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境的一年生鳉鱼，其卵具备抗脱水能力，可进入发育停滞的滞育（diapause）阶段，以此得以渡过原本难以生存的旱季。能够预示季节变化的环境信号，可调控鱼卵是在发育中途进入滞育阶段，还是跳过该滞育过程转而进行直接发育。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，发现产滞育卵的能力在非洲和南美洲鳉鱼中至少独立演化了六次。我们进一步以这些演化支的代表性物种为研究对象，结果显示：与进行直接发育的胚胎相比，进入滞育的胚胎其颅区与循环系统的发育显著受限。这种沿不同发育路径的分化始于发育中途，远早于滞育的启动阶段，正处于所谓发育约束最强的时期——系统发生保守期（phylotypic period）。最后我们发现，进入滞育状态会伴随代谢速率的急剧下降，同时胚胎的长期存活率显著提升。因此，在系统发生保守期出现的形态分化，可使进入滞育的胚胎通过将资源从高能耗器官中调配出来以节约能量，从而在全年多数时间都需以休眠状态埋藏于土壤中、被卵壳包裹的严酷环境中，提升自身存活概率。我们的研究结果表明，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，进而在脊椎动物发育本应高度保守的这一时期，催生了显著的演化分化。