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

• Published in: Proceedings of the National Academy of Sciences - PNAS Vol. 119; no. 23; p. e2122580119
• Main Authors: Anderson, Noelle, Jaron, Kamil S, Hodson, Christina N, Couger, Matthew B, Ševčík, Jan, Weinstein, Brooke, Pirro, Stacy, Ross, Laura, Roy, Scott William
• Format: Journal Article
• Language: English
• Published: United States National Academy of Sciences 07.06.2022
• Subjects: Animals; Biological Sciences; Chromosomes; Diploidy; Evolution; Evolution, Molecular; Evolutionary genetics; Genes; Genome - genetics; Genomes; Haploidy; Hemizygosity; Hypotheses; Invertebrates; Male; Males; Mutation; Sex; Sex determination; Sex Determination Processes; Sex ratio; Species; X Chromosome - genetics; X chromosomes; haplodiploidy; genomic conflict; insects; sex chromosomes; sex determination
• ISSN: 0027-8424; 1091-6490; 1091-6490
• DOI: 10.1073/pnas.2122580119

Haplodiploidy 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-linked genes promote the evolution of male haploidy by facilitating purging recessive deleterious mutations. The Intragenomic Conflict Hypothesis holds that conflict between genes drives genetic system turnover; under this model, X-linked genes could promote the evolution of male haploidy due to conflicts with autosomes over sex ratios and genetic transmission. We studied lineages where we can distinguish these hypotheses: species with germline PGE that retain an XX/X0 sex determination system (gPGE+X). Because evolving PGE in these cases involves changes in 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 7 gPGE+X species’ genomes with 11 related species with typical XX/XY or XX/X0 genetic systems, representing three transitions to gPGE. We find highly increased X linkage in both modern and ancestral genomes of gPGE+X species compared to non-gPGE relatives and recover a significant positive correlation between percent X linkage and the evolution of gPGE. These empirical results substantiate longstanding proposals for a role for intragenomic conflict in the evolution of genetic systems such as HD/PGE.