Arginine Vasotocin and Neuropeptide Y Vary with Seasonal Life-History Transitions in Garter Snakes

Abstract

Transitions between life-history stages are often accompanied by dramatic behavioral switches that result from a shift in motivation to pursue one resource over another. While the neuroendocrine mechanisms that regulate such behavioral transitions are poorly understood, arginine vasotocin (AVT) and neuropeptide Y (NPY) are excellent candidates because they modulate reproductive and feeding behavior, respectively. We asked if seasonal changes in AVT and NPY are concomitant with the seasonal migration to and from the feeding grounds in red-sided garter snakes (Thamnophis sirtalis parietalis). Male and female snakes were collected in different migratory states during both the spring and fall. The total number of AVT- and NPY-immunoreactive (ir) cells was then quantified in each brain region of interest. To correct for potential variation in region volume related to sexually dimorphic body size in this species, we first determined that snout-vent length is an accurate proxy for regional brain volume. We then corrected each individual's ir cell number by its SVL to directly compare seasonal changes in AVT and NPY between males and females. Within the supraoptic nucleus, both males and females had more AVT-ir cells during the fall compared with spring. As predicted, males had significantly more AVT-ir cells during the spring mating season in the hypothalamus (HYP) and bed nucleus of the stria terminalis, brain regions important in regulating reproductive behavior. Females also had significantly more AVT-ir cells in the HYP during the spring, as well as a significantly higher number of hypothalamic AVT cells than males. During the fall, males had significantly more NPY-ir cells in the cortex and posterior HYP compared with spring, possibly reflecting increased feeding behavior during summer foraging. Females did not exhibit significant main effects of season on NPY-ir cell number in any region. Neither AVT- nor NPY-ir cell number varied significantly with migratory status, but we did observe significant changes related to seasonal transitions in reproductive state. Our results indicate that changes in brain AVT and NPY are associated with seasonal transitions in reproductive and foraging behaviors, and may be involved in mediating sex differences in the timing of life-history events.

Molecular and Neuroendocrine Approaches to Understanding Trade-offs: Food, Sex, Aggression, Stress, and Longevity—An Introduction to the Symposium

“…Other anorexigenic molecules include glucagon-like peptide, cholecystokinin, estradiol, kisspeptin, dopamine, and α-melanocyte stimulating hormone. Many of these chemical messengers stimulate HPG function, courtship and copulatory behavior, maternal behavior, growth, maturation, and many aspects of the immune response, and many are involved in seasonal cycles of feeding and breeding ( Hobbs et al 2012 ; Schneider et al 2013 ; Kriegsfeld et al 2015 ; Ashley and Demas 2017 ; Deviche et al 2017 ; Lucas et al 2017 ). Thus, systems that orchestrate trade-offs can be mediated by a wide array of molecules.…”

“…With regard to annual cycles, many warm-blooded species that inhabit temperate zones must reconcile the benefits of immediate reproduction with the costs of high offspring and parent mortality at low ambient temperatures, particularly when cold temperatures are accompanied by low food availability. This group of symposium papers includes new and reviewed information about the trade-offs in seasonally breeding, temperate zone bats ( Willis 2017 ), voles ( Ferkin 2017 ), hamsters ( Schneider et al 2017 ), birds ( Deviche et al 2017 ), and snakes ( Lucas et al 2017 ). In many such species, reproductive processes are suppressed to conserve energy for thermogenesis, and the hypothalamic–pituitary–gonadal (HPG) system is inhibited in direct response to the resulting energy deficits or to indirect cues that predict the onset of winter (reviewed by Bairlein and Gwinner 1994 ; Bronson 1989 ).…”

“…Both of these strategies provide the benefit of avoiding costs associated with cold ambient temperatures and/or low food availability, but have associated costs, such as compromised immune function and/or loss of restorative sleep (e.g., Willis 2017 and reviewed by Alerstam and Lindstrom 1990 ). Specific interactions between environmental cues and neuroendocrine systems create important species and sex differences in seasonal life history strategies (e.g., reviewed by Bentley et al 2017 ; Davies and Deviche 2014 ; Ferkin 2017 ; Lucas et al 2017 , in this symposium). In addition to annual cycles, estrous/menstrual cycles are associated with trade-offs.…”

“…This species hibernates in winter, emerges in spring, immediately engages in a two-week period of fasting and frenzied mating behavior, and then abruptly reverses priorities as it migrates to the feeding grounds. These behavioral transitions are associated with changes in a number of chemical messengers including arginine vasotocin and neuropeptide Y (NPY) ( Lucas et al 2017 ). Pierre Deviche reviewed the diversity of neuroendocrine mechanisms involved in the allocation of resources in birds with emphasis on the HPG and hypothalamic-pituitary-adrenal (HPA) systems ( Deviche et al 2017 ).…”

“…Adult offspring of lactationally food-restricted dams showed reduced levels of attractivity, proceptivity, and receptivity, which are likely to influence their reproductive success ( Ferkin 2017 ). All of the contributors are working on different physiological systems, including the stress response ( Bentley et al 2017 ), hibernation ( Willis 2017 ), immunity ( Crespi and Travis 2017 ), ingestive behavior ( Brozek et al 2017 ; Crespi and Travis 2017 ; Emmons 2017 ; Ferkin 2017 ; Lucas et al 2017 ; Schneider et al 2017 ), and reproduction ( Brozek et al 2017 ; Crespi and Travis 2017 ; Deviche et al 2017 ; Emmons 2017 ; Ferkin 2017 ; Lucas et al 2017 ; Schneider et al 2017 ). Not all contributors to this symposium are testing specific hypotheses about microevolutionary trade-offs, and many of the contributors are primarily concerned with neuroendocrine mechanisms.…”