Scott C. France - Abstracts

2013 Brugler, M.R., D.M. Opresko, S.C. France. The evolutionary history of the order Antipatharia (Cnidaria: Anthozoa: Hexacorallia) as inferred from mitochondrial and nuclear DNA: Implications for black coral taxonomy and systematics. Zoological Journal of the Linnean Society 169:312-361 [doi:]

Although black corals inhabit all the world’s oceans, they have been relatively understudied as ~185 of 247 species occur at depths >50 meters. Antipatharians have been included in several phylogenetic studies; however, sample sizes are small and taxonomic coverage minimal. Low levels of mitochondrial (mt) sequence divergence within Scleractinia and Octocorallia are assumed to apply to all anthozoans, although no formal study has been conducted on the order Antipatharia. To quantify genetic variation in the black coral mitogenome, we analyzed DNA sequences of the two longest intergenic regions (IGRs) and cox3-cox1 for 26 of 41 genera, representing all families and subfamilies. We also quantified divergence at the intraspecific level using six mtIGRs and their flanking protein-coding genes and rDNA for 100+ colonies of Antipathes griggi. Utilizing sequence data from the two mtIGRs, cox3-cox1, as well as nuclear 18S and 28S, we constructed the first multi-locus phylogenies of the Antipatharia. Reconstructions revealed that species in the genus Stichopathes are split across two families, Sibopathes macrospina groups among North Atlantic Parantipathes (suggesting the actinopharynx and mesenteries were secondarily lost) and three families are polyphyletic. These and other results provide novel, independent insights into the evolutionary history of antipatharians and support placement of species into higher-level groupings based on microscopic skeletal features rather than gross colony morphology. An illustrated key to the seven currently-recognized families is also provided.

2013 Pante E., E. Heestand-Saucier, S.C. France. Molecular and morphological data support reclassification of the octocoral genus Isidoides. Invertebrate Systematics 27:365-378 [doi:]

The rare octocoral genus Isidoides Nutting, 1910 was originally placed in the Gorgonellidae (now the Ellisellidae), even though it showed a remarkable similarity to the Isidae (now the Isididae). Isidoides was not classified in the Isididae mostly because the type specimen lacked skeletal nodes, a defining characteristic of that family. The genus was later assigned to the Chrysogorgiidae based on sclerite morphology. Specimens were recently collected in the southwestern Pacific, providing material for genetic analysis and detailed characterization of the morphology, and allowing us to consider the systematic placement of this taxon within the suborder Calcaxonia. A previously-reported phylogeny allowed us to reject monophyly with the Chrysogorgiidae, and infer a close relationship with the Isididae subfamily Keratoisidinae. While scanning for molecular variation across mitochondrial genes, we discovered a novel gene order that is, based on available data, unique among metazoans. Despite these new data, the systematic placement of Isidoides is still unclear, as (1) the phylogenetic relationships among Isididae subfamilies remain poorly resolved, (2) genetic distances between mitochondrial mtMutS sequences from Isidoides and Keratoisidinae are characteristic of intra-familial distances, and (3) mitochondrial gene rearrangements may occur among confamilial genera. For these reasons, and because a revision of the Isididae is beyond the scope of this contribution, we amend the familial placement of Isidoides to incertae sedis

2012 Pante E., S.C. France, A. Couloux, C. Cruaud, C.S. McFadden, S. Samadi & L. Watling. Deep-sea origin and in-situ diversication of chrysogorgiid octocorals. PLoS ONE 7: e38357 [14 pp] (Open Access: doi:10.1371/journal.pone.0038357)

Chrysogorgiidae Verrill, 1883 make it noteworthy as a model system to study radiation and diversification in the deep sea. Here we provide the first comprehensive phylogenetic analysis of the Chrysogorgiidae, and compare phylogeny and depth distribution. Phylogenetic relationships among 10 of 14 currently-described Chrysogorgiidae genera were inferred based on mitochondrial (mtMutS, cox1) and nuclear (18S) markers. Bathymetric distribution was estimated from multiple sources, including museum records, a literature review, and our own sampling records (985 stations, 2345 specimens). Genetic analyses suggest that the Chrysogorgiidae as currently described is a polyphyletic family. Shallow-water genera, and two of eight deep-water genera appear more closely related to other octocoral families than to the remainder of the monophyletic, deep-water chrysogorgiid genera. Monophyletic chrysogorgiids are composed of strictly (Iridogorgia Verrill, 1883, MetallogorgiaVersluys, 1902, Radicipes Stearns, 1883, Pseudochrysogorgia Pante & France, 2010) and predominantly (Chrysogorgia Duchassaing & Michelotti, 1864) deep-sea genera that diversified in situ. This group is sister to gold corals (Primnoidae Milne Edwards, 1857) and deep-sea bamboo corals (Keratoisidinae Gray, 1870), whose diversity also peaks in the deep sea. Nine species of Chrysogorgia that were described from depths shallower than 200 m, and mtMutS haplotypes sequenced from specimens sampled as shallow as 101 m, suggest a shallow-water emergence of some Chrysogorgia species.

