Gene Regulatory Evolution in Cold-Adapted Fly Populations Neutralizes Plasticity and May Undermine Genetic Canalization

Gene Regulatory Evolution in Cold-Adapted Fly Populations Neutralizes Plasticity and May Undermine Genetic Canalization
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DOI:
10.1093/gbe/evac050
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发表时间:
2022-04-19
影响因子:
3.3
通讯作者:
Pool, John E.
Pool, John E.
中科院分区:
生物学2区
文献类型:
--
作者:
Huang, Yuheng;Lack, Justin B.;Pool, John E.

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适应性进化、表型可塑性和管道化之间的关系仍然不完全清楚。关于适应性进化是否会增强或反对塑性反应,理论和实证研究提出了相互矛盾的观点。基因调控性状为研究可塑性和适应性之间的关系提供了极好的潜力,它们现在可以在转录组水平上进行研究。在这里,我们利用了三对密切相关的黑腹果蝇自然种群,它们来自不同的热环境,反映了三个不同的耐寒性进化实例。我们测量了在温暖和寒冷的实验室环境中基因表达水平和选择性剪接(内含子使用)的转录组范围内的可塑性。我们发现基因表达和选择性剪接的可疑适应性变化倾向于中和祖先的塑性反应。此外,我们研究了适应性进化可以导致选择的基因调控性状去管化的假设。我们发现强有力的证据表明,在冷适应种群中,疑似适应性基因表达(而不是剪接)的变化比假定的中性变化更容易受到近亲繁殖的遗传扰动。我们发现一些证据表明,这些模式可能反映了伴随适应的遗传通道化的丧失,尽管其他过程包括搭便车隐性有害变异也可能起作用。我们的发现增强了我们对适应性进化背景下基因调控的遗传和环境影响的理解。
The relationships between adaptive evolution, phenotypic plasticity, and canalization remain incompletely understood. Theoretical and empirical studies have made conflicting arguments on whether adaptive evolution may enhance or oppose the plastic response. Gene regulatory traits offer excellent potential to study the relationship between plasticity and adaptation, and they can now be studied at the transcriptomic level. Here, we take advantage of three closely related pairs of natural populations of Drosophila melanogaster from contrasting thermal environments that reflect three separate instances of cold tolerance evolution. We measure the transcriptome-wide plasticity in gene expression levels and alternative splicing (intron usage) between warm and cold laboratory environments. We find that suspected adaptive changes in both gene expression and alternative splicing tend to neutralize the ancestral plastic response. Further, we investigate the hypothesis that adaptive evolution can lead to decanalization of selected gene regulatory traits. We find strong evidence that suspected adaptive gene expression (but not splicing) changes in cold-adapted populations are more vulnerable to the genetic perturbation of inbreeding than putatively neutral changes. We find some evidence that these patterns may reflect a loss of genetic canalization accompanying adaptation, although other processes including hitchhiking recessive deleterious variants may contribute as well. Our findings augment our understanding of genetic and environmental effects on gene regulation in the context of adaptive evolution.