Department of Plant and Microbial Biology, University of California, Berkeley, Berkeley, CA 94720, USA.
Graduate Program in the Biology of Aging, University of Southern California, Los Angeles, CA 90095, USA.
G3 (Bethesda). 2021 Jul 14;11(7). doi: 10.1093/g3journal/jkab139.
Many familiar traits in the natural world-from lions' manes to the longevity of bristlecone pine trees-arose in the distant past, and have long since fixed in their respective species. A key challenge in evolutionary genetics is to figure out how and why species-defining traits have come to be. We used the thermotolerance growth advantage of the yeast Saccharomyces cerevisiae over its sister species Saccharomyces paradoxus as a model for addressing these questions. Analyzing loci at which the S. cerevisiae allele promotes thermotolerance, we detected robust evidence for positive selection, including amino acid divergence between the species and conservation within S. cerevisiae populations. Because such signatures were particularly strong at the chromosome segregation gene ESP1, we used this locus as a case study for focused mechanistic follow-up. Experiments revealed that, in culture at high temperature, the S. paradoxus ESP1 allele conferred a qualitative defect in biomass accumulation and cell division relative to the S. cerevisiae allele. Only genetic divergence in the ESP1 coding region mattered phenotypically, with no functional impact detectable from the promoter. Our data support a model in which an ancient ancestor of S. cerevisiae, under selection to boost viability at high temperature, acquired amino acid variants at ESP1 and many other loci, which have been constrained since then. Complex adaptations of this type hold promise as a paradigm for interspecies genetics, especially in deeply diverged traits that may have taken millions of years to evolve.
自然界中有许多熟悉的特征——从狮子的鬃毛到扁柏的长寿——都起源于遥远的过去，并且早已在各自的物种中固定下来。进化遗传学的一个关键挑战是弄清楚物种定义特征是如何以及为什么出现的。我们使用酵母酿酒酵母相对于其姊妹种酿酒酵母的耐热性生长优势作为模型来解决这些问题。分析 S. cerevisiae 等位基因促进耐热性的基因座，我们检测到了强烈的正选择证据，包括物种之间的氨基酸差异和 S. cerevisiae 群体内的保守性。由于在染色体分离基因 ESP1 处的这些特征特别强，因此我们将该基因座作为重点机制后续研究的案例研究。实验表明，在高温培养物中，与 S. cerevisiae 等位基因相比，S. paradoxus 的 ESP1 等位基因在生物量积累和细胞分裂方面表现出定性缺陷。只有 ESP1 编码区的遗传差异在表型上起作用，从启动子中无法检测到任何功能影响。我们的数据支持这样一种模型，即在 S. cerevisiae 的一个古老祖先中，为了在高温下提高生存能力而受到选择，在 ESP1 和许多其他基因座中获得了氨基酸变体，此后这些变体一直受到限制。这种复杂的适应性为种间遗传学提供了一个范例，尤其是对于可能需要数百万年才能进化的深度分化特征。
