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
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E-mail: [email protected]
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
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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.
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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 after reaching safety. Trills are elicited by slower-moving, primarily terrestrial, predators and usually cause listeners to post (a bipedal stance accompanied by visual scanning), with or without changing location (Mateo 1996a). Types of call reflect both type of predator and the urgency of response (Robinson 1981; see also Owings and Virginia 1978). In the natal burrow, pups experience a relatively dark, quiet environment, and do not begin to hear alarm calls routinely until just before their natal emergence. When young emerge as nearly weaned juveniles, they leave their quiet, well protected natal burrow and enter a drastically different environment, one that includes increased visual and auditory stimulation, and predators, as well as other ground squirrels that both produce and respond to alarm calls. A few days after natal emergence, the young begin to explore their surrounding area that includes other burrows, although the natal burrow will remain the activity center for juveniles for about 2 weeks. In the month after emergence, juveniles must become independent of their mother, undergo natal dispersal, establish a hibernaculum, and gain adequate weight to survive the winter, all while avoiding predators,
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important for survival. This might seem counterintuitive, since one might expect survival-behaviors to develop through closed programs (Mayr 1974). Accordingly, some have argued that behaviors important for survival, such as avoidance of predators, or responses to alarm calls, should develop without experience (Tinbergen 1953; Hinde 1954; Bolles 1970; Magurran 1990; Curio 1993). Alternatively, others suggest that survival-behaviors are best learned or acquired, perhaps through experience with predators (e.g., Vitale 1989; Cheney and Seyfarth 1990; Mateo 1996a; Griffin 2004; Nelson et al. 2013). Such nature–nurture distinctions are no longer formally endorsed, but are still found in the literature despite agreement by most biologists that behavior is neither innate nor acquired, but instead develops epigenetically as an animal interacts with the series of environments it encounters, both pre-natally and post-natally (Lehrman 1970; Gottlieb 1976; Johnston 1987; West and King 2008). Despite the vulnerability of the young to predation, open developmental programs might be adaptive when the context of predation varies among age groups or among populations, thereby favoring plasticity of species-typical behaviors (Johnston 1982; Shettleworth 1998; Richerson and Boyd 2001). For a young animal, its mother is one of the most salient aspects of its environment, and she can have a significant influence on her offspring’s acquisition of anti-predator repertoires, foraging skills, and social strategies.
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which can account for over 60% of juvenile mortality (Sherman 1976; Holekamp 1984; Jenkins and Eshelman 1984; Sherman and Morton 1984; Mateo 1996a). Of the 40% of juveniles who survive their first summer, more than half will not survive their first hibernation, due to insufficient body fat (Murie and Boag 1984; J.M. Mateo, unpublished data).
Development of responses to alarm calls Young ground squirrels need to learn which animals to fear, to which alarm calls to respond, and in what way. By what processes do juveniles acquire their responses to alarm-calls? To find out, I conducted a series of playback studies with free-living and captive U. beldingi in the eastern Sierra of California. Before natal emergence, U. beldingi pups do not show different behavioral responses to playbacks, but do exhibit different physiological responses to the two alarm calls. Specifically, the heart rates of 20- to 24-day-old pups decrease in response to playbacks of whistles and increase to trills (Fig. 1; Mateo 1996b). Just after natal emergence, juveniles still do not discriminate behaviorally between these calls, or even among alarm calls and other conspecific and heterospecific vocalizations. It takes 5 days for juveniles to learn to respond selectively to alarm calls and to ignore calls not associated with threatening stimuli. During these initial days, juveniles also learn the correct behavioral response for each type of call, although motoric responses continue to change quantitatively over the next several weeks. During this time up to 60% of juveniles disappear, many to predation (Fig. 2; Mateo 1996a). Experimental work pairing novel sounds with visual stimuli has shown that appropriate behavioral responses to the type of
Fig. 2 Percentage of newly emergent juveniles exhibiting a response to alarm-call and non-alarm call playbacks on their first and fifth day above ground. Numbers above bars represent the total number of responders and non-responders. Asterisks represent significant difference (P50.001) in likelihood of response to call types (reprinted from Mateo 1996a).
call can be acquired through associative learning (e.g., Mateo 1995, 2007; Shriner 1999).
Effects of mothers on juveniles’ responses In U. beldingi, this learning is facilitated by experience in hearing the calls as well as observations of adults’ reactions Juveniles attend to and model adults’ responses, particularly those of their mother rather than those of other nearby females (Mateo 1996a; Mateo and Holmes 1997; see also Seyfarth and Cheney 1980; Meno et al. 2013). On their first day aboveground, juveniles are significantly more likely to respond to alarm-call playbacks if their mother is present than if she is absent, but by day 5 her presence no longer influences the likelihood of response. Furthermore, juveniles adopt a style of response similar to that of their mother, and remain alert for extended periods if she does (Fig. 3); they also show more exaggerated vigilance if she does. These patterns of response persist at later ages, even when the mother is not visible at the time (Mateo 1996a; Mateo and Holmes 1997). If maternal responses are locally adapted to the types of threat of predation in the natal area, then offspring who adopt their mother’s styles might be favored. Mothers with natal burrows at the edge of meadows are more reactive to alarm calls and remain alert longer than do those from the center of a meadow (Mateo 1996a). This difference in vigilance may reflect increased vulnerability to predators near the edge (Elgar 1989; Hik et al. 2001; Anderson and Boutin 2002; Lazarus 2003; Morrell et al. 2011; Shi et al. 2011; but see Hirsch and Morrell 2011). Mothers’ reactions, which serve as models for juveniles’ responses, can reflect the mothers’ own
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Fig. 1 The percentage of animals responding with either tachycardia (open bars) or bradycardia (solid bars) to each playback stimulus just prior to the age of natal emergence. Bars total to 100% for each playback stimulus for each cohort. Numbers in parentheses represent the total number of young exhibiting increased or decreased heart rates following that playback stimulus. Brackets represent significance (**P50.05) of differences in the direction of heart-rate responses to stimuli based on McNemar’s Change Tests (reprinted from Mateo 1996b).
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Fig. 3 (Upper panel) Paired mean durations of response (seconds) of juveniles and their dams to same playback. (Lower panel) Paired mean durations of response of juveniles and unrelated adult females to same playback category. The linear regression lines are shown. Reprinted from Mateo and Holmes (1997).
Effects of glucocorticoids on response development
vulnerabilities (indirect maternal influence), or can be a form of maternal care, becoming more vigilant if they locate their natal burrow, and thus their offspring, in a dangerous area (at the edge from where predators appear) and less vigilant if in a safer region (center; direct maternal influences) (Mateo and Holmes 1997). Because U. beldingi juveniles model their responses after their mother, they are also more responsive and vigilant following playbacks of alarm calls if reared on the edge of a meadow than in the center (Mateo 1996a). These differences are apparent regardless of the individual’s location in the meadow at the time of the playback. However, they are not evident until young have been aboveground for at least 5 days, suggesting that some experience (either with the location or with their mothers’ responses) is required. Because of microhabitat-specific maternal effects on responses, U. beldingi can optimize both their foraging and anti-predator efforts, allowing juveniles (and adults) to gain adequate bodyweight before hibernation without expending energy on unnecessary vigilance (Mateo and Holmes 1999). In addition, females often establish territories near their mothers in later years (J.M. Mateo, unpublished
Maternal effects via physiological phenotype (e.g., diet, hormones, and photoperiod) can influence offspring’s physiology, which in turn can influence their behavioral responses to predators. Natal emergence of young ground squirrels is rather synchronous, with most litters emerging within a 10-day period, and tends to draw predators (Mateo 1996a). During this time, direct encounters with predators, observations of sudden, rapid responses of nearby adults, and experience with hearing loud alarm calls likely cause acute changes in circulating glucocorticoids of adults and offspring alike (Mateo 2009). The range of levels of cortisol depends on the particular stressor as well as on an individual’s hypothalamic–pituitary– adrenal (HPA) axis. Maternal responses to stress can affect the HPA functioning of their offspring, and thus a mother’s hormonal patterns can have longlasting effects on those of her young (e.g. Catalani 1997; and free-living animals: Love and Williams 2008, McCormick 1998, Sheriff et al. 2010, J. M. Mateo, unpubl. data; reviewed in by Champagne 2009, Meaney et al. (2007). This non-genetic transmission of adrenal functioning could have adaptive consequences for the offspring. Importantly, maternal glucocorticoids can affect the rate at which young learn behaviors important for survival. In laboratory rodents, glucocorticoids
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data), so adopting location-specific responses would be adaptive. However, given males’ dispersal, these inter-generational effects could be neutral or maladaptive, depending on where males settle. Microhabitat-specific adaptations are also evident in other species of ground squirrels. For example, studies of Arctic ground squirrels and California ground squirrels, as well as and rock squirrels (Urocitellus parryii, Otospermphilus beecheyi, Otospermphilus variegatus) demonstrated that animals sympatric with predatory snakes need to develop and maintain anti-snake behaviors, whereas responses to snakes are no longer evident in the anti-predator repertoires of animals living in habitats without snakes (Coss and Owings 1985; Goldthwaite et al. 1990; Coss et al. 1993; Owings et al. 2001). Such responses, then, would not necessarily be present upon first encounter with predators, but would be acquired rapidly with additional experience, perhaps through observational learning of their mother’s responses, through local enhancement (e.g., Swaisgood et al. 1999; also see Heyes (1999) and Nicol (1995) for critical discussions of social learning).
