Abstract

Background Lacerta viridis and Lacerta bilineata are sister species of European green lizards (eastern and western clades, respectively) that, until recently, were grouped together as the L. viridis complex. Genetic incompatibilities were observed between lacertid populations through crossing experiments, which led to the delineation of two separate species within the L. viridis complex. The population history of these sister species and processes driving divergence are unknown. We constructed the first high-quality de novo genome assemblies for both L. viridis and L. bilineata through Illumina and PacBio sequencing, with annotation support provided from transcriptome sequencing of several tissues. To estimate gene flow between the two species and identify factors involved in reproductive isolation, we studied their evolutionary history, identified genomic rearrangements, detected signatures of selection on non-coding RNA, and on protein-coding genes.FindingsHere we show that gene flow was primarily unidirectional from L. bilineata to L. viridis after their split at least 1.15 million years ago. We detected positive selection of the non-coding repertoire; mutations in transcription factors; accumulation of divergence through inversions; selection on genes involved in neural development, reproduction, and behavior, as well as in ultraviolet-response, possibly driven by sexual selection, whose contribution to reproductive isolation between these lacertid species needs to be further evaluated.ConclusionThe combination of short and long sequence reads resulted in one of the most complete lizard genome assemblies. The characterization of a diverse array of genomic features provided valuable insights into the demographic history of divergence among European green lizards, as well as key species differences, some of which are candidates that could have played a role in speciation. In addition, our study generated valuable genomic resources that can be used to address conservation-related issues in lacertids.

Highlights

  • Understanding what species are and the processes driving their emergence have been two central issues in biology [1]

  • These studies aiming at the so-called speciation genes revealed at least three general patterns: (i) many genes involved in post-zygotic incompatibilities show accelerated evolution [2]; (ii) incompatibilities often involve a disproportionate number of genes located on sex chromosomes [3, 4]; and (iii) misexpression is often observed in hybrids, suggesting that gene regulation is an important component of speciation [5,6,7]

  • Since the genome of L. viridis had better contiguity than L. bilineata, L. viridis was used as the reference to predict genomic variants, structural variants (SVs) and single-nucleotide polymorphisms between the two taxa

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Summary

Introduction

Understanding what species are and the processes driving their emergence have been two central issues in biology [1]. Genes involved in reproductive isolation were mainly identified in model organisms, such as Drosophila [2]. To estimate gene flow between the two species and identify factors involved in reproductive isolation, we studied their evolutionary history, identified genomic rearrangements, detected signatures of selection on non-coding RNA, and on protein-coding genes. We detected positive selection of the non-coding repertoire; mutations in transcription factors; accumulation of divergence through inversions; selection on genes involved in neural development, reproduction, and behavior, as well as in ultraviolet-response, possibly driven by sexual selection, whose contribution to reproductive isolation between these lacertid species needs to be further evaluated. The characterization of a diverse array of genomic features provided valuable insights into the demographic history of divergence among European green lizards, as well as key species differences, some of which are candidates that could have played a role in speciation.

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