Simon E. Coppard

Formation of the Isthmus of Panama

Independent evidence from rocks, fossils, and genes converge on a cohesive narrative of isthmus formation in the Pliocene. The formation of the Isthmus of Panama stands as one of the greatest natural events of the Cenozoic, driving profound biotic transformations on land and in the oceans. Some recent studies suggest that the Isthmus formed many millions of years earlier than the widely recognized age of approximately 3 million years ago (Ma), a result that if true would revolutionize our understanding of environmental, ecological, and evolutionary change across the Americas. To bring clarity to the question of when the Isthmus of Panama formed, we provide an exhaustive review and reanalysis of geological, paleontological, and molecular records. These independent lines of evidence converge upon a cohesive narrative of gradually emerging land and constricting seaways, with formation of the Isthmus of Panama sensu stricto around 2.8 Ma. The evidence used to support an older isthmus is inconclusive, and we caution against the uncritical acceptance of an isthmus before the Pliocene.

Escape and Aggregation Responses of Three Echinoderms to Conspecific Stimuli

In marine invertebrates, waterborne chemical stimuli mediate responses including prey detection and predator avoidance. Alarm and flight, in response to damaged conspecifics, have been reported in echinoderms, but the nature of the stimuli involved is not known. The responses of Asterias rubens Linnaeus, Psammechinus miliaris (Gmelin), and Echinus esculentus Linnaeus to conspecifics were tested in a choice chamber against a control of clean seawater (no stimulus). All three species showed statistically significant movement toward water conditioned by whole animals or homogenate of test epithelium. P. miliaris and E. esculentus displayed a statistically significant avoidance reaction, moving away from conspecific coelomic fluid, gut homogenate, and gonad homogenate. A. rubens was indifferent to conspecific coelomic fluid, pyloric cecum homogenate, and gonad homogenate but moved away from cardiac gut homogenate. P. miliaris was indifferent to gametes, but the other two species were significantly attracted to them. No species showed preference for one particular side of the chamber during trials to balance water flow. These echinoderms can distinguish between homogenates of conspecific tissues that might be exposed when a predator damages the test, and those that may emanate from the exterior surface during normal activities.

Latin America Echinoderm Biodiversity and Biogeography: Patterns and Affinities

We investigated the current patterns of diversity by country and by class of echinoderms, and analyzed their biogeographical, depth, and habitat or substratum affinities, using the database of the appendix of this book. Traditionally, the area has been divided into five biogeographical Regions and nine Provinces that cover a wide climate range. Currently, the echinoderm fauna of Latin America and Canary islands is constituted by 1,539 species, with 82 species of Crinoidea, 392 species of Asteroidea, 521 species of Ophiuroidea, 242 species of Echinoidea and 302 species of Holothuroidea. Species richness is highly variable among the different countries. The number of species for the countries is highly dependent on its coast length. The echinoderm fauna of the Panamic, Galapagos and the Chilean regions are biogeographically related. Other regions that are closely related are the Caribbean, West Indian, Lusitania and Brazilian. Cosmopolitan species are an important component in all the regions. Affinities between faunas are a consequence of the combination of climatic and trophic factors, connectivity as a function of distance, currents patterns and historical processes. Moreover, different environmental factors would be responsible for the faunal composition and species distribution at different spatial scales. The bathymetrical distribution of the echinoderm classes and the species richness varies according to the depth range and the ocean. Most species occurred at depths between 20 and 200 m. The Caribbean-Atlantic regions are richest in shallow depths, while the Pacific coast has higher values in deeper waters. The domination of each class in each substrate and habitat categories also varies differentially along each coast.

Phylogeography of the sand dollar genus Mellita: cryptic speciation along the coasts of the Americas.

Sand dollars of the genus Mellita are members of the sandy shallow-water fauna. The genus ranges in tropical and subtropical regions on the two coasts of the Americas. To reconstruct the phylogeography of the genus we sequenced parts of the mitochondrial cytochrome oxidase I and of 16S rRNA as well as part of the nuclear 28S rRNA gene from a total of 185 specimens of all ten described morphospecies from 31 localities. Our analyses revealed the presence of eleven species, including six cryptic species. Sequences of five morphospecies do not constitute monophyletic molecular units and thus probably represent ecophenotypic variants. The fossil-calibrated phylogeny showed that the ancestor of Mellita diverged into a Pacific lineage and an Atlantic+Pacific lineage close to the Miocene/Pliocene boundary. Atlantic M. tenuis, M. quinquiesperforata and two undescribed species of Mellita have non-overlapping distributions. Pacific Mellita consist of two highly divergent lineages that became established at different times, resulting in sympatric M. longifissa and M. notabilis. Judged by modern day ranges, not all divergence in this genus conforms to an allopatric speciation model. Only the separation of M. quinquiesperforata from M. notabilis is clearly due to vicariance as the result of the completion of the Isthmus of Panama. The molecular phylogeny calibrated on fossil evidence estimated this event as having occurred ~3 Ma, thus providing evidence that, contrary to a recent proposal, the central American Isthmus was not completed until this date.

