Accelerated Evolution of Tissue-Specific Genes Mediates Divergence Amidst Gene Flow in European Green Lizards

Abstract

The European green lizards of the Lacerta viridis complex consist of two closely related species, L. viridis and Lacerta bilineata that split less than 7 million years ago in the presence of gene flow. Recently, a third lineage, referred to as the "Adriatic" was described within the L. viridis complex distributed from Slovenia to Greece. However, whether gene flow between the Adriatic lineage and L. viridis or L. bilineata has occurred and the evolutionary processes involved in their diversification are currently unknown. We hypothesized that divergence occurred in the presence of gene flow between multiple lineages and involved tissue-specific gene evolution. In this study, we sequenced the whole genome of an individual of the Adriatic lineage and tested for the presence of gene flow amongst L. viridis, L. bilineata, and Adriatic. Additionally, we sequenced transcriptomes from multiple tissues to understand tissue-specific effects. The species tree supports that the Adriatic lineage is a sister taxon to L. bilineata. We detected gene flow between the Adriatic lineage and L. viridis suggesting that the evolutionary history of the L. viridis complex is likely shaped by gene flow. Interestingly, we observed topological differences between the autosomal and Z-chromosome phylogenies with a few fast evolving genes on the Z-chromosome. Genes highly expressed in the ovaries and strongly co-expressed in the brain experienced accelerated evolution presumably contributing to establishing reproductive isolation in the L. viridis complex.

Keywords: Lacerta bilineata; Lacerta viridis; Adriatic lineage; diversification; gene flow; genome; tissue-specific evolution; transcriptomes.