Nikki Rendon | Indiana University (original) (raw)

Papers by Nikki Rendon

Chemical communication plays an integral role in social behavior by facilitating social encounter... more Chemical communication plays an integral role in social behavior by facilitating social encounters, allowing for
the evaluation of social partners, defining territories and advertising information such as species and sex.
Odors provide information about the social environment for rodents and other mammals; however, studies identifying
chemical compounds and their functions have thus far focused primarily on a few species. In addition, considerably
less attention has been focused on how environmental factors and behavioral context alter these
compounds during periods of reproductive quiescence. We examined the effects of photoperiod and social context
on chemical communication in the seasonally breeding Siberian hamster which displays modest territorial
aggression during long “summer-like” days, but increased aggression in short “winter-like” days. We collected
urine samples from long- and short-day male hamsters to investigate how photoperiod and subsequent changes
in reproductive phenotype alter urinary volatile compound profiles. Next, we identified changes in urinary compounds
before and after an aggressive encounter. Male hamsters exhibited a diverse urinary profile across photoperiods;
however, long-day reproductive males showed higher levels of individual compounds when
compared to short-day non-reproductive males. In addition, individual compounds were altered following an aggressive
encounter; some changed only in long days whereas others changed regardless of photoperiod. Further,
aggression and circulating levels of testosterone were positively correlated with urinary compounds in long-, but
not short-day males. These findings suggest both photoperiod- and aggression-specific physiological regulation
of urinary compounds in this species and contribute to a greater understanding of chemical communication more
broadly.

Chemical communication in the Siberian hamster (Phodopus sungorus) involves cues from urine, fece... more Chemical communication in the Siberian hamster (Phodopus sungorus) involves cues from urine, feces, as well as the ventral gland and supplemental sacculi glands. There are 48 constituent compounds in the ventral gland secretion of male Siberian hamsters, including constituents with typical steroidal mass spectra that remain unidentified. Such steroidal compounds present in reproductively active males suggests that the volatile profile in the ventral gland and other modes of chemical communication can vary seasonally and in relation to hormonal status. Seasonally breeding species exhibit many physiological and behavioral changes that occur during the transition from non-breeding to breeding condition. In the Siberian hamster, a long day breeder, these physiological changes are mediated by sex steroid hormones in response to photoperiod (i.e. elevated testosterone during breeding season, compared to basal testosterone during non breeding season), and aggressiveness increases significa...

There is a well-established positive relationship between gonadal steroids and aggression. In som... more There is a well-established positive relationship between gonadal steroids and aggression. In some seasonally breeding species, however, aggression often persists or is increased during short
“winter-like” days when the gonads are regressed and circulating levels of gonadal steroids are relatively low. Although the mechanisms underlying short-day increases in aggression are not fully known, the adrenal androgen dehydroepiandrosterone (DHEA) has been suggested as an alternative neuroendocrine mechanism regulating seasonal aggression. We used two complementary experimental approaches to examine the bi directional actions of DHEA and aggression in female Siberian hamsters, a seasonal rodent that displays increased aggression concomitant with elevated circulating DHEA in short days. In Experiment 1, we examined the effects of aggressive interactions on DHEA concentrations before and after an aggressive encounter in long- and short-day hamsters. Serum DHEA was altered in a photoperiod-dependent manner, with decreased DHEA levels in response to aggression in short- but not long-day hamsters. Next, we experimentally induced adrenal DHEA release via injections of exogenous ACTH and assessed changes in aggressive behavior across photoperiods. We show a robust increase in aggression in short compared with long days during baseline aggression trials; however, aggression was not significantly increased further in response to ACTH in either photoperiod during post- ACTH aggression trials. These findings suggest that DHEA plays a role in the regulation of short-day aggression, while also highlighting the need for additional studies addressing the causal relationship between DHEA and aggression in this and others species.

