Contrasting environmental drivers of genetic of genetic and phenotypic divergence in an Andean poison frog

Phenotypic and genetic divergence are shaped by the homogenizing effects
of gene flow and the differentiating processes of genetic drift and local
adaptation. Herein, we examined the mechanisms that underlie phenotypic
(size and color) and genetic divergence in 35 populations (535
individuals) of the poison frog Epipedobates anthonyi along four
elevational gradients (0–1800 m asl) in the Ecuadorian Andes. We found
phenotypic divergence in size and color despite relatively low genetic
divergence at neutral microsatellite loci. Genetic and phenotypic
divergence were both explained by landscape resistance between sites
(isolation-by-resistance, IBR), likely due to a cold and dry mountain
ridge between the northern and southern elevational transects that limits
dispersal and separates two color morphs. Moreover, environmental
differences among sites also explained genetic and phenotypic divergence,
suggesting isolation-by-environment (IBE). When northern and southern
transects were analyzed separately, genetic divergence was predicted
either by distance (isolation-by-distance, IBD; northern) or environmental
resistance between sites (IBR; southern). In contrast, phenotypic
divergence was primarily explained by environmental differences among
sites, supporting the IBE hypothesis. These results indicate that although
distance and geographic barriers are important drivers of population
divergence, environmental variation has a two-fold effect on population
divergence. On the one hand, landscape resistance between sites reduces
gene flow (IBR), while on the other hand, environmental differences among
sites exert divergent selective pressures on phenotypic traits (IBE). Our
work highlights the importance of studying both genetic and phenotypic
divergence to better understand the processes of population divergence and
speciation along ecological gradients.

表型分化（phenotypic divergence）与遗传分化（genetic divergence）的形成，受制于基因流（gene flow）的同质化效应，以及遗传漂变（genetic drift）与局部适应（local adaptation）的分化性过程。本研究针对厄瓜多尔安第斯山脉沿4条海拔梯度（0–1800米海拔，asl）的35个种群（共535个个体）的安东尼箭毒蛙（Epipedobates anthonyi），探究其表型（体型与体色）及遗传分化的潜在机制。研究发现，尽管中性微卫星位点（microsatellite loci）的遗传分化程度较低，但种群在体型与体色上仍存在显著表型分化。遗传与表型分化均可用种群间的景观阻力（landscape resistance）解释，即阻力隔离（isolation-by-resistance, IBR），这可能缘于南北海拔样带间寒冷干燥的山脊限制了扩散，并分隔了两种体色形态。此外，种群间的环境差异同样可解释遗传与表型分化，提示存在环境隔离（isolation-by-environment, IBE）现象。当分别分析南北样带时，遗传分化分别由地理距离预测，即距离隔离（isolation-by-distance, IBD，北部样带），或由种群间的环境阻力（IBR，南部样带）预测。与之相对，表型分化主要由种群间的环境差异所解释，这支持了环境隔离（IBE）假说。上述结果表明，尽管地理距离与地理屏障是种群分化的重要驱动因素，但环境变异对种群分化具有双重作用：一方面，种群间的景观阻力会降低基因流，即阻力隔离（IBR）；另一方面，种群间的环境差异会对表型性状施加差异化的选择压力，即环境隔离（IBE）。本研究强调，同时探究遗传与表型分化，有助于更深入地理解生态梯度下种群分化与物种形成的过程。