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Maternal effects resulting in population differences Maternal effects via behavioral and physiological processes can result in populational differences in offspring’s survival tactics. Over 2 years I quantified the activity budgets and anti-predator responses of adult U. beldingi living in three different Californian habitats and likely experiencing different predation pressures. At one of these sites, which is visually closed (predators and escape burrows are difficult to see), animals responding to alarm calls remain alert longer and show more exaggerated responses than do adults living in two populations that likely experience less intense predation pressure. They also spend more time alert and less time foraging than do adults at the other two sites (Mateo 2007b; see also Ferrari et al. 2009). Urocitellus beldingi living in the closed site also have lower fecal glucocorticoid levels than do adults at the other two sites. These lower levels of corticoids can be interpreted as reflecting predictable risk of predation at this closed site, and allow animals to mount large acute elevations in cortisol
Fig. 4 (Upper panel) Juvenile fecal corticoids, measured at the conclusion of the spatial-learning study. Because cortisol of juveniles reared by mothers given medium and high doses of exogenous hydrocortisone was lower than that of control juveniles, they are referred to as LOW1 and LOW2 CORT groups, respectively. (Lower panel) Numbers of trials required to reach criterion in a complex spatial maze. Different letters over columns indicate significant differences based on Bonferroni-adjusted post-hoc pairwise t-test comparisons for significant ANOVAs (reprinted from Mateo 2008). Data on associative learning task, including juveniles with experimentally increased cortisol, not shown.
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(as well as the peripheral actions of epinephrine; McGaugh 1989) have an inverted-U-shaped effect on learning and memory. Very low or very high levels of corticoids can lead to hypo-arousal or hyper-arousal and poor selective attention to input and thus impair consolidation of new memories. Moderate elevation of corticoids is optimal for attention to stimuli and consolidation of memories (reviewed by Lupien and McEwen 1997; de Kloet et al. 1999; Roozendaal 2000). Maternal glucocorticoids are transmitted to mammalian offspring during gestation and lactation and can have long-term effects on the offspring’s endocrinology (e.g., Barbazanges et al. 1996; Catalani et al. 2002; Schopper et al. 2012). This ‘‘set point’’ may promote learning of anti-predator responses, particularly in animals inhabiting areas with high predation pressure. I explored this possibility by exogenously manipulating maternal cortisol in U. beldingi during lactation to determine its effect on the offspring’s cortisol and learning. Specifically, I compared juveniles with low or moderately elevated levels of baseline cortisol on two learning tasks. First, I used an associative learning task to determine whether the groups differed in their ability to acquire or retain an association between a warning call and the appropriate behavioral response. I also tested the groups in a novel, complex maze (Habitrail MiniMaze for Mice ) to assess their speed of spatial learning. Experimentally decreased basal cortisol levels (via maternal treatment) interfered with learning and memory compared with moderate elevation of cortisol (Mateo 2008; see Fig. 4). In a related experiment, juveniles of untreated mothers had very high levels of baseline cortisol because of hydrocortisone in their drinking water; they also exhibited impaired acquisition and memory in an associative learning task (Mateo 2008). In free-living juveniles, cortisol is moderately elevated for about 5 days after natal emergence (Mateo 2006), which may facilitate acquisition of spatial memory of a three-dimensional environment and responses to alarm calls during a sensitive period of learning. This novel demonstration of the inverted-U-shaped function in a wild animal suggests that natural selection has favored a hormonal profile facilitating rapid acquisition of important survival behaviors (see also Bokony et al. 2014; Meylan and Clobert 2005; Pravosudov 2003; Thaker et al. 2010; and Uller and Olsson 2006 for effects of glucocorticoids on learning and survival in wild or wild-caught animals). It also indicates the degree to which maternal effects can enhance or inhibit learning by offspring.
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Maternal effects and kin recognition Finally, recall that in U. beldingi, trill alarm calls are considered nepotistic, favoring the evolution of kinrecognition abilities (Mateo 2002) that can facilitate appropriate expression of these anti-predator calls. Maternal effects on kin preferences are well documented in ground squirrels. The most common social behavior among juveniles is play, and young prefer to play with littermates and other kin over non-kin; this discrimination among juveniles is typically mediated by olfactory cues (Urocitellus columbianus, Urocitellus beldingi, Callospermophilus lateralis) (Waterman 1986; Holmes 1994, 1995; Mateo 2003). In U. beldingi, mothers are important for the development and crystallization of these preferences for kin. Juveniles reared in a semi-natural enclosure without their mothers fail to develop play–partner preferences. However, when mothers are present but unable to intervene in social interactions, preferences for littermates still develop, suggesting that a mother’s role is indirect. Indeed, it is a mother’s presence at night in the burrow system that attracts her offspring to sleep together, resulting in the establishment of kin preferences (Holmes and Mateo 1998). Play is thought to lay a foundation for adult kin preferences and nepotism, and therefore is expected to vary with kinship (Michener 1983; Holmes 1994). In some sciurids, however, even in the absence of nepotism, juveniles develop kin-recognition abilities and kin biases (e.g., C. lateralis), which might function in the avoidance of inbreeding (Michener 1983; Mateo 2002).
Conclusions Parental effects can help shape offspring’s behavioral repertoires, tuning them to the appropriate physiological, environmental, and social contexts. They will be favored when parents and their offspring experience similar social and physical environments and thus similar availability of resources, predation pressure, and social dynamics. Plasticity in survival behaviors can be adaptive when number and kinds of predators are variable. This plasticity can occur at multiple scales, across both space and time. Variation in the intensity of the risk of predation, quality of surrounding habitat, and predictability of the number and types of local predors can result in open developmental programs. Modification of behaviors through experience will allow animals to maximize foraging and growth, without increasing the risk of predation, according to their local conditions. Future work could determine the fitness outcomes of plasticity and the parental effects of dispersing and migrating animals, or in changing environments due to climatic change or urbanization. Interdisciplinary approaches will help to identify physiological and behavioral mechanisms underlying developmental plasticity.
Funding The National Science Foundation (IBN 93-11508, IBN 98-08704, and IOB 05-17137) and the National Institutes of Health (MH63921-01A1) funded collection of the data discussed here.
References Anderson EM, Boutin S. 2002. Edge effects on survival and behaviour of juvenile red squirrels (Tamiasciurus hudsonicus). Can J Zool 80:1038–46. Barbazanges A, Piazza PV, Le Moal M, Maccari S. 1996. Maternal glucocorticoid secretion mediates long-term effects of prenatal stress. J Neurosci 16:3943–9. Bokony V, Lendvai AZ, Va´ga´si CI, Pa˘tras L, Pap PL, Ne´meth J, Vincze E, Papp S, Preiszner B, Seress G, et al. 2014. Necessity or capacity? Physiological state predicts problem-solving performance in house sparrows. Behav Ecol 25:124–35. Bolles RC. 1970. Species-specific defense reactions and avoidance learning. Psychol Rev 77:32–48. Boonstra R, McColl CJ. 2000. Contrasting stress response of male Arctic ground squirrels and red squirrels. J Exp Zool 286:390–404. Cairns RB, Gariepy JL, Hood KE. 1990. Development, microevolution, and social behavior. Psychol Rev 97:49–65. Catalani A. 1997. Neonatal exposure to glucocorticoids: longterm endocrine and behavioral effects. Dev Brain Dysfunct 10:393–404.