2011 Watling, L., & S.C. France. A New Genus and Species of Bamboo Coral (Octocorallia: Isididae: Keratoisidinae) from the New England Seamounts. Bulletin of the Peabody Museum of Natural History 52:209-220 (doi:

Sampling along the New England Seamount Chain has produced a large number of new octocoral species, especially of the bamboo corals in the subfamily Keratoisidinae. The new genus described here is unusual in that it branches from the internodes yet has sclerites at the base of the polyp body that are arranged obliquely, and in having tentacles that can be pulled completely into the top of the polyp over the retracted oral disk. The genus and species are characterized using both morphological and molecular data.

2011 Watling, L., S.C. France, E. Pante & A. Simpson. Biology of Deep-Water Octocorals. Advances in Marine Biology 60:41-122 (doi: 10.1016/B978-0-12-385529-9.00002-0)

Although deep-sea corals have been known to a handful of scientists and a large number of fishermen for at least two centuries, it is only over the last decade or so that there has been a surge of interest in their biology and ecology, largely a result of conservation concerns connected to the increasing exploitation of deep-sea resources. In this review we document what is known about taxonomy, phylogeny, biogeography, ecology and reproductive biology of deep-sea octocorals (Cnidaria, Anthozoa, Octocorallia) and highlight areas where knowledge is especially lacking.
Most families (30 of 45) of octocorals have representatives living in the deep sea, and some families are restricted to, or show a diversity maximum, below 200 m. In particular, the calcaxonian families Chrysogorgiidae, Isididae, and Primnoidae are common, abundant and diverse in deeper waters, and available genetic data suggest they underwent an extensive in situ deep-sea radiation from a common ancestor.
Many genera are widely distributed in the North Atlantic and the Pacific Oceans, however the patterns are incomplete because relatively few specimens have been collected in the South Atlantic, Indian, eastern Pacific, and Southern Oceans. Much of the taxonomy of deep-sea octocorals comes from the late 19th- and early 20th centuries and an inherent problem is that many species are known only from their type material, which in most cases consists of just a few specimens, and thus many genera are in need of revision. Increased collection and taxonomic revision will most likely alter our understanding of deep-sea octocoral biogeography.
Many deep-sea octocoral colonies are long-lived (to more than 400 years) and large (10-500 cm in height) and provide a wide range of biogenic habitats to other invertebrate species. Most of the known invertebrate symbionts are commensalistic, and appear to live on a narrow range of host species. Conversely, symbionts may be quite rare on some deep-sea octocoral species. The most commonly observed symbionts come from the phyla Cnidaria, Annelida, Mollusca, Arthropoda (Crustacea), and Echinodermata.
There is a general paucity of knowledge about reproductive processes in deep-sea octocorals, although it is clear they exhibit sexual reproductive strategies in common with their shallow-water counterparts. In all deep-sea species so far examined, gonochorism predominates at the colony level, and gonadal asynchrony seems to be the rule. Modes of asexual reproduction (budding, fission, parthenogenesis, etc.) that occur frequently in many shallow-water species have yet to be observed among deep-sea octocorals.
Deep-water octocorals are of conservation concern. They are a common component of benthic communities on seamounts and ridges throughout the world, and are known also from continental and island slopes, especially in canyons. Loss of coral communities has been documented where bottom trawls have been used to catch a variety of deep-sea fish. Deep-water octocorals are one of the primary groups of organisms covered under the term "vulnerable marine ecosystem" (VME) and it is, therefore, important that we document their taxonomic diversity and understand aspects of their biology so that management can be better informed and these long-lived organisms protected.

