Evolution of Green Blood in New Guinea Lizards: Phylogenomics, Biogeography, and Comparative Genomics

Non-model organisms with evolutionary novelties and complex distributions can provide valuable insight into the mechanisms underlying biological diversity. Green blood is one of the most unusual vertebrate physiologies and has repeatedly evolved in lizards from the megadiverse island of New Guinea. An unusually high concentration of the toxic green bile pigment biliverdin causes the green coloration of these lizards\u27 blood, muscles, and bones. This dissertation uncovered the complex history of this novel trait (Chapter 2), identified protein-coding sequences that underlie green blood in lizards (Chapter 3), and explored evolutionary processes that drive genetic diversity in high-elevation lizards. To accurately trace the evolutionary history of green blood in lizards, I inferred a species phylogeny for red- and green-blooded tropical lizards using thousands of genomic regions. Surprisingly, I found robust support for the non-monophyly of green-blooded lizards. Using ancestral state reconstruction and Bayesian inference of character traits, I found support for four independent origins of green blood with no losses. To identify genes contributing to the green-blood phenotype, I compared transcriptomic data from 2 species of green-blooded lizards with those from 2 red-blooded relatives by examining protein coding sequences and gene expression differences across 2 tissue types. I found a suite of genes evolving under positive selection and hundreds of genes that are differentially expressed between green- and red-blooded lizards. Importantly, I identified a handful of protein families (albumins, ATP-binding cassette transporters, albumins, and cytochrome P450 monooxygenases) from our candidate gene set that are involved in biliverdin metabolism and likely contribute to the green blood phenotype. Understanding the underlying genomic and proteomic changes that have allowed these lizards to remain jaundice-free may translate to non-traditional approaches to specific health problems. Finally, I explored the biogeography of a species of high-elevation New Guinea lizards distributed across several disjunct mountain ranges. Using population genomics and biogeographical reconstructions, I identified substantial genetic structuring among 4-6 Papuascincus stanleyanus populations highlighting the cryptic genetic diversity in this species. Our analyses also suggest that the current distribution of these lizards on disjunct mountaintops is the result of repeated colonization from low-elevation sister taxa, rather than dispersal across low-elevation regions during glacial cycling. Using recent next-generation sequencing methods, I combined phylogenomics, biogeography, ecology, and genomics to explore processes that drive biological diversity in this system extensively