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

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 Hypo...

Full description

Saved in:
Bibliographic Details
Published inProceedings 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
LanguageEnglish
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
Online AccessGet full text

Cover

More Information
Summary: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.
Bibliography:ObjectType-Article-1
SourceType-Scholarly Journals-1
ObjectType-Feature-2
content type line 23
Edited by Harmit Malik, Fred Hutchinson Cancer Research Center, Seattle, WA; received February 3, 2022; accepted April 8, 2022
Author contributions: N.A., L.R., and S.W.R. designed research; N.A., K.S.J., C.N.H., M.B.C., B.W., and S.P. performed research; N.A. and J.Š. contributed new reagents/analytic tools; N.A., K.S.J., C.N.H., and B.W. analyzed data; N.A., B.W., and S.W.R. wrote the paper; and K.S.J., C.N.H., and L.R. contributed writing and editing.
ISSN:0027-8424
1091-6490
1091-6490
DOI:10.1073/pnas.2122580119