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


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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    • "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.
    Molluscan Research 11/2013; 33(4). DOI:10.1080/13235818.2013.801394 · 0.51 Impact Factor
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    • "Divergent lineages of ''sp. 2'' did not have obvious morphological or developmental differences, and were only 5.9% distant, below the REST for E. ornata ($8%) and within the range of intra-specific COI variation noted for other sacoglossans (Ellingson and Krug, 2006; Trathen, 2010; Rico, 2012; Vendetti et al., 2012; Vo, 2013). "
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    ABSTRACT: 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.
    Molecular Phylogenetics and Evolution 07/2013; 69(3). DOI:10.1016/j.ympev.2013.07.009 · 3.92 Impact Factor
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    • "Key words: molecular phylogenetic analysis, haplotype network, COI, 16S rRNA, cryptic species The clade Sacoglossa is a group of gastropods that is known for several remarkable attributes including intracellular retention of chloroplasts sequestered from food algae (kleptoplasty) (Händeler et al. 2009), horizontal gene transfer (Pierce et al. 2003), and a reproductive polymorphism (poecilogony) (Ellingson and Krug 2006, Vendetti et al. 2012). The group comprises almost 400 nominal species of which ca. 300 are considered valid (Jensen 2007). "
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    ABSTRACT: Species of the genus Elysia Risso, 1818 have relatively few external characters useful for species identification, and features such as papillae and/or color markings on the body surface are often used to classify and identify species. Elysia atroviridis Baba, 1955 and E. setoensis Hamatani, 1968, for example, have been described as distinct based mainly on such characters. Close examinations of 46 specimens identifiable as either species collected from nine localities in Japan revealed that many specimens exhibited mixed features of the two species. Detailed comparisons of radular morphology could also not differentiate the two species. With phylogenetic analyses based on COI and 16S rRNA (1072 bp in total), all of the examined specimens formed a single clade with very little variation among specimens. The AMOVA of the specimen haplotypes showed there was no significant genetic differentiation in relation to differences in external morphology, geographic region, or algal host. Our results indicate that E. atroviridis and E. setoensis are conspecific. In contrast, cryptic species were found in two other clades of congeners, indicating that further taxonomic scrutiny is needed within the genus.
    American Malacological Bulletin 02/2013; 31(1):25-37. DOI:10.4003/006.031.0114 · 0.94 Impact Factor
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