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，拥有抗干燥卵，可进入发育停滞的滞育（diapause）阶段，从而得以渡过原本不宜生存的旱季。那些潜在预示季节变化的环境信号，可调控鱼卵在发育中途进入滞育阶段，或是跳过该滞育过程直接发育。本研究基于鳉形目（Cyprinodontiformes）超级矩阵系统发育树的构建与一系列比较分析，证实产滞育卵的能力至少在非洲和南美洲的鳉鱼中独立演化了六次。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，进入滞育的胚胎的头部与循环系统发育显著受限。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，此时恰好处于被认为发育约束最强的阶段——胚型期（phylotypic period）。最后，我们发现进入滞育的胚胎伴随代谢率的显著下降，同时长期胚胎存活率也随之提升。因此，在胚型期发生的形态分化，可使进入滞育的胚胎通过将资源从能量消耗高昂的器官中转移出去，从而节省能量，进而在需要全年大部分时间以休眠状态埋于土壤、被卵壳包裹的环境中，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，从而在脊椎动物原本保守的发育阶段中催生了显著的演化分化。