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

Noelle Anderson, Kamil S. Jaron, Christina N. Hodson, Matthew B. Couger, Jan Ševčík, Brooke Weinstein, Stacy Pirro, Laura Ross, Scott William Roy

Research output: Contribution to journalArticlepeer-review

Abstract

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.
Original languageEnglish
Article numbere2122580119
Number of pages24
JournalProceedings of the National Academy of Sciences (PNAS)
Volume119
Issue number23
DOIs
Publication statusPublished - 7 Jun 2022

Keywords

  • sex chromosomes
  • sex determination
  • haplodiploidy
  • genome elimination
  • genomic conflict
  • insects
  • Diptera
  • springtail

Fingerprint

Dive into the research topics of 'Gene-rich X chromosomes implicate intragenomic conflict in the evolution of bizarre genetic systems'. Together they form a unique fingerprint.

Cite this