Evolution of gamete attraction molecules: evidence for purifying selection in speract and its receptor, in the pantropical sea urchin Diadema.

Many free‐spawning marine invertebrates, such as sea urchins, lack any courtship or assortative mating behavior. Mate recognition in such cases occur at the gametic level, and molecules present on the sperm and egg are major determinants of species‐specific fertilization. These molecules must also coevolve in relation to each other in order to preserve functional integrity. When sea urchins release their gametes in seawater, diffusible molecules from the egg, termed sperm‐activating peptides, activate and attract the sperm to swim toward the egg, initiating a series of interactions between the gametes. Although the compositions and diversity of such sperm‐activating peptides have been characterized in a variety of sea urchins, little is known about the evolution of their genes. Here we characterize the genes encoding the sperm‐activating peptide of the egg (speract) and its receptor on the sperm, and examine their evolutionary dynamics in the sea urchin genus Diadema, in the interest of determining whether they are involved in reproductive isolation between the species. We found evidence of purifying selection on several codon sites in both molecules and of selectively neutral evolution in others. The diffusible speract peptide that activates sperm is invariant across species, indicating that Diadema egg peptides do not discriminate between con‐ and hetero‐specific sperm at this stage of the process. Speract and its receptor do not contribute to reproductive isolation in Diadema.

Echinoderm Diversity in Panama: 144 Years of Research Across the Isthmus

Panama has a diverse echinoderm fauna with 414 species recorded. This is comprised of 21 species of crinoids, 130 species of ophiuroids, 83 species of asteroids, 78 species of echinoids and 102 species of holothuroids. With the exception of crinoids, diversity of echinoderms in Panama is greater in the Pacific (270 species) than in the Caribbean (154 species). This contrasts to other invertebrate groups (e.g. corals, sponges and bryozoans), where unequal rates of speciation, extinction and migration have resulted in greater diversity in the Caribbean than in the Pacific. The earliest published article that included work on echinoderms from Panama dates back to Addison Emery Verrill in 1867, where he described new genera and species. This began a period of exploration during which most echinoderms species from Panamanian waters were described. From its inception in 1961, the Smithsonian Tropical Research Institute marine program in Panama has generated extensive ecological and evolutionary echinoderm research. This includes work on species distributions, population sizes, reproductive cycles, grazing and food preferences, associated organisms, bioerosion, and species die-offs. The majority of molecular phylogeographic studies in Panama have focused on echinoids, with only a few molecular studies on asteroids and ophiuroids, and none on crinoids or holothuroids. Sustainable aquaculture of echinoderms in Panama has not been developed, while the illegal extraction of beche-de-mer continues to put pressure on holothuroid populations.

A new genus of mellitid sand dollar (Echinoidea: Mellitidae) from the eastern Pacific coast of the Americas

Lanthonia gen. nov. Coppard 2016 is a genus of clypeasteroid sand dollar whose members inhabit shallow, sandy waters from Mexico (including the Gulf of California) to Colombia in the tropical and subtropical eastern Pacific. Lanthonia includes Lanthonia longifissa (Michelin, 1858) and Lanthonia grantii (Mortensen, 1948), with L. longifissa hereby designated as the type species. Both L. longifissa and L. grantii were previously placed in the genus Mellita (L. Agassiz, 1841). However, levels of genetic divergence between a lineage containing L. longifissa and L. grantii and a lineage containing all other species of Mellita, including the type species M. quinquiesperforata (Leske, 1778), indicate genus level differentiation. The systematic interpretation of this group also supports the designation of this new genus as it allows the tree topology to be recovered from the nomenclature and clarifies the historical biogeography of these clades. This has resulted in members of both lineages today being sympatric in the eastern Pacific. Members of Lanthonia are morphologically differentiated from the type species of Mellita and all Pacific Mellita in having very narrow ambulacral regions between the food grooves and the ambulacral lunules on the oral surface, these being very broad in both M. quinquiesperforata and M. notabilis. The dentation of the bidentate pedicellariae also differentiate these genera, with small peripheral teeth present along the edge of the blade in species of Lanthonia and one to three enlarged intersecting teeth present distally in all species of Mellita.