2011 de Buron, I., S.C. France, V.A. Connors, W.A. Roumillat, & L.C. Tsoi. Philometrids of the southern flounder Paralichthys lethostigma: a multidimensional approach to determine their diversity. Journal of Parasitology 97: 466-475 (

Two species of philometrid nematode , Philometra overstreeti and Philometroides paralichthydis, infect the southern flounder, Paralichthys lethostigma. Individuals of P. overstreeti are located between the teeth and inside the bony part of the branchial arches of the fish. Individuals of P. paralichthydis are associated with the bones of the buccal cavity and among muscles that control the dorsal and anal fins. Sequencing of part of the cytochrome oxidase I gene revealed 4 distinct genetic clades, each corresponding exactly to the respective 4 locations of the parasites in the host, suggesting the need for taxonomic revision. We hypothesized that each clade represented a separate species and, because the worms are morphologically indistinguishable, compared population level parameters of the clades comprising each currently recognized species. For each currently recognized species, the presence of worms from one clade was negatively correlated with the presence of worms from the other. Results also indicated significant differences between the clades in prevalences relative to both biotic and abiotic factors. Results clearly indicated major differences in the ecology of the philometrids constituting each clade. Taken as a whole, molecular and ecological data support the contention that the 4 genetic clades are likely 4 distinct species.

2011 McFadden, C.S., Y. Benayahu, E. Pante, J.N. Thoma, P.A. Nevarez and S.C. France. Limitations of Mitochondrial Gene Barcoding in Octocorallia. Molecular Ecology Resources 11: 19-31 (

The widespread assumption that COI and other mitochondrial genes will be ineffective DNA barcodes for anthozoan cnidarians has not been well tested for most anthozoans other than scleractinian corals. Here we examine the limitations of mitochondrial gene barcoding in the sub-class Octocorallia, a large, diverse and ecologically important group of anthozoans. Pairwise genetic distance values (uncorrected p) were compared for three candidate barcoding regions: the Folmer region of COI; a fragment of the octocoral-specific mitochondrial protein-coding gene, msh1; and an extended barcode of msh1 plus COI and a short, adjacent intergenic region (igr1). Intraspecific variation was <0.5%, with most species exhibiting no variation in any of the three gene regions. Interspecific divergence was also low: 18.5% of congeneric morphospecies shared identical COI barcodes, and there was no discernible barcoding gap between intra- and interspecific p values. In a case study to assess regional octocoral biodiversity, COI and msh1 barcodes each identified 70% of morphospecies. In a second case study, a nucleotide character-based analysis correctly identified 70% of species in the temperate genus Alcyonium. Although interspecific genetic distances were 2X greater for msh1 than COI, each marker identified similar numbers of species in the two case studies, and the extended COI+igr1+msh1 barcode more effectively discriminated sister taxa in Alcyonium. Although far from perfect for species identification, a COI+igr1+msh1 barcode nonetheless represents a valuable addition to the depauperate set of characters available for octocoral taxonomy.

2010 Pante E and France SC. Pseudochrysogorgia bellona n. gen., n. sp.: a new genus and species of chrysogorgiid octocoral (Coelenterata, Anthozoa) from the Coral Sea. Zoosystema 32: 595-612

A new genus and species of deep-sea Chrysogorgiidae Verrill, 1883, Pseudochrysogorgia bellona n. gen. n. sp., is described from colonies collected in the Coral Sea, West of New Caledonia (southwestern Pacifi c Ocean). Th ese specimens bear resemblance to the genera Chrysogorgia Duchassaing & Michelotti, 1864 (dichotomously-subdivided branches arising from the main stem in a spiraling fashion; polyps characterized by ornamented sclerites) and Metallo gorgia Versluys, 1902 (colony monopodial, hexagonal branching pattern). Additional material collected North of New Zealand (Otara Seamount) is used to complete the description of this new genus. Its taxonomic rank is discussed in light of morphology- and DNA-based phylogenetic inference and analysis of genetic distances among deep-sea chrysogorgiid genera.

