Graduate School of Natural Science and Technology, Okayama University, Kita-ku, Okayama, Okayama, Japan.
Institute of Environmental Toxicology, Joso, Ibaraki, Japan.
J Hered. 2019 Mar 5;110(2):183-193. doi: 10.1093/jhered/esy060.
Although organisms belonging to different species and subspecies sometimes produce fertile offspring, a hallmark of the speciation process is reproductive isolation, characterized by hybrid sterility (HS) due to failure in gametogenesis. In mammals, HS is usually exhibited by males, the heterogametic sex. The phenotypic manifestations of HS are complex. The most frequently observed are abnormalities in both autosomal and sex chromosome interactions that are linked to meiotic prophase arrest or postmeiotic spermiogenesis aberrations and lead to defective or absent gametes. The aim of this study was to determine the HS phenotypes in intersubspecific F1 mice produced by matings between Mus musculus molossinus-derived strains and diverse Mus musculus domesticus-inbred laboratory mouse strains. Most of these crosses produced fertile F1 offspring. However, when female BALB/cJ (domesticus) mice were mated to male JF1/MsJ (molossinus) mice, the (BALBdomxJF1mol)F1 males were sterile, whereas the (JF1molxBALBdom)F1 males produced by the reciprocal crossings were fertile; thus the sterility phenotype was asymmetric. The sterile (BALBdomxJF1mol) F1 males exhibited a high rate of meiotic metaphase arrest with misaligned chromosomes, probably related to a high frequency of XY dissociation. Intriguingly, in the sterile (BALBdomxJF1mol)F1 males we observed aberrant allele-specific expression of several meiotic genes, that play critical roles in important meiotic events including chromosome pairing. Together, these observations of an asymmetrical HS phenotype in intersubspecific F1 males, probably owing to meiotic defects in the meiotic behavior of the XY chromosomes pair and possibly also transcriptional misregulation of meiotic genes, provide new models and directions for understanding speciation mechanisms in mammals.
尽管属于不同物种和亚种的生物体有时会产生可育后代，但物种形成过程的一个标志是生殖隔离，其特征是杂种不育（HS），这是由于配子发生失败导致的。在哺乳动物中，HS 通常由雄性表现出来，雄性是异型配子性别。HS 的表型表现是复杂的。最常观察到的是常染色体和性染色体相互作用的异常，这些异常与减数分裂前期阻滞或减数分裂后精子发生异常有关，并导致配子缺陷或缺失。本研究的目的是确定由来自 Mus musculus molossinus 衍生的品系与不同的 Mus musculus domesticus 近交实验室小鼠品系杂交产生的亚物种 F1 小鼠中的 HS 表型。这些杂交大多数产生了可育的 F1 后代。然而，当雌性 BALB/cJ（domesticus）小鼠与雄性 JF1/MsJ（molossinus）小鼠交配时，（BALBdomxJF1mol）F1 雄性是不育的，而由相反交配产生的（JF1molxBALBdom）F1 雄性是可育的；因此，不育表型是不对称的。不育的（BALBdomxJF1mol）F1 雄性表现出高比例的中期减数分裂停滞，染色体排列不齐，可能与 XY 分离的高频率有关。有趣的是，在不育的（BALBdomxJF1mol）F1 雄性中，我们观察到几个减数基因的等位基因特异性表达异常，这些基因在包括染色体配对在内的重要减数事件中起着关键作用。总的来说，这些观察结果表明，亚物种 F1 雄性中的不对称 HS 表型可能是由于 XY 染色体对的减数行为缺陷以及减数基因的转录失调引起的，为理解哺乳动物的物种形成机制提供了新的模型和方向。
