Ignacio T. Moore’s research while affiliated with Virginia Tech and other places

The neurogenomic mechanisms mediating male–male reproductive cooperative behaviours remain unknown. We leveraged extensive transcriptomic and behavioural data on a neotropical bird species ( Pipra filicauda ) that performs cooperative courtship displays to understand these mechanisms. In this species, the cooperative display is modulated by testosterone, which promotes cooperation in non‐territorial birds, but suppresses cooperation in territory holders. We sought to understand the neurogenomic underpinnings of three related traits: social status, cooperative display behaviour and testosterone phenotype. To do this, we profiled gene expression in 10 brain nuclei spanning the social decision‐making network (SDMN), and two key endocrine tissues that regulate social behaviour. We associated gene expression with each bird's behavioural and endocrine profile derived from 3 years of repeated measures taken from free‐living birds in the Ecuadorian Amazon. We found distinct landscapes of constitutive gene expression were associated with social status, testosterone phenotype and cooperation, reflecting the modular organization and engagement of neuroendocrine tissues. Sex‐steroid and neuropeptide signalling appeared to be important in mediating status‐specific relationships between testosterone and cooperation, suggesting shared regulatory mechanisms with male aggressive and sexual behaviours. We also identified differentially regulated genes involved in cellular activity and synaptic potentiation, suggesting multiple mechanisms underpin these genomic states. Finally, we identified SDMN‐wide gene expression differences between territorial and floater males that could form the basis of ‘status‐specific’ neurophysiological phenotypes, potentially mediated by testosterone and growth hormone. Overall, our findings provide new, systems‐level insights into the mechanisms of cooperative behaviour and suggest that differences in neurogenomic state are the basis for individual differences in social behaviour.

Understanding stress ecology in snakes is important to anticipate individual and population-level consequences of different types of stressors and plan for conservation efforts. Additionally, an understanding of stress ecology in snakes broadens the basic understanding of stress responses across vertebrates. We review a variety of metrics available to assess stress and provide context and resources where these metrics have been applied in snakes. We then explore how these metrics change as snakes respond to different types of stressors. Throughout, we highlight gaps in understanding, and summarize important future research directions to establish a more comprehensive understanding of snake stress ecology.

Emerging fungal pathogens are a direct threat to vertebrate biodiversity. Elucidating the mechanisms by which mycoses impact host fitness is an important step towards effective prediction and management of disease outcomes in populations. The vertebrate acute stress response is an adaptive mechanism that allows individuals to meet challenges to homeostasis and survival in dynamic environments. Disease may cause stress, and coping with fungal infections may require shifts in resource allocation that alter the ability of hosts to mount an acute response to other external stressors. We examined the glucocorticoid and glycemic response to acute capture stress in a population of free-living pygmy rattlesnakes, Sistrurus miliarius, afflicted with an emerging mycosis (ophidiomycosis) across seasons. In all combinations of disease status and season, acute capture stress resulted in a significant glucocorticoid and glycemic response. While disease was not associated with elevated baseline or stress-induced corticosterone (CORT), disease was associated with an increased glucocorticoid stress response (post-stress minus baseline) across seasons. Both baseline and stress-induced glucose were lower in snakes with ophidiomycosis compared to uninfected snakes. The relationship between glucose and pre- and post-stress CORT depended on infection status, and positive correlations were only observed in uninfected snakes. The variables which explained CORT and glucose levels were different. The pattern of CORT was highly seasonal (winter high - summer low) and negatively related to body condition. Glucose, on the other hand, did not vary seasonally or with body condition and was strongly related to sex (male high - female low). Our results highlight the fact that circulating CORT and glucose are sensitive to different intrinsic and extrinsic predictor variables and support the hypothesis that disease alters the acute physiological stress response. Whether the effects of ophidiomycosis on the acute stress response result in sublethal effects on fitness should be investigated in future studies.

Organismal behavior, with its tremendous complexity and diversity, is generated by numerous physiological systems acting in coordination. Understanding how these systems evolve to support differences in behavior within and among species is a longstanding goal in biology that has captured the imagination of researchers who work on a multitude of taxa, including humans. Of particular importance are the physiological determinants of behavioral evolution, which are sometimes overlooked because we lack a robust conceptual framework to study mechanisms underlying adaptation and diversification of behavior. Here, we discuss a framework for such an analysis that applies a "systems view" to our understanding of behavioral control. This approach involves linking separate models that consider behavior and physiology as their own networks into a singular vertically integrated behavioral control system. In doing so, hormones commonly stand out as the links, or edges, among nodes within this system. To ground our discussion, we focus on studies of manakins (Pipridae), a family of Neotropical birds. These species have numerous physiological and endocrine specializations that support their elaborate reproductive displays. As a result, manakins provide a useful example to help imagine and visualize the way systems concepts can inform our appreciation of behavioral evolution. In particular, manakins help clarify how connectedness among physiological systems-which is maintained through endocrine signaling-potentiate and/or constrain the evolution of complex behavior to yield behavioral differences across taxa. Ultimately, we hope this review will continue to stimulate thought, discussion, and the emergence of research focused on integrated phenotypes in behavioral ecology and endocrinology.

