Department of Biology, University of North Carolina at Chapel Hill, Chapel Hill, North Carolina, United States of America.
Department of Integrative Biology and Museum of Vertebrate Zoology, University of California, Berkeley, California, United States of America.
PLoS One. 2019 Jul 10;14(7):e0218899. doi: 10.1371/journal.pone.0218899. eCollection 2019.
Genetic incompatibilities constitute the final stages of reproductive isolation and speciation, but little is known about incompatibilities that occur within recent adaptive radiations among closely related diverging populations. Crossing divergent species to form hybrids can break up coadapted variation, resulting in genetic incompatibilities within developmental networks shaping divergent adaptive traits. We crossed two closely related sympatric Cyprinodon pupfish species-a dietary generalist and a specialized molluscivore-and measured expression levels in their F1 hybrids to identify regulatory variation underlying the novel craniofacial morphology found in this recent microendemic adaptive radiation. We extracted mRNA from eight day old whole-larvae tissue and from craniofacial tissues dissected from 17-20 day old larvae to compare gene expression between a total of seven F1 hybrids and 24 individuals from parental species populations. We found 3.9% of genes differentially expressed between generalists and molluscivores in whole-larvae tissues and 0.6% of genes differentially expressed in craniofacial tissue. We found that 2.1% of genes were misregulated in whole-larvae hybrids whereas 19.1% of genes were misregulated in hybrid craniofacial tissues, after correcting for sequencing biases. We also measured allele specific expression across 15,429 heterozygous sites to identify putative compensatory regulatory mechanisms underlying differential expression between generalists and molluscivores. Together, our results highlight the importance of considering misregulation as an early indicator of genetic incompatibilities in the context of rapidly diverging adaptive radiations and suggests that compensatory regulatory divergence drives hybrid gene misregulation in developing tissues that give rise to novel craniofacial traits.
遗传不兼容性构成了生殖隔离和物种形成的最后阶段，但对于在密切相关的分化群体中最近的适应性辐射内发生的不兼容性知之甚少。杂交分歧物种形成杂种可以打破共适应的变异，导致塑造分歧适应性特征的发育网络内的遗传不兼容性。我们将两个密切相关的共生 Cyprinodon 小鱼种——一种饮食广泛的杂食性物种和一种专门的食贝类物种——进行杂交，测量它们的 F1 杂种中的表达水平，以确定在这个最近的微地方性适应性辐射中发现的新颅面形态背后的调节变异。我们从 8 天大的整个幼虫组织和从 17-20 天大的幼虫解剖的颅面组织中提取 mRNA，以比较总共 7 个 F1 杂种和来自亲本物种群体的 24 个个体之间的基因表达。我们发现，在整个幼虫组织中，杂食性和食贝类之间差异表达的基因有 3.9%，而在颅面组织中差异表达的基因有 0.6%。我们发现，在整个幼虫杂种中，有 2.1%的基因被错误调控，而在杂种颅面组织中，有 19.1%的基因被错误调控，这是在纠正测序偏差后得出的结果。我们还在 15429 个杂合位点上测量了等位基因特异性表达，以鉴定在杂食性和食贝类之间差异表达的潜在补偿调节机制。总的来说，我们的研究结果强调了在快速分化的适应性辐射背景下，将错误调控视为遗传不兼容性的早期指标的重要性，并表明补偿性调节分歧导致了发育组织中杂种基因的错误调控，从而产生了新的颅面特征。
