**The AGA grants EECG Research Awards each year to graduate and post-doctoral researchers who are at a critical point in their research, where additional funds would allow them to conclude their research project and prepare it for publication. EECG awardees also get the opportunity to hone their science communication and write three posts over their grant tenure for the AGA Blog. In the first in the series, our EECG awardees write about their research and their interests as an ’embarkation’.
About the Author: Chris Robinson is a 3rd year PhD candidate in Bob Cox’s lab at the University of Virginia. He is interested in how gene regulation evolves across species, allowing for the development of different phenotypic patterns. His work uses hormonal manipulations, transcriptomics, and cellular imaging to understand how traits are gained and lost among closely related species. Chris loves to run and believes that this hobby is advantageous for being a capable lizard catcher! He tweets at @CDRism.
The diversity in animal coloration has long fascinated biologists, not only for the different roles it plays in organisms’ lives, but also because it can be stunningly beautiful. The color of an animal, or part of an animal, can help with crypsis, advertise danger, or be used to attract mates. Often, males and females of a species can be differently colored, and much time and energy has been devoted to understand the proximate and ultimate mechanisms that underlie these differences.
When males and females are sexually dichromatic, that is, present their own color patterns, sex-specific coloration must be produced using the same autosomal genome. There are several mechanisms that can facilitate this phenomenon, but my work investigates how a hormone, namely the sex steroid hormone testosterone, leads to sex-specific gene transcription and phenotypic development (Figure 1). Generally, testosterone is a masculinizing agent (Hau 2007) that is circulated at substantially higher levels in males than in females. When testosterone binds to its receptor, the bound receptor complex is translocated to the nucleus and binds to androgen response elements, which are 15-nucleotide motifs that allow the receptor to interact directly with chromatin. These interactions then lead to transcriptional activation or repression, which can depend upon sex- and region-specific cofactor recruitment. As a consequence of sex differences in testosterone levels, male and female transcriptomes become less correlated throughout ontogeny and their between-sex genetic correlations are decomposed, allowing for sex-specific phenotypes to develop (Cox et al. 2017).
Lizards in the genus Sceloporus offer a unique study system in which to gain insight about how testosterone regulates gene expression to facilitate sexual dichromatism specifically, and sexual dimorphism more broadly. In most Sceloporus species, males have vibrant ventral coloration that is greatly reduced or absent in females (Figure 2). In sexually dimorphic species, testosterone drives these differences (Cox et al. 2005), such that the development of coloration coincides with maturational increases of testosterone. However, coloration has been independently gained in females approximately eight times and independently lost in males approximately 13 times (Wiens 1999). Therefore, there have been many instances where interactions between testosterone and the genome have evolved such that females may develop coloration without maturational increases in testosterone and males do not develop coloration despite maturational increases in testosterone. My work uses different clades of Sceloporus lizards to uncover 1) how testosterone influences coloration at the organismal level, 2) how testosterone structures cellular architecture among dimorphic species, species with colorful females, and species with non-colorful males, and 3) how testosterone influences transcriptomic profiles among these same species to develop a clear picture of how testosterone facilitates the development on sexual dichromatism in some species, but not in others.
To begin this work, I have collected juvenile eastern fence lizards (S. undulatus), which are sexually dimorphic, and striped plateau lizards (S. virgatus), which have males and females without ventral coloration, from New Jersey and Arizona respectively. Using testosterone implants, I have confirmed that testosterone induces ventral coloration in S. undulatusbut has no effect in S. virgatus. I have collected ventral skin tissue from my experiment and extracted RNA from these samples to characterize gene expression profiles in colorful vs non-colorful skin. My #EECG2021 Award will be used to sequence transcriptomes from the S. virgatus samples. Using these data, with sequence data already collected from S. undulatus, I will work to identify genes that are responsive to testosterone in both species and genes that are responsive only in the dimorphic species. From these, I can identify genes from color-producing pathways that are differentially regulated by testosterone between species to uncover how the regulation of gene expression evolves to facilitate unique sex-specific coloration.
Multiple clades of Sceloporus have all three coloration patterns represented, so there is ample opportunity to repeat these experiments and analyses across the phylogeny. When this work is completed, my work will have uncovered a proximate mechanism by which evolution can convergently produce sex-specific phenotypic patterns, and potentially make inferences about whether evolution proceeds along the same paths in different clades. I am very excited to move this work forward and really understand color production at multiple levels within this remarkable genus. Thank you, AGA, for this opportunity!
Cox RM, Skelly SL, Leo A, John-Alder HB (2005) Testosterone regulates sexually dimorphic coloration in the eastern fence lizard, Sceloporus undulatus. Copeia. 2005: 597-608.
Cox RM, Cox CL, McGlothlin JW, Card DC, Andrew AL, Castoe TA (2017) Hormonally mediated increases in sex-biased gene expression accompany the breakdown of between-sex genetic correlations in a sexually dimorphic lizard. The American Naturalist. 189: 315-332.
Hau M (2007) Regulation of male traits by testosterone: implications for the evolution of vertebrate life histories. BioEssays. 29: 133-144.
Wiens JJ (1999) Phylogenetic evidence for multiple losses of a sexually selected character in phrynosomatid lizards. Proceedings of the Royal Society of London B: Biological Sciences. 266: 1529-1535.