Department of Ecology and Evolutionary Biology, University of Toronto, Toronto, Canada.
Los Alamos National Laboratory, Los Alamos, New Mexico, United States of America.
PLoS Genet. 2021 Mar 5;17(3):e1009409. doi: 10.1371/journal.pgen.1009409. eCollection 2021 Mar.
When gene regulatory networks diverge between species, their dysfunctional expression in inter-species hybrid individuals can create genetic incompatibilities that generate the developmental defects responsible for intrinsic post-zygotic reproductive isolation. Both cis- and trans-acting regulatory divergence can be hastened by directional selection through adaptation, sexual selection, and inter-sexual conflict, in addition to cryptic evolution under stabilizing selection. Dysfunctional sex-biased gene expression, in particular, may provide an important source of sexually-dimorphic genetic incompatibilities. Here, we characterize and compare male and female/hermaphrodite transcriptome profiles for sibling nematode species Caenorhabditis briggsae and C. nigoni, along with allele-specific expression in their F1 hybrids, to deconvolve features of expression divergence and regulatory dysfunction. Despite evidence of widespread stabilizing selection on gene expression, misexpression of sex-biased genes pervades F1 hybrids of both sexes. This finding implicates greater fragility of male genetic networks to produce dysfunctional organismal phenotypes. Spermatogenesis genes are especially prone to high divergence in both expression and coding sequences, consistent with a "faster male" model for Haldane's rule and elevated sterility of hybrid males. Moreover, underdominant expression pervades male-biased genes compared to female-biased and sex-neutral genes and an excess of cis-trans compensatory regulatory divergence for X-linked genes underscores a "large-X effect" for hybrid male expression dysfunction. Extensive regulatory divergence in sex determination pathway genes likely contributes to demasculinization of XX hybrids. The evolution of genetic incompatibilities due to regulatory versus coding sequence divergence, however, are expected to arise in an uncorrelated fashion. This study identifies important differences between the sexes in how regulatory networks diverge to contribute to sex-biases in how genetic incompatibilities manifest during the speciation process.
当物种间的基因调控网络发生分歧时，它们在种间杂交个体中的功能失调表达可能会产生遗传不兼容性，从而导致内在的合子后生殖隔离的发育缺陷。顺式和反式作用的调节分歧除了在稳定选择下的隐式进化外，还可以通过适应、性选择和雌雄间冲突的定向选择来加速。功能失调的性别偏向基因表达，特别是，可能提供了性异形遗传不兼容性的重要来源。在这里，我们描述并比较了兄弟线虫物种秀丽隐杆线虫和 C. nigoni 的雄性和雌性/雌雄同体的转录组图谱，以及它们的 F1 杂种中的等位基因特异性表达，以剖析表达分歧和调节功能障碍的特征。尽管有证据表明基因表达受到广泛的稳定选择，但性别偏向基因的表达失调在两性 F1 杂种中普遍存在。这一发现表明，雄性遗传网络更容易产生功能失调的个体表型。精子发生基因在表达和编码序列中都特别容易发生高度分歧，这与 Haldane 法则的“更快的雄性”模型以及杂种雄性的高不育性一致。此外，与雌性偏向和性别中性基因相比，雄性偏向基因的显性表达更为普遍，X 连锁基因的顺反式补偿调节分歧过多，突显了杂交雄性表达功能障碍的“大 X 效应”。性别决定途径基因的广泛调节分歧可能导致 XX 杂种的去男性化。然而，由于调节序列与编码序列的分歧而导致遗传不兼容性的进化预计会以不相关的方式发生。本研究确定了性别之间在调节网络分歧方面的重要差异，这些差异有助于在物种形成过程中，遗传不兼容性如何表现出性别偏见。
