School of Biological Sciences, Institute of Evolutionary Biology, The University of Edinburgh, Edinburgh, United Kingdom.
Mol Biol Evol. 2021 May 19;38(6):2566-2581. doi: 10.1093/molbev/msab052.
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 only eliminated from sperm, but also heterochromatinized 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 toward 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.
遗传冲突被认为是非孟德尔遗传生殖系统进化的关键驱动因素，在这种遗传模式中，父母对后代的遗传组成贡献不均等。非孟德尔遗传的最显著例子之一是父本基因组消除（PGE），这是一种在节肢动物中反复进化的单倍二倍体形式。在 PGE 中，雄性是二倍体，但只传递母系遗传的染色体，而父系遗传的同源染色体则被排除在精子之外。这种不对称遗传被认为是通过父本和母本基因组在向后代传递过程中的进化军备竞赛而进化而来的。在几个 PGE 进化枝中，如粉蚧（半翅目：粉蚧科），父本染色体不仅从精子中消除，而且在早期发育中也异染色质化并被认为保持不活跃，这可能是由于父本和母本基因组之间的遗传冲突所致。在这里，我们在雄性粉蚧中进行了亲本来源等位基因特异性转录组分析，结果表明表达总体上偏向母本基因组。然而，高达 70%的体细胞表达基因在某种程度上是父本表达的，而父本基因组在雄性生殖道中的表达则受到更多限制，只有 20%的基因显示出父本的贡献。我们还表明，亲本来源特异性基因表达模式在不同基因型之间非常相似，并且具有完全双亲表达的基因显示出更高的分子进化率。我们的研究结果提供了昆虫中全基因组基因组印记的最清晰例证，并增强了我们对 PGE 的理解，这将有助于未来对这种不寻常生殖策略起源的进化理论的实证检验。
