Gene-rich X chromosomes implicate intragenomic conflict in the evolution of bizarre genetic systems

Abstract Haplodiploidy and paternal genome elimination (HD/PGE) are common in animals, having evolved at least two dozen times. HD/PGE typically evolves from male heterogamety (i.e., systems with X chromosomes), however why X chromosomes are important for the evolution of HD/PGE remains debated. The Haploid Viability Hypothesis argues that X chromosomes promote the evolution of male haploidy by facilitating purging recessive deleterious mutations. The Intragenomic Conflict Hypothesis instead argues that X chromosomes promote the evolution of male haploidy due to conflicts with autosomes over sex ratios and transmission. To test these hypotheses, we studied lineages that combine germline PGE with XX/X0 sex determination (gPGE+X systems). Because the evolution of such systems involves changes in genetic transmission but not increases in male hemizygosity, a high degree of X linkage in these systems is predicted by the Intragenomic Conflict Hypothesis but not the Haploid Viability Hypothesis. Through de novo genome sequence, we compared the genomes of 7 species with gPGE+X systems and 10 related species with typical XX/XY or XX/X0 genetic systems. We find highly increased X-linkage in modern and ancestral genomes of gPGE+X species, with an estimated 30 times more X-linked genes than in non-gPGE+X relatives. These results suggest a general role for intragenomic conflict in the origins of PGE/HD. These findings are among the first empirical results supporting a role for intragenomic conflict in the evolution of novel genetic systems.