Emergence and stabilisation of a neo-Y chromosome in nematode species with rare males

Abstract

How do sex chromosomes evolve in the transition to asexuality? So far, species that depart from canonical sexual reproduction - for example, parthenogens with rare sex, or species where the paternal genome is set aside - have been found to carry either no sex chromosomes, or sex chromosomes but no male-specific sex chromosome (i. e., no Y). Here we reveal that, in Mesorhabditis nematodes, a new Y chromosome emerged once, from sexual ancestors, in species that have transitioned into an unconventional mode of reproduction called autopseudogamy. In this reproductive system, females produce clonal females plus rare ([~]10%) males that are needed for fertilisation, but that do not contribute to the female genome. Analysing the Y chromosomes of two autopseudogamous species, we found high levels of degeneration, most likely due to loss of recombination, and two additional conserved features: i) they accumulated male-beneficial genes, and ii) they display a strong fertilisation drive, in that mainly Y-bearing sperm fertilise female oocytes. Both features are likely evolutionarily favourable in the context of autopseudogamy. Our results suggest that male-specific chromosomes can still be maintained in systems with rare, and possibly genetically useless, males.