Contrasting Evolutionary Trajectories Under Paternal Genome Elimination in Male and Female Citrus Mealybugs

Most studies of sex-biased genes explore their evolution in familiar chromosomal sex determination systems, leaving the evolution of sex differences under alternative reproductive systems unknown. Here we explore the system of paternal genome elimination employed by mealybugs (Hemiptera: Pseudococcidae) which have no sex chromosomes. Instead, all chromosomes are autosomal and inherited in two copies, but sex is determined by the ploidy of expression. Females express both parental alleles, but males reliably silence their paternally inherited chromosomes, creating genome-wide haploid expression in males and diploid expression in females. Additionally, sons do not express alleles directly inherited from their fathers, potentially disrupting the evolution of male-benefiting traits. To understand how these dynamics impact molecular evolution, we generated sex-specific RNAseq, a new gene annotation, and whole-genome population sequencing of the citrus mealybug, Planococcus citri. We found that genes expressed primarily in females hold more variation and evolve more quickly than those expressed in males or both sexes. Conversely, we found more apparent adaptation in genes expressed mainly in males than in those expressed in females. Put together, in this paternal genome elimination system there is slower change on the male side but, by increasing selective scrutiny, an increase in the degree of adaptation in these genes. These results expand our understanding of evolution in a non-Mendelian genetic system and the data we generated should prove useful for future research on this pest insect.