Abstract

A fundamental tenet of maternal effects assumes that maternal variance over time should have discordant consequences for offspring traits across litters. Yet, seldom are parents observed across multiple reproductive bouts, with few studies considering anthropogenic disturbances as an ecological driver of maternal effects. We observed captive coyote (Canis latrans) pairs over two successive litters to determine whether among‐litter differences in behavior (i.e., risk‐taking) and hormones (i.e., cortisol and testosterone) corresponded with parental plasticity in habituation. Thus, we explicitly test the hypothesis that accumulating experiences of anthropogenic disturbance reduces parental fear across reproductive bouts, which should have disparate phenotypic consequences for first‐ and second‐litter offspring. To quantify risk‐taking behavior, we used foraging assays from 5–15 weeks of age with a human observer present as a proxy for human disturbance. At 5, 10, and 15 weeks of age, we collected shaved hair to quantify pup hormone levels. We then used a quantitative genetic approach to estimate heritability, repeatability, and between‐trait correlations. We found that parents were riskier (i.e., foraged more frequently) with their second versus first litters, supporting our prediction that parents become increasingly habituated over time. Second‐litter pups were also less risk‐averse than their first‐litter siblings. Heritability for all traits did not differ from zero (0.001–0.018); however, we found moderate support for repeatability in all observed traits (r = 0.085–0.421). Lastly, we found evidence of positive phenotypic and cohort correlations among pup traits, implying that cohort identity (i.e., common environment) contributes to the development of phenotypic syndromes in coyote pups. Our results suggest that parental habituation may be an ecological cue for offspring to reduce their fear response, thus emphasizing the role of parental plasticity in shaping their pups’ behavioral and hormonal responses toward humans.

Highlights

  • Maternal effects have the potential to drive both the direction and strength of evolutionary change in a population (Bonduriansky & Day, 2009; Marshall & Uller, 2007; Wolf, Brodie, Cheverud, Moore, & Wade, 1998)

  • Our four main questions are as follows: (a) is parental fear of humans reduced over time; (b) does among‐year plasticity in parental fear pre‐ dict among‐litter plasticity in risk‐taking behavior; (c) do endocrine traits differ between first and sec‐ ond‐litter siblings; and (d) are offspring traits repeatable and her‐ itable? We address these questions in a captive system because the experimental design of among‐litter studies often requires recapture and repeated measures that are difficult to obtain in the wild

  • The combination of prior experiences paired with current environ‐ mental context induce parental plasticity over multiple reproduc‐ tive bouts (Plaistow et al, 2007; Uller, 2008; Uller et al, 2013), FIGURE 4 Hormonal differences among first‐ and second‐litter offspring in hair cortisol and testosterone concentrations at 5, 10, and 15 weeks of age

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Summary

| INTRODUCTION

Maternal effects have the potential to drive both the direction and strength of evolutionary change in a population (Bonduriansky & Day, 2009; Marshall & Uller, 2007; Wolf, Brodie, Cheverud, Moore, & Wade, 1998). Previous empirical work provides evidence to suggest that wildlife perceive humans as predators, and as such, display fear responses that are qualitatively similar to those exhibited in the presence of natural predators (Blumstein, 2006; Carrete & Tella, 2017; Rebolo‐Ifran et al, 2015) This is the case for carnivores, as several recent studies suggest behavioral and eco‐ logical patterns of such species are directly modified as a func‐ tion of anthropogenic disturbance This study represents a novel integration of parental effects theory with human‐wildlife interactions to assess how human disturbance may contribute to transgenerational plasticity

| METHODS
| DISCUSSION
CONFLICT OF INTEREST

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