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Creators/Authors contains: "Rubenstein, Dustin R."

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  1. Free, publicly-accessible full text available September 1, 2024
  2. Abstract

    The hypothalamic–pituitary–adrenal (HPA) axis coordinates an organism's response to environmental stress. The responsiveness and sensitivity of an offspring's stress response may be shaped not only by stressors encountered in their early post‐natal environment but also by stressors in their parent's environment. Yet, few studies have considered how stressors encountered in both of these early life environments may function together to impact the developing HPA axis. Here, we manipulated stressors in the parental and post‐natal environments in a population of house sparrows (Passer domesticus) to assess their impact on changes in DNA methylation (and corresponding gene expression) in a suite of genes within the HPA axis. We found that nestlings that experienced early life stress across both life‐history periods had higher DNA methylation in a critical HPA axis gene, the glucocorticoid receptor (NR3C1). In addition, we found that the life‐history stage when stress was encountered impacted some genes (HSD11B1, NR3C1andNR3C2) differently. We also found evidence for the mitigation of parental stress by post‐natal stress (inHSD11B1andNR3C2). Finally, by assessing DNA methylation in both the brain and blood, we were able to evaluate cross‐tissue patterns. While some differentially methylated regions were tissue‐specific, we found cross‐tissue changes inNR3C2andNR3C1, suggesting that blood is a suitable tissue for assessing DNA methylation as a biomarker of early life stress. Our results provide a crucial first step in understanding the mechanisms by which early life stress in different life‐history periods contributes to changes in the epigenome of the HPA axis.

     
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  3. Cooperatively breeding vertebrates are common in unpredictable environments where the costs and benefits of providing offspring care fluctuate temporally. To balance these fitness outcomes, individuals of cooperatively breeding species often exhibit behavioural plasticity according to environmental conditions. Although individual variation in cooperative behaviours is well-studied, less is known about variation in plasticity of social behaviour. Here, we examine the fitness benefits, plasticity and repeatability of nest guarding behaviour in cooperatively breeding superb starlings ( Lamprotornis superbus ). After demonstrating that the cumulative nest guarding performed at a nest by all breeders and helpers combined is a significant predictor of reproductive success, we model breeder and helper behavioural reaction norms to test the hypothesis that individuals invest more in guarding in favourable seasons with high rainfall. Variation in nest guarding behaviour across seasons differed for individuals of different reproductive status: breeders showed plastic nest guarding behaviour in response to rainfall, whereas helpers did not. Similarly, we found that individual breeders show repeatability and consistency in their nest guarding behaviour while individual helpers did not. Thus, individuals with the potential to gain direct fitness benefits exhibit greater plasticity and individual-level repeatability in cooperative behaviour. 
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  4. Climate-driven oscillating selection maintains a dispersal polyphenism, driving the formation of an avian mixed-kin society. 
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  5. Abstract

    Although eusocial animals often achieve ecological dominance in the ecosystems where they occur, many populations are unstable, resulting in local extinction. Both patterns may be linked to the characteristic demography of eusocial species—high reproductive skew and reproductive division of labor support stable effective population sizes that make eusocial groups more competitive in some species, but also lower effective population sizes that increase susceptibility to population collapse in others. Here, we examine the relationship between demography and social organization in Synalpheus snapping shrimps, a group in which eusociality has evolved recently and repeatedly. We show using coalescent demographic modeling that eusocial species have had lower but more stable effective population sizes across 100,000 generations. Our results are consistent with the idea that stable population sizes may enable competitive dominance in eusocial shrimps, but they also suggest that recent population declines are likely caused by eusocial shrimps’ heightened sensitivity to environmental changes, perhaps as a result of their low effective population sizes and localized dispersal. Thus, although the unique life histories and demography of eusocial shrimps have likely contributed to their persistence and ecological dominance over evolutionary time scales, these social traits may also make them vulnerable to contemporary environmental change.