Historically, research on the neuroendocrinology of aggression has been dominated by the paradigm... more Historically, research on the neuroendocrinology of aggression has been dominated by the paradigm that the brain receives sex steroid hormones, such as testosterone (T), from the gonads, and then these gonadal hormones modulate behaviorally relevant neural circuits. While this paradigm has been extremely useful for advancing the field, recent studies reveal important alternatives. For example, most vertebrate species are seasonal breeders, and many species show aggression outside of the breeding season, when the gonads are regressed and circulating levels of gonadal steroids are relatively low. Studies in diverse avian and mammalian species suggest that adrenal dehydroepiandrosterone (DHEA), an androgen precursor and prohormone, is important for the expression of aggression when gonadal T synthesis is low. Circulating DHEA can be converted into active sex steroids within the brain. In addition, the brain can synthesize sex steroids de novo from cholesterol, thereby uncoupling brain steroid levels from circulating steroid levels. These alternative mechanisms to provide sex steroids to specific neural circuits may have evolved to avoid the costs of high circulating T levels during the non-breeding season. Physiological indicators of season (e.g., melatonin) may allow animals to switch from one neuroendocrine mechanism to another across the year. DHEA and neurosteroids are likely to be important for the control of multiple behaviors in many species, including humans. These studies yield fundamental insights into the regulation of DHEA secretion, the mechanisms by which DHEA affects behavior, and the brain regions and neural processes that are modulated by DHEA. It is clear that the brain is an important site of DHEA synthesis and action.

Testosterone mediates aggression in many vertebrates. In some species, aggression remains high du... more Testosterone mediates aggression in many vertebrates. In some species, aggression remains high during the non-breeding season (e.g., winter), when testosterone levels are low. In Siberian hamsters (Phodopus sungorus), we have demonstrated photoperiodic changes in aggression with hamsters housed in short, “winter-like” days displaying significantly more territorial aggression than long-day animals, despite low levels of testosterone. The mechanisms by which photoperiod regulates aggression, however, remain largely unknown. Adrenocortical hormones (e.g., glucocorticoids) have been implicated in mediating seasonal aggression; circulating concentrations of these hormones have been correlated with aggression in some species. The goal of this study was to examine the role of cortisol and glucocorticoid receptors in mediating photoperiodic changes in aggression in male Siberian hamsters. Males were housed in long or short days and treated with either exogenous cortisol or vehicle. Circulating levels of cortisol, adrenal cortisol content, and aggression were quantified. Lastly, photoperiodic effects on glucocorticoid receptor (GR) protein levels were quantified in limbic brain regions associated with aggression, including medial prefrontal cortex, amygdala, and hippocampus. Short-day hamsters were more aggressive than long-day hamsters, however cortisol treatment did not affect aggression. Photoperiod had no effect on serum or adrenal cortisol or GR levels in the brain regions examined. Taken together, these data suggest that increases in cortisol levels do
not cause increases associated with short-day aggression, and further that GR protein levels are not associated with photoperiodic changes in aggression. The results of this study contribute to our understanding of the role of adrenocortical steroids in mediating seasonal aggression.

Seasonal variation in social behavior is often accompanied by seasonal variation in communication... more Seasonal variation in social behavior is often accompanied by seasonal variation in communication. In mammals, how seasonal environmental cues influence aggressive vocalizations remains underexplored. Photoperiod is the primary cue coordinating seasonal responses in most temperate zone animals, including Siberian hamsters (Phodopus sungorus), a species that undergoes reproductive inhibition and increased aggression in winter. During same-sex aggressive encounters, hamsters emit both broadband calls (BBCs) and ultrasonic vocalizations (USVs) that indicate aggression and the vocalizer's sex, respectively; however, it is not known whether these rodents adjust specific elements of their vocal repertoire to reflect their photoperiod-induced seasonal phenotypes. To address this, we recorded vocalizations emitted during dyadic interactions between male or female pairs of hamsters housed in long or short photoperiods and measured serum testosterone levels. USV emission rate remained stable across photoperiods, but proportional use of USV subtypes varied in novel ways: ‘jump’ USVs were sensitive to seasonal phenotype, but not the vocalizer's sex, whereas ‘plain’ USVs were sensitive only to the sex of the vocalizer. BBC emission rate varied with seasonal phenotype; short-day non-reproductive hamsters produced more BBCs and demonstrated increased aggression compared with reproductive hamsters. Testosterone, however, was not related to vocalization rates. Collectively, these findings demonstrate that changes in the vocal repertoire of Siberian hamsters reflect sex, aggression, and seasonal phenotype, suggesting that both BBCs and USVs are important signals used during same-sex social encounters.