2010 Wagner D, Brugler MR, Opresko DM, France SC, Montgomery AD and Toonen R. Using morphometrics, in situ observations and genetic characters to distinguish amongst commercially valuable Hawaiian black coral species; a redescription of Antipathes grandis Verrill, 1928 (Antipatharia: Antipathidae). Invertebrate Systematics 24: 271-290

The commercially valuable Hawaiian black coral Antipathes grandis is redescribed based on reexamination of the holotype from the Bernice P. Bishop Museum and field collections of 34 specimens from depths of 27–127 m. The first scanning electron micrographs of A. grandis skeletal spines are provided, along with a series of in situ colour photographs and morphometric measurements of spines and polyps. Three colour morphotypes were collected in the field (red, pale red, and white), none of which could be differentiated based on morphological or genetic characters (two mitochondrial and two nuclear markers). In situ observations are used in conjunction with morphological and genetic characters to distinguish amongst the commercially valuable Hawaiian black coral species A. grandis and A. griggi. A. grandis is differentiated from A. griggi by its finer and more irregular branching, smaller and more closely-spaced polyps, and conical spines that are smaller and not characterized by bifurcations towards their apex. Morphologically, the species most closely resembling A. grandis is A. caribbeana from the Caribbean. Among analyzed congenerics, DNA sequences of A. grandis were likewise most similar to those of A. caribbeana for three of the four molecular markers used in this study. A combination of low genetic variability, incomplete taxonomic sampling, and unexpected similarity between A. caribbeana and the unbranched whip coral Stichopathes cf. occidentalis, hindered our ability to determine the sister relationship of A. grandis. However, in no phylogenetic reconstruction did A. grandis group sister to its sympatric congener A. griggi.

2010 France, S.C., E. Pante, M. R. Brugler and J.L. van der Ham. On the evolution of deep-sea octocorals and antipatharians: Patterns revealed from molecular phylogenies. Integrative and Comparative Biology 50(Suppl. 1): E56-E56 [Conference abstract](online)

The discovery of high species diversity in the bathyal benthos has focused questions on the origin of deep-sea species and the processes that lead to speciation in this comparatively monotonous environment. We are exploring these questions using deep-sea corals as a model system, specifically three families of "gorgonians" (Anthozoa: Octocorallia) - Chrysogorgiidae, Isididae, and Primnoidae - and black corals (Anthozoa: Hexacorallia: Antipatharia), whose taxonomic diversity and abundance reach a maximum at depths >200 meters, although shallow-water representatives are known from each group. Phylogenetic analyses of DNA sequences reveal both the Chrysogorgiidae and Isididae are polyphyletic, but it is the inclusion of shallow-water taxa in these families that appear to be the cause: the strictly deep-sea genera cluster on robust monophyletic clades. The Primnoidae are monophyletic (except for the genus Acanthoprimnoa, whose placement on the tree may be affected by very long branch lengths), with shallow-water emergence at high latitudes for some species. The relationships among the deep-water clades from the different families remain unresolved due to short internal branch lengths in the phylogeny, an indication of a relatively-rapid radiation in the past coupled with the low substitution rate observed among octocorals. Among the black corals, the two families whose species are restricted to bathyal depths group as a monophyletic clade, distinct from families dominated by shelf-dwelling species. Our dataset still suffers from incomplete taxon sampling - a reflection of the difficulty of obtaining rare deep-sea specimens - but provides support that evolutionary radiations from deep-sea ancestors are common among these corals.

2010 McFadden, C.S., J.A. Sanchez and S.C. France. Molecular Phylogenetic Insights into the Evolution of Octocorallia: A Review. Integrative and Comparative Biology 50(3): 389-410 (doi: 10.1093/icb/icq056)

The anthozoan sub-class Octocorallia, comprising approximately 3000 species of soft corals, gorgonians, and sea pens, remains one of the most poorly understood groups of the phylum Cnidaria. Efforts to classify the soft corals and gorgonians at the suprafamilial level have long thwarted taxonomists, and the subordinal groups in current use are widely recognized to represent grades of colony forms rather than clades. Molecular phylogenetic analyses of the sub-class do not support either the current morphologically based subordinal or familial-level taxonomy. To date, however, the resolution necessary to propose an alternative, phylogenetic classification of Octocorallia or to elucidate patterns of morphological evolution within the group is lacking. Attempts to understand boundaries between species and interspecific or intraspecific phylogenetic relationships have been hampered by the very slow rate of mitochondrial gene evolution in Octocorallia, and a consequent dearth of molecular markers with variation sufficient to distinguish species (or sometimes genera). A review of the available ITS2 sequence data for octocorals, however, reveals a yet-unexplored phylogenetic signal both at sequence and secondary-structure levels. In addition, incongruence between mitochondrial and nuclear gene trees suggests that hybrid speciation and reticulate evolution may be an important mechanism of diversification in some genera. Emerging next-generation genomic-sequencing technologies offer the best hope for a breakthrough in our understanding of phylogenetic relationships and of evolution of morphological traits in Octocorallia. Genome and transcriptome sequencing may provide enough characters to resolve relationships at the deepest levels of the octocoral tree, while simultaneously offering an efficient means to screen for new genetic markers variable enough to distinguish species and populations.

