The fourth in the behind-the-scenes series for the Journal of Animal Ecology’s Animal Social Network Special Issue, this blog post is provided by Ben Vernasco and Roslyn Dakin and tells the #StoryBehindThePaper for the article “Testosterone‐mediated behaviour shapes the emergent properties of social networks“, which was recently published in the Journal of Animal Ecology Animal Social Networks Special Issue.

Hiking through dense Amazonian rainforest, you are likely to find yourself in an area where you can hear multiple high-pitched whistles coming from different directions. If you are in the terra firme or várzea forests of the Northwestern Amazon Basin, you may be hearing the sound of male wire-tailed manakins advertising that they are ready. Ready to dance!

The Neotropical manakins (family Pipridae) are a fascinating group of birds in which males exhibit lek-breeding behaviors, colorful plumages, and complex, acrobatic courtship displays. Over the course of their long lifespan (10-15 years or more, depending on the species), males of these tiny, jewel-like birds must compete to acquire one of the few territories potentially available at a given lek. New territories are rarely formed, and opportunities for a male to rise in social rank are only available when a territory-holding male dies. Despite the intense male-male competition and high reproductive skew, males of some species interact in ways that more closely resemble a dance rather than a fight.

Among wire-tailed manakins, for example, males will solicit other males to join them in performing a metabolically-demanding display that includes elements so rapid that they are impossible to follow with the naked eye. These interactions are not just eye-catching, they are also essential. In this species, a male’s sociality is closely related to his ability to secure a territory and reproduce. Many of these male-male social partnerships will last for years, while others dissolve with time. The result is a complex system where each lek represents a dynamic social network. But what drives variation in social structure from one lek to another, and through time? Why are some social networks more stable than others?

To understand the causes and consequences of manakin social dynamics, Brandt Ryder began studying the wire-tailed manakin population at the Tiputini Biodiversity Station in Ecuador in 2002. His research showed that male wire-tailed manakins maintain long-term partnerships and that these partnerships do not depend upon patterns of genetic relatedness¹. Brandt and his coauthors found that a young male’s social behavior predicts his probability of becoming a territory-holder² and, among territory-holders, more social males sire more offspring³. Brandt’s initial work identified the adaptive significance of male wire-tailed manakin social behavior and paved the way for future studies describing the proximate mechanisms mediating individual variation.

The neuroendocrine system is a prominent mediator of variation in social behaviors. In the case of breeding behaviors like those of male wire-tailed manakins, the hormone testosterone and its associated endocrine signaling components are thought to be sources of individual differences. Indeed, observational and experimental studies support the idea that, in wire-tailed manakins, more social territory-holding males exhibit lower testosterone^4,5. The results showing testosterone mediates individual differences in social behavior led our research team to ask if patterns of circulating testosterone can also explain the social network dynamics of male wire-tailed manakins. Measuring the social dynamics of wire-tailed manakins at such a fine scale, however, required the development of a tracking technology that is lightweight enough to use on these tiny birds and also robust enough to survive the challenging conditions of the Amazon Rainforest⁶.

In a recent study published in JAE, our research team made use of this novel tracking system to test the molecular causes of social network dynamics in free-living animals⁷. Our study describes remarkably fine-scale patterns of male-male social interactions in the wire-tailed manakin, and shows that the temporal patterns of the male manakin groups depend on the endocrine phenotypes of the interacting males. Social networks composed of males with above-average testosterone had more diffuse interaction patterns, more temporal variability, and less behavioral similarity among social partners. These three properties of high-testosterone social networks are also expected to reduce the benefits of cooperation, based on evolutionary theory. Hence, our findings support the hypothesis that reduced sociality may be a cost of maintaining high testosterone⁸.

Our work represents one of few studies to connect a molecular trait with the group-level social dynamics of animals in the wild. Social networks can have dramatic effects on numerous biological processes, including patterns of disease transmission, information spread, and natural selection on behavior. Social network dynamics also depend on a multitude of behavioral and physiological processes that occur at the individual, dyad, and group levels. Bridging these individual-level processes with group-level dynamics is extremely challenging, but such studies are essential for understanding the causes and consequences of animal sociality.

1. Ryder, T.B., Blake, J.G., Parker, P.G., Loiselle, B.A., 2011. The composition, stability, and kinship of reproductive coalitions in a lekking bird. Behav. Ecol. 22, 282–290. doi:10.1093/beheco/arq213
2. Ryder, T.B., McDonald, D.B., Blake, J.G., Parker, P.G., Loiselle, B.A., 2008. Social networks in the lek-mating wire-tailed manakin (Pipra filicauda). Proc. Biol. Sci. 275, 1367–74. doi:10.1098/rspb.2008.0205
3. Ryder, T.B., Parker, P.G., Blake, J.G., Loiselle, B.A., 2009. It takes two to tango: reproductive skew and social correlates of male mating success in a lek-breeding bird. Proc. R. Soc. B Biol. Sci. 276, 2377–2384. doi:10.1098/rspb.2009.0208
4. Ryder, T.B., Dakin, R., Vernasco, B.J., Evans, B.S., Horton, B.M., Moore, I.T., 2020. Testosterone Modulates Status-Specific Patterns of Cooperation in a Social Network. Am. Nat. 195, 82–94. doi:10.1086/706236
5. Vernasco, B.J., Horton, B.M., Moore, I.T., Ryder, T.B., 2020. Reduced cooperative behavior as a cost of high testosterone in a lekking passerine bird. Behav. Ecol. 31, 401–410. doi:10.1093/beheco/arz201
6. Ryder, T.B., Horton, B.M., van den Tillaart, M., Morales, J.D.D., Moore, I.T., 2012. Proximity data-loggers increase the quantity and quality of social network data. Biol. Lett. 8, 917–920. doi:10.1098/rsbl.2012.0536
7. Dakin, R., Moore, I.T., Horton, B.M., Vernasco, B.J., Ryder, T.B., 2021. Testosterone‐mediated behaviour shapes the emergent properties of social networks. J. Anim. Ecol. 90, 131–142. doi:10.1111/1365-2656.13305
8. Vernasco, B.J., Moore, I.T., 2020. Testosterone as a mediator of the tradeoff between cooperation and competition in the context of cooperative reproductive behaviors. Gen. Comp. Endocrinol. 288, 113369. doi:10.1016/j.ygcen.2019.113369

Read the paper

Read the full paper here: Dakin, R, Moore, IT, Horton, BM, Vernasco, BJ, Ryder, TB. Testosterone‐mediated behaviour shapes the emergent properties of social networks. J Anim Ecol. 2021; 90: 131– 142. https://doi.org/10.1111/1365-2656.13305