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 new reproductive and sex determining systems. In particular, reproductive strategies 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 to their offspring, while the paternal homologues are excluded from sperm. This asymmetric inheritance is thought to have evolved through an evolutionary arms race between paternal and maternal genomes over transmission to future generations. In several clades with PGE, 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. Such paternal genome silencing could alleviate genetic conflict between paternal alleles over transmission.However, it is unclear if paternal chromosomes are indeed genetically inert in both soma and germline. Here, we present a parent-of-origin allele-specific transcriptome analysis in male mealybugs. We show that expression is globally biased towards the maternal genome, but detect activity of paternal chromosomes in both somatic and reproductive tissues. Up to 70% of somatically-expressed genes are to some degree paternally-expressed. However, paternal genome expression is much more restricted in the testis, with only 20% of genes showing paternal contribution. Finally, we show that the patterns of parent-of-origin-specific gene expression are remarkably similar across genotypes and that those genes with biparental expression show elevated rates of molecular evolution. Our results provide the clearest example yet of genome-wide genomic imprinting (parent-of-origin specific gene expression) in insects. Furthermore, it enhances our understanding of PGE, which will aid future empirical tests of evolutionary theory regarding the origin of this unusual reproductive strategy.

Sex-specific expression and DNA methylation in a species with extreme sexual dimorphism and paternal genome elimination

“…It is likely these differences are due to the unusual reproductive strategy of this species, paternal genome elimination. Based on our key finding of a lack of direct association between differential DNA methylation and differential gene expression, paired with recent findings by de la Filia et al (2020) that show males display mostly haploid gene expression, we hypothesise DNA methylation may play a trans -acting role in ploidy compensation in this species, although this is speculation and requires experimental testing. Finally, we have identified a large number of differentially expressed genes between sexes mirroring the extreme sexual-dimorphism exhibited in this species and we have found no evidence for sex-specific alternative splicing of doublesex orthologs in P. citri .…”

“…The sex-determination system in P. citri is unknown and alternative splicing of the doublesex gene has been implicated in sex-determination in the vast majority of insect species (Wexler et al , 2019). We therefore checked to see if any genes orthologous to the Drosophila melanogaster doublesex gene (as determined in: de la Filia et al , 2020) were alternatively spliced. There were five genes in the current annotation ( P.citri v0 mealybug.org) which are othlogous to D. melanogaster doublesex ( g1737 , g2969 , g11101 , g11102 and g36454 ).…”

“…We hypothesise this pattern, along with the identification of intergenic DNA methylation, is a result of the unusual reproductive strategy employed by this species, paternal genome elimination. Males with PGE have approximately half of their genome in a heterochromatic state (Hughes-Schrader, 1948; Brown and Nur, 1964; Bongiorni and Prantera, 2003; de la Filia et al , 2020). In mammals and plants, DNA methylation is associated with the formation of heterochromatin (Suzuki and Bird, 2008).…”

“…Overall hypermethylation in females suggests DNA methylation in males and females may serve different functions. We hypothesise that one function of hypermethylation in females could be to act as a mechanism of ploidy compensation, as due to paternal chromosome silencing, most genes show haploid expression in males (de la Filia et al , 2020). There is evidence for possible ploidy compensation via DNA methylation in other insects.…”

“…However, males subsequently eliminate paternally-inherited chromosomes during spermatogenesis and only transmit maternally-inherited chromosomes to their offspring (Brown and Nelson-Rees, 1961). Furthermore, in P. citri males, paternally-inherited chromosomes are heterochromatinised in early development (Brown and Nur, 1964; Bongiorni et al , 2001) and thus gene expression shows a maternal bias (de la Filia et al , 2020). Females, on the other hand, do not undergo the process of PGE and both maternally and paternally-derived chromosomes remain euchromatic throughout development (Brown and Nur, 1964).…”