A cryptic radiation of Caribbean sea slugs revealed by integrative analysis: Cyerce 'antillensis' (Sacoglossa: Caliphyllidae) is six distinct species.

Integrative studies have revealed cryptic radiations in several Caribbean lineages of heterobranch sea slugs, raising questions about the evolutionary mechanisms that promote speciation within the tropical Western Atlantic. Cyerce Bergh, 1871 is a genus comprising 12 named species in the family Caliphyllidae that lack the photosynthetic ability of other sacoglossans but are noted for vibrant colours on the large cerata (dorsal leaf-like appendages) that characterize many species. Two species are widely reported from the Caribbean: Cyerce cristallina (Trinchese, 1881) and Cyerce antillensis Engel, 1927. Here, we present an integrative assessment of diversity in Caribbean Cyerce. Four methods of molecular species delimitation supported seven species in samples from the Caribbean and adjacent subtropical Western Atlantic. Six delimited species formed a monophyletic lineage in phylogenetic analyses but were > 9% divergent at the barcoding COI locus and could be differentiated using ecological, reproductive and/or morphological traits. We redescribe C. antillensis, a senior synonym for the poorly known Cyerce habanensis Ortea & Templado, 1988, and describe five new species. Evolutionary shifts in algal host use, penial armature and larval life history might have acted synergistically to promote the rapid divergence of endemic species with restricted distributions in this radiation, substantially increasing global diversity of the genus.

Phylogenomic resolution of the root of Panpulmonata, a hyperdiverse radiation of gastropods: new insight into the evolution of air breathing.

Transitions to terrestriality have been associated with major animal radiations including land snails and slugs in Stylommatophora (>20 000 described species), the most successful lineage of 'pulmonates' (a non-monophyletic assemblage of air-breathing gastropods). However, phylogenomic studies have failed to robustly resolve relationships among traditional pulmonates and affiliated marine lineages that comprise clade Panpulmonata (Mollusca, Gastropoda), especially two key taxa: Sacoglossa, a group including photosynthetic sea slugs, and Siphonarioidea, intertidal limpet-like snails with a non-contractile pneumostome (narrow opening to a vascularized pallial cavity). To clarify the evolutionary history of the panpulmonate radiation, we performed phylogenomic analyses on datasets of up to 1160 nuclear protein-coding genes for 110 gastropods, including 40 new transcriptomes for Sacoglossa and Siphonarioidea. All 18 analyses recovered Sacoglossa as the sister group to a clade we named Pneumopulmonata, within which Siphonarioidea was sister to the remaining lineages in most analyses. Comparative modelling indicated shifts to marginal habitat (estuarine, mangrove and intertidal zones) preceded and accelerated the evolution of a pneumostome, present in the pneumopulmonate ancestor along with a one-sided plicate gill. These findings highlight key intermediate stages in the evolution of air-breathing snails, supporting the hypothesis that adaptation to marginal zones played an important role in major sea-to-land transitions.

Functionally non-redundant paralogs spe-47 and spe-50 encode FB-MO associated proteins and interact with him-8.

The activation of C. elegans spermatids to crawling spermatozoa is affected by a number of genes including spe-47. Here, we investigate a paralog to spe-47: spe-50, which has a highly conserved sequence and expression, but which is not functionally redundant to spe-47. Phylogenetic analysis indicates that the duplication event that produced the paralogs occurred prior to the radiation of the Caenorhabditis species included in the analysis, allowing a long period for the paralogs to diverge in function. Furthermore, we observed that knockout mutations in both genes, either alone or together, have little effect on sperm function. However, hermaphrodites harboring both knockout mutations combined with a third mutation in the him-8 gene are nearly self-sterile due to a sperm defect, even though they have numerous apparently normal sperm within their spermathecae. We suggest that the sperm in these triple mutants are defective in fusing with oocytes, and that the effect of the him-8 mutation is unclear but likely due to its direct or indirect effect on local chromatin structure and function.

A biting commentary: Integrating tooth characters with molecular data doubles known species diversity in a lineage of sea slugs that consume "killer algae".

Predicting biotic resistance to highly invasive strains of "killer algae" (Caulerpa spp.) requires understanding the diversity and feeding preferences of native consumers, including sea slugs in family Oxynoidae. Past studies reported low algal host specificity for Oxynoe (6 spp.) and Lobiger (4 spp.), but these taxonomically challenging slugs may represent species complexes of unrecognized specialists that prefer different Caulerpa spp. Here, we assess global diversity of these genera by integrating gene sequences with morphological data from microscopic teeth and internal shells, the only hard parts in these soft-bodied invertebrates. Four delimitation methods applied to datasets comprising mtDNA and/or nuclear alleles yielded up to 16 species hypotheses for samples comprising five nominal taxa, including five highly divergent species in Lobiger and five in Oxynoe. Depending on the analysis, a further four to six species were recovered in the O. antillarum-viridis complex, a clade in which mitochondrial divergence was low and nuclear alleles were shared among lineages. Bayesian species delimitation using only morphological data supported most candidate species, however, and integrative analyses combining morphological and genetic data fully supported all complex members. Collectively, our findings double the recognized biodiversity in Oxynoidae, and illustrate the value of including data from traits that mediate fast-evolving ecological interactions during species delimitation. Preference for Caulerpa spp. and radular tooth characteristics covaried among newly delimited species, highlighting an unappreciated degree of host specialization and coevolution in these taxa that may help predict their role in containing outbreaks of invasive algae.

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.