Data from: Convergent evolution of alternative developmental trajectories associated with diapause in African and South American killifish

Annual killifish adapted to life in seasonally ephemeral water-bodies exhibit desiccation resistant eggs that can undergo diapause, a period of developmental arrest, enabling them to traverse the otherwise inhospitable dry season. Environmental cues that potentially indicate the season can govern whether eggs enter a stage of diapause mid-way through development or skip this diapause and instead undergo direct development. We report, based on construction of a supermatrix phylogenetic tree of the order Cyprinodontiformes and a battery of comparative analyses, that the ability to produce diapause eggs evolved independently at least six times within African and South American killifish. We then show in species representative of these lineages that embryos entering diapause display significant reduction in development of the cranial region and circulatory system relative to direct-developing embryos. This divergence along alternative developmental pathways begins mid-way through development, well before diapause is entered, during a period of purported maximum developmental constraint (the phylotypic period). Finally, we show that entering diapause is accompanied by a dramatic reduction in metabolic rate and concomitant increase in long-term embryo survival. Morphological divergence during the phylotypic period thus allows embryos undergoing diapause to conserve energy by shunting resources away from energetically costly organs thereby increasing survival chances in an environment that necessitates remaining dormant, buried in the soil and surrounded by an eggshell for much of the year. Our results indicate that adaptation to seasonal aquatic environments in annual killifish imposes strong selection during the embryo stage leading to marked diversification during this otherwise conserved period of vertebrate development.

适应于季节性临时水体生存的一年生鳉鱼，其卵具备抗脱水特性，可进入发育停滞的滞育（diapause）阶段，从而得以渡过原本无法生存的旱季。可预示季节变化的环境信号，能够调控胚胎在发育中途进入滞育阶段，或是跳过该过程直接完成发育。本研究通过构建鳉形目（Cyprinodontiformes）的超级矩阵系统发育树，并开展一系列比较分析，证实产滞育卵的能力在非洲与南美洲的鳉鱼类群中独立演化了至少六次。随后，我们以这些演化支的代表性物种为研究对象，发现相较于直接发育的胚胎，进入滞育的胚胎的颅区与循环系统发育显著受到抑制。这两种发育路径的分化始于发育中期——远早于滞育启动之时——正值被认为是发育约束最强的系统发生型时期（phylotypic period）。最后，我们证实进入滞育会伴随代谢速率的大幅降低，同时胚胎的长期存活率显著提升。由此可见，在系统发生型时期发生的形态分化，可使进入滞育的胚胎将资源从高能耗器官转移，从而节约能量，进而在全年多数时间都需以卵壳包裹、埋于土壤中处于休眠状态的环境中，提升存活概率。本研究结果表明，一年生鳉鱼对季节性水生环境的适应，会在胚胎阶段施加强烈的选择压力，从而在脊椎动物发育本应高度保守的这一时期，引发显著的演化分化。