KRUG LAB - EVOLUTIONARY AND LARVAL ECOLOGY OF MARINE INVERTEBRATES
Planktotrophic (top) vs. lecithotrophic (bottom) egg mass of A. willowi.
Poecilogony - Variable larval development modes
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1. Costasiella ocellifera. Only seven animal species are confirmed to have dimorphic egg sizes that result in feeding (planktotrophic) and non-feeding (lecithotrophic) larvae within the same taxon, a polymorphism termed poecilogony. Remarkably, five are sea slugs in Sacoglossa. We study poecilogonous sea slugs to understand the causes and consequences of shifts in larval type within a species. Recently, we reported the consequences of losing dispersive larvae at the population level in the Caribbean sea slug Costasiella ocellifera (Ellingson & Krug 2016). Four populations produced primarily aplanktonic embryos that metamorphose within benthic egg masses, and were genetically isolated from a large, panmictic metapopulation producing dispersive, planktotrophic larvae. Aplanktonic populations had reduced genetic diversity at both mitochondrial and nuclear microsatellite loci, and showed evidence of reinforcement, rarely mating with neighboring planktotrophic demes. Interpopulation crosses had reduced hatching success, consistent with selection favoring assortative mating; loss of larval stages may thus shrink the spatial scale at which speciational processes occur in the marine realm.
2. Alderia willowi. Identifying why populations switch from dispersing to non-dispersing larvae should yield insight into how natural selection drives the evolution of alternative larval strategies, an outstanding question in life-history evolution. We described A. willowi after molecular and morphological data revealed populations south of Bodega Harbor, CA were distinct from A. modesta, its northern (and exclusively planktotrophic) congener (Ellingson & Krug 2006; Krug et al. 2007). Alderia willowi is the only known animal in which an individual can produce both planktotrophic and lecithotrophic larvae during its lifetime (Krug 2007). Although all opisthobranch sea slugs are hermaphrodites, A. willowi is the only species confirmed to self-fertilize in the recent literature (Smolensky et al. 2009). This species was named in joint tribute to willow trees, beloved by my grandmother and which the cerata of Alderia resemble, and the character Willow from TV's Buffy the Vampire Slayer who displayed a similarly flexible sexual behavior.
Field populations of A. willowi seasonally switch to non-dispersive lecithotrophic larvae in the summer, a potential adaptation to the historical closure of estuaries during the dry season, when water levels are low in Californian lagoons. Rearing experiments showed that slugs raised at high temperature and salinity produced primarily lecithotrophic larvae, while those raised at low temperature and salinity produced mostly planktotrophic larvae (Krug et al. 2012). Thus, slugs use environmental cues to produce dispersive larvae during the rainy season when the input of runoff opens estuaries to the coastal ocean, suggesting selection favors lecithotrophy when dispersal is rendered unlikely by physical transport regimes.
Alderia willowi
Phylogenetic analysis of mtDNA from 233 specimens of Alderia from 15 north-Pacific estuaries shows two divergent clades >18% different at COI. The northern A. modesta (blue) ranges west to Russia and into the Atlantic; A. willowi (red) occurs south of Tomales Bay, CA. Unmarked haplotypes were from planktotrophic specimens (both species); dark circles mark lecithotrophic A. willowi, green triangles haplotypes shared by slugs differing in larval type.
3. Elysia pusilla. We confirmed using genetic and larval biological data that Elysia pusilla is another case of poecilogony (Vendetti et al. 2012). This small elysiid is probably the most common Elysia species in the tropical Indo-Pacific, where its secondarily flattened and reduced parapodial side-flaps help it adhere to flattended blades of the host alga Halimeda. This species either exhibits exceptional phylogeographic structure or is a cryptic species complex: six clades, each restricted to different islands or regions, were 11-19% divergent at the barcoding COI locus. This is a species-level difference in Sacoglossa, but we found no morphological evidence for cryptic species; regardless, lineages do not disperse, despite planktotrophy predominating in most populations. Selection against dispersal in this species is consistent with both the expression of lecithotrophy and the high degree of genetic isolation among populations. Ongoing work is quantifying larval behavior in this species to further understand the emergence of exceptional genetic structure in a common species despite apparently high potential for dispersal and connectivity.
Elysia pusilla on Halimeda
Planktotrophic (left) and lecithotrophic (right) egg masses of E. pusilla