2009 van der Ham, J.L., M.R. Brugler and S.C. France. Exploring the utility of an indel-rich, mitochondrial intergenic region as a molecular barcode for bamboo corals (Octocorallia: Isididae) Marine Genomics 2: 183-192 (

The DNA barcoding initiative has advocated the use of the 5'-end (~658bp) of mitochondrial (mt) cytochrome c oxidase I (cox1) to genetically distinguish species. However, this has proven difficult within the subclass Octocorallia due to extraordinarily low substitution rates within mt protein-coding genes. Intergenic regions (IGRs), which have been little examined among octocorals, may be subject to high mutation rates and have proven useful target regions at both the interspecific and population levels of metazoans. Herein we examine a mt IGR (igr4) between the cytochrome b (cob) and NADH dehydrogenase subunit 6 (nad6) genes among species of the bamboo coral subfamily Keratoisidinae to evaluate its utility for barcoding and phylogenetic studies. Among 77 keratoisidin specimens, we found igr4 to vary in length between either 42bp (Acanella Gray, 1870 and Orstomisis Bayer, 1990) or 302-605bp (Isidella Gray, 1857, Lepidisis Verrill, 1883, and Keratoisis Wright, 1869, and two undescribed genera). We interpreted the short igr4 sequence of Acanella eburnea (Pourtalčs, 1868) as potentially indicative of additional mt genome-related novelties and thus sequenced its entire mt genome; gene content and gene order were the same as in a previously-sequenced bamboo coral mt genome. Alignment of the longer igr4 sequences included 108 parsimony-informative characters, as well as numerous indels ranging from 2-262bp in length. Uncorrected pairwise 'p' distances indicated sequence variation of 0-27.2%, as compared to 0-4.8% among the same specimens for the MutS homolog (msh1), currently the most widely sequenced octocorallian mt gene, and <0.4% for cytochrome-c oxidase subunit 1 (cox1) for a subset of the taxa. Despite the greater levels of variation, fewer unique haplotypes were observed at igr4 compared to msh1; however, in combination, the two gene regions revealed increased mt haplotype diversity relative to either gene region on their own.

2009 Thoma, J.N., E. Pante, M.R. Brugler and S.C. France. Deep-sea octocorals and antipatharians show no evidence of seamount-scale endemism in the NW Atlantic. Marine Ecology Progress Series 397: 25-35 (Open Access:

Seamounts are undersea mountains commonly characterized by accelerated currents, exposed hard-substrates, and relatively high biomass and biodiversity. Hydrographic features associated with seamounts have led authors to hypothesize that benthic invertebrate populations from geographically-separated seamounts (and the continental slope) may experience varying degrees of genetic isolation, resulting in high levels of endemism.   While this hypothesis has been tested for multiple taxonomic groups in the Pacific, it has rarely been addressed in the Atlantic.   Herein, we test the null hypothesis that the geographic ranges of corals from NW Atlantic seamounts are restricted to individual seamounts.   We examined 188 octocoral and 50 antipatharian colonies (representing six and two genera, respectively) from 14 seamounts spanning 1700 km and the adjacent continental margin and estimated their genetic variation using mitochondrial loci ( msh1 for all octocorals, as well as an intergenic region for isidids, and three multi-gene spanning segments for antipatharians).   Well-sampled haplotypes were not geographically isolated on individual seamounts, thus refuting the hypothesis of local endemism of coral fauna on the New England Seamounts and Corner Seamounts. The narrow geographic distribution of rare haplotypes is most likely due to under-sampling rather than endemism. Our results do not preclude that cryptic variation and endemism not revealed by mitochondrial DNA may become evident should more variable markers be developed.

