The influence of the father on offspring development in the striped mouse

When males of a species follow different reproductive strategies in different habitats, one might expect the strategy adopted to maximize fitness payoffs under particular ecological conditions. Striped mice (Rhabdomys pumilio) males in the moist grasslands of South Africa follow a roaming mating strategy, visiting several receptive females, and do not participate in parental care. In contrast, males in the arid succulent karoo are permanent members of social groups and help care for young. We predicted that paternal care leads to fitness benefits in striped mice from the succulent karoo but not from the grasslands. Experiments were conducted simultaneously in both locations under captive seminatural conditions to study offspring growth and survival to weaning in two experimental groups: father absent and father present. In the succulent karoo, offspring development was faster when the father was present, but the father's absence did not affect offspring growth in the grasslands. The significantly lower night temperatures in the succulent karoo compared to the grasslands negatively influenced offspring development during the first 3 days after birth, which in turn influenced offspring development until weaning. Exposure to low temperatures is energetically costly to free-living mice, as indicated by a greater loss of body weight during cold spring nights than warmer summer nights. We suggest that paternal care, particularly huddling of pups, improves offspring development in the succulent karoo, whereas the presence or absence of the father does not appear to directly influence offspring growth in the grasslands. The influence of the father on offspring development in the striped mouse Carsten Schradin and Neville Pillay Ecophysiological Studies Research Group, School of Animal, Plant and Environmental Sciences, University of the Witwatersrand, Private Bag 3, Wits 2050, Johannesburg, South Africa When males of a species follow different reproductive strategies in different habitats, one might expect the strategy adopted to maximize fitness payoffs under particular ecological conditions. Striped mice (Rhabdomys pumilio) males in the moist grasslands of South Africa follow a roaming mating strategy, visiting several receptive females, and do not participate in parental care. In contrast, males in the arid succulent karoo are permanent members of social groups and help care for young. We predicted that paternal care leads to fitness benefits in striped mice from the succulent karoo but not from the grasslands. Experiments were conducted simultaneously in both locations under captive seminatural conditions to study offspring growth and survival to weaning in two experimental groups: father absent and father present. In the succulent karoo, offspring development was faster when the father was present, but the father’s absence did not affect offspring growth in the grasslands. The significantly lower night temperatures in the succulent karoo compared to the grasslands negatively influenced offspring development during the first 3 days after birth, which in turn influenced offspring development until weaning. Exposure to low temperatures is energetically costly to free-living mice, as indicated by a greater loss of body weight during cold spring nights than warmer summer nights. We suggest that paternal care, particularly huddling of pups, improves offspring development in the succulent karoo, whereas the presence or absence of the father does not appear to directly influence offspring growth in the grasslands. [Behav Ecol 16:450–455 (2005)] Social flexibility, that is, intraspecific variation in social systems, is widely distributed among vertebrates (Lott, 1984). Differences in ecological conditions may well underpin these differences in social organization (Lott, 1991). In the pied kingfisher (Ceryle rudis), unrelated males associate with breeding pairs as helpers in habitats with poor or difficult foraging conditions, whereas only related males remain as helpers in habitats with a good food supply (Reyer, 1980, 1984). In the golden jackal (Canis aureus), groups of up to 20 individuals form in populations living in habitats with high food abundance, whereas monogamous pairs form in areas of low food abundance (Macdonald, 1979). Studies of social flexibility have considered mainly bird models, in which both ultimate and proximate explanations for social flexibility have been investigated (e.g., Davies et al., 1996; Parish and Coulson, 1998; Smith, 1995; Wingfield et al., 1990, 2000). Although social flexibility is also common in mammals (Lott, 1991), the reasons underlying such flexibility are seldom known and, if known, are poorly understood (McGuire and Getz, 1995). For example, prairie voles (Microtus ochrogaster) can be monogamous, solitary promiscuous, or polygynous dependingon the area inwhich theyoccur (Roberts et al., 1998) or even within the same population (McGuire and Getz, 1998), but the reasons for these variations in mating systems are not understood (McGuire and Getz, 1995). One mammal that offers a good opportunity for studying the ecological reasons for population differences in social organization is the African striped mouse (Rhabdomys pumilio). The striped mouse is a small (40 g), diurnal muroid rodent that occurs throughout southern Africa and parts of East Africa, inhabiting a wide range of habitats including moist grasslands and arid deserts (Kingdon, 1974). Whereas the striped mouse is solitary in grasslands (Brooks, 1974; Perrin, 1980; Schradin and Pillay, 2005b; Willan and Meester, 1989), it forms social groups in desert habitats (Schradin and Pillay, 2004). In the succulent karoo, a desert habitat, males are permanently associated with social groups containing several communally breeding females and share their territory with these females (Schradin and Pillay, 2004). Males also interact amicably with juveniles, retrieve pups (Schradin and Pillay, 2003), and participate in infant care inside the nest (unpublished data). In contrast, striped mice males in grasslands are solitary and do not associate with juveniles. Instead, males follow a roaming mating strategy, utilizing large home ranges that overlap with the home ranges of several females; males visit females only for mating (Schradin and Pillay, 2005b; Willan, 1982; Willan and Meester, 1989). In captivity, however, striped mice males from both the semimoist highveld grasslands and the arid succulent karoo of South Africa display well-developed paternal care (Schradin and Pillay, 2003). Evolutionary theory predicts that paternal care should occur only if it improves the father’s fitness (Trivers, 1972). Whether ornot paternal care leads to an increase infitnessmight depend on ecological conditions. It has been predicted, but never shown, that rodent males may exhibit flexibility in their social behavior, providing paternal care only under ecological conditions where this behavior improves fitness (Dewsbury, 1985). Accordingly, we predicted that paternal care leads to a higher fitness benefits for striped mice fathers in the arid succulent karoo than for fathers in the semimoist highveld grasslands. The likely ecological explanation for these differences in benefits was expected to be a difference inminimumnight temperature. As night temperatures are lower in the succulent karoo than in the highveld grasslands, huddling of the pups by the father might yield a significantly higher energetic benefit for offspring in the colder succulent karoo than in warmer grasslands. Paternal care in rodents enhances offspring development when animals are kept under conditions simulating the cold Address correspondence to C. Schradin. E-mail: schradin@mweb. co.za. Received 30 January 2004; revised 6 September 2004; accepted 22 October 2004. Behavioral Ecology doi:10.1093/beheco/ari015 Advance Access publication 8 December 2004 Behavioral Ecology vol. 16 no. 2 International Society for Behavioral Ecology 2004; all rights reserved. night temperatures experienced in nature (Cantoni and Brown, 1997; Gubernick et al., 1993) but not when animals are kept under ideal laboratory conditions with optimal ambient temperatures (Gerling and Yahr, 1979; Gubernick et al., 1993). In this study, we investigated whether the presence or absence of the father influenced the preweaning growth and survival of litters in the succulent karoo and in the highveld grasslands. Experiments were conducted simultaneously in both locations under captive seminatural conditions in which mice experienced natural variation in ambient temperatures. MATERIALS AND METHODS