Evolution of multiple sex-chromosomes associated with dynamic genome reshuffling in Leptidea wood-white butterflies

Atsuo Yoshido,Anna Voleníková,Petr Nguyen,Jan Šafář,František Marec,Kristýna Pospíšilová,Jan Provazník,Roger Vila,Jindra Šíchová

doi:10.1038/s41437-020-0325-9

Abstract

Sex-chromosome systems tend to be highly conserved and knowledge about their evolution typically comes from macroevolutionary inference. Rapidly evolving complex sex-chromosome systems represent a rare opportunity to study the mechanisms of sex-chromosome evolution at unprecedented resolution. Three cryptic species of wood-white butterflies—Leptidea juvernica, L. sinapis and L. reali—have each a unique set of multiple sex-chromosomes with 3–4 W and 3–4 Z chromosomes. Using a transcriptome-based microarray for comparative genomic hybridisation (CGH) and a library of bacterial artificial chromosome (BAC) clones, both developed in L. juvernica, we identified Z-linked Leptidea orthologs of Bombyx mori genes and mapped them by fluorescence in situ hybridisation (FISH) with BAC probes on multiple Z chromosomes. In all three species, we determined synteny blocks of autosomal origin and reconstructed the evolution of multiple sex-chromosomes. In addition, we identified W homologues of Z-linked orthologs and characterised their molecular differentiation. Our results suggest that the multiple sex-chromosome system evolved in a common ancestor as a result of dynamic genome reshuffling through repeated rearrangements between the sex chromosomes and autosomes, including translocations, fusions and fissions. Thus, the initial formation of neo-sex chromosomes could not have played a role in reproductive isolation between these Leptidea species. However, the subsequent species-specific fissions of several neo-sex chromosomes could have contributed to their reproductive isolation. Then, significantly increased numbers of Z-linked genes and independent neo-W chromosome degeneration could accelerate the accumulation of genetic incompatibilities between populations and promote their divergence resulting in speciation.

Highlights

Sex chromosomes (XY/XX in male heterogamety and WZ/ ZZ in female heterogamety) are known to play an important role in fundamental evolutionary processes, such as sex determination, inheritance of sex-specific traits, adaptation and speciation
For this purpose we have developed a couple of genomic tools in L. juvernica, namely a female transcriptome-based microarray for comparative genomic hybridisation (CGH) and a bacterial artificial chromosome (BAC) library from females
To find BAC clones derived from W chromosomes in L. juvernica, we screened the BAC library using fluorescence in situ hybridisation (FISH)-based screening (Supplementary Fig. S1)

Summary

Introduction

Sex chromosomes (XY/XX in male heterogamety and WZ/ ZZ in female heterogamety) are known to play an important role in fundamental evolutionary processes, such as sex determination, inheritance of sex-specific traits, adaptation and speciation. A large contribution of the X chromosome to reproductive isolation (the so-called ‘large X-effect’) is well established, especially in Drosophila species (Presgraves 2008). In some organisms with female heterogamety, Z-linked genes or traits contribute significantly to speciation and adaptation, referred to as the ‘large Z-effect’ (Qvarnström and Bailey 2009). Sex-limited Y or W chromosomes are frequently associated with sex-specific traits. Several studies suggest that the Y chromosome plays a role in reproductive isolation of some organisms (Sweigart 2010; Campbell et al 2012).

Methods

Results

Conclusion