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

Abstract

AbstractHaplodiploidy and paternal genome elimination (HD/PGE) are common in invertebrates, having evolved at least two dozen times, all 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 posits that X chromosomes promote the evolution of male haploidy by facilitating purging recessive deleterious mutations. The Intragenomic Conflict Hypothesis instead holds that conflict between genes drives genetic system turnover; under this model, X chromosomes could promote the evolution of male haploidy due to conflicts with autosomes over sex ratios and transmission. We studied lineages in which we can test these hypotheses: species that exhibit germline PGE and retain an XX/X0 sex determination system (gPGE+X). Because evolving PGE in these cases involves changes in genetic transmission without 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. To quantify the degree of X linkage, we sequenced and compared the genomes of 7 species with gPGE+X systems and 11 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 compared to non-gPGE relatives, and recover a robust positive correlation between X linkage and gPGE. These are among the first empirical results supporting a role for intragenomic conflict in the evolution of novel genetic systems such as HD/PGE.Significance StatementSex determination systems such as haplodiploidy, in which males’ gene transmission is haploid, are surprisingly common, however, the evolutionary paths to these systems are poorly understood. X chromosomes may play a particularly important role, either by increasing survival of males with only maternal genomes, or due to conflicts between X-chromosomal and autosomal genes. We studied X-chromosome gene richness in springtails and two fly families in which males are diploid as adults but only transmit their maternally-inherited haploid genome. We find that species with such atypical systems have far more X chromosomal genes than related diploid species. These results suggest that conflict between elements within the genome drives the evolution of unusual sex determination systems.