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Regurgitated food sharing in vampire bats is a cooperative behavior that has garnered scientific interest as an example of reciprocal helping among kin and non-kin. The amount of food given is estimated via the duration of mouth-licking. However, a growing body of evidence across other animal taxa, especially social insects, shows that mouth-to-mouth material transfer can serve many functions besides food sharing. In this review, we asked whether and to what extent mouth-licking in the common vampire bat (Desmodus rotundus) could be explained by functions other than regurgitated food sharing. We first review the evidence, including new analyses of published data, that food sharing occurs during mouth-licking bouts in vampire bats. We then review interpretations of mouth-licking in other mammal species and assess the likelihood that various hypothetical functions suggested in other species could occur in vampire bats. We conclude that the primary function of prolonged bouts of mouth-licking in vampire bats is sharing of ingested blood, but that microbial sharing is another likely benefit, and that short bouts of mouth-licking also function as social signals of begging or offering of food. Future work on this behavior should keep alternative explanations in mind when interpreting observations. 

Abstract In seasonally breeding animals, the costs and benefits of territorial aggression should vary over time; however, little work thus far has directly examined the scope and adaptive value of individual-level plasticity in aggression across breeding stages. We explore these issues using the tree swallow (Tachycineta bicolor), a single-brooded bird species in which females compete for limited nesting sites. We measured aggressiveness in nearly 100 females within 3 different stages: (1) shortly after territory-establishment, (2) during incubation, and (3) while caring for young chicks. Based on the timing, direction, and magnitude of behavioral changes between stages, we used k-means clustering to categorize each female’s behavior into a “plasticity type.” We then tested whether plasticity type and stage-specific aggression varied with key performance metrics. About 40% of females decreased aggressiveness across consecutive breeding stages to some degree, consistent with population-level patterns. 33% of females exhibited comparatively little plasticity, with moderate to low levels of aggression in all stages. Finally, 27% of females displayed steep decreases and then increases in aggression between stages; females exhibiting this pattern had significantly lower body mass while parenting, they tended to hatch fewer eggs, and they had the lowest observed overwinter survival rates. Other patterns of among-stage changes in aggressiveness were not associated with performance. These results reveal substantial among-individual variation in behavioral plasticity, which may reflect diverse solutions to trade-offs between current reproduction and future survival. 

Uncovering the genomic bases of phenotypic adaptation is a major goal in biology, but this has been hard to achieve for complex behavioral traits. Here, we leverage the repeated, independent evolution of obligate cavity-nesting in birds to test the hypothesis that pressure to compete for a limited breeding resource has facilitated convergent evolution in behavior, hormones, and gene expression. We used an integrative approach, combining aggression assays in the field, testosterone measures, and transcriptome-wide analyses of the brain in wild-captured females and males. Our experimental design compared species pairs across five avian families, each including one obligate cavity-nesting species and a related species with a more flexible nest strategy. We find behavioral convergence, with higher levels of territorial aggression in obligate cavity-nesters, particularly among females. Across species, levels of testosterone in circulation were not associated with nest strategy, nor aggression. Phylogenetic analyses of individual genes and co-regulated gene networks revealed more shared patterns of brain gene expression than expected by drift, but the scope of convergent gene expression evolution was limited to a small percent of the genome. When comparing our results to other studies that did not use phylogenetic methods, we suggest that accounting for shared evolutionary history may reduce the number of genes inferred as convergently evolving. Altogether, we find that behavioral convergence in response to shared ecological pressures is associated with largely independent gene expression evolution across different avian families, punctuated by a narrow set of convergently evolving genes. 