Downloaded from http://icb.oxfordjournals.org/ at FAKHEBISCONSORTIUM2006 on October 16, 2014
(Mateo 2007b) that would facilitate escape from predators and promote enhanced vigilance while also enhancing storage of glucose for the approaching hibernation. Thus, animals are locally adapted to their risk of predation, both behaviorally and physiologically, thereby allowing them to balance tradeoffs among foraging, vigilance, and anti-predator behaviors. Because mothers can influence the ontogeny of their offspring’s anti-predator behaviors (Mateo 1996a; Mateo and Holmes 1997), their offspring should exhibit repertoires that are appropriate for their population (see also Fraser and Gilliam 1987; Boonstra and McColl 2000; Hik et al. 2001; Wingfield 2004; Reeder and Kramer 2005; Clinchy et al. 2011). This would be adaptive for both sons and daughters, as natal dispersal is typically constrained to within their current population (Holekamp 1984), although as noted above adaptations to microhabitats may be maladaptive for sons.
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Hamilton WD. 1964. The genetical evolution of social behaviour, I. II. J Theor Biol 7:1–52. Hanken J, Sherman PW. 1981. Multiple paternity in Belding’s ground squirrel litters. Science 212:351–3. Hanson MT, Coss RG. 1997. Age differences in the response of California ground squirrels (Spermophilus beecheyi) to avian and mammalian predators. J Comp Psychol 111:174–84. Heyes CM. 1999. Social learning in animals: categories and mechanisms. Biol Rev 69:207–31. Hik DS, McColl CJ, Boonstra R. 2001. Why are Arctic ground squirrels more stressed in the boreal forest than in alpine meadows? Ecoscience 8:275–88. Hinde RA. 1954. Factors governing the changes in strength of a partially inborn response, as shown by the mobbing behaviour of the chaffinch (Fringilla coelebs).1. The nature of the response, and an examination of its course. Proc R Soc Ser B Biol Sci 142:306–31. Hirsch BT, Morrell LJ. 2011. Measuring marginal predation in animal groups. Behav Ecol 22:648–56. Holekamp KE. 1984. Natal dispersal in Belding’s ground squirrels (Spermophilus beldingi). Behav Ecol Sociobiol 16:21–30. Holmes WG. 1994. The development of littermate preferences in juvenile Belding’s ground squirrels. Anim Behav 48:1071–84. Holmes WG. 1995. The ontogeny of littermate preferences in juvenile golden-mantled ground squirrels: Effects of rearing and relatedness. Anim Behav 50:309–22. Holmes WG, Mateo JM. 1998. How mothers influence the development of litter-mate preferences in Belding’s ground squirrels. Anim Behav 55:1555–70. Jenkins SH, Eshelman BD. 1984. Spermophilus beldingi. Mammal Spec 221:1–8. Johnston TD. 1982. Selective costs and benefits in the evolution of learning. In: Rosenblatt JS, Hinde RA, Beer C, Busnel M-C, editors. Advances in the study of behavior. Vol. 12. New York: Academic Press. p. 65–106. Johnston TD. 1987. The persistence of dichotomies in the study of behavioral development. Dev Rev 7:149–82. Lazarus J. 2003. Vigilance and group size: early studies, the edge effect, secondary defences, the double advantage tradeoff and the future. Behav Process 63:129–31. Leger DW, Berney-Key SD, Sherman PW. 1984. Vocalizations of Belding’s ground squirrels (Spermophilus beldingi). Anim Behav 32:753–64. Lehrman DS. 1970. Semantic and conceptual issues in the nature–nurture problem. In: Aronson LR, Tobach E, Lehrman DS, Rosenblatt JS, editors. Development and evolution of behavior. San Francisco (CA): W. H. Freeman. p. 17–52. Love OP, Williams TD. 2008. Plasticity in the adrenocortical response of a free-living vertebrate: the role of preand post-natal developmental stress. Horm Behav 54: 496–505. Love OP, McGowan PO, Sheriff MJ. 2013. Maternal adversity and ecological stressors in natural populations: the role of stress axis programming in individuals, with implications for populations and communities. Funct Ecol 27:81–92.
Downloaded from http://icb.oxfordjournals.org/ at FAKHEBISCONSORTIUM2006 on October 16, 2014
Catalani A, Casolini P, Cigliana G, Scaccianoce S, Consoli C, Cinque C, Zuena AR, Angelucci L. 2002. Maternal corticosterone influences behavior, stress response and corticosteroid receptors in the female rat. Pharmacol Biochem Behav 73:105–14. Champagne F, Curley JP. 2009. The transgenerational influence of maternal care on offspring gene expression and behavior in rodents. In: Maestripieri D, Mateo JM, editors. Maternal effects in mammals. Chicago (IL): University of Chicago Press. p. 182–202. Cheney DL, Seyfarth RM. 1990. How monkeys see the world. Chicago (IL): University of Chicago Press. Clinchy M, Zanette L, Charlier TD, Newman AEM, Schmidt KL, Boonstra R, Soma KK. 2011. Multiple measures elucidate glucocorticoid responses to environmental variation in predation threat. Oecologia 166:607–14. Coss RG, Owings DH. 1985. Restraints on ground squirrel antipredator behavior: adjustments over multiple time scales. In: Johnston TD, Pietrewicz AT, editors. Issues in the ecological study of learning. Hillsdale (NJ): Lawrence Erlbaum Associates. p. 167–200. Coss RG, Guse KL, Poran NS, Smith DG. 1993. Development of antisnake defenses in California ground squirrels (Spermophilus beecheyi): II. Microevolutionary effects of relaxed selection from rattlesnakes. Behaviour 124:137–64. Curio E. 1993. Proximate and developmental aspects of antipredator behavior. In: Slater PJB, Rosenblatt JS, Snowdon CT, Milinski M, editors. Advances in the study of behavior. Vol. 22. New York: Academic Press. p. 135–238. de Kloet ER, Oitzl MS, Joels M. 1999. Stress and cognition: are corticosteroids good or bad guys? Trends Neurosci 22:422–6. Elgar MA. 1989. Predator vigilance and group size in mammals and birds: a critical review of the empirical evidence. Biol Rev Camb Phil Soc 64:13–33. Ferrari C, Bogliani G, von Hardenberg A. 2009. Alpine marmots (Marmota marmota) adjust vigilance behaviour according to environmental characteristics of their surrounding. Ethol Ecol Evol 21:355–64. Fisher RA. 1930. The genetical theory of natural selection. Oxford: Clarendon Press. Fraser DF, Gilliam JF. 1987. Feeding under predation hazard: response of the guppy and Hart’s rivulus from sites with contrasting predation hazard. Behav Ecol Sociobiol 21:203–9. Goldthwaite RO, Coss RG, Owings DH. 1990. Evolutionary dissipation of an antisnake system: differential behavior by California and Arctic ground squirrels in above- and below-ground contexts. Behaviour 112:246–69. Gottlieb G. 1976. The roles of experience in the development of behavior and the nervous system. In: Gottlieb G, editor. Studies on the development of behavior and the nervous system. Vol 3. Neural and Behavioral Specificity. New York: Academic Press. p. 25–53. Griffin AS. 2004. Social learning about predators: a review and prospectus. Learn Behav 32:131–40. Haldane JBS. 1932. The causes of evolution. New York: Longmans Green.
