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

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.

The Dryas iulia Genome Supports Multiple Gains of a W Chromosome from a B Chromosome in Butterflies

“…This result is consistent with similar findings in K. inachus ( Yang et al 2020 ), Danaus plexippus ( Mongue et al 2017 ), and Spodoptera exigua ( Zhang et al 2019 ), which all possess a W chromosome that lacks sequence homology to the Z or autosomes. To our knowledge, cytogenic and PCR-based studies have only shown clear homology between derived or neosex chromosomes, and never to putatively ancestral sex chromosomes in Lepidoptera (e.g., Yoshido et al 2020 ).…”

An Investigation of ZZ/ZW and XX/XY Sex Determination Systems in North African Catfish (Clarias gariepinus, Burchell, 1822)

“…Although transposable elements can be dispersed on many chromosomes or even throughout the entire genome, large amplification of the elements are often found on sex chromosomes in many organisms ( Ahmad et al, 2020 ; Koomgun et al, 2020 ; Laopichienpong et al, 2020 ; Yoshido et al, 2020 ). The presence of accumulated TEs leads to the establishment of heterochromatin, and possibly also to TE recombination between non-homologous copies.…”

Multiple sex chromosomes in teleost fishes from a cytogenetic perspective: state of the art and future challenges

“…Recently, it was shown that early differentiation of multiple sex chromosomes in Drosophila miranda was accompanied by the massive amplification of gene copies leading to their tandemly repeated arrangement on both X and Y chromosomes [ 112 ]. Similarly, the amplification of genes linked to complex multiple sex chromosome systems was observed also in wood white butterflies of the genus Leptidea [ 113 ], suggesting that the mechanism could be a common feature of sex chromosome differentiation. Thus, a combination of gene amplification with the frequent sex chromosome turnover observed in fishes, both possibly induced by increasing mutation load, could systematically create novel selectable variation and thus considerably increase the adaptive potential in fishes (cf.…”