Classic findings have demonstrated an important role for sex steroids as regulators of aggression... more Classic findings have demonstrated an important role for sex steroids as regulators of aggression, but this relationship is lacking within some environmental contexts. In mammals and birds, the adrenal androgen dehydroepiandrosterone (DHEA), a non-gonadal precursor of biologically active steroids, has been linked to aggression. Although females, like males, use aggression when competing for limited resources, the mechanisms underlying female aggression remain understudied. Here, we propose a previously undescribed endocrine mechanism regulating female aggression via direct action of the pineal hormone melatonin on adrenal androgens. We examined this in a solitary hamster species, Phodopus sungorus, in which both sexes are highly territorial across the seasons, and display increased aggression concomitant with decreased serumlevels of sex steroids in short ‘winter-like’ days. Short- but not long-day females had increased adrenal DHEA responsiveness co-occurring with morphological changes in the adrenal gland. Further, serum DHEA and total adrenal DHEA content were elevated in short days. Lastly, melatonin increased DHEA and aggression and stimulated DHEA release from cultured adrenals. Collectively, these findings demonstrate that DHEA is a key peripheral regulator of aggression and that melatonin coordinates a ‘seasonal switch’ from gonadal to adrenal regulation of aggression by direct action on the adrenal glands.

Vocalizations constitute an important channel of communication for many vertebrates. Classes of v... more Vocalizations constitute an important channel of communication for many vertebrates. Classes of vocalizations may be closely associated with particular contexts or behaviours, and variation within classes may convey information on individual identity, sex or motivational state. Rodent vocal communication has largely been studied within a reproductive context, but rodents also utter vocalizations during aggressive encounters with same-sex conspecifics. In this work we investigated same-sex vocal behaviour of Siberian hamsters, a mammalian model species for studying aggression. Males and females produced two main classes of vocalizations: high-frequency (>20 kHz), narrowband vocalizations (ultrasonic vocalizations; USVs) and lower-frequency, broadband vocalizations (broadband calls; BBCs). USVs and BBCs were further classified into subtypes based on spectrotemporal characteristics. With these classifications, we made the predictions that hamsters would utter distinct subcategories of calls, that there would be sex differences in call usage, and that BBCs would be more closely associated with aggressive behaviours than USVs. While there were no sex differences in the total number of USVs or BBCs produced by a pair, the use of vocalization subcategories varied by sex, with females uttering more variable USVs and more ‘rattle’ BBCs than males. In conjunction with these differences in vocal behaviour, the sexes also differed in aggression. Across both sexes, variation in aggressive behaviour correlated with variation in the number of ‘squeak’ BBCs and ‘rattle’ BBCs, whereas USVs were not related to aggression. Thus, BBCs constitute a distinct vocalization type with an important role in aggressive communication for hamsters.

Thesis Chapters by Nikki Rendon

Gonadal hormones are key regulators of behavior through their actions on the central nervous syst... more Gonadal hormones are key regulators of behavior through their actions on the central nervous system (CNS). To date, studies of aggression have overwhelmingly focused on actions of the gonadal hormone testosterone in the CNS. This ‘central’ dogma has resulted in an oversimplified framework of the neuroendocrine mechanisms underlying aggression. Evidence across taxa and sexes, however, demonstrates the lack of a consistent relationship between gonadal steroids and aggression, suggesting alternative, non-gonadal mechanisms that regulate this behavior. In order to fill this knowledge gap, I examined extra-gonadal neuroendocrine mechanisms regulating aggression in a year-round highly territorial mammal, Siberian hamsters. Within this seasonal context, I manipulated ambient day length (photoperiod) and melatonin, the biochemical signal of day length, to induce variation in reproductive phenotype and behavior. Hamsters responded to both photoperiod and melatonin by altering reproductive competence and displaying concomitant changes in behavior. Specifically, short-day females displayed increased aggression despite non-functional gonads and relatively low levels of the gonadal estrogen, estradiol, compared with long-day animals that displayed low aggression despite functional gonads. In this dissertation, I first examined how reproductive phenotype influences underlying variation in behavior across seasonal transitions and provide evidence for changes in estrogen-mediated mechanisms. Next, I manipulated temporal patterns of melatonin to show that females differentially alter aggression and modes of steroid metabolic conversion. Further, I illustrate bi-directional actions of adrenal steroids and behavior in a season-dependent manner. Finally, I propose an alternative mechanism in which the adrenal androgen, dehydroepiandrosterone (DHEA), serves as a key peripheral regulator of aggression and that melatonin coordinates a ‘seasonal switch’ from gonadal to adrenal regulation of aggression by direct action on adrenal glands. Using a whole-organism approach to probe the interconnectivity of target tissues, I show that aggression is differentially regulated across seasons, and highlight that DHEA serves a critical, but underappreciated role in the regulation of behavior. By examining the interactions of physiology and behavior across ecological contexts and time, these data expand the existing framework of the neuroendocrine regulation of social behavior and have broad applications to the evolution of behavior by highlighting key endocrine players natural selection could act upon.