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-dependentdiversificationwereneverperformed.Molecularphylogenies ofdiverse groups instead suggested lecithotrophs accumulatewithout diversifyingdue to frequent, unidirectional character change.Although lecithotrophy has repeatedly originated inmost phyla, no adult trait has been correlatedwith 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. [Development mode; gastropod; lecithotrophy; macroevolution; planktotrophy; Sacoglossa; species selection.] Species selection results when the diversification rate of a lineage is character-state dependent (Stanley 1975; Jablonski 2008). Despite resurgent interest in comparative studies of species selection, it remains challenging to identify traits linked with shifts in diversification rate (RaboskyandMcCune2009;Rabosky and Goldberg 2015). Ideally, candidate traits that may trigger species selection should be mechanistically linked to speciation and extinction, and change state often enough to provide the evolutionary replication needed for statistical analysis (Jablonski 2008; Goldberg et al. 2010). In marine invertebrates, larval development mode is a binary trait long thought to affect the evolutionary success of a lineage (Shuto 1974; Strathmann 1985). Larvae must either feed in the plankton to complete development (planktotrophy), or have enough yolk to complete metamorphosis without feeding (lecithotrophy) (Levin and Bridges 1995). Planktotrophic larvae may be carried long distances by ocean currents while feeding, maintaining gene flow among populations of benthic animals (Pechenik 1999; Bradbury et al. 2008). Lecithotrophic taxa have an abbreviated larval period that reduces dispersal, often resulting in genetically subdivided and locally adapted populations (Vermeij 1982; Selkoe and Toonen 2011). As lecithotrophic eggs are more energetically expensive to produce, selection on dispersal is inherently correlated with adult per-offspring investment (Marshall and Morgan 2011). However, we still understand little about the selective regimes that favor, or the long-term results of, changes in larval type. Marine life-history evolution tends to be unidirectional, from planktotrophy to lecithotrophy (Gould 1982; but see Rouse 2000; Collin et al. 2007). Developmental and phylogenetic studies suggest reversals are rare due to constraints on re-evolving complex feeding structures that are often reduced in transitions to lecithotrophic development (Strathmann 1978; Wray 1995). Despite involving substantial and largely irreversible changes, shifts to lecithotrophy have occurred frequently in most clades, creating a naturally replicated experiment with which to evaluate the evolutionary origins and consequences of reduced dispersal. Theory has long held that planktotrophy should impede speciation by slowing divergence among demes while buffering against local extinction (Scheltema 1971, 1978). For 40 years, studies of the gastropod fossil record reported lecithotrophs had elevated rates of both speciation and extinction, and tended to accumulate faster over time in someneogastropodclades 1 Systematic Biology Advance Access published September 18, 2015