Heterochromatin and genetic conflict

Abstract

Meiosis is a dangerous business. The two alleles in diploid organisms share an evolutionary interest in the survival and reproduction of their host individual; however, as soon as they segregate into haploid gametes, these alleles find themselves competing for transmission to the next generation (1). In males, the development of all four meiotic products into functional gametes fosters the evolution of alleles that disrupt the development or viability of gametes carrying the alternate allele. Systems that distort Mendelian segregation (hence, segregation distorters) typically comprise at least two loci: a trans-acting drive locus (such as a gene that encodes a poison) that targets alleles that are sensitive to the poison at a second, linked locus (2). A major impediment to the evolution of segregation distorters is the requirement that the poisonous allele be tightly linked to resistant alleles at the target locus; otherwise, distorters will commit suicide when paired with a sensitive allele (3). As a result, segregation distorters on autosomes are invariably associated with inversions that suppress recombination between the distorter and target loci. In contrast, heteromorphic sex chromosomes, where the Y chromosome is highly degenerated, can facilitate the evolution of segregation distorters because the X and Y frequently share little homologous sequence and do not recombine along most or all of their length. Thus, sex-chromosome segregation distorters that distort the sex ratio of the progeny of males that carry them (hence, sex-ratio distorters) are predicted to evolve frequently (4). The presence of sex-ratio distorters in populations selects for resistant Y chromosomes and autosomal suppressors that restore male fertility and a balanced sex ratio, and may lead to either balanced polymorphisms or open-ended arms races between loci that function in the male germ line (5). A recent study in PNAS has identified a gene required for sex-ratio distortion in Drosophila simulans (6), providing novel insight into the genetic and molecular mechanisms used by these selfish elements and their effects on genome evolution and species formation.The recurrent evolution of sex-ratio distorters and suppressors may contribute to otherwise puzzling observations regarding the genetics and evolution of spermatogenesis in animals with XY sex chromosomes. First, at least 10% of protein-coding genes in the Drosophila melanogaster genome are expressed solely in the male germ line, and ∼two-thirds of all D. melanogaster genes whose expression is restricted to a single tissue are expressed specifically in testes. In contrast, less than 1% of the D. melanogaster genome is specified for function during oogenesis (7). Thus, in Drosophila, an extraordinarily large fraction of the genome is dedicated to spermatogenesis. Second, in both Diptera and mammals, testis-specific genes show exceptionally high rates of regulatory and protein sequence evolution (8, 9), comprise the majority of new lineage-or species-specific genes (10), and these ne...

Lateral Thinking: How Histone Modifications Regulate Gene Expression

“…Alternatively, the fact that three of the six HP1 genes could not be assigned as homologous to any of the Drosophila HP1 genes in this study may suggest a dynamic pattern of diversification within P. citri or in the Hemiptera. Indeed, HP1 gene family evolution is dynamic and studies continue to discover HP1 paralogs that are unique to certain species (Levine et al, 2012), such as HP1D2 in D. simulans which evolved 25 million years ago and has been lost at least twice in the Drosophila genus (Meiklejohn, 2016). Therefore, P. citri may have evolved HP1 genes unique to the species or to the Hemiptera.…”

Selfish X chromosomes and speciation

“…Here, the maternal‐effect killer is produced in the diploid megaspore mother cell, and haploid megaspores that fail to inherit the killer allele from their hybrid mothers are inviable. Additional indirect evidence of drive‐driven speciation comes from a few additional cases of well‐characterized speciation genes with a role in heterochromatinization, which is a process targeted by several well‐studied drivers (Meiklejohn, ). Their rapid evolution and divergence have been understood as an example of perpetual evolution of both male and female meiotic drivers (Bayes & Malik, ; Presgraves, ).…”

Engineered sex distortion in the global agricultural pestCeratitis capitata

“…This suggests that sex distorters targeting repeats could be engineered with relative ease in species with an abundance of X-specific heterochromatin, likely a common occurrence in many insects. The fact that the mere presence of a sex chromosome specific repeat sequence constitutes a sufficient substrate for the operation of a highly-efficient distortion trait also supports the notion that the evolution of both X and Y specific sequence heterochromatin could to a large extent drive and in turn be driven by the evolutionary dynamics of sexually antagonistic selfish genes 30 . A downside of selecting such “junk” DNA targets may be the low level of functional conservation which would facilitate the selection for resistance, although the actual mechanism by which X-shredding eliminates X-bearing gametes remains unknown and hence also the pathways via which resistance is likely to arise.…”