DOI: 10.5061/dryad.88mv3
title: Data from: Species selection favors dispersive life histories in sea slugs, but higher per-offspring investment drives shifts to short-lived larvae

description: 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.
description: Figure S1, 16S secondary
 structure model for SacoglossaSecondary structure
 model for a portion of the mitochondrial large ribosomal subunit rRNA
 (16S) gene for Elysia crispata; positions conserved across Mollusca are
 bolded.Fig
 S1, 16S secondary structure
 model.pdfFigure S2, Alignment of
 partial 16S gene sequencesAlignment of partial 16S
 gene sequences for all taxa, annotated according to secondary structure.
 Regions of ambiguous alignment (indicated by green shaded boxes marked
 “X”) were manually deleted prior to analyses.Fig S2, full 16S alignment
 annotated.pdfFigure S3, Annotated
 alignment of partial 28S rDNA sequencesAlignment of a portion
 of the nuclear large ribosomal subunit rRNA (28S) gene for all taxa,
 showing annotated secondary structure based on features conserved across
 Metazoa. Regions of ambiguous alignment (indicated by green shaded boxes
 marked “X”) were manually deleted prior to analyses.Fig S3, 28S alignment
 annotated.pdfFigure S4, Individual
 gene trees (a-d), BI consensus tree (e), and ML tree with two data
 partitions (f)Supplementary
 phylogenetic trees, including individual ML gene trees for each locus
 based on partial sequences of the (a) mitochondrial COI (658 bp), (b)
 mitochondrial 16S rRNA (404 bp), (c) nuclear 28S rRNA (1392 bp), and (c)
 nuclear H3 (328 bp) genes; (e) the BI consensus phylogram; and (f) the ML
 phylogram and significant bootstrap support values when using two data
 partitions as per PartitionFinder.Fig S4a-f, gene trees, BI
 consensus, ML alt
 partitioned.pdfFigure S5, Collapsed
 phylogeny showing distribution of species richness and development
 modesDistribution of species
 diversity among supported clades on the ML phylogeny of Sacoglossa.
 Traditional genera or genus-level clades were collapsed in proportion to
 known species richness, listed for each group. Species diversity and a
 pruned tree were used as inputs for ML tests of state-dependent speciation
 rates using the BiSSE model. Larval development mode for terminal taxa are
 coded as: P, planktotrophic; L, lecithotrophic; ?, unknown. The number of
 species with each development mode (or missing data) is given in
 parentheses for collapsed clades or terminals representing multiple taxa,
 in the same order (P,L,?). The sum of these values represents the total
 number of species known in a clade, including undescribed candidate
 species identified in the present work. Red branches indicate shifts in
 diversification detected by MEDUSA that are independent of larval
 development mode. Traditional families are named to the right of, and
 delimited by, colored horizontal bars; bolded family names are
 traditionally placed in superfamily Limapontioidea. Select higher clade
 names are given on branches.Fig S5, BiSSE tree
 v4.pdfFigure S6, Posterior
 distributions of rate parameters from dependent models of correlated trait
 evolutionPosterior distributions
 of parameters from dependent models of trait evolution, allowing ECY and
 development mode to evolve in a correlated manner. Transition rates are
 labeled as in Fig. 2. Z = percentage of time a rate was in the zero
 bin.Fig S6,
 dep model rate dist.tifTable S1, Sampled taxa
 and collection detailsSpecies names, sample
 codes and collection details for sequenced taxa used in phylogenetic
 analyses. Blank cells reflect missing information for sequence data
 obtained from a public database.Table_S1_sampled_taxa+collection_details_v6.docTable S2, Developmental character data for SacoglossaDevelopmental character data for Sacoglossa including larval development mode, presence/absence and pattern of extra-capsular yolk (ECY), mean egg diameter (± SD), and mean larval shell width (± SD) at hatching. Taxa are listed alphabetically by traditional family within higher clades, and then by binomial name within family. Generic names in quotation marks denote taxa that do not group with most other members of the genus to which they are traditionally assigned.Table_S2_devel_data_v7_refs.xlsTable S3, NCBI accession numbersAccession numbers from the National Center for Bioinformatics database for sequences generated and/or analyzed in this study.Table_S3_accession_nos.xlsTable S4, BiSSE model fit using a pruned input tree and global estimate of unsampled taxaComparison of BiSSE models correcting for missing data with a pruned input tree and one overall estimate of the percentage of unsampled taxa (69%), with either (a) one rate of character change, or (b) rates of reversal (q10) constrained to be rare (&lt;1%) relative to gains of lecithotrophy (q01).Table S4, split BiSSE model fit, % missing taxa.docTable S5, BiSSE parameter estimates using a percentage of unsampled taxa to correct for missing dataMaximum-likelihood parameter estimates for BiSSE models, correcting for missing data using an overall percentage of unsampled taxa (69%). The ML tree (Fig. 3) was pruned of terminals missing character data, and used as the input tree for BiSSE analyses with three phylogenetic partitions across Sacoglossa, and either (A) one rate of character change, or (B) rates of reversal to planktotrophy (q10) constrained to be rare (&lt;1%) relative to forward rates (q01). Estimates from the preferred model are bolded, with alternatives shown in descending order of AIC scores.Table S5, split BiSSE params, % missing taxa.docTable S6, References cited in Table 4References cited in Table 4, from which data on development modes were taken for select clades in Heterobranchia and Caenogastropoda.Table S6, references v2.doc