Poecilogony and population genetic structure in Elysia pusilla (Heterobranchia: Sacoglossa), and reproductive data for five sacoglossans that express dimorphisms in larval development.
ABSTRACT Credible cases of poecilogony, the production of two distinct larval morphs within a species, are extremely rare in marine invertebrates, yet peculiarly common in a clade of herbivorous sea slugs, the Sacoglossa. Only five animal species have been reported to express dimorphic egg sizes that result in planktotrophic and lecithotrophic larvae: the spionid polychaete Streblospio benedicti and four sacoglossans distributed in temperate estuaries or the Caribbean. Here, we present developmental and genetic evidence for a fifth case of poecilogony via egg-size dimorphism in the Sacoglossa and the first example from the tropical Indo-Pacific. The sea slug Elysia pusilla produced both planktotrophic and lecithotrophic larvae in Guam and Japan. Levels of genetic divergence within populations were markedly low and rule out cryptic species. However, divergence among populations was exceptionally high (10-12% at the mitochondrial cytochrome c oxidase I locus), illustrating that extensive phylogeographic structure can persist in spite of the dispersal potential of planktotrophic larvae. We review reproductive, developmental, and ecological data for the five known cases of poecilogony in the Sacoglossa, including new data for Costasiella ocellifera from the Caribbean. We hypothesize that sacoglossans achieve lecithotrophy at smaller egg sizes than do related clades of marine heterobranchs, which may facilitate developmental plasticity that is otherwise vanishingly rare among animals. Insight into the environmental drivers and evolutionary results of shifts in larval type will continue to be gleaned from population-level studies of poecilogonous taxa like E. pusilla, and should inform life-history theory about the causes and consequences of alternative development modes in marine animals.
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ABSTRACT: Dimorphisms occur when alternative developmental pathways produce discrete phenotypes within a species, and may promote evolutionary novelty in morphology, life history, and behavior. Among marine invertebrates, intra-specific dimorphism in larval type (poecilogony) is notably rare, but should provide insight into the selective forces acting on larval strategies. Most established cases of poecilogony appear to be allelic polymorphisms, with local expression regulated by population-genetic processes. Here, we present evidence that dimorphic larval development in the sea slug Alderia willowi is a seasonal polyphenism; the type of larvae produced by an adult slug depends on the rearing environment in which that slug matured. In field surveys of 1996-1999 and 2007-2009, the population in Mission Bay, San Diego (California, USA) produced only short-lived lecithotrophic larvae in summer and early fall, but a varying proportion of slugs expressed planktotrophy in winter and spring. In laboratory experiments, slugs reared under summer conditions (high temperature, high salinity) produced the highest proportion of lecithotrophic offspring, whereas winter conditions (low temperature, low salinity) induced the lowest proportion of lecithotrophy. The shift to a nondispersive morph under summer conditions may be an adaptive response to historical closure of coastal wetlands during the dry season in southern California, which would inhibit dispersal by larvae of back-bay taxa. In most animal polyphenisms, a single larval type is produced and the rearing environment determines which adult phenotype develops. In contrast, alternative larval morphs are produced by A. willowi in response to seasonal cues experienced by the adult stage, varying the phenotype and dispersal potential of offspring. As the only known case of polyphenism in mode of larval development, A. willowi should become a model organism for mechanistic studies of dimorphism and the evolution of alternative life histories.Integrative and Comparative Biology 05/2012; 52(1):161-72. · 3.02 Impact Factor
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ABSTRACT: The fossil record of marine gastropods has been used as evidence to support the operation of species selection; namely, that species with limited dispersal differentially increase in numbers because they are more likely to speciate than widely dispersing species. This conclusion is based on a tacit phylogenetic assumption that increases in species with limited dispersal are solely the result of speciation within monophyletic groups with low dispersal. To test this assumption, we reconstructed a phylogeny from nuclear sequence data for 70 species of the marine gastropod genus Conus and used it to map the evolution of developmental mode. All eight species without planktonic life history phases recently and independently evolved this characteristic from ancestors with planktonic larval phases, showing that transitions in developmental mode are common in this group. A simple model of species diversification shows that such shifts can control the relative numbers of species with and without dispersing larval stages, leading to apparent species selection. Such results challenge the conclusion that increases in the number of nonplanktonic species relative to species with planktonic larvae over geologic time is necessarily a result of higher rates of speciation of nonplanktonic lineages and show that demonstration of species selection requires a phylogenetic framework.Proceedings of the National Academy of Sciences 09/1999; 96(18):10272-7. · 9.74 Impact Factor
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ABSTRACT: When conditions fluctuate unpredictably, selection may favor bet-hedging strategies that vary offspring characteristics to avoid reproductive wipe-outs in bad seasons. For many marine gastropods, the dispersal potential of offspring reflects both maternal effects (egg size, egg mass properties) and larval traits (development rate, habitat choice). I present data for eight sea slugs in the genus Elysia (Opisthobranchia: Sacoglossa), highlighting potentially adaptive variation in traits like offspring size, timing of metamorphosis, hatching behavior, and settlement response. Elysia zuleicae produced both planktotrophic and lecithotrophic larvae, a true case of poecilogony. Both intracapsular and post-hatching metamorphosis occurred among clutches of "Boselia" marcusi, E. cornigera, and E. crispata, a dispersal dimorphism often misinterpreted as poecilogony. Egg masses of E. tuca hatched for up to 16 days but larvae settled only on the adult host alga Halimeda, whereas most larvae of E. papillosa spontaneously metamorphosed 5-7 days after hatching. Investment in extra-capsular yolk may allow mothers to increase larval size relative to egg size and vary offspring size within and among clutches. Flexible strategies of larval dispersal and offspring provisioning in Elysia spp. may represent adaptations to the patchy habitat of these specialized herbivores, highlighting the evolutionary importance of variation in a range of life-history traits.Biological Bulletin 07/2009; 216(3):355-72. · 1.23 Impact Factor