Fitness differences between parapatric lake and stream stickleback revealed by a field transplant

Molecular comparisons of populations diverging into ecologically different environments often reveal strong differentiation in localized genomic regions, with the remainder of the genome being weakly differentiated. This pattern of heterogeneous genomic divergence, however, is rarely connected to direct measurements of fitness differences among populations. We here do so by performing a field enclosure experiment in threespine stickleback fish residing in a lake and in three replicate adjoining streams, and displaying weak yet heterogeneous genomic divergence between these habitats. Tracking survival over 29 weeks, we consistently find that lake genotypes transplanted into the streams suffer greatly reduced viability relative to local stream genotypes and that the performance of F1 hybrid genotypes is intermediate. This observed selection against migrants and hybrids combines to a total reduction in gene flow from the lake into streams of around 80%. Overall, our study identifies a strong reproductive barrier between parapatric stickleback populations, and cautions against inferring weak fitness differences between populations exhibiting weak overall genomic differentiation.

针对分化至不同生态环境的种群开展的分子比较研究通常会发现，基因组局部区域存在显著分化，而基因组其余区域的分化程度则较弱。然而，这种异质基因组分化模式，却极少与种群间适合度（fitness）差异的直接测定建立关联。本研究通过对栖息于湖泊与三处重复相邻溪流的三刺棘鱼（threespine stickleback）开展野外围栏实验，实现了这一关联——这些生境中的种群间呈现出微弱却异质的基因组分化特征。通过追踪29周内的存活情况，我们始终观测到：移植至溪流的湖泊种群基因型，相较于本地溪流种群基因型，存活力大幅下降；而F1杂交基因型的适合度表现则处于中间水平。上述针对迁移者与杂交个体的选择作用，共同使得湖泊向溪流的基因流总量降低了约80%。综上，本研究证实了邻域分布的三刺棘鱼种群间存在强烈的生殖隔离屏障，并警示学界：不应仅凭种群整体基因组分化程度较弱，就推断其适合度差异亦较为微小。