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

Abstract

Genetic conflict is considered a key driver in the evolution of reproductive systems with non-Mendelian inheritance, where parents do not contribute equally to the genetic makeup of their offspring. One of the most extraordinary examples of non-Mendelian inheritance is paternal genome elimination (PGE), a form of haplodiploidy which has evolved repeatedly across arthropods. Under PGE, males are diploid but only transmit maternally-inherited chromosomes, while the paternally-inherited homologues are excluded from sperm. This asymmetric inheritance is thought to have evolved through an evolutionary arms race between the paternal and maternal genomes over transmission to future generations. In several PGE clades, such as the mealybugs (Hemiptera: Pseudococcidae), paternal chromosomes are not just eliminated from sperm, but also heterochromatinised early in development and thought to remain inactive, which could result from genetic conflict between parental genomes. Here, we present a parent-of-origin allele-specific transcriptome analysis in male mealybugs showing that expression is globally biased towards the maternal genome. However, up to 70% of somatically-expressed genes are to some degree paternally-expressed, while paternal genome expression is much more restricted in the male reproductive tract, with only 20% of genes showing paternal contribution. We also show that parent-of-origin-specific gene expression patterns are remarkably similar across genotypes, and that genes with completely biparental expression show elevated rates of molecular evolution. Our results provide the clearest example yet of genome-wide genomic imprinting in insects and enhance our understanding of PGE, which will aid future empirical tests of evolutionary theory regarding the origin of this unusual reproductive strategy.

Diversity of Modes of Reproduction and Sex Determination Systems in Invertebrates, and the Putative Contribution of Genetic Conflict

“…These different fitness effects likely contribute to their maintenance in different environments (whether any kind of antagonistic selection is involved in this case is unknown). The detection of some paternal expression in somatic tissues of the mealybug Planococcus citri, a species with paternal genome elimination, is consistent with a potential tug of war between the maternal and paternal genomes, thought to underlie the evolution of this unusual system [121]. The systematic application of these evolutionary and population genomics methods to various clades with a range of reproductive modes and sex determining systems, combined with clear predictions of the effects of various types of genetic conflict on patterns of genetic variation and gene expression, will be crucial for elucidating the evolutionary forces at play in creating and maintaining this diversity.…”

Sexual antagonism in haplodiploids

“…For simplicity, we henceforth assume that both gene copies are fully expressed under PGE, a scenario that captures autosomal expression in several PGE clades including springtails, lice and fungus gnat and gall midge flies (de la Filia et al 2015, Table 1). It also captures the evolution of a subset of genes and tissues in species where paternal genome is silenced, such as mealybugs, as silencing appears to be incomplete (de la Filia et al 2021). In contrast species with germline PGE (Table 1) are equivalent to arrhenotokous species as males become fully haploid early in development.…”

“…However, among PGE systems there is diversity in the extent of somatic paternal genome expression. This may occur either because the whole or part of the paternal genome is eliminated early in development (embryonic PGE), such that somatic tissues are actually haploid, or because the paternal-genome is silenced, such that certain tissues are functionally haploid (Burt and Trivers 2006; de la Filia et al 2021). If a locus is exclusively maternally expressed, then marginal fitness effects are identical to those given for arrhenotoky.…”

“…Focussing on PGE, we can explore how, depending on which gene copy controls the trait, the potential for feminisation may change. This is particularly relevant as the extent of expression in males from the maternal-origin and paternal-origin copies may vary across loci, tissues, and species (Burt and Trivers 2006; Gardner and Ross 2014; de la Filia et al 2021). Allowing for a proportion y of a locus’s expression in a male to come from the paternal-origin copy, and a proportion 1 − y to come from the maternal-origin copy, we find that the potential for feminisation is F = 1/(1 − y ).…”

The B chromosome of Pseudococcus viburni: a selfish chromosome that exploits whole-genome meiotic drive

“…In males of all mealybugs without B chromosomes, under PGE all paternally-inherited chromosomes are eliminated during spermatogenesis (Nur 1980 and citations therein) . In addition, in most male tissues paternal chromosomes are heavily condensed through heterochromatinization and are transcriptionally suppressed (Brown and Nur 1964;Bongiorni et al 2001;de la Filia et al 2020, Figure 1) . During male meiosis, chromosomes segregate based on their parental origin during anaphase II, which involves a monopolar spindle that only interacts with the euchromatic maternal set while the heterochromatic paternal complement lags behind (Bongiorni et al 2004) .…”