Department of Ecology and Evolutionary Biology, University of Toronto, Toronto, Canada.
Department of Plant Pathology, Washington State University, Pullman, Washington, USA.
Proc Biol Sci. 2021 Jan 13;288(1942):20202483. doi: 10.1098/rspb.2020.2483.
Evolutionary biologists typically envision a trait's genetic basis and fitness effects occurring within a single species. However, traits can be determined by and have fitness consequences for interacting species, thus evolving in multiple genomes. This is especially likely in mutualisms, where species exchange fitness benefits and can associate over long periods of time. Partners may experience evolutionary conflict over the value of a multi-genomic trait, but such conflicts may be ameliorated by mutualism's positive fitness feedbacks. Here, we develop a simulation model of a host-microbe mutualism to explore the evolution of a multi-genomic trait. Coevolutionary outcomes depend on whether hosts and microbes have similar or different optimal trait values, strengths of selection and fitness feedbacks. We show that genome-wide association studies can map joint traits to loci in multiple genomes and describe how fitness conflict and fitness feedback generate different multi-genomic architectures with distinct signals around segregating loci. Partner fitnesses can be positively correlated even when partners are in conflict over the value of a multi-genomic trait, and conflict can generate strong mutualistic dependency. While fitness alignment facilitates rapid adaptation to a new optimum, conflict maintains genetic variation and evolvability, with implications for applied microbiome science.
进化生物学家通常设想一个特征的遗传基础和适合度效应发生在一个单一的物种内。然而，特征可以由相互作用的物种决定，并对其适合度产生影响，因此在多个基因组中进化。这在互惠关系中尤其可能，在这种关系中，物种之间相互交换适合度利益，并可以在很长一段时间内相互关联。合作伙伴可能会对多基因组特征的价值产生进化冲突，但这种冲突可以通过互惠的积极适合度反馈得到缓解。在这里，我们开发了一个宿主-微生物互惠关系的模拟模型，以探索多基因组特征的进化。共同进化的结果取决于宿主和微生物是否具有相似或不同的最佳特征值、选择强度和适合度反馈。我们表明，全基因组关联研究可以将共同特征映射到多个基因组中的基因座上，并描述适应度冲突和适应度反馈如何产生不同的多基因组结构，在分离的基因座周围具有不同的信号。即使合作伙伴在多基因组特征的价值上存在冲突，合作伙伴的适应度也可以呈正相关，而冲突可以产生强烈的互利依赖。虽然适应度一致有助于快速适应新的最优状态，但冲突会保持遗传变异和可进化性，这对应用微生物组科学具有重要意义。
