Island-specific evolution of a sex-primed autosome in the planarian Schmidtea mediterranea

Abstract The sexual biotype of the planarian Schmidtea mediterranea is a hermaphrodite indigenous to Tunisia and several Mediterranean islands. Here, we isolated individual chromosomes and used sequencing, Hi-C and linkage mapping to assemble a chromosome-scale genome reference. The linkage map revealed an extremely low rate of recombination on chromosome 1. We confirmed suppression of recombination on chromosome 1 by quantifying recombination events in individual sperm and oocytes. We showed that the extensive heterozygous regions, previously designated as J and V haplotypes, comprise essentially all of chromosome 1. Genome sequencing of individuals isolated in the wild indicated that this heterozygosity has evolved specifically in populations from Sardinia and Corsica. We found that chromosome 1 acquired many genes that determine the development of female and male reproductive systems, along with haplotype-specific expression of such sex specific genes. These molecular signatures and restricted recombination in a hermaphrodite led us to propose that chromosome 1 is a sex-primed autosome, providing direct molecular evidence for the traditional model of how sex chromosomes may have evolved from autosomes.