Animals must adjust dynamically their behavior and other traits to a social environment that is constantly changing. For example, the strategies and the signals that individuals use to attract mates and breed often depend on social status relative to others in the population, and that status can fluctuate as group composition changes and/or other individuals change in rank. Accordingly, the hormonal and genetic mechanisms that underlie such behaviors and signals are likely to be sensitive to social conditions, allowing individuals to adjust accordingly. Yet, we know relatively little about these mechanisms, particularly in wild populations living under natural conditions. 

Our National Science Foundation project, “Social Environment Effects on Hormones and the Integrated Behavioral Phenotype,” examined the mechanisms that allow for behavioral flexibility, and the ways that those mechanisms evolve, using Austral-Asian fairywrens (genus Malurus) as a model system. These bird species are uniquely suited to such a study because they show pronounced variation, across both individuals and populations, in the visual signals that individuals use to attract mates, and a great deal is known about the effects of hormones (particularly androgens like testosterone) on the expression of these signals. 

On facet of our research focused on the Red-backed Fairywren, where males can breed in either ornamented red/black or female-like brown plumage coloration, with pronounced behavioral differences between the plumage types. Results from our research on this species clearly show that fluctuating androgen levels allow young males to adjust their behavioral and signaling phenotype to match their own social environment. In particular, social interactions during the non-breeding season, such as attention from females, cause male androgen levels to increase, which in turn affect the plumage type and associated behaviors that males exhibit during the subsequent breeding season. Our genomic analyses went on to reveal a number of genes that likely affect the acquisition of colorful carotenoid plumage coloration, and that are differentially expressed by red/black versus brown males and also by young males implanted with androgens versus controls lacking androgen implants. We also obtained results on differences in gene expression in behavior-relevant brain areas between males and females, male phenotypes, and testosterone-treated males. Finally, we obtained results showing that the breeding phenotype of older males, who are more established in their social rank, are much less dependent on androgens compared to the breeding phenotype of younger males. Taken together, these results reveal some of the mechanisms by which young males are able to adjust their phenotype to match a variable and unpredictable social environment. They also help to understand if and how the hormone testosterone acts as a mechanism of integration of plumage and behavior components of phenotype. 

The other facet of our project focuses on the White-shouldered Fairywren, where females can be either brown or male-like (black/white) in coloration. Here, our research focused on the fact that while it is common for males and females of the same species to look and behave differently, the mechanism(s) that integrate appearance and behavior to be male-like versus female-like are unclear. We found that androgens are linked to aggression in female white-shouldered wrens, but only partially turn on the non-melanic components of male-like plumage in experimentally implanted females. A small suite of genes that are differentially expressed in the growing feathers of male-like females are also differentially expressed in the growing feathers of cryptic females that have been administered testosterone. Intriguingly, we also found that androgens lead to the expression of male-like red (carotenoid-based) plumage in female red-backed fairywrens, but not to expression of male-like black (melanic) plumage, as we saw in white-shouldered fairywrens. Together, these results indicate that testosterone and other hormones affect directly the expression of genes underlying sexual dimorphism seen in some plumage traits, but not others.

Overall, this research has contributed to a better understanding of the hormonal and genetic mechanisms that allow animals to adjust to a constantly changing social environment. It has led to the publication of over 25 papers in professional journals and numerous presentations at national and international professional meetings. It facilitated collaboration across three laboratories in the US and internationally with a Max-Planck-Institute in Germany. It also facilitated training and interaction of graduate students in the collaborating research teams, and offered unique opportunities for numerous undergraduate students to train in techniques and principles of field biology, ecology, and physiology. This collaborative project helped integrate and bridge disconnected fields across the biological sciences, and informed the science community as well as the public about the roles of ecological factors, physiological mechanisms, and genes in generating phenotypic variation and biological diversity. 

Last Modified: 02/08/2020
Modified by: Jordan Karubian