Gene expression across tissues, sex, and life stages in the sea urchin Tripneustes gratilla

The pan-tropical sea urchin Tripneustes gratilla is an ecologically and economically important shallow water algal grazer. The aquaculture of T. gratilla has spurred growing interest in the population biology of the species, and by extension the generation of more molecular resources. To this purpose, de novo transcriptomes of T. gratilla were generated for two adults, a male and a female, as well as for a cohort of approximately 1,000 plutei larvae. Gene expression profiles of three adult tissue samples were quantified and compared. These samples were of gonadal tissue, the neural ring, and pooled tube feet and pedicellariae. Levels of shared and different gene expression between sexes, as well as across functional categories of interest, including the immune system, toxins, genes involved in fertilization, and sensory genes are highlighted. Differences in expression of Sex determining Region Y-related High Mobility Group box groups and general isoform expression between the sexes is observed. Additionally an expansion of the tumor suppressor DMBT1 was observed in T. gratilla when compared to the annotated genome of the sea urchin Strongylocentrotus purpuratus. The draft transcriptome of T. gratilla is presented here in order to facilitate more genomic level analysis of de-novo sea urchin systems.

A phylogenomic resolution of the sea urchin tree of life

Background Echinoidea is a clade of marine animals including sea urchins, heart urchins, sand dollars and sea biscuits. Found in benthic habitats across all latitudes, echinoids are key components of marine communities such as coral reefs and kelp forests. A little over 1,000 species inhabit the oceans today, a diversity that traces its roots back at least to the Permian. Although much effort has been devoted to elucidating the echinoid tree of life using a variety of morphological data, molecular attempts have relied on only a handful of genes. Both of these approaches have had limited success at resolving the deepest nodes of the tree, and their disagreement over the positions of a number of clades remains unresolved. Results We performed de novo sequencing and assembly of 17 transcriptomes to complement available genomic resources of sea urchins and produce the first phylogenomic analysis of the clade. Multiple methods of probabilistic inference recovered identical topologies, with virtually all nodes showing maximum support. In contrast, the coalescent-based method ASTRAL-II resolved one node differently, a result apparently driven by gene tree error induced by evolutionary rate heterogeneity. Regardless of the method employed, our phylogenetic structure deviates from the currently accepted classification of echinoids, with neither Acroechinoidea (all euechinoids except echinothurioids), nor Clypeasteroida (sand dollars and sea biscuits) being monophyletic as currently defined. We demonstrate the strength and distribution of phylogenetic signal throughout the genome for novel resolutions of these lineages and rule out systematic biases as possible explanations. Conclusions Our investigation substantially augments the molecular resources available for sea urchins, providing the first transcriptomes for many of its main lineages. Using this expanded genomic dataset, we resolve the position of several clades in agreement with early molecular analyses but in disagreement with morphological data. Our efforts settle multiple phylogenetic uncertainties, including the position of the enigmatic deep-sea echinothurioids and the identity of the sister clade to sand dollars. We offer a detailed assessment of evolutionary scenarios that could reconcile our findings with morphological evidence, opening up new lines of research into the development and evolutionary history of this ancient clade.

Gene expression across tissues, sex, and life stages in the sea urchin Tripneustes gratilla [Toxopneustidae, Odontophora, Camarodonta]

The pan-tropical sea urchin Tripneustes gratilla is an ecologically and economically important shallow water algal grazer. The aquaculture of T. gratilla has spurred growing interest in the population biology of the species, and by extension the generation of more molecular resources. To this purpose, de novo transcriptomes of T. gratilla were generated for two adults, a male and a female, as well as for a cohort of approximately 1000 plutei larvae. Gene expression profiles of three adult tissue samples were quantified and compared. These samples were of gonadal tissue, the neural ring, and pooled tube feet and pedicellariae. Levels of shared and different gene expression between sexes, as well as across functional categories of interest, including the immune system, toxins, genes involved in fertilization, and sensory genes are highlighted. Differences in expression of isoforms between the sexes and Sex determining Region Y-related High Mobility Group box groups is observed. Additionally an expansion of the tumor suppressor DMBT1 is observed in T. gratilla when compared to the annotated genome of the sea urchin Strongylocentrotus purpuratus. The draft transcriptome of T. gratilla is presented here in order to facilitate more genomic level analysis of emerging model sea urchin systems.