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Meylan S, Clobert J. 2005. Is corticosterone-mediated phenotype development adaptive? Maternal corticosterone treatment enhances survival in male lizards. Horm Behav 48:44–52. Meylan S, Miles DB, Clobert J. 2012. Hormonally mediated maternal effects, individual strategy and global change. Phil Trans R Soc B Biol Sci 367:1647–64. Michener GR. 1983. Kin identification, matriarchies, and the evolution of sociality in ground-dwelling sciurids. In: Eisenberg JF, Kleiman DG, editors. Advances in the study of mammalian behavior. Shippensburg (PA): American Society of Mammalogists. p. 528–72. Morrell LJ, Ruxton GD, James R. 2011. Spatial positioning in the selfish herd. Behav Ecol 22:16–22. Mousseau TA, Fox CW. 1998. Maternal effects as adaptations. Oxford: Oxford University Press. Murie JO, Boag DA. 1984. The relationship of body weight to overwinter survival in Columbian ground squirrels. J Mammal 65:688–90. Nelson AB, Alemadi SD, Wisenden BD. 2013. Learned recognition of novel predator odour by convict cichlid embryos. Behav Ecol Sociobiol 67:1269–73. Nicol CJ. 1995. The social transmission of information and behaviour. Appl Anim Behav Sci 44:79–98. Owings DH, Hennessy DF. 1984. The importance of variation in sciurid visual and vocal communication. In: Murie JO, Michener GR, editors. The biology of grounddwelling squirrels: annual cycles, behavioral ecology, and sociality. Lincoln: University of Nebraska Press. p. 169–200. Owings DH, Virginia RA. 1978. Alarm calls of California ground squirrels (Spermophilus beecheyi). Z Tierpsychol 46:58–70. Owings DH, Coss RG, McKernon D, Rowe MP, Arrowood PC. 2001. Snake-directed antipredator behavior of rock squirrels (Spermophilus variegatus): population differences and snake-species discrimination. Behaviour 138:575–95. Poran NS, Coss RG. 1990. Development of antisnake defenses in California ground squirrels (Spermophilus beecheyi): I. Behavioral and immunological relationships. Behaviour 112:222–45. Pravosudov VV. 2003. Long-term moderate elevation of corticosterone facilitates avian food-caching behaviour and enhances spatial memory. Proc R Soc Lond Ser B: Biol Sci 270:2599–604. Reeder DM, Kramer KM. 2005. Stress in free-ranging mammals: integrating physiology, ecology, and natural history. J Mammal 86:225–35. Reinhold K. 2002. Maternal effects and the evolution of behavioral and morphological characters: a literature review indicates the importance of extended maternal care. J Hered 93:400–5. Richerson PJ, Boyd R. 2001. Built for speed, not for comfort: Darwinian theory and human culture. Hist Phil Life Sci 23:425–65. Robinson SR. 1980. Antipredator behaviour and predator recognition in Belding’s ground squirrels. Anim Behav 28:840–52. Robinson SR. 1981. Alarm communication in Belding’s ground squirrels. Z Tierpsychol 56:150–68.
Downloaded from http://icb.oxfordjournals.org/ at FAKHEBISCONSORTIUM2006 on October 16, 2014
Lupien SJ, McEwen BS. 1997. The acute effects of corticosteroids on cognition: integration of animal and human model studies. Brain Res Rev 24:1–27. Magurran AE. 1990. The inheritance and development of minnow anti-predator behaviour. Anim Behav 39:834–42. Mateo JM. 1995. The development of alarm-call responses in free-living and captive Belding’s ground squirrels, Spermophilus beldingi [PhD thesis]. University of Michigan. Mateo JM. 1996a. The development of alarm-call response behaviour in free-living juvenile Belding’s ground squirrels. Anim Behav 52:489–505. Mateo JM. 1996b. Early auditory experience and the ontogeny of alarm-call discrimination in Belding’s ground squirrels (Spermophilus beldingi). J Comp Psychol 110:115–24. Mateo JM. 2002. Kin-recognition abilities and nepotism as a function of sociality. Proc R Soc Lond Ser B Biol Sci 269:721–7. Mateo JM. 2003. Kin recognition in ground squirrels and other rodents. J Mammal 84:1163–81. Mateo JM. 2006. Developmental and geographic variation in stress hormones in wild Belding’s ground squirrels (Spermophilus beldingi). Horm Behav 50:718–25. Mateo JM. 2007a. Ontogeny of adaptive behaviors. In: Wolff JO, Sherman PW, editors. Rodent societies. Chicago (IL): University of Chicago Press. p. 195–206. Mateo JM. 2007b. Ecological and physiological correlates of anti-predator behaviors of Belding’s ground squirrels (Spermophilus beldingi). Behav Ecol Sociobiol 62:37–49. Mateo JM. 2008. Inverted-U shape relationship between cortisol and learning in ground squirrels. Neurobiol Learn Mem 89:582–90. Mateo JM. 2009. Maternal influences on development, social relationships and survival behaviors. In: Maestripieri D, Mateo JM, editors. Maternal effects in mammals. Chicago (IL): University of Chicago Press. p. 133–58. Mateo JM, Holmes WG. 1997. Development of alarm-call responses in Belding’s ground squirrels: the role of dams. Anim Behav 54:509–24. Mateo JM, Holmes WG. 1999. Plasticity of alarm-call response development in Belding’s ground squirrels (Spermophilus beldingi, Sciuridae). Ethology 105:193–206. Mayr E. 1974. Behavior programs and evolutionary strategies. Am Sci 62:650–9. McAdam AG. 2009. Maternal effects on evolutionary dynamics in wild small mammals. In: Maestripieri D, Mateo JM, editors. Maternal effects in mammals. Chicago (IL): University of Chicago Press. p. 64–82. McCormick MI. 1998. Behaviorally induced maternal stress in a fish influences progeny quality by a hormonal mechanism. Ecology 79:1873–83. McGaugh JL. 1989. Involvement of hormonal and neuromodulatory systems in the regulation of memory storage. Annu Rev Neurosci 12:255–87. Meaney MJ, Szyf M, Seckl JR. 2007. Epigenetic mechanisms of perinatal programming of hypothalamic–pituitary–adrenal function and health. Trends Mol Med 13: 269–77. Meno W, Coss RG, Perry S. 2013. Development of snakedirected antipredator behavior by wild white-faced capuchin monkeys: II. Influence of the social environment. Am J Primatol 75:292–300.
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Shriner WM. 1999. Antipredator responses to a previously neutral sound by free-living adult golden-mantled ground squirrels, Spermophilus lateralis (Sciuridae). Ethology 105:747–57. Stamps J. 2003. Behavioural processes affecting development: Tinbergen’s fourth question comes of age. Anim Behav 66:1–13. Swaisgood RR, Owings DH, Rowe MP. 1999. Conflict and assessment in a predator–prey system: ground squirrels versus rattlesnakes. Anim Behav 57:1033–44. Thaker M, Vanak AT, Lima SL, Hews DK. 2010. Stress and aversive learning in a wild vertebrate: the role of corticosterone in mediating escape from a novel stressor. Am Nat 175:50–60. Tinbergen N. 1953. Social behaviour in animals. New York: John Wiley & Sons. Uller T, Olsson M. 2006. Direct exposure to corticosterone during embryonic development influences behaviour in an ovoviviparous lizard. Ethology 112:390–7. Vitale AF. 1989. Changes in anti-predator responses of wild rabbits, Oryctolagus cuniculus (L.), with age and experience. Behaviour 110:47–61. Waterman JM. 1986. Behaviour and use of space by juvenile Columbian ground squirrels. Can J Zool 64:1121–7. West MJ, King AP. 2008. Deconstructing innate illusions: reflections on nature–nurture-niche from an unlikely source. Phil Psychol 21:383–95. Wingfield JC. 2004. Control of behavioural strategies for capricious environments. Anim Behav 66:807–16. Wright S. 1931. Evolution in Mendelian populations. Genetics 16:97–159.
Downloaded from http://icb.oxfordjournals.org/ at FAKHEBISCONSORTIUM2006 on October 16, 2014
Roozendaal B. 2000. Glucocorticoids and the regulation of memory consolidation. Psychoneuroendocrinology 25:213–38. Schopper H, Palme R, Ruf T, Huber S. 2012. Effects of prenatal stress on hypothalamic–pituitary–adrenal (HPA) axis function over two generations of guinea pigs (Cavia aperea f. porcellus). Gen Comp Endocrinol 176:18–27. Seyfarth RM, Cheney DL. 1980. The ontogeny of vervet monkey alarm calling behavior: a preliminary report. Z Tierpsychol 54:37–56. Sheriff MJ, Love OP. 2013. Determining the adaptive potential of maternal stress. Ecol Lett 16:271–80. Sheriff MJ, Krebs CJ, Boonstra R. 2010. The ghosts of predators past: population cycles and the role of maternal programming under fluctuating predation risk. Ecology 91:2983–94. Sherman PW. 1976. Natural selection among some groupliving organisms [PhD thesis]. University of Michigan. Sherman PW. 1977. Nepotism and the evolution of alarm calls. Science 197:1246–53. Sherman PW. 1981. Kinship, demography, and Belding’s ground squirrel nepotism. Behav Ecol Sociobiol 8:251–9. Sherman PW. 1985. Alarm calls of Belding’s ground squirrels to aerial predators: nepotism or self-preservation? Behav Ecol Sociobiol 17:313–23. Sherman PW, Morton ML. 1984. Demography of Belding’s ground squirrels. Ecology 65:1617–28. Shettleworth S. 1998. Cognition, evolution, and behavior. New York: Oxford University Press. Shi JB, Li DQ, Xiao WF. 2011. Influences of sex, group size, and spatial position on vigilance behavior of Przewalski’s gazelles. Acta Theriol 56:73–9.
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Development, Maternal Effects, and Behavioral Plasticity Jill M. Mateo1 Department of Comparative Human Development, 5730 South Woodlawn Avenue, Chicago, IL 60637, USA
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E-mail: [email protected]
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: [email protected].
