Data from: Species selection favors dispersive life histories in sea slugs, but higher per-offspring investment drives shifts to short-lived larvae

For 40 years, paleontological studies of marine gastropods have suggested that species selection favors lineages with short-lived (lecithotrophic) larvae, which are less dispersive than long-lived (planktotrophic) larvae. Although lecithotrophs appeared to speciate more often and accumulate over time in some groups, lecithotrophy also increased extinction rates, and tests for state-dependent diversification were never performed. Molecular phylogenies of diverse groups instead suggested lecithotrophs accumulate without diversifying due to frequent, unidirectional character change. Although lecithotrophy has repeatedly originated in most phyla, no adult trait has been correlated with shifts in larval type. Thus, both the evolutionary origins of lecithotrophy and its consequences for patterns of species richness remain poorly understood. Here, we test hypothesized links between development mode and evolutionary rates using likelihood-based methods and a phylogeny of 202 species of gastropod molluscs in Sacoglossa, a clade of herbivorous sea slugs. Evolutionary quantitative genetics modeling and stochastic character mapping supported 27 origins of lecithotrophy. Tests for correlated evolution revealed lecithotrophy evolved more often in lineages investing in extra-embryonic yolk, the first adult trait associated with shifts in development mode across a group. However, contrary to predictions from paleontological studies, species selection actually favored planktotrophy; most extant lecithotrophs originated through recent character change, and did not subsequently diversify. Increased offspring provisioning in planktotrophs thus favored shifts to short-lived larvae, which led to short-lived lineages over macroevolutionary time scales. These findings challenge long-standing assumptions about the effects of alternative life histories in the sea. Species selection can explain the long-term persistence of planktotrophy, the ancestral state in most clades, despite frequent transitions to lecithotrophy.四十年来，海洋腹足类（marine gastropods）的古生物学研究始终表明，物种选择更青睐拥有短寿命幼虫的支系：这类幼虫为卵黄营养型（lecithotrophic），其扩散能力弱于长寿命的浮游营养型（planktotrophic）幼虫。尽管在部分类群中，卵黄营养型类群似乎更易发生物种形成并随时间累积，但卵黄营养型同时也会提升灭绝速率，且此前从未有研究开展过依赖性状的分化速率（state-dependent diversification）检验。与之相对，多个类群的分子系统发育研究显示，卵黄营养型类群的累积并非源于物种分化，而是频繁单向性状转变的结果。尽管卵黄营养型在绝大多数门类中多次独立起源，但目前尚未发现任何成体性状与幼虫类型的转变存在关联。因此，无论是卵黄营养型的演化起源，还是其对物种丰富度格局的影响，迄今仍未得到清晰阐释。本研究借助基于似然的方法（likelihood-based methods），结合囊舌类（Sacoglossa，一类植食性海蛞蝓支系）202种腹足类软体动物的系统发育树，检验了发育模式与演化速率之间的假设关联。演化数量遗传学建模与随机性状映射分析支持卵黄营养型至少独立起源27次。相关演化关联检验显示，卵黄营养型在那些为胚胎外卵黄提供投资的支系中更易演化——这是首个在类群水平上与发育模式转变相关的成体性状。然而，与古生物学研究的预测相悖，物种选择实际上更青睐浮游营养型：绝大多数现存卵黄营养型类群均源自近期的性状转变，且未发生后续的物种分化。由此可见，浮游营养型类群增加的后代抚育投入，反而推动了向短寿命幼虫的演化转变，进而在宏演化时间尺度上形成了短命支系。这些发现挑战了学界关于海洋中不同生活史策略的长期固有认知。尽管频繁发生向卵黄营养型的演化转变，但物种选择可以解释浮游营养型——大多数类群的祖先性状——的长期存续。