title: Species Selection Favors Dispersive Life Histories in Sea Slugs, but Higher Per-Offspring Investment Drives Shifts to Short-Lived Larvae.
abstract: 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.
authors.affiliation: Department of Biological Sciences, California State University, Los Angeles, CA 90032-8201, USA; pkrug@calstatela.edu.
authors.forename: Patrick J
authors.initials: PJ
authors.lastname: Krug
authors.affiliation: Department of Biological Sciences, California State University, Los Angeles, CA 90032-8201, USA;
authors.forename: Jann E
authors.initials: JE
authors.lastname: Vendetti
authors.affiliation: Department of Biological Sciences, California State University, Los Angeles, CA 90032-8201, USA;
authors.forename: Ryan A
authors.initials: RA
authors.lastname: Ellingson
authors.affiliation: Oregon Institute of Marine Biology, University of Oregon, PO Box 5389, Charleston, OR 97420, USA;
authors.forename: Cynthia D
authors.initials: CD
authors.lastname: Trowbridge
authors.affiliation: Coastal Branch of Natural History Museum and Institute, Chiba, 123 Yoshio, Katsuura, 299-5242, Japan;
authors.forename: Yayoi M
authors.initials: YM
authors.lastname: Hirano
authors.affiliation: Department of Biological Sciences, California State University, Los Angeles, CA 90032-8201, USA;
authors.forename: Danielle Y
authors.initials: DY
authors.lastname: Trathen
authors.affiliation: Department of Biological Sciences, California State University, Los Angeles, CA 90032-8201, USA;
authors.forename: Albert K
authors.initials: AK
authors.lastname: Rodriguez
authors.affiliation: Faculty of Science and Technology, Prince of Songkla University, Pattani 94000, Thailand;
authors.forename: Cornelis
authors.initials: C
authors.lastname: Swennen
authors.affiliation: Western Australian Museum, Kew Street, Welshpool, Perth, WA 6106, Australia; and.
authors.forename: Nerida G
authors.initials: NG
authors.lastname: Wilson
authors.affiliation: Department of Biological Sciences, California State Polytechnic University, Pomona, CA 91768, USA.
authors.forename: Ángel A
authors.initials: ÁA
authors.lastname: Valdés
mesh_terms: D000818:Animals; D059001:Aquatic Organisms / Q000145:classification / Q000254:growth & development / Q000502:physiology; D049851:Gastropoda / Q000145:classification* / Q000235:genetics / Q000254:growth & development / Q000502:physiology; D007814:Larva; D008018:Life Cycle Stages / Q000502:physiology; D008957:Models, Genetic; D010802:Phylogeny; D012098:Reproduction; D012641:Selection, Genetic
keywords: Development mode; Sacoglossa; gastropod; lecithotrophy; macroevolution; planktotrophy; species selection