Article

Poecilogony and Population Genetic Structure in Elysia pusilla (Heterobranchia: Sacoglossa), and Reproductive Data for Five Sacoglossans that Express Dimorphisms in Larval Development

Department of Biological Sciences, California State University, Los Angeles, CA 90032-8201, USA.
Integrative and Comparative Biology (Impact Factor: 2.93). 06/2012; 52(1):138-50. DOI: 10.1093/icb/ics077
Source: PubMed

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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    • "Thus, shared development mode may better predict hybrid compatibility than genetic distance, and local shifts in larval type may be an unrecognized driver of speciation in the sea. Of the seven species confirmed to exhibit egg-size dimorphism , four are found in Sacoglossa, a clade of herbivorous sea slugs (Vendetti et al. 2012). A fifth candidate species is Costasiella ocellifera from Florida (FL), United States and the Caribbean. "
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    ABSTRACT: Population-level consequences of dispersal ability remain poorly understood, especially for marine animals in which dispersal is typically considered a species-level trait governed by oceanographic transport of microscopic larvae. Transitions from dispersive (planktotrophic) to non-dispersive, aplanktonic larvae are predicted to reduce connectivity, genetic diversity within populations, and the spatial scale at which reproductive isolation evolves. However, larval dimorphism within a species is rare, precluding population-level tests. We show the sea slug Costasiella ocellifera expresses both larval morphs in Florida and the Caribbean, regions with divergent mitochondrial lineages. Planktotrophy predominated at 11 sites, 10 of which formed a highly connected and genetically diverse Caribbean metapopulation. Four populations expressed mainly aplanktonic development and had markedly reduced connectivity, and lower genetic diversity at one mitochondrial and six nuclear loci. Aplanktonic dams showed partial post-zygotic isolation in most inter-population crosses, regardless of genetic or geographic distance to the sire's source, suggesting outbreeding depression affects fragmented populations. Dams from genetically isolated and neighboring populations also exhibited pre-mating isolation, consistent with reinforcement contingent on historical interaction. By increasing self-recruitment and genetic drift, the loss of dispersal may thus initiate a feedback loop resulting in the evolution of reproductive isolation over small spatial scales in the sea. This article is protected by copyright. All rights reserved.
    Full-text · Article · Dec 2015 · Evolution
    • "Egg masses of some sacoglossans, especially the superfamily Plakobranchoidea, have extra-capsular yolk (Clark et al., 1979; Boucher, 1983; Jensen, 2001). Egg size, capsule size, number of eggs per egg mass and development type, have been reviewed in a few papers (Clark & Jensen, 1981; Jensen, 2001), and poecilogony is known for a few species (Krug et al., 2007; Vendetti et al., 2012). The spawning process has been observed for a few species (Kawaguti & Yamasu, 1960, 1966; Reid, 1964; Jensen, 1986), but the present study is the first time the spawning process of a sacoglossan species has been documented by video. "
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    ABSTRACT: Spawning was observed in the laboratory and documented by video for a specimen of Lobiger viridis Pease, 1863 (Mollusca: Gastropoda: Heterobranchia: Sacoglossa) from Changi East, Singapore. The spawning animal shaped the egg mass with its mouth-area and the anterior rim of its foot. The head moved from side to side, presumably adding secretions, as the egg mass progressed. The egg mass was shaped as a more or less irregular, elongate spiral. It took approximately three hours to complete the first egg mass, and a second fertile egg mass was produced after 24 hours. The eggs were yellow when deposited but turned pale after several days as shelled veliger larvae developed. A single egg mass was estimated to contain more than 20,000 eggs. Preserved egg capsules were approximately 120 × 90 μm, and veligers had distinct statocysts but no eyes when they were ready to hatch. At this stage veliger shells had maximum diameters of about 106 μm.
    No preview · Article · Jul 2015 · The Raffles bulletin of zoology
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    • "There are a number of examples of variance in reproductive traits between sympatric sister species of marine invertebrates that can be explained by differing reproductive strategies (Pickford 1949; Byrne et al. 1999; Ellingson and Krug 2006). This also applies to cases of poecilogony (Levin 1984; Vendetti et al. 2012) in which differences in reproductive investment drive large differences between two egg size classes. However, examples that demonstrate significant variance in egg size among co-occurring closely related species that share the same reproductive strategy remain particularly rare. "
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    ABSTRACT: Although variance in life history parameters is well known from comparisons among broad phylogenetic groups of marine invertebrates, there is still an outstanding need to increase empirical studies that compare closely related species. If the species under study share a recent common ancestor and developmental strategy, there is an opportunity to contrast maternal investment against interspecific variation while controlling for evolutionary distance. Furthermore, when these species co-occur, it allows for exploration of potential character displacement. We examined egg size and other factors related to reproduction in four closely related species, co-occurring nudibranchs belonging to the monophyletic Chromodoris planar spawning clade. The duration of oviposition appeared to be conserved and may be phylogenetically constrained in these four co-occurring species. In contrast, egg size differed significantly among species, but was not influenced by parental body length or position within the egg mass for any of the species. The number of egg mass whorls also varied, but did not correspond to the interspecific differences in parental body length. These results suggest that some significant differences exist among these sympatric Chromodoris species that may be candidate traits for character displacement. These characters would need to be re-measured in geographic areas where the studied Chromodoris species do not co-occur.
    Full-text · Article · Nov 2013 · Molluscan Research
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