When hosts have a long coevolutionary history with their parasites, fitness costs of chronic infection have often been assumed to be negligible. Yet, experimental manipulation of infections sometimes reveals effects of parasites on their hosts, particularly during reproduction. Whether these effects translate into fitness costs remains unclear. Here, we present the results of an experimental study conducted in a free-ranging population of red-winged blackbirds (Agelaius phoeniceus) naturally experiencing a high prevalence of haemosporidian infections, with more than 95% of breeding adults infected with parasites from one or more haemosporidian genus. To assess effects of infection during reproduction, we manipulated adult red-winged blackbird females' parasite burden by administering an anti-haemosporidian medication before onset of egg-laying. Experimental reduction of infection resulted in significant benefits to mothers and their offspring. Medicated females laid heavier clutches, invested more in incubation and provisioning behaviour, and produced more fledglings than control females. Nestlings of medicated females had higher haematocrit, higher blood glucose, and lower reactive oxygen metabolites than nestlings of control females. Overall, our results provide evidence that, even in a species with high prevalence of infection, parasites can lead to decreased maternal investment and offspring quality, substantially reducing fitness.

The neurogenomic mechanisms mediating cooperative behaviors are understudied. We leveraged extensive transcriptomic and behavioral data on a neotropical bird (Pipra filicauda) that perform cooperative courtship displays to better understand the underlying mechanisms. Cooperative display is modulated by testosterone, it promotes cooperation in non-territorial birds, but suppresses cooperation in territory holders. We sought to understand the neurogenomic underpinnings of these three related traits: social status, cooperative behavior, and testosterone phenotype. To do this, we profiled gene expression in 10 brain nuclei spanning the social decision-making network (SDMN), and two key endocrine tissues that regulate social behavior. We associated gene expression with each bird's behavioral and endocrine profile derived from 3 years of repeated measures taken from free-living birds in the Ecuadorian Amazon. We found distinct landscapes of constitutive gene expression were associated with social status, testosterone phenotype, and cooperation, reflecting the modular organization and engagement of neuroendocrine tissues. Sex-steroid and neuropeptide signaling appeared to be important in mediating status-specific relationships between testosterone and cooperation, suggesting shared regulatory mechanisms with male aggressive and sexual behaviors. We also identified differentially regulated genes involved in cellular activity and synaptic potentiation, suggesting multiple mechanisms underpin these genomic states. Finally, we identified SDMN-wide gene expression differences between territorial and floater males that could form the basis of status-specific neurophysiological phenotypes, potentially mediated by testosterone and growth hormone. Overall, our findings provide new, systems-level insights into the mechanisms of cooperative behavior, and suggest that differences in neurogenomic state are the basis for individual differences in social behavior.

Background Wildlife conservation often focuses on establishing protected areas. However, these conservation zones are frequently established without adequate knowledge of the movement patterns of the species they are designed to protect. Understanding movement and foraging patterns of species in dynamic and diverse habitats can allow managers to develop more effective conservation plans. Threatened lemurs in Madagascar are an example where management plans and protected areas are typically created to encompass large, extant forests rather than consider the overall resource needs of the target species. Methods To gain an understanding of golden-crowned sifaka ( Propithecus tattersalli ) movement patterns, including space use and habitat selection across their range of inhabited forest types, we combined behavior data with Dynamic Brownian Bridge Movement Models and Resource Selection Functions. We also examined the influence of abiotic, biotic, and anthropogenic factors on home range size, movement rates, and foraging patterns. Results We found that home range size and movement rates differed between seasons, with increased core area size and movement in the rainy season. Forest type also played a role in foraging behavior with sifaka groups in the humid forest avoiding roads in both seasons, groups in the dry deciduous forest avoiding road networks in the rainy season, and groups in the moderate evergreen forest displaying no selection or avoidance of road networks while foraging. Conclusion Our study illustrates the importance of studying primate groups across seasons and forest types, as developing conservation plans from a single snapshot can give an inaccurate assessment of their natural behavior and resources needs of the species. More specifically, by understanding how forest type influences golden-crowned sifaka movement and foraging behavior, conservation management plans can be made to the individual forest types inhabited (dry deciduous, moderate evergreen, humid, littoral, etc.), rather than the region as a whole.