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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.
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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 after reaching safety. Trills are elicited by slower-moving, primarily terrestrial, predators and usually cause listeners to post (a bipedal stance accompanied by visual scanning), with or without changing location (Mateo 1996a). Types of call reflect both type of predator and the urgency of response (Robinson 1981; see also Owings and Virginia 1978). In the natal burrow, pups experience a relatively dark, quiet environment, and do not begin to hear alarm calls routinely until just before their natal emergence. When young emerge as nearly weaned juveniles, they leave their quiet, well protected natal burrow and enter a drastically different environment, one that includes increased visual and auditory stimulation, and predators, as well as other ground squirrels that both produce and respond to alarm calls. A few days after natal emergence, the young begin to explore their surrounding area that includes other burrows, although the natal burrow will remain the activity center for juveniles for about 2 weeks. In the month after emergence, juveniles must become independent of their mother, undergo natal dispersal, establish a hibernaculum, and gain adequate weight to survive the winter, all while avoiding predators,
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important for survival. This might seem counterintuitive, since one might expect survival-behaviors to develop through closed programs (Mayr 1974). Accordingly, some have argued that behaviors important for survival, such as avoidance of predators, or responses to alarm calls, should develop without experience (Tinbergen 1953; Hinde 1954; Bolles 1970; Magurran 1990; Curio 1993). Alternatively, others suggest that survival-behaviors are best learned or acquired, perhaps through experience with predators (e.g., Vitale 1989; Cheney and Seyfarth 1990; Mateo 1996a; Griffin 2004; Nelson et al. 2013). Such nature–nurture distinctions are no longer formally endorsed, but are still found in the literature despite agreement by most biologists that behavior is neither innate nor acquired, but instead develops epigenetically as an animal interacts with the series of environments it encounters, both pre-natally and post-natally (Lehrman 1970; Gottlieb 1976; Johnston 1987; West and King 2008). Despite the vulnerability of the young to predation, open developmental programs might be adaptive when the context of predation varies among age groups or among populations, thereby favoring plasticity of species-typical behaviors (Johnston 1982; Shettleworth 1998; Richerson and Boyd 2001). For a young animal, its mother is one of the most salient aspects of its environment, and she can have a significant influence on her offspring’s acquisition of anti-predator repertoires, foraging skills, and social strategies.
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which can account for over 60% of juvenile mortality (Sherman 1976; Holekamp 1984; Jenkins and Eshelman 1984; Sherman and Morton 1984; Mateo 1996a). Of the 40% of juveniles who survive their first summer, more than half will not survive their first hibernation, due to insufficient body fat (Murie and Boag 1984; J.M. Mateo, unpublished data).
Development of responses to alarm calls Young ground squirrels need to learn which animals to fear, to which alarm calls to respond, and in what way. By what processes do juveniles acquire their responses to alarm-calls? To find out, I conducted a series of playback studies with free-living and captive U. beldingi in the eastern Sierra of California. Before natal emergence, U. beldingi pups do not show different behavioral responses to playbacks, but do exhibit different physiological responses to the two alarm calls. Specifically, the heart rates of 20- to 24-day-old pups decrease in response to playbacks of whistles and increase to trills (Fig. 1; Mateo 1996b). Just after natal emergence, juveniles still do not discriminate behaviorally between these calls, or even among alarm calls and other conspecific and heterospecific vocalizations. It takes 5 days for juveniles to learn to respond selectively to alarm calls and to ignore calls not associated with threatening stimuli. During these initial days, juveniles also learn the correct behavioral response for each type of call, although motoric responses continue to change quantitatively over the next several weeks. During this time up to 60% of juveniles disappear, many to predation (Fig. 2; Mateo 1996a). Experimental work pairing novel sounds with visual stimuli has shown that appropriate behavioral responses to the type of
Fig. 2 Percentage of newly emergent juveniles exhibiting a response to alarm-call and non-alarm call playbacks on their first and fifth day above ground. Numbers above bars represent the total number of responders and non-responders. Asterisks represent significant difference (P50.001) in likelihood of response to call types (reprinted from Mateo 1996a).
call can be acquired through associative learning (e.g., Mateo 1995, 2007; Shriner 1999).
Effects of mothers on juveniles’ responses In U. beldingi, this learning is facilitated by experience in hearing the calls as well as observations of adults’ reactions Juveniles attend to and model adults’ responses, particularly those of their mother rather than those of other nearby females (Mateo 1996a; Mateo and Holmes 1997; see also Seyfarth and Cheney 1980; Meno et al. 2013). On their first day aboveground, juveniles are significantly more likely to respond to alarm-call playbacks if their mother is present than if she is absent, but by day 5 her presence no longer influences the likelihood of response. Furthermore, juveniles adopt a style of response similar to that of their mother, and remain alert for extended periods if she does (Fig. 3); they also show more exaggerated vigilance if she does. These patterns of response persist at later ages, even when the mother is not visible at the time (Mateo 1996a; Mateo and Holmes 1997). If maternal responses are locally adapted to the types of threat of predation in the natal area, then offspring who adopt their mother’s styles might be favored. Mothers with natal burrows at the edge of meadows are more reactive to alarm calls and remain alert longer than do those from the center of a meadow (Mateo 1996a). This difference in vigilance may reflect increased vulnerability to predators near the edge (Elgar 1989; Hik et al. 2001; Anderson and Boutin 2002; Lazarus 2003; Morrell et al. 2011; Shi et al. 2011; but see Hirsch and Morrell 2011). Mothers’ reactions, which serve as models for juveniles’ responses, can reflect the mothers’ own
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Fig. 1 The percentage of animals responding with either tachycardia (open bars) or bradycardia (solid bars) to each playback stimulus just prior to the age of natal emergence. Bars total to 100% for each playback stimulus for each cohort. Numbers in parentheses represent the total number of young exhibiting increased or decreased heart rates following that playback stimulus. Brackets represent significance (**P50.05) of differences in the direction of heart-rate responses to stimuli based on McNemar’s Change Tests (reprinted from Mateo 1996b).
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Fig. 3 (Upper panel) Paired mean durations of response (seconds) of juveniles and their dams to same playback. (Lower panel) Paired mean durations of response of juveniles and unrelated adult females to same playback category. The linear regression lines are shown. Reprinted from Mateo and Holmes (1997).
Effects of glucocorticoids on response development
vulnerabilities (indirect maternal influence), or can be a form of maternal care, becoming more vigilant if they locate their natal burrow, and thus their offspring, in a dangerous area (at the edge from where predators appear) and less vigilant if in a safer region (center; direct maternal influences) (Mateo and Holmes 1997). Because U. beldingi juveniles model their responses after their mother, they are also more responsive and vigilant following playbacks of alarm calls if reared on the edge of a meadow than in the center (Mateo 1996a). These differences are apparent regardless of the individual’s location in the meadow at the time of the playback. However, they are not evident until young have been aboveground for at least 5 days, suggesting that some experience (either with the location or with their mothers’ responses) is required. Because of microhabitat-specific maternal effects on responses, U. beldingi can optimize both their foraging and anti-predator efforts, allowing juveniles (and adults) to gain adequate bodyweight before hibernation without expending energy on unnecessary vigilance (Mateo and Holmes 1999). In addition, females often establish territories near their mothers in later years (J.M. Mateo, unpublished
Maternal effects via physiological phenotype (e.g., diet, hormones, and photoperiod) can influence offspring’s physiology, which in turn can influence their behavioral responses to predators. Natal emergence of young ground squirrels is rather synchronous, with most litters emerging within a 10-day period, and tends to draw predators (Mateo 1996a). During this time, direct encounters with predators, observations of sudden, rapid responses of nearby adults, and experience with hearing loud alarm calls likely cause acute changes in circulating glucocorticoids of adults and offspring alike (Mateo 2009). The range of levels of cortisol depends on the particular stressor as well as on an individual’s hypothalamic–pituitary– adrenal (HPA) axis. Maternal responses to stress can affect the HPA functioning of their offspring, and thus a mother’s hormonal patterns can have longlasting effects on those of her young (e.g. Catalani 1997; and free-living animals: Love and Williams 2008, McCormick 1998, Sheriff et al. 2010, J. M. Mateo, unpubl. data; reviewed in by Champagne 2009, Meaney et al. (2007). This non-genetic transmission of adrenal functioning could have adaptive consequences for the offspring. Importantly, maternal glucocorticoids can affect the rate at which young learn behaviors important for survival. In laboratory rodents, glucocorticoids
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data), so adopting location-specific responses would be adaptive. However, given males’ dispersal, these inter-generational effects could be neutral or maladaptive, depending on where males settle. Microhabitat-specific adaptations are also evident in other species of ground squirrels. For example, studies of Arctic ground squirrels and California ground squirrels, as well as and rock squirrels (Urocitellus parryii, Otospermphilus beecheyi, Otospermphilus variegatus) demonstrated that animals sympatric with predatory snakes need to develop and maintain anti-snake behaviors, whereas responses to snakes are no longer evident in the anti-predator repertoires of animals living in habitats without snakes (Coss and Owings 1985; Goldthwaite et al. 1990; Coss et al. 1993; Owings et al. 2001). Such responses, then, would not necessarily be present upon first encounter with predators, but would be acquired rapidly with additional experience, perhaps through observational learning of their mother’s responses, through local enhancement (e.g., Swaisgood et al. 1999; also see Heyes (1999) and Nicol (1995) for critical discussions of social learning).
