Species Selection Favors Dispersive Life Histories in Sea Slugs, but Higher Per-Offspring Investment Drives Shifts to Short-Lived Larvae

• Published in: Systematic biology Vol. 64; no. 6; pp. 983 - 999
• Main Authors: Krug, Patrick J., Vendetti, Jann E., Ellingson, Ryan A., Trowbridge, Cynthia D., Hirano, Yayoi M., Trathen, Danielle Y., Rodriguez, Albert K., Swennen, Cornelis, Wilson, Nerida G., Valdés, Ángel A.
• Format: Journal Article
• Language: English
• Published: England Oxford University Press 01-11-2015
• Subjects: Animals; Aquatic Organisms - classification; Aquatic Organisms - growth & development; Aquatic Organisms - physiology; Evolutionary biology; Gastropoda - classification; Gastropoda - genetics; Gastropoda - growth & development; Gastropoda - physiology; Genetics; Larva; Larvae; Life Cycle Stages - physiology; Macroevolution; Models, Genetic; Mollusks; Offspring; Paleontology; Phylogeny; Regular; Reproduction; Selection, Genetic; Shellfish; Species richness; Development mode; planktotrophy; species selection; lecithotrophy; macroevolution; gastropod; Sacoglossa
• ISSN: 1063-5157; 1076-836X
• DOI: 10.1093/sysbio/syv046

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.