Shifting habitats, morphology and selective pressures: developmental polyphenism in an adaptive radiation of Hawaiian spiders

Particularly intriguing examples of adaptive radiation are those in which lineages show parallel or convergent evolution, suggesting utilization of similar genetic or developmental pathways. The current study focuses on an adaptive radiation of Hawaiian “spiny-leg” spiders in which diversification is associated with repeated convergent evolution leading to similar sets of ecomorphs on each island. However, two species on the oldest islands in the archipelago exhibit variability, occurring as two different ecomorphs. More derived species on the younger islands show much less variability, any one species displaying a single ecomorph. We measured ecomorphological features within individuals over time to determine the nature of the variability. Then, using transcriptomes, we conducted lineage-based tests for selection under varying models and analyses of gene tree versus species tree incongruencies. Our results provide strong evidence that variability in color in Tetragnatha kauaiensis and T. polychromata is associated with development within individuals (polyphenism). Moreover, a total of 28 loci showed a signature of selection associated with loss of the color-changing phenotype, and 37 loci showed a signature of selection associated with the colonization of a new environment. The results illustrate how developmental polyphenism might provide an avenue for the repeated evolution of ecomorphs during adaptive radiation.

适应性辐射（adaptive radiation）中尤为引人关注的案例，是那些演化谱系呈现平行或趋同演化的类群，这表明它们借助了相似的遗传或发育通路。本研究聚焦于夏威夷“棘足”蜘蛛的一次适应性辐射事件，其物种分化与反复的趋同演化相关，最终在每个岛屿上形成了相似的生态形态型（ecomorphs）集合。不过，该群岛最古老岛屿上的两个物种存在表型变异，可呈现两种不同的生态形态型。而分布于更年轻岛屿的衍生物种，其表型变异程度显著更低，单一物种仅呈现单一生态形态型。我们通过对个体的生态形态特征开展历时性测量，以明确该变异的本质。随后，我们借助转录组（transcriptomes）开展了基于谱系的选择检验，涵盖多种演化模型，并分析了基因树与物种树的不一致性。研究结果为考艾岛长脚蛛（Tetragnatha kauaiensis）和多色长脚蛛（T. polychromata）的体色变异与个体发育过程中的表型多态性（polyphenism）相关这一结论，提供了强有力的证据。此外，共计28个基因位点呈现出与体色变化表型丢失相关的选择信号，另有37个基因位点呈现出与新环境定殖相关的选择信号。本研究结果阐明了发育表型多态性如何为适应性辐射过程中生态形态型的反复演化提供可行路径。