Evolutionary lability in Hox cluster structure and gene expression in Anolis lizards

Evol Lett. 2019 Aug 6;3(5):474-484. doi: 10.1002/evl3.131. eCollection 2019 Oct.

Abstract

Hox genes orchestrate development by patterning the embryonic axis. Vertebrate Hox genes are arranged in four compact clusters, and the spacing between genes is assumed to be crucial for their function. The genomes of squamate reptiles are unusually rich and variable in transposable elements (TEs), and it has been suggested that TE invasion is responsible for the Hox cluster expansion seen in snakes and lizards. Using de novo TE prediction on 17 genomes of lizards and snakes, I show that TE content of Hox clusters are generally 50% lower than genome-wide TE levels. However, two distantly related lizards of the species-rich genus Anolis have Hox clusters with a TE content that approaches genomic levels. The age distribution of TEs in Anolis lizards revealed that peaks of TE activity broadly coincide with speciation events. In accordance with theoretical models of Hox cluster regulation, I find that Anolis species with many TEs in their Hox clusters show aberrant Hox gene expression patterns, suggesting a functional link between TE accumulation and embryonic development. These results are consistent with the hypothesis that TEs play a role in developmental processes as well as in evolutionary diversifications.

Keywords: Comparative studies; Hox genes; Macroevolution; gene expression; squamates; transposable elements.