How does behavior evolve?

The Johnson lab group is interested in the ecological factors that influence social behaviors and the physiological mechanisms that underlie those behaviors. Most of the lab’s work uses Caribbean lizards in the genus Anolis, or anoles, but we’re also exploring the diversity of lizards that occur at our local field sites in south-central Texas. We use field observations, laboratory experiments, molecular genetics, neuroendocrine techniques, and comparative methodology to explore behavioral evolution.

Click on the images below or scroll down to learn more about our research!

One of the main avenues of research in the Johnson lab is the study of the muscular and hormonal traits that underlie behavior, and how those traits differ among species. In this work, we combine approaches from behavioral ecology and behavioral neuroscience to examine how variation in social behaviors is associated with variation in mechanistic traits.

We focus this work on a group of 30 species of anoles, which exhibit two types of social behavior that are particularly interesting for this research. First, these lizards use a throat fan called a dewlap to communicate with other lizards. The dewlap is extended and retracted using one pair of muscles (the ceratohyoids) on each side of the throat. When the ceratohyoid muscles contract, the dewlap extends, and when they relax, the dewlap is retracted. Second, when male lizards copulate, they move their hemipenes using just two muscles - one to evert the hemipenes out of the tail, and the other to retract them back into the tail.

We measure the frequency of dewlap extension and copulation behaviors in the field to determine how different species use these two behaviors (and the muscles that support them) at different rates, and then bring samples of muscle tissue into the lab. There, we study how muscles that are used differently differ in a wide range of physiological traits, such as cell size and number, androgen sensitivity, and enzyme function.

We also use this general approach to study the mechanisms of behavior in a wide diversity of lizards in Texas, including spiny lizards, whiptails, geckos, skinks, and earless lizards. In this work, we have examined how differences in lizard brain morphology are associated with chemical and visual modes of communication, how temperature influences brain and behavior, how lizards use their tails to communicate with predators and conspecifics, and how muscles and behavior change as a juvenile lizard develops into an adult.

This work is funded by NSF IOS 1257021 to M.A. Johnson (2013-2018).

Representative publications:

Johnson, M.A., B.K. Kircher, and D.J. Castro. 2018. The evolution of androgen receptor expression and behavior in Anolis lizard forelimb muscles. Journal of Comparative Physiology A 204: 71-79.

Robinson, C.D., M.S. Patton, B.M. Andre, and M.A. Johnson. 2015. Convergent evolution of brain morphology and communication modalities in lizards. Current Zoology 61: 281-291.

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Another major theme of the research in the Johnson Lab involves how anole lizards use color to communicate with each other. Some of these studies have involved understanding how the dewlap - which can vary remarkably in color, pattern, and size, even within the same population of lizards - can send different information to other lizards. Other studies (in both the field and lab) have examined how anoles communicate with each other by changing their entire body color, often within seconds! In this work, we consider questions such as, do males and females use body color changes in the same ways? Is body temperature associated with body color? Does color communicate dominance or subordinance in a competitive interaction? Does parasite load influence body color in lizards?

Representative publications:

Bush, J.M., M.M. Quinn, E.C. Balreira, and M.A. Johnson. 2016. How do lizards determine dominance? Applying ranking algorithms to animal social behavior. Animal Behaviour 118: 65-74.

Cook, E.G., T.G. Murphy, and M.A. Johnson. 2013. Colorful displays signal male quality in a tropical anole lizard. Naturwissenschaften 100: 993-996.

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During the past several years, we have also been working to understand how variation in male and female reproductive tissues influence their behavior and physiology. Much of this recent work in our lab has focused on testis morphology, and in collaboration with Dr. Ariel Kahrl of Stockholm University, we are now considering how sperm morphology is associated with this variation as well. We are examining how variation in testis architecture evolves in association with variation in sperm cell shape, and quantifying variation in these traits within species.

Representative publications:

Johnson, M.A., M. V. Lopez, T.K. Whittle, B.K. Kircher, A.K. Dill, D. Varghese, and J. Wade. 2014. The evolution of copulation frequency and the mechanisms of reproduction in male Anolis lizards. Current Zoology 60:768-777.

Johnson, M.A., J.L. Caton, R.E. Cohen, J.R. Vandecar, and J. Wade. 2010. The burden of motherhood: the effect of reproductive load on female lizard locomotor, foraging, and social behavior. Ethology 116: 1217-1225.

Johnson, M.A. and J. Wade. 2010. Behavioral display systems across nine Anolis lizard species: sexual dimorphisms in structure and function. Proceedings of the Royal Society of London: B 277:1711-1719.

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In line with our general interests in the evolution of mechanisms of behavior, the Johnson Lab has been participating in a large-scale collaboration studying patterns of hormone variation across vertebrates. Dr. Maren Vitousek of Cornell University and Dr. Michele Johnson have coordinated this effort since 2012. To address questions of hormonal evolution, our initial work required the compilation of a database of hormone measures, recently published as HormoneBase (available at hormonebase.org). The HormoneBase Consortium is now using this database to examine how circulating levels of androgens and glucocorticoids in free-living vertebrates are associated with life history traits, metabolism, speciation rates, and conservation status.

Representative publications:

Vitousek, M.N.1, M.A. Johnson1, J.W. Donald, C.D. Francis, M.J. Fuxjager, W. Goymann, M. Hau, J.F. Husak, B.K. Kircher, R. Knapp, L.B. Martin, E.T. Miller, L.A. Schoenle, J. Uehling*, and T.D. Williams. 2018. HormoneBase, a population-level database of steroid hormone levels across vertebrates. Scientific Data 5:180097. 1Indicates shared first authorship.

Johnson, M.A., C.D. Francis, E.T. Miller, C.J. Downs, and M.N. Vitousek. 2018. Detecting bias in large-scale comparative analysis: Methods for expanding the scope of hypothesis-testing with HormoneBase. Integrative and Comparative Biology 58:720-728.

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