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Maternal effects resulting in population differences Maternal effects via behavioral and physiological processes can result in populational differences in offspring’s survival tactics. Over 2 years I quantified the activity budgets and anti-predator responses of adult U. beldingi living in three different Californian habitats and likely experiencing different predation pressures. At one of these sites, which is visually closed (predators and escape burrows are difficult to see), animals responding to alarm calls remain alert longer and show more exaggerated responses than do adults living in two populations that likely experience less intense predation pressure. They also spend more time alert and less time foraging than do adults at the other two sites (Mateo 2007b; see also Ferrari et al. 2009). Urocitellus beldingi living in the closed site also have lower fecal glucocorticoid levels than do adults at the other two sites. These lower levels of corticoids can be interpreted as reflecting predictable risk of predation at this closed site, and allow animals to mount large acute elevations in cortisol
Fig. 4 (Upper panel) Juvenile fecal corticoids, measured at the conclusion of the spatial-learning study. Because cortisol of juveniles reared by mothers given medium and high doses of exogenous hydrocortisone was lower than that of control juveniles, they are referred to as LOW1 and LOW2 CORT groups, respectively. (Lower panel) Numbers of trials required to reach criterion in a complex spatial maze. Different letters over columns indicate significant differences based on Bonferroni-adjusted post-hoc pairwise t-test comparisons for significant ANOVAs (reprinted from Mateo 2008). Data on associative learning task, including juveniles with experimentally increased cortisol, not shown.
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(as well as the peripheral actions of epinephrine; McGaugh 1989) have an inverted-U-shaped effect on learning and memory. Very low or very high levels of corticoids can lead to hypo-arousal or hyper-arousal and poor selective attention to input and thus impair consolidation of new memories. Moderate elevation of corticoids is optimal for attention to stimuli and consolidation of memories (reviewed by Lupien and McEwen 1997; de Kloet et al. 1999; Roozendaal 2000). Maternal glucocorticoids are transmitted to mammalian offspring during gestation and lactation and can have long-term effects on the offspring’s endocrinology (e.g., Barbazanges et al. 1996; Catalani et al. 2002; Schopper et al. 2012). This ‘‘set point’’ may promote learning of anti-predator responses, particularly in animals inhabiting areas with high predation pressure. I explored this possibility by exogenously manipulating maternal cortisol in U. beldingi during lactation to determine its effect on the offspring’s cortisol and learning. Specifically, I compared juveniles with low or moderately elevated levels of baseline cortisol on two learning tasks. First, I used an associative learning task to determine whether the groups differed in their ability to acquire or retain an association between a warning call and the appropriate behavioral response. I also tested the groups in a novel, complex maze (Habitrail MiniMaze for Mice ) to assess their speed of spatial learning. Experimentally decreased basal cortisol levels (via maternal treatment) interfered with learning and memory compared with moderate elevation of cortisol (Mateo 2008; see Fig. 4). In a related experiment, juveniles of untreated mothers had very high levels of baseline cortisol because of hydrocortisone in their drinking water; they also exhibited impaired acquisition and memory in an associative learning task (Mateo 2008). In free-living juveniles, cortisol is moderately elevated for about 5 days after natal emergence (Mateo 2006), which may facilitate acquisition of spatial memory of a three-dimensional environment and responses to alarm calls during a sensitive period of learning. This novel demonstration of the inverted-U-shaped function in a wild animal suggests that natural selection has favored a hormonal profile facilitating rapid acquisition of important survival behaviors (see also Bokony et al. 2014; Meylan and Clobert 2005; Pravosudov 2003; Thaker et al. 2010; and Uller and Olsson 2006 for effects of glucocorticoids on learning and survival in wild or wild-caught animals). It also indicates the degree to which maternal effects can enhance or inhibit learning by offspring.
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Maternal effects and kin recognition Finally, recall that in U. beldingi, trill alarm calls are considered nepotistic, favoring the evolution of kinrecognition abilities (Mateo 2002) that can facilitate appropriate expression of these anti-predator calls. Maternal effects on kin preferences are well documented in ground squirrels. The most common social behavior among juveniles is play, and young prefer to play with littermates and other kin over non-kin; this discrimination among juveniles is typically mediated by olfactory cues (Urocitellus columbianus, Urocitellus beldingi, Callospermophilus lateralis) (Waterman 1986; Holmes 1994, 1995; Mateo 2003). In U. beldingi, mothers are important for the development and crystallization of these preferences for kin. Juveniles reared in a semi-natural enclosure without their mothers fail to develop play–partner preferences. However, when mothers are present but unable to intervene in social interactions, preferences for littermates still develop, suggesting that a mother’s role is indirect. Indeed, it is a mother’s presence at night in the burrow system that attracts her offspring to sleep together, resulting in the establishment of kin preferences (Holmes and Mateo 1998). Play is thought to lay a foundation for adult kin preferences and nepotism, and therefore is expected to vary with kinship (Michener 1983; Holmes 1994). In some sciurids, however, even in the absence of nepotism, juveniles develop kin-recognition abilities and kin biases (e.g., C. lateralis), which might function in the avoidance of inbreeding (Michener 1983; Mateo 2002).
Conclusions Parental effects can help shape offspring’s behavioral repertoires, tuning them to the appropriate physiological, environmental, and social contexts. They will be favored when parents and their offspring experience similar social and physical environments and thus similar availability of resources, predation pressure, and social dynamics. Plasticity in survival behaviors can be adaptive when number and kinds of predators are variable. This plasticity can occur at multiple scales, across both space and time. Variation in the intensity of the risk of predation, quality of surrounding habitat, and predictability of the number and types of local predors can result in open developmental programs. Modification of behaviors through experience will allow animals to maximize foraging and growth, without increasing the risk of predation, according to their local conditions. Future work could determine the fitness outcomes of plasticity and the parental effects of dispersing and migrating animals, or in changing environments due to climatic change or urbanization. Interdisciplinary approaches will help to identify physiological and behavioral mechanisms underlying developmental plasticity.
Funding The National Science Foundation (IBN 93-11508, IBN 98-08704, and IOB 05-17137) and the National Institutes of Health (MH63921-01A1) funded collection of the data discussed here.
References Anderson EM, Boutin S. 2002. Edge effects on survival and behaviour of juvenile red squirrels (Tamiasciurus hudsonicus). Can J Zool 80:1038–46. Barbazanges A, Piazza PV, Le Moal M, Maccari S. 1996. Maternal glucocorticoid secretion mediates long-term effects of prenatal stress. J Neurosci 16:3943–9. Bokony V, Lendvai AZ, Va´ga´si CI, Pa˘tras L, Pap PL, Ne´meth J, Vincze E, Papp S, Preiszner B, Seress G, et al. 2014. Necessity or capacity? Physiological state predicts problem-solving performance in house sparrows. Behav Ecol 25:124–35. Bolles RC. 1970. Species-specific defense reactions and avoidance learning. Psychol Rev 77:32–48. Boonstra R, McColl CJ. 2000. Contrasting stress response of male Arctic ground squirrels and red squirrels. J Exp Zool 286:390–404. Cairns RB, Gariepy JL, Hood KE. 1990. Development, microevolution, and social behavior. Psychol Rev 97:49–65. Catalani A. 1997. Neonatal exposure to glucocorticoids: longterm endocrine and behavioral effects. Dev Brain Dysfunct 10:393–404.
