Selection drives convergent gene expression changes during transitions to co-sexuality in haploid sexual systems

Guillaume Cossard (1, 2, 3) , Olivier Godfroy (2) , Zofia Nehr (2) , Corinne Cruaud (4) , J. Mark Cock (2, 3) , Agnieszka Lipinska (2, 3) , Susana Coelho (2, 3)

1 DEE - Department of Ecology and Evolution [UNIL, Lausanne] = Département d'écologie et évolution
2 SBR - Station biologique de Roscoff = Roscoff Marine Station
3 LBI2M - Laboratoire de Biologie Intégrative des Modèles Marins
4 GENOSCOPE - Genoscope - Centre national de séquençage [Evry]

Co-sexuality has evolved repeatedly from unisexual (dioicous) ancestors across a wide range of taxa. However, the molecular changes underpinning this important transition remain unknown, particularly in organisms with haploid sexual systems such as bryophytes, red algae and brown algae. Here we explore four independent events of emergence of co-sexuality from unisexua lancestors in brown algal clades to examine the nature, evolution and degree of convergence of gene expression changes that accompany the breakdown of dioicy. The amounts of male versus female phenotypic differences in dioicous species were not correlated with the extent of sex-biased gene expression, in stark contrast to what is observed in animals. Although sex-biased genes exhibited a high turnover rate during brown alga diversification, some of their predicted functions were conserved across species. Transitions to co-sexuality consistently involved adaptive gene expression shifts and rapid sequence evolution, particularly for male-biased genes. Gene expression in co-sexual species was more similar to that in females rather than males of related dioicous species, suggesting that co-sexuality may have arisen from ancestral females. Finally, extensive convergent gene expression changes, driven by selection, were associated with the transition to co-sexuality. Together, our observations provide insights on how co-sexual systems arise from ancestral, haploid UV sexual systems.

Mots clés: Evolutionary genetics; Marine biology

Domaines: Sciences du Vivant [q-bio]

Guillaume Cossard, Olivier Godfroy, Zofia Nehr, Corinne Cruaud, J. Mark Cock, et al.. Selection drives convergent gene expression changes during transitions to co-sexuality in haploid sexual systems. Nature Ecology & Evolution, 2022, 6, pp.579-589. ⟨10.1038/s41559-022-01692-4⟩. ⟨hal-03619076⟩