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.

中文翻译：

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沉默父亲基因的雄性：完整单倍体基因组的基因组印记


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，在非孟德尔遗传中，父母对其后代的基因构成的贡献并不相同。非孟德尔遗传最非凡的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 下，雄性是二倍体，但仅传递母系遗传的染色体，而父系遗传的同源染色体被排除在精子之外。这种不对称遗传被认为是通过父本和母本基因组之间关于传递给后代的进化军备竞赛而进化而来的。在一些 PGE 进化枝中，例如粉虱（半翅目：假球虫科），父本染色体不仅从精子中消除，而且在发育早期异染色质化并被认为保持不活跃，这可能是由于亲本基因组之间的遗传冲突造成的。在这里，我们提出了雄性粉蚧的亲本等位基因特异性转录组分析，表明表达总体偏向于母体基因组。然而，高达70%的体细胞表达基因在某种程度上是父系表达的，而父系基因组表达在男性生殖道中受到更多限制，只有20%的基因显示出父系贡献。我们还表明，不同基因型的亲本特异性基因表达模式非常相似，并且具有完全双亲表达的基因显示出较高的分子进化速率。 我们的结果提供了昆虫全基因组基因组印记的最清晰例子，并增强了我们对 PGE 的理解，这将有助于未来对有关这种不寻常繁殖策略起源的进化理论进行实证检验。