climate constraints shape feeding ecology and thereby bill shape and indirectly the structure of trill calls in their song (Podos, 2010). Ecological selection for beak size results in acoustic and population divergence through assortative mating. Sexual selection following host shifts is strongly supported for treehoppers (McNett and Cocroft, 2008), in which the frequency of a pure tone mating signal favors species divergence. Sexual selection for song complexity along a gradient and drift are proposed to explain song divergence in greenish warblers (Irwin et al., 2008), whereas only drift is suggested to be the driving force for divergence in singing mice (Campbell et al., 2010).

Disentangling the relative contributions of these selective forces for the evolution of acoustic divergence and species diversity is urgently needed (Wilkins et al., 2013). For primates, a first and important step in this direction is to study the extent that acoustic divergence in communication is present and biologically relevant. It is also important to examine these aspects in genetically characterized species with known sympatric and allopatric distribution and varying in ranges, habitat, and body mass.

Introduction

Many conservation biologists consider the lemurs of Madagascar to be one of the world's highest conservation priorities (Rylands and Konstant, 2000; Allnutt et al., 2008; Kremen et al., 2008). Of the 103 extant lemurs species monitored under the International Union for Conservation of Nature (IUCN) Red List, 70.8% (N = 73 species) are endangered or critically endangered. Moreover, 6 lemurs are on the most recent list of the 25 most endangered primates: Eulemur flavifrons, Lepilemur septentrionalis, Propithecus candidus, Microcebus berthae, Varecia rubra, and Indri indri (Mittermeier et al., 2012). Considerable research and conservation efforts have been applied to studies of some threatened lemur species and their forest habitats (e.g., Kremen et al., 1999; Seddon et al., 2000; Andrianandrasana et al., 2005). As a result of these efforts, there is a rich literature on the status of some rare lemur species and the need for concerted efforts to integrate local communities with conservation biology programs in the establishment and maintenance of protected areas (Schwitzer et al., 2014). However, most of these efforts have been applied to diurnal, large-bodied taxa, such as species in the genus Propithecus (Banks et al., 2007; Patel and Andrianandrasana, 2008; Irwin et al., 2009; Quéméré et al., 2010).

Although the Cheirogaleidae represents the most speciose lemur family, with 35 species described to date (Chapter 2; IUCN), there are relatively few data on the conservation assessments and threats experienced by taxa in this family compared to large-bodied, diurnal taxa in Madagascar. This lack of conservation attention arises, in part, from suggestions that small-bodied, nocturnal taxa have relatively low extinction risks, are ubiquitous in their geographic distribution, suffer least from anthropogenic disturbance (e.g., hunting and deforestation), and have physiological adaptations such as torpor and hibernation in many species that mitigate extinction threats (Cardillo, 2003; Liow et al., 2009; Hanna and Cardillo, 2014). The most endangered cheirogaleids have not benefitted from conservation campaigns focusing on charismatic species, due largely to their nocturnality and concomitant difficulties in visual access for tourists. Recent assessments of extinction risks in lemurs indicate increased conservation concerns for many cheirogaleids, particularly in light of studies indicating the critical role of some species as seed dispersers for endemic fruiting plants (Valenta et al., 2013), and their high levels of phylogenetic diversity (Lehman, 2006).