Award: OCE-1130072

Most marine animals produce tiny, planktonic larval stages that can either (a) spend a month feeding and growing in the plankton, or (b) hatch as larger non-feeding larvae that swim for only a few days, or even hatch as miniature adults with no swimming period. It was long assumed that feeding larvae were transported great distances by ocean currents while they matured, but this was recently challenged by some studies. We tested these hypotheses using a group of sea slugs called sacoglossans, in which related species often differ in the type of larvae they produce, and focused on Caribbean species as there are detailed models of which locations should be connected by migration via currents. We found that species with short-lived, big larvae did generally experience less gene flow (the consequence of migration) among sites, confirming such larvae are less dispersive. However, in one such species, larvae evolved swimming behaviors that seem to help them get into surface currents and hence be transported far from hatching sites, increasing genetic mixing among populations. We also discovered that several species produce non-dispersive larvae in low-nutrient, clear waters of the central Caribbean, but produce feeding larvae (which are also dispersive) in the more nutrient-rich waters along the coast of Central and South America, which increases gene flow among those populations. Thus, the absence of planktonic food in tropical waters can be one factor selecting against dispersive larvae, which can cause populations to become genetically and demographically isolated. Notably, the Florida Keys population was genetically distinctive in most of the 19 species we studied across the Caribbean. The fast-moving Gulf Stream current likely acts like a barrier to gene flow into and out of Florida, by whisking planktonic larvae into the North Atlantic. Populations of tropical marine animals in the Keys may thus warrant special conservation measures, as they are unlikely to be quickly replenished from the Caribbean should their populations crash locally. The consequences of evolutionary shifts from dispersive to non-dispersive larvae are also profound. Classic studies of the fossil record argued for 40 years that non-dispersive development was a "winning" strategy in the long-term, causing a lineage to differentiate into many daughter species. However, our research showed that shifts from a migratory to a non-dispersive life history trades off short-term gain for long-term failure. Wherever ocean circulation limits the movement of planktonic larvae in and out, dispersal can be selected against, and non-dispersive larval development evolves. However, in the long run (over evolutionary timescales) this strategy dooms most lineages to eventual extinction. Thus, the "winners" in most marine invertebrate groups tend to be lineages that retain the potential for long-distance dispersal by producing long-lived, feeding larvae. Our results also contribute to applied problems in drug discovery and biological control of invasive algae. One "species" called Elysia ornata was reported to occur throughout the tropics, and to contain compounds called kahalalides currently in trial as potential anti-cancer drugs. By studying DNA sequences, adult anatomy, and larval features, we showed that there are eight related but distinct species being called "ornata." Obviously, it is critical to know which species contain potential cancer drugs, and which have not yet been screened for chemotherapeutic agents; our work showcases the importance of taxonomy and species identification in poorly studied groups. We similarly studied species called "E. tomentosa", and found up to 10 species were being lumped under this name. Species in this complex eat toxic, highly invasive "killer algae" (Caulerpa taxifolia and related seaweeds) that have invaded the Mediterranean, California, Japan and Australia. Sea slugs may be useful as biological control agents but little is presently known about their feeding specificity, and our lab is the only one that can presently tell species in this complex apart. A better understanding of species diversity in sea slug groups that eat introduced algae may generally help to predict where such algae will establish a foothold around the globe. Naming these species of sea slugs will furthermore allow scientists to communicate their findings about this group. Lastly, some sacoglossans have the remarkable ability to store functional chloroplasts (the part of plant cells that performs photosynthesis) from their meals. Instead of being digested, the hijacked chloroplasts continue to pump out nutrients for the slug, in some species for many months. Species that can sustain chloroplasts are used to study the early stages of intracellular symbioses, which led to the evolution of chloroplasts themselves from bacterial ancestors over a billion years ago. Our studies revealed that one such "species", Plakobranchus ocellatus, is actually at least 10 distinct species presently unrecognized by science. Studies of different species that use the same name can create confusion by reaching inconsistent or contradictory results; recognizing and describing the true species richness in a group is therefore critical for effective scientific study of the species involved. Last Modified: 07/17/2017 Submitted by: Patrick J Krug