Development, Maternal Effects, and Behavioral Plasticity

Integrative and Comparative Biology Integrative and Comparative Biology, volume 54, number 5, pp. 841–849 doi:10.1093/icb/icu044 Society for Integrative and Comparative Biology SYMPOSIUM Development, Maternal Effects, and Behavioral Plasticity Jill M. Mateo1 Department of Comparative Human Development, 5730 South Woodlawn Avenue, Chicago, IL 60637, USA 1 E-mail: Synopsis Behavioral, hormonal, and genetic processes interact reciprocally, and differentially affect behavior depending on ecological and social contexts. When individual differences are favored either between or within environments, developmental plasticity would be expected. Parental effects provide a rich source for phenotypic plasticity, including anatomical, physiological, and behavioral traits, because parents respond to dynamic cues in their environment and can, in turn, influence offspring accordingly. Because these inter-generational changes are plastic, parents can respond rapidly to changing environments and produce offspring whose phenotypes are well suited for current conditions more quickly than occurs with changes based on evolution through natural selection. I review studies on developmental plasticity and resulting phenotypes in Belding’s ground squirrels (Urocitellus beldingi), an ideal species, given the competing demands to avoid predation while gaining sufficient weight to survive an upcoming hibernation, and the need for young to learn their survival behaviors. I will show how local environments and perceived risk of predation influence not only foraging, vigilance, and anti-predator behaviors, but also adrenal functioning, which may be especially important for obligate hibernators that face competing demands on the storage and mobilization of glucose. Mammalian behavioral development is sensitive to the social and physical environments provided by mothers during gestation and lactation. Therefore, maternal effects on offspring’s phenotypes, both positive and negative, can be particularly strong. Introduction Since the Modern Synthesis (Fisher 1930; Wright 1931; Haldane 1932), it has been well demonstrated that the traits of offspring are affected by parental genotypes, but recent attention has been paid to parental effects, or the ways in which a parent’s genotype or the environment influence the phenotype of the offspring. Parental effects may stem from the parents’ biotic and abiotic habitats, diet, physiology, and behavior. Such plastic, inter-generational effects can be adaptive, as parents respond quickly to changing environments and can produce offspring with traits well suited to current conditions (similar to the ‘‘maternal match hypothesis’’ of Love et al. [2013]; see also Cairns et al. 1990; Mousseau and Fox 1998). Less often considered, however, are negative maternal effects, when offspring resemble parental strategies in changed environments, and these strategies are not successful under the new conditions. See also Sheriff and Love (2013) for how ‘‘maternally derived stress’’ can have positive or negative outcomes for offspring, depending on their future environment, and Meylan et al. (2012) for how maternal effects can lead to adaptive responses to rapid climatic change. In mammals, behavioral development is highly sensitive to the physical and social environments provided by mothers during pre-natal and postnatal development (Reinhold 2002). Maternal physiology, food choices, habitat, and social partners can have substantive and lasting effects on offspring’s phenotypes. Functionally, these effects can be adaptive if offspring develop in environments similar to their mothers. They also contribute to individual variation within a population, with selection favoring alternative phenotypes depending on spatial and temporal changes in environmental and social conditions (reviewed by Stamps 2003; see also Mateo 2007a; McAdam 2009; Sheriff et al. 2010). Maternal effects can significantly influence the development of adaptive behaviors, including behaviors Advanced Access publication May 11, 2014  The Author 2014. Published by Oxford University Press on behalf of the Society for Integrative and Comparative Biology. All rights reserved. For permissions please email: . From the symposium ‘‘Adaptation or Developmental Constraint? Uniting Evolutionary Theory and Empirical Studies of Phenotypic Plasticity’’ presented at the annual meeting of the Society for Integrative and Comparative Biology, January 3–7, 2014 at Austin, Texas. 842 Maternal effects on survival behaviors in Belding’s ground squirrels Here I review several studies of anti-predator behavior to illustrate the potential for maternal effects on survival tactics, using Belding’s ground squirrels (Urocitellus beldingi) as a model. Ground squirrels are vulnerable to both aerial and terrestrial predators, and most species produce alarm calls that warn of danger from predators (see Owings and Hennessy 1984; Sherman and Morton 1984; Mateo 1996a, 2007b). Many species also are vulnerable to starvation or freezing during hibernation and must effectively negotiate the trade-off between watching for predators and gaining weight for hibernation. In addition, the fast developmental rate of young allows for both observational and experimental studies of acquisition of anti-predator behaviors across a range of environments (e.g., Poran and Coss 1990; Coss et al. 1993; Mateo 1995; Hanson and Coss 1997). Urocitellus beldingi are 200–500 g, groupliving, diurnal rodents found in alpine and subalpine regions of the western United States. They are socially active above ground between April and August and hibernate the remainder of the year (Jenkins and Eshelman 1984). Females mate with multiple males (up to nine) shortly after emerging from torpor, and after 25 days give birth to a litter of four to eight pups, which they rear by themselves in an underground natal burrow (J. Hanken and P.W. Sherman 1981, personal observation). Young first come above ground (emerge) as 4-week-old juveniles (P.W. Sherman and M.L. Morton 1984, personal observation). Two to three weeks after emergence, juvenile males begin to disperse (Holekamp 1984). Because females do not disperse, they can live near female kin, favoring the evolution of nepotism (Hamilton 1964). Females with close kin (mothers, daughter, and sisters) are more likely to give risky alarm calls than are females without close kin (Sherman 1977). They also help defend the territories of their close female kin from potentially infanticidal intruders (Sherman 1981). Belding’s ground squirrels emit two sonographically and auditorily distinct alarm calls, whistles and trills, that elicit different behavioral responses and serve different functions (Sherman 1977, 1985; Robinson 1980; Leger et al. 1984; Mateo 1996a). Whistles are elicited by fast-moving, typically aerial, predators and result in evasive behaviors such as running to a burrow or entering it, and scanning the area only af (...truncated)