Contemporary ecotypic divergence during a recent range expansion was facilitated by adaptive introgression

Although rapid phenotypic evolution during range expansion associated with colonization of contrasting habitats has been documented in several taxa, the evolutionary mechanisms that underlie such phenotypic divergence have less often been investigated. A strong candidate for rapid ecotype formation within an invaded range is the three-spine stickleback in the Lake Geneva region of central Europe. Since its introduction only about 140 years ago, it has undergone a significant expansion of its range and its niche, now forming phenotypically differentiated parapatric ecotypes that occupy either the pelagic zone of the large lake or small inlet streams, respectively. By comparing museum collections from different times with contemporary population samples, we here reconstruct the evolution of parapatric phenotypic divergence through time. Using genetic data from modern samples, we infer the underlying invasion history. We find that parapatric habitat-dependent phenotypic divergence between the lake and stream was already present in the first half of the twentieth century, but the magnitude of differentiation increased through time, particularly in antipredator defence traits. This suggests that divergent selection between the habitats occurred and was stable through much of the time since colonization. Recently, increased phenotypic differentiation in antipredator defence traits likely results from habitat-dependent selection on alleles that arrived through introgression from a distantly related lineage from outside the Lake Geneva region. This illustrates how hybridization can quickly promote phenotypic divergence in a system where adaptation from standing genetic variation was constrained.

尽管已有多个分类群被报道在与异质生境定殖相关的范围扩张过程中发生快速表型进化，但这类表型分化背后的演化机制却较少得到深入研究。在入侵范围内快速形成生态型的典型候选类群，便是中欧日内瓦湖区域的三刺棘鱼（three-spine stickleback）。自约140年前被引入以来，该物种的分布范围与生态位均发生了显著扩张，目前已形成表型分化的邻域生态型（parapatric ecotypes），分别栖息于大型湖泊的远洋带与小型入湖水道中。本研究通过对比不同时期的馆藏标本与当代种群样本，重建了邻域表型分化随时间的演化历程；并借助现代样本的遗传数据，推断了其入侵历史。研究发现，早在20世纪上半叶，湖泊与溪流生境间已存在依生境分化的邻域表型差异，但分化程度随时间推移不断提升，尤以反捕食防御性状（antipredator defence traits）为甚。这表明自定殖以来的大部分时间里，不同生境间存在歧化选择且相对稳定。近期反捕食防御性状的表型分化加剧，可能源于日内瓦湖区域外的远缘类群通过渐渗（introgression）引入的等位基因在不同生境下受到依生境选择作用。本研究揭示了在依赖现存遗传变异（standing genetic variation）的适应过程受到约束的系统中，杂交如何快速促进表型分化。