On each of the Greater Antillean islands, habitat-specialist Anolis ecomorphs have independently evolved complex suites of shared phenotypes and behaviors. This remarkable convergence has motivated the work of generations of anolologists. With anoles entering the once-exclusive club of genome-enabled organisms, a new line of investigation has become possible: Is the convergence observed in anole ecomorphs caused by molecular convergence? Such convergence can take many forms, including shared changed at individuals sites, or shared changes in the rates of protein evolution of individual genes.
Russ Corbett-Detig of UCSC sought to answer this question using whole-genome sequence data from 12 species – four from each of the Trunk-Ground, Trunk-Crown, and Grass-Bush ecomorphs drawn from different islands and different evolutionary lineages. Accurately detecting molecular convergence is fraught and much recent research has focused on avoiding pitfalls that could lead to a positively misleading inference of convergence where none actually exists. Previous studies have trumpeted amazing cases of molecular convergence in a variety of animals, only to be later shown to be artifacts of data analysis.
Corbett-Detig did everything right. He used null models that account for the expected background levels of convergence caused by processes other than natural selection. He found no evidence of extra shared non-synonymous mutations in any of the three ecomorph groups. Similarly, he found no signal of shared changed in protein evolution in Trunk-Ground or Trunk-Crown but Grass-Bush anoles seemed to share elevated rates of changes in many genes. This result was exciting, but Corbett-Detig dug deeper and discovered a new way this type of analysis could be mislead – two of the four Grass-Bush anoles exhibited accelerated evolution across their entire genomes and, as a result, seemed to share faster rates at more genes than expected by chance. When Corbett-Detig corrected for this bias, the signal of convergence disappeared.
While this result was in one sense disappointing, it is also fascinating and suggests the evolutionary pathways to shared ecomorphological traits are numerous and strongly influenced by contingency. Furthermore, anole ecomorphs have evolved such a stunning set of similarities that other forms of convergence like genome structure, gene family expansion, or convergence in gene regulation may still hold the key to understanding the genetic basis the remarkable convergence of Anolis ecomorph classes.