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

Abstract

Haplodiploidy and paternal genome elimination (HD/PGE) are common in animals, having evolved at least two dozen times. HD/PGE typically evolves 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 argues that X chromosomes promote the evolution of male haploidy by facilitating purging recessive deleterious mutations. The Intragenomic Conflict Hypothesis instead argues that X chromosomes promote the evolution of male haploidy due to conflicts with autosomes over sex ratios and transmission. To test these hypotheses, we studied lineages that combine germline PGE with XX/X0 sex determination (gPGE+X systems). Because the evolution of such systems involves changes in genetic transmission but not 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. Through de novo genome sequence, we compared the genomes of 7 species with gPGE+X systems and 10 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, with an estimated 30 times more X-linked genes than in non-gPGE+X relatives. These results suggest a general role for intragenomic conflict in the origins of PGE/HD. These findings are among the first empirical results supporting a role for intragenomic conflict in the evolution of novel genetic systems.

Sexual antagonism in haplodiploids

“…For instance, sciarid flies not only have male PGE, but also an XO sex chromosome system (Metz 1938;Rieffel and Crouse 1966), thus allowing a within-organism comparison of these inheritance systems in relation to sexual antagonism. This is also true of some other groups with germline PGE such as gall midges and globular springtails (Gallun and Hatchett 1969;White 1977;Dallai 2000;Anderson et al 2020). In these groups we may expect femalebeneficial variants to be enriched on the autosomes, whilst male-beneficial ones would be expected to be overrepresented on the sex chromosomes, regardless of assumptions about dominance, making this a more straightforward prediction than between autosomes and sex chromosomes in conventional eumendelian systems (Rice 1984;Patten 2019).…”

Evolution of gene-rich germline restricted chromosomes in black-winged fungus gnats through introgression (Diptera: Sciaridae)

“…In order to better understand how old the GRCs are, we reconstructed the phylogenetic placement of GRC genes in Sciaroidea (the superfamily which contains Sciaridae and Cecidomyiidae, which both carry GRCs, and several other gnat families). We used a set of universal single-copy orthologs (BUSCO) identified in recently published draft genomes for 13 species within Sciaroidea and outgroup species ( Sylvicola fuscatus ) [27] ( Supplementary Fig 5 ). We identified 340 BUSCO genes that were duplicated in our B. coprophila genome with one copy on the GRC and one copy on either an autosome or the X chromosome (i.e.…”

“…We utilized draft genome assemblies for 14 Sciaroidea species and 2 species outside the Sciaroidea, most of which we obtained from Anderson et al [27] with the exception of Mayetiola destructor , which we obtained from NCBI (accession: GCA_000149195.1). We conducted a BUSCO analysis (version 4.0.2) [55] using the insecta database (insecta_odb10) on each genome assembly, along with our B. coprophila assembly, to identify single copy orthologs in each genome.…”

“…However, if Haig’s theory is correct GRCs, paternal genome elimination, and X chromosome elimination as a means of sex determination evolved independently in these two clades. There is recent evidence suggesting that the X chromosomes in Cecidomyiidae and Sciaridae are not related [27], but besides this, how the reproduction systems in both the Cecidomyiidae and Sciaridae evolved remains a mystery and very little empirical work has been done on this topic in either clade.…”

Males That Silence Their Father’s Genes: Genomic Imprinting of a Complete Haploid Genome

“…This provides a transmission advantage to mothers through their sons, and the evolution of PGE has been frequently framed as an outcome of intragenomic conflict between parental genomes in males—and therefore between the males’ parents—by maternally inherited genomes being able to manipulate spermatogenesis to enhance their own transmission ( Bull 1979 ; Herrick and Seger 1999 ; Ross et al. 2010 ; Normark and Ross 2014 ; Anderson et al. 2020 ).…”