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Offspring from females breeding in competitive social environments are often exposed to more testosterone (T) during embryonic development, which can affect traits from growth to behavior in potentially adaptive ways. Despite the important role of maternally derived steroids in shaping offspring development, the molecular mechanisms driving these processes are currently unclear. Here, we use tree swallows (Tachycineta bicolor) to explore the effects of the maternal social environment on yolk T concentrations and genome-wide patterns of neural gene expression in embryos. We measured aggressive interactions among females breeding at variable densities and collected their eggs at two timepoints, including the day laid to measure yolk T concentrations and on embryonic day 11 to measure gene expression in whole brain samples. We found that females breeding in high-density sites experienced elevated rates of physical aggression and their eggs had higher yolk T concentrations. A differential gene expression and weighted gene co-expression network analysis indicated that embryos from high-density sites experienced an upregulation of genes involved in hormone, circulatory, and immune processes, and these gene expression patterns were correlated with yolk T levels and aggression. Genes implicated in neural development were additionally downregulated in embryos from high-density sites. These data highlight how early neurogenomic processes may be affected by the maternal social environment, giving rise to phenotypic plasticity in offspring., Competing Interests: Declaration of competing interest All authors declare that they have no competing interests., (Copyright © 2024 Elsevier Inc. All rights reserved.)

Studies of the evolutionary causes and consequences of variation in circulating glucocorticoids (GCs) have begun to reveal how they are shaped by selection. Yet the extent to which variation in circulating hormones reflects variation in other important regulators of the hypothalamic-pituitary-adrenal (HPA) axis, and whether these relationships vary among populations inhabiting different environments, remain poorly studied. Here, we compare gene expression in the brain of female tree swallows (Tachycineta bicolor) from populations that breed in environments that differ in their unpredictability. We find evidence of inter-population variation in the expression of glucocorticoid and mineralocorticoid receptors in the hypothalamus, with the highest gene expression in a population from an extreme environment, and lower expression in a population from a more consistent environment as well as in birds breeding at an environmentally variable high-altitude site that are part of a population that inhabits a mixture of high and low altitude habitats. Within some populations, variation in circulating GCs predicted differences in gene expression, particularly in the hypothalamus. However, some patterns were present in all populations, whereas others were not. These results are consistent with the idea that some combination of local adaptation and phenotypic plasticity may modify components of the HPA axis affecting stress resilience. Our results also underscore that a comprehensive understanding of the function and evolution of the stress response cannot be gained from measuring circulating hormones alone, and that future studies that apply a more explicitly evolutionary approach to important regulatory traits are likely to provide significant insights., (Copyright © 2022 Elsevier Inc. All rights reserved.)

The ovary plays an important role in mediating both a female's response to her social environment and communicating it to her developing offspring via maternal effects. Past work has focused on how ovarian hormones respond to competition, but we know little about how the broader ovarian transcriptomic landscape changes, either during or after competition, giving us a narrow perspective on how socially induced phenotypes arise. Here, we experimentally generated social competition among wild, cavity-nesting female birds (tree swallows, Tachycineta bicolor), a species in which females lack a socially induced rise in circulating testosterone but they nevertheless increase allocation to eggs. After territory settlement, we reduced availability of nesting cavities, generating heightened competition; within 24 h we reversed the manipulation, causing aggressive interactions to subside. We measured ovarian transcriptomic responses at the peak of competition and 48 h later, along with date-matched controls. Network analyses indicated that competing females experienced an immediate and temporary decrease in the expression of genes involved in the early stages of steroidogenesis, and this was moderately correlated with plasma testosterone; however, two days after competition had ended, there was a marked increase in the expression of genes involved in the final stages of steroidogenesis, including HSD17B1. Gene networks related to the cell cycle, muscle performance, and extracellular matrix organization also displayed altered activity. Although the functional consequences of these findings are unclear, they shed light on socially responsive ovarian genomic mechanisms that could potentially exert lasting effects on behavior, reproduction, and maternal effects., (Copyright © 2022 Elsevier Inc. All rights reserved.)

The bi-directional links between hormones and behavior have been a rich area of research for decades. Theory on the evolution of testosterone (T) was greatly advanced by the challenge hypothesis, which presented a framework for understanding interspecific, seasonal, and social variation in T levels in males, and how they are shaped by the competing demands of parental care and male-male competition. Female competition is also widespread in nature, although it is less clear whether or how the challenge hypothesis applies to females. Here, we evaluate this issue in four parts: (1) We summarize and update prior analyses of seasonal plasticity and interspecific variation in T in females. (2) We evaluate experimental links between T and female aggression on shorter timescales, asking how T manipulations affect aggression and conversely, how social manipulations affect T levels in female mammals, birds, lizards, and fishes. (3) We examine alternative mechanisms that may link aggression to the social environment independently of T levels in circulation. (4) We present a case study, including new data analyses, in an aggressive female bird (the tree swallow, Tachycineta bicolor) to explore how variation in tissue-level processing of T may bridge the gap between circulating T and variation in behavior that is visible to natural selection. We close by connecting these multivariate levels of sex steroid signaling systems alongside different temporal scales (social, seasonal, and evolutionary) to generate broadly applicable insights into how animals respond to their social environment, regardless of whether they are male or female., (Copyright © 2019 Elsevier Inc. All rights reserved.)

