Marshall Hollie, de la Filia Andrés G, Cavalieri Ross, Mallon Eamonn B, Clark John M, Ross Laura
School of Biological Sciences, Institute of Evolutionary Biology, The University of Edinburgh, Edinburgh, United Kingdom.
The Department of Genetics and Genome Biology, University of Leicester, Leicester, United Kingdom.
Evol Lett. 2024 Feb 6;8(3):455-465. doi: 10.1093/evlett/qrae003. eCollection 2024 Jun.
Paternal genome elimination (PGE) is a non-Mendelian inheritance system, described in numerous arthropod species, in which males develop from fertilized eggs, but their paternally inherited chromosomes are eliminated before or during spermatogenesis. Therefore, PGE males only transmit their maternally inherited set of chromosomes to their offspring. In addition to the elimination of paternal chromosomes, diverse PGE species have also repeatedly evolved the transcriptional silencing of the paternal genome, making males effectively haploid. However, it is unclear if this paternal chromosome silencing is mechanistically linked to the chromosome elimination or has evolved at a later stage, and if so, what drives the haploidization of males under PGE. In order to understand these questions, here we study the human louse, , which represents an ideal model system, as it appears to be the only instance of PGE where males eliminate, but not silence their paternal chromosomes, although the latter remains to be shown conclusively. In this study, we analyzed parent-of-origin allele-specific expression patterns in male offspring of crosses between head and body lice ecotypes. We show that hybrid adult males of display biparental gene expression, which constitutes the first case of a species with PGE in which genetic activity of paternal chromosomes in the soma is not affected by embryonic silencing or (partial or complete) elimination. We did however also identify a small number of maternally biased genes (potentially imprinted genes), which may be involved in the elimination of paternal chromosomes during spermatogenesis. Finally, we have identified genes that show ecotype-specific expression bias. Given the low genetic diversity between ecotypes, this is suggestive for a role of epigenetic processes in ecotype differences.
父本基因组消除(PGE)是一种非孟德尔遗传系统,在众多节肢动物物种中都有描述。在该系统中,雄性由受精卵发育而来,但其父本遗传的染色体在精子发生之前或过程中被消除。因此,PGE雄性仅将其母本遗传的染色体组传递给后代。除了消除父本染色体外,多种PGE物种还多次进化出父本基因组的转录沉默,使雄性有效地成为单倍体。然而,目前尚不清楚这种父本染色体沉默在机制上是否与染色体消除相关,或者是否在后期进化而来,如果是这样,是什么驱动了PGE下雄性的单倍体化。为了理解这些问题,我们在此研究了人类虱子,它代表了一个理想的模型系统,因为它似乎是PGE的唯一实例,即雄性消除但不沉默其父本染色体,尽管这一点还有待最终证实。在本研究中,我们分析了头虱和体虱生态型杂交后代雄性中的亲本等位基因特异性表达模式。我们发现杂交成年雄性表现出双亲基因表达,这构成了具有PGE的物种中的首例,即体细胞中父本染色体的遗传活性不受胚胎沉默或(部分或完全)消除的影响。然而,我们确实也鉴定出了少数母本偏向基因(可能是印记基因),它们可能参与精子发生过程中父本染色体的消除。最后,我们鉴定出了表现出生态型特异性表达偏向的基因。鉴于生态型之间的遗传多样性较低,这表明表观遗传过程在生态型差异中发挥了作用。