Background Wildlife conservation often focuses on establishing protected areas, however, these conservation zones are frequently developed without adequate knowledge of the movement patterns of the species they are designed to protect. Understanding movement and foraging patterns of species in dynamic and diverse habitats can allow managers to develop more effective conservation plans. Threatened lemurs in Madagascar are an example where management plans and protected areas are typically created to encompass large, remaining forests rather than the resource needs of the target species. Methods To gain an understanding of golden-crowned sifaka ( Propithecus tattersalli ) movement patterns, including space use and habitat selection, across their range of inhabited forest types, we combined behavior data with Dynamic Brownian Bridge Movement Models and Resource Selection Functions. We also examined the influence of abiotic, biotic, and anthropogenic factors on home range size, movement rates, and foraging patterns. ResultsWe found that home range size and movement rates differed between seasons, with increased core area size and movement in the rainy season. Forest type also played a role in foraging behavior with lemur groups in humid forest avoiding roads in both seasons, groups in the dry deciduous forest avoiding road networks in the rainy season, and groups in the moderate evergreen forest displaying no selection or avoidance of road networks while foraging. Conclusion Our study illustrates the importance of studying primate groups across seasons as well as across forest types, as developing conservation plans as a single snapshot can give an inaccurate assessment of their natural behavior and resources needs. More specifically, by understanding how forest type influences golden-crowned sifaka movement and foraging behavior, we can make conservation management plans specific to the individual forest types they inhabit (humid, moderate evergreen, dry deciduous, littoral, etc.), rather than the region as a whole.

Sexually transmitted microbes are hypothesized to influence the evolution of reproductive strategies. Though frequently discussed in this context, our understanding of the reproductive microbiome is quite nascent. Indeed, testing this hypothesis first requires establishing a baseline understanding of the temporal dynamics of the reproductive microbiome and of how individual variation in reproductive behavior and age influence the assembly and maintenance of the reproductive microbiome as a whole. Here, we ask how mating activity, breeding stage, and age influence the reproductive microbiome. We use observational and experimental approaches to explain variation in the cloacal microbiome of free‐living, female tree swallows (Tachycineta bicolor). Using microsatellite‐based parentage analyses, we determined the number of sires per brood (a proxy for female mating activity). We experimentally increased female sexual activity by administering exogenous 17ß‐estradiol. Lastly, we used bacterial 16S rRNA amplicon sequencing to characterize the cloacal microbiome. Neither the number of sires per brood nor the increased sexual activity of females significantly influenced female cloacal microbiome richness or community structure. Female age, however, was positively correlated with cloacal microbiome richness and influenced overall community structure. A hypothesis to explain these patterns is that the effect of sexual activity and the number of mates on variation in the cloacal microbiome manifests over an individual's lifetime. Additionally, we found that cloacal microbiome alpha diversity (Shannon Index, Faith's phylogenetic distance) decreased and community structure shifted between breeding stages. This is one of few studies to document within‐individual changes and age‐related differences in the cloacal microbiome across successive breeding stages. More broadly, our results contribute to our understanding of the role that host life history and behavior play in shaping the cloacal microbiomes of wild birds. In this paper, we ask the question: how do mating activity, breeding stage, and age influence female reproductive microbiomes? We address this question using observational and experimental approaches to explain both between‐ and within‐individual variation in the cloacal microbiome of free‐living, female birds that exhibit differences in extra‐pair paternity rates. We found that female age and breeding stage, but not number of mates or experimentally elevated sexual activity (via 17ß‐estradiol implants), significantly influenced cloacal microbiome alpha diversity and explained variation in bacterial community structure.

The neotropical manakins (family Pipridae) provide a great opportunity for integrative studies of sexual selection as nearly all of the 51 species are lek-breeding, an extreme form of polygyny, and highly sexually dimorphic both in appearance and behavior. Male courtship displays are often elaborate and include auditory cues, both vocal and mechanical, as well as visual elements. In addition, the displays are often extremely rapid, highly acrobatic, and, in some species, multiple males perform coordinated displays that form the basis of long-term coalitions. Male manakins also exhibit unique neuroendocrine, physiological, and anatomical adaptations to support the performance of these complex displays and the maintenance of their intricate social systems. The Manakin Genomics Research Coordination Network (Manakin RCN, https://www.manakinsrcn.org) has brought together researchers (many in this symposium and this issue) from across disciplines to address the implications of sexual selection on evolution, ecology, behavior, and physiology in manakins. The objective of this paper is to present some of the most pertinent and integrative manakin research as well as introducing the papers presented in this issue. The results discussed at the manakin symposium, part of the 2021 Society for Integrative and Comparative Biology Conference, highlight the remarkable genomic, behavioral, and physiological adaptations as well as the evolutionary causes and consequences of strong sexual selection pressures that are evident in manakins.