RT Journal Article
SR Electronic
T1 Gene-rich X chromosomes implicate intragenomic conflict in the evolution of bizarre genetic systems
JF bioRxiv
FD Cold Spring Harbor Laboratory
SP 2020.10.04.325340
DO 10.1101/2020.10.04.325340
A1 Noelle Anderson
A1 Kamil S. Jaron
A1 Christina N. Hodson
A1 Matthew B. Couger
A1 Jan Ševčík
A1 Brooke Weinstein
A1 Stacy Pirro
A1 Laura Ross
A1 Scott William Roy
YR 2022
UL http://biorxiv.org/content/early/2022/01/18/2020.10.04.325340.abstract
AB 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 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 Statement Sex 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.Competing Interest StatementThe authors have declared no competing interest.