Testosterone (T) is a sex steroid hormone that often varies seasonally and mediates trade-offs between territorial aggression and parental care. Prior work has provided key insights into the 'top-down' hypothalamic control of this seasonal plasticity in T, yet mechanisms acting outside of the brain may also influence circulating T levels. We hypothesized that peripheral mechanisms may be especially critical for females, because peripheral regulation may mitigate the costs of systemically elevated T. Here, we begin to test this hypothesis using a seasonal comparative approach, measuring gene expression in peripheral tissues in tree swallows (Tachycineta bicolor), a songbird with intense female-female competition and T-mediated aggression. We focused on the gonad and liver for their role in T production and metabolism, respectively, and we contrasted females captured during territory establishment versus incubation. During territory establishment, when T levels are highest, we found elevated gene expression of the hepatic steroid metabolizing enzyme CYP2C19 along with several ovarian steroidogenic enzymes, including the androgenic 5α-reductase. Despite these seasonal changes in gene expression along the steroidogenic pathway, we did not observe seasonal changes in sensitivity to upstream signals, measured as ovarian mRNA abundance of luteinizing hormone receptor. Together, these data suggest that differential regulation of steroidogenic gene expression in the ovary is a potentially major contributor to seasonal changes in T levels in females. Furthermore, these data provide a unique and organismal glimpse into tissue-specific gene regulation and its potential role in hormonal plasticity in females., (Copyright © 2018 Elsevier Inc. All rights reserved.)

Animal species display significant variation in personality traits among individuals, and two main coping styles have been identified and termed "proactive" and "reactive". Further, these coping styles appear to correlate directly with the strength of the physiological stress response exhibited by those individuals. In our study system, white laying hens are reactive, flighty, and exhibit large hormonal and behavioral responses to acute stress, while brown laying hens are proactive, exploratory, and exhibit low hormonal and behavioral responses to acute stress. The objective of the current study was to determine if personality type also corresponds to differences in multiple measures of stress when birds are subjected to a chronic stressor. We tested the responses of hens to chronic stress applied by providing feed according to an unpredictable schedule for 14 days, and measured corticosterone concentrations in circulation, expression of heat shock proteins (HSPs), molecules known to protect cells in response to stress, and the ratios of heterophils:lymphocytes in blood, two immune cells known to change in quantity in circulation during chronic stress. We predicted that white hens would show greater physiological responses to the chronic stress treatment. Plasma corticosterone levels significantly increased after 7 days of treatment and returned to baseline levels on day 14, but did not differ significantly between strains. H:L ratios, on the other hand, were significantly elevated by day 7 of treatment, and increased significantly more in brown hens than white. HSP70 and HSP90 expression levels were significantly higher after stress began in white hens than brown. Our results showed that brown hens were more reactive in one response (H:L ratios) while white hens were more reactive in another (HSP expression). These different reactions to the same stressor may represent different strategies for dealing with the same stressor., (Copyright © 2017. Published by Elsevier Inc.)

Territorial animals breeding in high-density environments are more likely to engage in aggressive competition with conspecifics for resources necessary for reproduction. In many avian species, increased competition among breeding females results in increased testosterone concentrations in egg yolks. Generally, elevated yolk testosterone increases nestling growth, competitive behaviors, and bold behavioral traits. However, few studies provide an environmental context with which to examine the potential adaptive benefits of these phenotypic changes. In this study, tree swallow (Tachycineta bicolor) breeding density was altered to modify levels of social competition and yolk testosterone. We measured nestling growth, competitive ability, and breathing rate in response to a stressor using a partial cross-foster design. Females breeding at high-density experienced more aggressive, competitive interactions and their eggs had higher testosterone concentrations. Nestlings that hatched in high-density environments grew faster and displayed more competitive behaviors and a higher breathing rate response to a stressor regardless of post-hatching density. Our study demonstrates that phenotypic plasticity occurs in response to yolk testosterone variation resulting from different breeding densities. These findings suggest that naturally-induced maternal effects prepare offspring for competitive environments, supporting the idea that maternal effects are adaptive., (© 2013.)