Adaptive divergence is the key evolutionary process generating biodiversity by means of natural selection. Yet, the conditions under which it can arise in the presence of gene flow remain contentious. To address this question, we subjected 132 sexually reproducing fission yeast populations, sourced from two independent genetic backgrounds, to disruptive ecological selection and manipulated the level of migration between environments. Contrary to theoretical expectations, adaptive divergence was most pronounced when migration was either absent (allopatry) or maximal (sympatry), but was much reduced at intermediate rates (parapatry and local mating). This effect was apparent across central life-history components (survival, asexual growth and mating) but differed in magnitude between ancestral genetic backgrounds. The evolution of some fitness components was constrained by pervasive negative correlations (trade-off between asexual growth and mating), while others changed direction under the influence of migration (for example, survival and mating). In allopatry, adaptive divergence was mainly conferred by standing genetic variation and resulted in ecological specialization. In sympatry, divergence was mainly mediated by novel mutations enriched in a subset of genes and was characterized by the repeated emergence of two strategies: an ecological generalist and an asexual growth specialist. Multiple loci showed consistent evidence for antagonistic pleiotropy across migration treatments providing a conceptual link between adaptation and divergence. This evolve-and-resequence experiment shows that rapid ecological differentiation can arise even under high rates of gene flow. It further highlights that adaptive trajectories are governed by complex interactions of gene flow, ancestral variation and genetic correlations.

适应性分歧是通过自然选择产生生物多样性的关键进化过程。然而，在基因流动存在的情况下它可以出现的条件仍然存在争议。为了解决这个问题，我们对来自两个独立遗传背景的 132 个有性繁殖的裂殖酵母种群进行了破坏性生态选择，并控制了环境之间的迁移水平。与理论预期相反，当迁移不存在（同源迁移）或最大迁移（同源迁移）时，适应性差异最为明显，但在中间速率（同源迁移和本地交配）下会大大降低。这种影响在主要生活史组成部分（生存、无性生长和交配）中很明显，但在祖先遗传背景之间的幅度不同。一些适应度成分的进化受到普遍负相关（无性生长和交配之间的权衡）的限制，而其他适应性成分的进化则在迁移的影响下改变了方向（例如，生存和交配）。在异域分布中，适应性分化主要由遗传变异赋予，并导致生态专业化。在同情中，分歧主要是由基因子集中富集的新突变介导的，其特征是两种策略的反复出现：生态通才和无性生长专家。多个基因座显示了跨迁移处理的拮抗多效性的一致证据，提供了适应和分歧之间的概念联系。这个进化和重测序实验表明，即使在高基因流动率下，也可以出现快速的生态分化。它进一步强调适应性轨迹受基因流、祖先变异和遗传相关性的复杂相互作用的控制。