     
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  6. Abstract

    Although social species as diverse as humans and ants are among the most abundant organisms on Earth, animals cooperate and form groups for many reasons. How these different reasons for grouping affect a species' ecological dominance remains unknown. Here we use a theoretical model to demonstrate that the different fitness benefits that animals receive by forming groups depend on the quality of their environment, which in turn impacts their ecological dominance and resilience to global change. We then test the model's key predictions using phylogenetic comparative analysis of >6500 bird species. As predicted, we find that cooperative breeders occurring in harsh and fluctuating environments have larger ranges and greater abundances than non‐cooperative breeders, but cooperative breeders occurring in benign and stable environments do not. Using our model, we further show that social species living in harsh and fluctuating environments will be less vulnerable to climate change than non‐social species.

     
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  7. vonHoldt, Bridgett (Ed.)
    Abstract Iridescence is widespread in the living world, occurring in organisms as diverse as bacteria, plants, and animals. Yet, compared to pigment-based forms of coloration, we know surprisingly little about the developmental and molecular bases of the structural colors that give rise to iridescence. Birds display a rich diversity of iridescent structural colors that are produced in feathers by the arrangement of melanin-containing organelles called melanosomes into nanoscale configurations, but how these often unusually shaped melanosomes form, or how they are arranged into highly organized nanostructures, remains largely unknown. Here, we use functional genomics to explore the developmental basis of iridescent plumage using superb starlings (Lamprotornis superbus), which produce both iridescent blue and non-iridescent red feathers. Through morphological and chemical analyses, we confirm that hollow, flattened melanosomes in iridescent feathers are eumelanin-based, whereas melanosomes in non-iridescent feathers are solid and amorphous, suggesting that high pheomelanin content underlies red coloration. Intriguingly, the nanoscale arrangement of melanosomes within the barbules was surprisingly similar between feather types. After creating a new genome assembly, we use transcriptomics to show that non-iridescent feather development is associated with genes related to pigmentation, metabolism, and mitochondrial function, suggesting non-iridescent feathers are more energetically expensive to produce than iridescent feathers. However, iridescent feather development is associated with genes related to structural and cellular organization, suggesting that, while nanostructures themselves may passively assemble, barbules and melanosomes may require active organization to give them their shape. Together, our analyses suggest that iridescent feathers form through a combination of passive self-assembly and active processes. 
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  8. Abstract

    Adaptive responses to ecological uncertainty may affect the dynamics of interspecific interactions and shape the course of evolution within symbioses. Obligate avian brood parasites provide a particularly tractable system for understanding how uncertainty, driven by environmental variability and symbiont phenology, influences the evolution of species interactions. Here, we use phylogenetically-informed analyses and a comprehensive dataset on the behaviour and geographic distribution of obligate avian brood parasites and their hosts to demonstrate that increasing uncertainty in thermoregulation and parental investment of parasitic young are positively associated with host richness and diversity. Our findings are consistent with the theoretical expectation that ecological risks and environmental unpredictability should favour the evolution of bet-hedging. Additionally, these highly consistent patterns highlight the important role that ecological uncertainty is likely to play in shaping the evolution of specialisation and generalism in complex interspecific relationships.

     
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  9. Abstract Negative feedback of the vertebrate stress response via the hypothalamic–pituitary–adrenal (HPA) axis is regulated by glucocorticoid receptors in the brain. Epigenetic modification of the glucocorticoid receptor gene (Nr3c1), including DNA methylation of the promoter region, can influence expression of these receptors, impacting behavior, physiology, and fitness. However, we still know little about the long-term effects of these modifications on fitness. To better understand these fitness effects, we must first develop a non-lethal method to assess DNA methylation in the brain that allows for multiple measurements throughout an organism’s lifetime. In this study, we aimed to determine if blood is a viable biomarker for Nr3c1 DNA methylation in two brain regions (hippocampus and hypothalamus) in adult European starlings (Sturnus vulgaris). We found that DNA methylation of CpG sites in the complete Nr3c1 putative promoter varied among tissue types and was lowest in blood. Although we identified a similar cluster of correlated Nr3c1 putative promoter CpG sites within each tissue, this cluster did not show any correlation in DNA methylation among tissues. Additional studies should consider the role of the developmental environment in producing epigenetic modifications in different tissues. 
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  10. null (Ed.)