In the British Isles, oligophagous marine herbivores, particularly the ascoglossan (ϭ sacoglossan) sea slug Elysia viridis, associate with the introduced green macroalga Codium fragile ssp. tomentosoides. Slugs prefer to associate with and consume the introduced C. fragile to the native C. tomentosum. Our investigation of adult, larval, and juvenile E. viridis focused on whether this association is attributable (1) to a host switch or (2) to an expansion from native hosts to the introduced C. fragile ssp. tomentosoides. Growth rates and maximum body sizes of E. viridis on introduced hosts were greater than on natives. Although the native Cladophora rupestris induced a high rate of slug metamorphosis, recently metamorphosed juvenile E. viridis (from Codium fragile-feeding parents) were generally not able to feed or grow on the native alga. In contrast, juveniles from Cladophora-feeding parents could eat Cladophora, although their performance was highly variable. Small, postlarval slugs (Ͻ800 m long) could not effectively puncture cell walls and extract algal cytoplasm and chloroplasts from Cladophora; slugs fed far more readily on the thin-walled C. fragile. The new association appeared to be a host switch such that Codium fragile feeders and their offspring had limited capacity to complete their life cycle on the native host Cladophora. Larval metamorphosis in E. viridis was greatest on potential host species, but larvae also responded to nonhost macrophytes and adult conspecifics. The generality of larval host-plant selection and larval metamorphosis enables oligophagous adult consumers to exploit spatially unpredictable novel hosts, to capitalize on newly available host plants, and to exhibit spatial and temporal variation in host-plant associations.
DNA barcoding can highlight taxa in which conventional taxonomy underestimates species richness, identifying mitochondrial lineages that may correspond to unrecognized species. However, key assumptions of barcoding remain untested for many groups of soft-bodied marine invertebrates with poorly resolved taxonomy. Here, we applied an integrative approach for species delimitation to herbivorous sea slugs in clade Sacoglossa, in which unrecognized diversity may complicate studies of drug discovery, plastid endosymbiosis, and biological control. Using the mitochondrial barcoding COI gene and the nuclear histone 3 gene, we tested the hypothesis that three widely distributed “species” each comprised a complex of independently evolving lineages. Morphological and reproductive characters were then used to evaluate whether each lineage was distinguishable as a candidate species. The “circumtropical” Elysia ornata comprised a Caribbean species and four Indo-Pacific candidate species that are potential sources of kahalalides, anti-cancer compounds. The “monotypic” and highly photosynthetic Plakobranchus ocellatus, used for over 60 years to study chloroplast symbiosis, comprised 10 candidate species. Finally, six candidate species were distinguished in the Elysia tomentosa complex, including potential biological control agents for invasive green algae (Caulerpa spp.). We show that a candidate species approach developed for vertebrates effectively categorizes cryptic diversity in marine invertebrates, and that integrating threshold COI distances with non-molecular character data can delimit species even when common assumptions of DNA barcoding are violated.
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.
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