Downloaded from http://icb.oxfordjournals.org/ at FAKHEBISCONSORTIUM2006 on October 16, 2014
(Mateo 2007b) that would facilitate escape from predators and promote enhanced vigilance while also enhancing storage of glucose for the approaching hibernation. Thus, animals are locally adapted to their risk of predation, both behaviorally and physiologically, thereby allowing them to balance tradeoffs among foraging, vigilance, and anti-predator behaviors. Because mothers can influence the ontogeny of their offspring’s anti-predator behaviors (Mateo 1996a; Mateo and Holmes 1997), their offspring should exhibit repertoires that are appropriate for their population (see also Fraser and Gilliam 1987; Boonstra and McColl 2000; Hik et al. 2001; Wingfield 2004; Reeder and Kramer 2005; Clinchy et al. 2011). This would be adaptive for both sons and daughters, as natal dispersal is typically constrained to within their current population (Holekamp 1984), although as noted above adaptations to microhabitats may be maladaptive for sons.
J. M. Mateo
Development and behavioral plasticity
Hamilton WD. 1964. The genetical evolution of social behaviour, I. II. J Theor Biol 7:1–52. Hanken J, Sherman PW. 1981. Multiple paternity in Belding’s ground squirrel litters. Science 212:351–3. Hanson MT, Coss RG. 1997. Age differences in the response of California ground squirrels (Spermophilus beecheyi) to avian and mammalian predators. J Comp Psychol 111:174–84. Heyes CM. 1999. Social learning in animals: categories and mechanisms. Biol Rev 69:207–31. Hik DS, McColl CJ, Boonstra R. 2001. Why are Arctic ground squirrels more stressed in the boreal forest than in alpine meadows? Ecoscience 8:275–88. Hinde RA. 1954. Factors governing the changes in strength of a partially inborn response, as shown by the mobbing behaviour of the chaffinch (Fringilla coelebs).1. The nature of the response, and an examination of its course. Proc R Soc Ser B Biol Sci 142:306–31. Hirsch BT, Morrell LJ. 2011. Measuring marginal predation in animal groups. Behav Ecol 22:648–56. Holekamp KE. 1984. Natal dispersal in Belding’s ground squirrels (Spermophilus beldingi). Behav Ecol Sociobiol 16:21–30. Holmes WG. 1994. The development of littermate preferences in juvenile Belding’s ground squirrels. Anim Behav 48:1071–84. Holmes WG. 1995. The ontogeny of littermate preferences in juvenile golden-mantled ground squirrels: Effects of rearing and relatedness. Anim Behav 50:309–22. Holmes WG, Mateo JM. 1998. How mothers influence the development of litter-mate preferences in Belding’s ground squirrels. Anim Behav 55:1555–70. Jenkins SH, Eshelman BD. 1984. Spermophilus beldingi. Mammal Spec 221:1–8. Johnston TD. 1982. Selective costs and benefits in the evolution of learning. In: Rosenblatt JS, Hinde RA, Beer C, Busnel M-C, editors. Advances in the study of behavior. Vol. 12. New York: Academic Press. p. 65–106. Johnston TD. 1987. The persistence of dichotomies in the study of behavioral development. Dev Rev 7:149–82. Lazarus J. 2003. Vigilance and group size: early studies, the edge effect, secondary defences, the double advantage tradeoff and the future. Behav Process 63:129–31. Leger DW, Berney-Key SD, Sherman PW. 1984. Vocalizations of Belding’s ground squirrels (Spermophilus beldingi). Anim Behav 32:753–64. Lehrman DS. 1970. Semantic and conceptual issues in the nature–nurture problem. In: Aronson LR, Tobach E, Lehrman DS, Rosenblatt JS, editors. Development and evolution of behavior. San Francisco (CA): W. H. Freeman. p. 17–52. Love OP, Williams TD. 2008. Plasticity in the adrenocortical response of a free-living vertebrate: the role of preand post-natal developmental stress. Horm Behav 54: 496–505. Love OP, McGowan PO, Sheriff MJ. 2013. Maternal adversity and ecological stressors in natural populations: the role of stress axis programming in individuals, with implications for populations and communities. Funct Ecol 27:81–92.
Downloaded from http://icb.oxfordjournals.org/ at FAKHEBISCONSORTIUM2006 on October 16, 2014
Catalani A, Casolini P, Cigliana G, Scaccianoce S, Consoli C, Cinque C, Zuena AR, Angelucci L. 2002. Maternal corticosterone influences behavior, stress response and corticosteroid receptors in the female rat. Pharmacol Biochem Behav 73:105–14. Champagne F, Curley JP. 2009. The transgenerational influence of maternal care on offspring gene expression and behavior in rodents. In: Maestripieri D, Mateo JM, editors. Maternal effects in mammals. Chicago (IL): University of Chicago Press. p. 182–202. Cheney DL, Seyfarth RM. 1990. How monkeys see the world. Chicago (IL): University of Chicago Press. Clinchy M, Zanette L, Charlier TD, Newman AEM, Schmidt KL, Boonstra R, Soma KK. 2011. Multiple measures elucidate glucocorticoid responses to environmental variation in predation threat. Oecologia 166:607–14. Coss RG, Owings DH. 1985. Restraints on ground squirrel antipredator behavior: adjustments over multiple time scales. In: Johnston TD, Pietrewicz AT, editors. Issues in the ecological study of learning. Hillsdale (NJ): Lawrence Erlbaum Associates. p. 167–200. Coss RG, Guse KL, Poran NS, Smith DG. 1993. Development of antisnake defenses in California ground squirrels (Spermophilus beecheyi): II. Microevolutionary effects of relaxed selection from rattlesnakes. Behaviour 124:137–64. Curio E. 1993. Proximate and developmental aspects of antipredator behavior. In: Slater PJB, Rosenblatt JS, Snowdon CT, Milinski M, editors. Advances in the study of behavior. Vol. 22. New York: Academic Press. p. 135–238. de Kloet ER, Oitzl MS, Joels M. 1999. Stress and cognition: are corticosteroids good or bad guys? Trends Neurosci 22:422–6. Elgar MA. 1989. Predator vigilance and group size in mammals and birds: a critical review of the empirical evidence. Biol Rev Camb Phil Soc 64:13–33. Ferrari C, Bogliani G, von Hardenberg A. 2009. Alpine marmots (Marmota marmota) adjust vigilance behaviour according to environmental characteristics of their surrounding. Ethol Ecol Evol 21:355–64. Fisher RA. 1930. The genetical theory of natural selection. Oxford: Clarendon Press. Fraser DF, Gilliam JF. 1987. Feeding under predation hazard: response of the guppy and Hart’s rivulus from sites with contrasting predation hazard. Behav Ecol Sociobiol 21:203–9. Goldthwaite RO, Coss RG, Owings DH. 1990. Evolutionary dissipation of an antisnake system: differential behavior by California and Arctic ground squirrels in above- and below-ground contexts. Behaviour 112:246–69. Gottlieb G. 1976. The roles of experience in the development of behavior and the nervous system. In: Gottlieb G, editor. Studies on the development of behavior and the nervous system. Vol 3. Neural and Behavioral Specificity. New York: Academic Press. p. 25–53. Griffin AS. 2004. Social learning about predators: a review and prospectus. Learn Behav 32:131–40. Haldane JBS. 1932. The causes of evolution. New York: Longmans Green.
