Data from: Comparative developmental transcriptomics reveals rewiring of a highly conserved gene regulatory network during a major life history switch in the sea urchin genus Heliocidaris

The ecologically significant shift in developmental strategy from planktotrophic (feeding) to lecithotrophic (nonfeeding) development in the sea urchin genus Heliocidaris is one of the most comprehensively studied life history transitions in any animal. Although the evolution of lecithotrophy involved substantial changes to larval development and morphology, it is not known to what extent changes in gene expression underlie the developmental differences between species, nor do we understand how these changes evolved within the context of the well-defined gene regulatory network (GRN) underlying sea urchin development. To address these questions, we used RNA-seq to measure expression dynamics across development in three species: the lecithotroph Heliocidaris erythrogramma, the closely related planktotroph H. tuberculata, and an outgroup planktotroph Lytechinus variegatus. Using well-established statistical methods, we developed a novel framework for identifying, quantifying, and polarizing evolutionary changes in gene expression profiles across the transcriptome and within the GRN. We found that major changes in gene expression profiles were more numerous during the evolution of lecithotrophy than during the persistence of planktotrophy, and that genes with derived expression profiles in the lecithotroph displayed specific characteristics as a group that are consistent with the dramatically altered developmental program in this species. Compared to the transcriptome, changes in gene expression profiles within the GRN were even more pronounced in the lecithotroph. We found evidence for conservation and likely divergence of particular GRN regulatory interactions in the lecithotroph, as well as significant changes in the expression of genes with known roles in larval skeletogenesis. We further use coexpression analysis to identify genes of unknown function that may contribute to both conserved and derived developmental traits between species. Collectively, our results indicate that distinct evolutionary processes operate on gene expression during periods of life history conservation and periods of life history divergence, and that this contrast is even more pronounced within the GRN than across the transcriptome as a whole.

海胆属（Heliocidaris）中，发育策略从浮游营养型（planktotrophic，即摄食型）向卵黄营养型（lecithotrophic，即非摄食型）的生态意义重大转变，是所有动物类群中研究最为全面的生活史转变事件之一。尽管卵黄营养型的演化涉及幼虫发育与形态的显著改变，但目前尚不清楚基因表达变化在多大程度上构成了物种间发育差异的分子基础，同时我们也未能明晰这些变化是如何在海胆发育所依托的明确基因调控网络（gene regulatory network, GRN）框架下演化的。为解答这些问题，我们采用RNA测序（RNA-seq）技术，对三个物种的全发育阶段基因表达动态进行了检测：卵黄营养型物种红海胆（Heliocidaris erythrogramma）、与其亲缘关系紧密的浮游营养型物种H. tuberculata，以及外类群浮游营养型物种杂色海胆（Lytechinus variegatus）。借助成熟的统计学分析方法，我们构建了一套全新的分析框架，用于识别、量化并明确转录组（transcriptome）及基因调控网络内基因表达谱的演化变化方向。研究发现，卵黄营养型演化过程中基因表达谱的重大变化数量，远多于浮游营养型物种维持保守发育的过程；同时，卵黄营养型物种中具有衍生表达谱的基因，作为一个整体展现出特定特征，与该物种大幅改写的发育程序相一致。与整个转录组相比，基因调控网络内部的基因表达谱变化在卵黄营养型物种中表现得更为显著。我们在卵黄营养型物种中检测到了特定基因调控网络调控交互作用的保守性与潜在分化的证据，同时也发现了已知参与幼虫骨骼发生的基因的表达发生了显著改变。我们进一步通过共表达分析，筛选出了一批功能未知的基因，这些基因可能参与了物种间保守与衍生的发育性状的形成。综上，本研究结果表明，在生活史保守与生活史分化的不同时期，存在不同的演化过程作用于基因表达，且这种差异在基因调控网络内比在整个转录组水平上更为突出。