Abstract Experimentally elevated testosterone (T) often leads to enhanced aggression, with examples across many different species, including both males and females. Indeed, the relationship between T and aggression is among the most well-studied and fruitful areas of research at the intersection of behavioral ecology and endocrinology. This relationship is also hypothesized to be bidirectional (i.e., T influences aggression, and aggression influences T), leading to four key predictions: (1) Individuals with higher T levels are more aggressive than individuals with lower T. (2) Seasonal changes in aggression mirror seasonal changes in T secretion. (3) Aggressive territorial interactions stimulate increased T secretion. (4) Temporary elevations in T temporarily increase aggressiveness. These predictions cover a range of timescales, from a single snapshot in time, to rapid fluctuations, and to changes over seasonal timescales. Adding further complexity, most predictions can also be addressed by comparing among individuals or with repeated sampling within individuals. In our review, we explore how the spectrum of results across predictions shapes our understanding of the relationship between T and aggression. In all cases, we can find examples of results that do not support the initial predictions. In particular, we find that Predictions 1–3 have been tested frequently, especially using an among-individual approach. We find qualitative support for all three predictions, though there are also many studies that do not support Predictions 1 and 3 in particular. Prediction 4, on the other hand, is something that we identify as a core underlying assumption of past work on the topic, but one that has rarely been directly tested. We propose that when relationships between T and aggression are individual-specific or condition-dependent, then positive correlations between the two variables may be obscured or reversed. In essence, even though T can influence aggression, many assumed or predicted relationships between the two variables may not manifest. Moving forward, we urge greater attention to understanding how and why it is that these bidirectional relationships between T and aggression may vary among timescales and among individuals. In doing so, we will move toward a deeper understanding on the role of hormones in behavioral adaptation. 

Abstract Competitive interactions often occur in series; therefore animals may respond to social challenges in ways that prepare them for success in future conflict. Changes in the production of the steroid hormone testosterone (T) are thought to mediate phenotypic responses to competition, but research over the past few decades has yielded mixed results, leading to several potential explanations as to why T does not always elevate following a social challenge. Here, we measured T levels in tree swallows (Tachycineta bicolor), a system in which females compete for limited nesting cavities and female aggression is at least partially mediated by T. We experimentally induced social challenges in two ways: (1) using decoys to simulate territorial intrusions and (2) removing subsets of nesting cavities to increase competition among displaced and territory-holding females. Critically, these experiments occurred pre-laying, when females are physiologically capable of rapidly increasing circulating T levels. However, despite marked aggression in both experiments, T did not elevate following real or simulated social challenges, and in some cases, socially challenged females had lower T levels than controls. Likewise, the degree of aggression was negatively correlated with T levels following a simulated territorial intrusion. Though not in line with the idea that social challenges prompt T elevation in preparation for future challenges, these patterns nevertheless connect T to territorial aggression in females. Coupled with past work showing that T promotes aggression, these results suggest that T may act rapidly to allow animals to adaptively respond to the urgent demands of a competitive event. 

Periods of social instability can elicit adaptive phenotypic plasticity to promote success in future competition. However, the underlying molecular mechanisms have primarily been studied in captive and laboratory-reared animals, leaving uncertainty as to how natural competition among free-living animals affects gene activity. Here, we experimentally generated social competition among wild, cavity-nesting female birds (tree swallows,Tachycineta bicolor). After territorial settlement, we reduced the availability of key breeding resources (i.e., nest boxes), generating heightened competition; within 24 h we reversed the manipulation, causing aggressive interactions to subside. We sampled females during the peak of competition and 48 h after it ended, along with date-matched controls. We measured transcriptomic and epigenomic responses to competition in two socially relevant brain regions (hypothalamus and ventromedial telencephalon). Gene network analyses suggest that processes related to energy mobilization and aggression (e.g., dopamine synthesis) were up-regulated during competition, the latter of which persisted 2 d after competition had ended. Cellular maintenance processes were also down-regulated after competition. Competition additionally altered methylation patterns, particularly in pathways related to hormonal signaling, suggesting those genes were transcriptionally poised to respond to future competition. Thus, experimental competition among free-living animals shifts gene expression in ways that may facilitate the demands of competition at the expense of self-maintenance. Further, some of these effects persisted after competition ended, demonstrating the potential for epigenetic biological embedding of the social environment in ways that may prime individuals for success in future social instability.