847
848
Meylan S, Clobert J. 2005. Is corticosterone-mediated phenotype development adaptive? Maternal corticosterone treatment enhances survival in male lizards. Horm Behav 48:44–52. Meylan S, Miles DB, Clobert J. 2012. Hormonally mediated maternal effects, individual strategy and global change. Phil Trans R Soc B Biol Sci 367:1647–64. Michener GR. 1983. Kin identification, matriarchies, and the evolution of sociality in ground-dwelling sciurids. In: Eisenberg JF, Kleiman DG, editors. Advances in the study of mammalian behavior. Shippensburg (PA): American Society of Mammalogists. p. 528–72. Morrell LJ, Ruxton GD, James R. 2011. Spatial positioning in the selfish herd. Behav Ecol 22:16–22. Mousseau TA, Fox CW. 1998. Maternal effects as adaptations. Oxford: Oxford University Press. Murie JO, Boag DA. 1984. The relationship of body weight to overwinter survival in Columbian ground squirrels. J Mammal 65:688–90. Nelson AB, Alemadi SD, Wisenden BD. 2013. Learned recognition of novel predator odour by convict cichlid embryos. Behav Ecol Sociobiol 67:1269–73. Nicol CJ. 1995. The social transmission of information and behaviour. Appl Anim Behav Sci 44:79–98. Owings DH, Hennessy DF. 1984. The importance of variation in sciurid visual and vocal communication. In: Murie JO, Michener GR, editors. The biology of grounddwelling squirrels: annual cycles, behavioral ecology, and sociality. Lincoln: University of Nebraska Press. p. 169–200. Owings DH, Virginia RA. 1978. Alarm calls of California ground squirrels (Spermophilus beecheyi). Z Tierpsychol 46:58–70. Owings DH, Coss RG, McKernon D, Rowe MP, Arrowood PC. 2001. Snake-directed antipredator behavior of rock squirrels (Spermophilus variegatus): population differences and snake-species discrimination. Behaviour 138:575–95. Poran NS, Coss RG. 1990. Development of antisnake defenses in California ground squirrels (Spermophilus beecheyi): I. Behavioral and immunological relationships. Behaviour 112:222–45. Pravosudov VV. 2003. Long-term moderate elevation of corticosterone facilitates avian food-caching behaviour and enhances spatial memory. Proc R Soc Lond Ser B: Biol Sci 270:2599–604. Reeder DM, Kramer KM. 2005. Stress in free-ranging mammals: integrating physiology, ecology, and natural history. J Mammal 86:225–35. Reinhold K. 2002. Maternal effects and the evolution of behavioral and morphological characters: a literature review indicates the importance of extended maternal care. J Hered 93:400–5. Richerson PJ, Boyd R. 2001. Built for speed, not for comfort: Darwinian theory and human culture. Hist Phil Life Sci 23:425–65. Robinson SR. 1980. Antipredator behaviour and predator recognition in Belding’s ground squirrels. Anim Behav 28:840–52. Robinson SR. 1981. Alarm communication in Belding’s ground squirrels. Z Tierpsychol 56:150–68.
Downloaded from http://icb.oxfordjournals.org/ at FAKHEBISCONSORTIUM2006 on October 16, 2014
Lupien SJ, McEwen BS. 1997. The acute effects of corticosteroids on cognition: integration of animal and human model studies. Brain Res Rev 24:1–27. Magurran AE. 1990. The inheritance and development of minnow anti-predator behaviour. Anim Behav 39:834–42. Mateo JM. 1995. The development of alarm-call responses in free-living and captive Belding’s ground squirrels, Spermophilus beldingi [PhD thesis]. University of Michigan. Mateo JM. 1996a. The development of alarm-call response behaviour in free-living juvenile Belding’s ground squirrels. Anim Behav 52:489–505. Mateo JM. 1996b. Early auditory experience and the ontogeny of alarm-call discrimination in Belding’s ground squirrels (Spermophilus beldingi). J Comp Psychol 110:115–24. Mateo JM. 2002. Kin-recognition abilities and nepotism as a function of sociality. Proc R Soc Lond Ser B Biol Sci 269:721–7. Mateo JM. 2003. Kin recognition in ground squirrels and other rodents. J Mammal 84:1163–81. Mateo JM. 2006. Developmental and geographic variation in stress hormones in wild Belding’s ground squirrels (Spermophilus beldingi). Horm Behav 50:718–25. Mateo JM. 2007a. Ontogeny of adaptive behaviors. In: Wolff JO, Sherman PW, editors. Rodent societies. Chicago (IL): University of Chicago Press. p. 195–206. Mateo JM. 2007b. Ecological and physiological correlates of anti-predator behaviors of Belding’s ground squirrels (Spermophilus beldingi). Behav Ecol Sociobiol 62:37–49. Mateo JM. 2008. Inverted-U shape relationship between cortisol and learning in ground squirrels. Neurobiol Learn Mem 89:582–90. Mateo JM. 2009. Maternal influences on development, social relationships and survival behaviors. In: Maestripieri D, Mateo JM, editors. Maternal effects in mammals. Chicago (IL): University of Chicago Press. p. 133–58. Mateo JM, Holmes WG. 1997. Development of alarm-call responses in Belding’s ground squirrels: the role of dams. Anim Behav 54:509–24. Mateo JM, Holmes WG. 1999. Plasticity of alarm-call response development in Belding’s ground squirrels (Spermophilus beldingi, Sciuridae). Ethology 105:193–206. Mayr E. 1974. Behavior programs and evolutionary strategies. Am Sci 62:650–9. McAdam AG. 2009. Maternal effects on evolutionary dynamics in wild small mammals. In: Maestripieri D, Mateo JM, editors. Maternal effects in mammals. Chicago (IL): University of Chicago Press. p. 64–82. McCormick MI. 1998. Behaviorally induced maternal stress in a fish influences progeny quality by a hormonal mechanism. Ecology 79:1873–83. McGaugh JL. 1989. Involvement of hormonal and neuromodulatory systems in the regulation of memory storage. Annu Rev Neurosci 12:255–87. Meaney MJ, Szyf M, Seckl JR. 2007. Epigenetic mechanisms of perinatal programming of hypothalamic–pituitary–adrenal function and health. Trends Mol Med 13: 269–77. Meno W, Coss RG, Perry S. 2013. Development of snakedirected antipredator behavior by wild white-faced capuchin monkeys: II. Influence of the social environment. Am J Primatol 75:292–300.
J. M. Mateo
Development and behavioral plasticity
Shriner WM. 1999. Antipredator responses to a previously neutral sound by free-living adult golden-mantled ground squirrels, Spermophilus lateralis (Sciuridae). Ethology 105:747–57. Stamps J. 2003. Behavioural processes affecting development: Tinbergen’s fourth question comes of age. Anim Behav 66:1–13. Swaisgood RR, Owings DH, Rowe MP. 1999. Conflict and assessment in a predator–prey system: ground squirrels versus rattlesnakes. Anim Behav 57:1033–44. Thaker M, Vanak AT, Lima SL, Hews DK. 2010. Stress and aversive learning in a wild vertebrate: the role of corticosterone in mediating escape from a novel stressor. Am Nat 175:50–60. Tinbergen N. 1953. Social behaviour in animals. New York: John Wiley & Sons. Uller T, Olsson M. 2006. Direct exposure to corticosterone during embryonic development influences behaviour in an ovoviviparous lizard. Ethology 112:390–7. Vitale AF. 1989. Changes in anti-predator responses of wild rabbits, Oryctolagus cuniculus (L.), with age and experience. Behaviour 110:47–61. Waterman JM. 1986. Behaviour and use of space by juvenile Columbian ground squirrels. Can J Zool 64:1121–7. West MJ, King AP. 2008. Deconstructing innate illusions: reflections on nature–nurture-niche from an unlikely source. Phil Psychol 21:383–95. Wingfield JC. 2004. Control of behavioural strategies for capricious environments. Anim Behav 66:807–16. Wright S. 1931. Evolution in Mendelian populations. Genetics 16:97–159.
Downloaded from http://icb.oxfordjournals.org/ at FAKHEBISCONSORTIUM2006 on October 16, 2014
Roozendaal B. 2000. Glucocorticoids and the regulation of memory consolidation. Psychoneuroendocrinology 25:213–38. Schopper H, Palme R, Ruf T, Huber S. 2012. Effects of prenatal stress on hypothalamic–pituitary–adrenal (HPA) axis function over two generations of guinea pigs (Cavia aperea f. porcellus). Gen Comp Endocrinol 176:18–27. Seyfarth RM, Cheney DL. 1980. The ontogeny of vervet monkey alarm calling behavior: a preliminary report. Z Tierpsychol 54:37–56. Sheriff MJ, Love OP. 2013. Determining the adaptive potential of maternal stress. Ecol Lett 16:271–80. Sheriff MJ, Krebs CJ, Boonstra R. 2010. The ghosts of predators past: population cycles and the role of maternal programming under fluctuating predation risk. Ecology 91:2983–94. Sherman PW. 1976. Natural selection among some groupliving organisms [PhD thesis]. University of Michigan. Sherman PW. 1977. Nepotism and the evolution of alarm calls. Science 197:1246–53. Sherman PW. 1981. Kinship, demography, and Belding’s ground squirrel nepotism. Behav Ecol Sociobiol 8:251–9. Sherman PW. 1985. Alarm calls of Belding’s ground squirrels to aerial predators: nepotism or self-preservation? Behav Ecol Sociobiol 17:313–23. Sherman PW, Morton ML. 1984. Demography of Belding’s ground squirrels. Ecology 65:1617–28. Shettleworth S. 1998. Cognition, evolution, and behavior. New York: Oxford University Press. Shi JB, Li DQ, Xiao WF. 2011. Influences of sex, group size, and spatial position on vigilance behavior of Przewalski’s gazelles. Acta Theriol 56:73–9.
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