2008 Brugler, M.R. and S.C. France. The mitochondrial genome of a deep-sea bamboo coral (Cnidaria, Anthozoa, Octocorallia, Isididae): genome structure and putative origins of replication are not conserved among octocorals. Journal of Molecular Evolution 67: 125-136

Octocoral mitochondrial (mt) DNA is subject to an exceptionally low rate of substitution, and it has been suggested that mt genome content and structure are conserved across the subclass, an observation that has been supported for most octocorallian families by phylogenetic analyses using PCR products spanning gene boundaries. However, failure to recover amplification products spanning the nad4L-msh1 gene junction in species from the family Isididae (bamboo corals) prompted us to sequence the complete mt genome of a deep-sea bamboo coral (undescribed species). Compared to the ''typical'' octocoral mt genome, which has 12 genes transcribed on one strand and 5 genes on the opposite (cox2, atp8, atp6, cox3, trnM), in the bamboo coral genome a contiguous string of 5 genes (msh1, rnl, nad2, nad5, nad4) has undergone an inversion, likely in a single event. Analyses of strand-specific compositional asymmetry suggest that (i) the light-strand origin of replication was also inverted and is adjacent to nad4, and (ii) the orientation of the heavy-strand origin of replication (OriH) has reversed relative to that of previously known octocoral mt genomes. Comparative analyses suggest that intramitochondrial recombination and errors in replication at OriH may be responsible for changes in gene order in octocorals and hexacorals, respectively. Using primers flanking the regions at either end of the inverted set of five genes, we examined closely related taxa and determined that the novel gene order is restricted to the deep-sea subfamily Keratoisidinae; however, we found no evidence for strand-specific mutational biases that may influence phylogenetic analyses that include this subfamily of bamboo corals.

2007 France, S.C. Genetic analysis of bamboo corals (Cnidaria: Octocorallia: Isididae): does lack of colony branching distinguish Lepidisis from Keratoisis? Bulletin of Marine Science 81: 323-333

Bamboo corals (family Isididae) are among the most easily recognized deep-water octocorals due to their articulated skeleton comprised of non-sclerite calcareous internodes alternating with proteinaceous nodes. Most commonly encountered in the deep-sea are species in the subfamily Keratoisidinae, including the genera Acanella Gray, 1870, Isidella Gray, 1857, Keratoisis Wright, 1869, and Lepidisis Verrill, 1883. Systematists have debated whether Lepidisis and Keratoisis should be defined on the basis of “colony branching.” Although recent taxonomic keys use “colonies unbranched” to distinguish Lepidisis, the original description of the genus included both branched and unbranched morphologies, with both forms also classified in Keratoisis. This study analyzed mitochondrial DNA sequence variation from isidids collected between 500–2250 m depth to address the following question: are unbranched, whip-like bamboo corals in the subfamily Keratoisidinae monophyletic? DNA sequences of the msh1 gene (1426 nucleotides) from 32 isidids were used to construct a phylogeny. Coding of gaps provided additional informative characters for taxon discrimination. The results show five well-supported clades, all grouping both branched and unbranched colony morphologies; there was no single monophyletic clade of unbranched Keratoisidinae. The msh1 phylogeny suggests that the distinction between the genera Lepidisis and Keratoisis should not be based on whether or not colonies branch.

2007 Brugler, M.R. and S.C. France. The complete mitochondrial genome of the black coral Chrysopathes formosa (Cnidaria:Anthozoa:Antipatharia) supports classification of antipatharians within the subclass Hexacorallia. Molecular Phylogenetics and Evolution 42: 776-788

Black corals comprise a globally distributed shallow- and deep-water taxon whose phylogenetic position within the Anthozoa has been debated. We sequenced the complete mitochondrial genome of the antipatharian Chrysopathes formosa to further evaluate its phylogenetic relationships. The circular mitochondrial genome (18,398 bp) consists of 13 energy pathway protein-coding genes and two ribosomal RNAs, but only two transfer RNA genes (trnM and trnW), as well as a group I intron within the nad5 gene that contains the only copies of nad1 and nad3. No novel genes were found in the antipatharian mitochondrial genome. Gene order and genome content are most similar to those of the sea anemone Metridium senile (subclass Hexacorallia), with differences being the relative location of three contiguous genes (cox2-nad4-nad6) and absence (from the antipatharian) of a group I intron within the cox1 gene. Phylogenetic analyses of multiple protein-coding genes support classifying the Antipatharia within the subclass Hexacorallia and not the subclass Ceriantipatharia; however, the sister-taxon relationships of black corals within Hexacorallia remain inconclusive.

2006 McFadden, C.S., S.C. France, J.A. Sánchez and P. Alderslade. A molecular phylogenetic analysis of the Octocorallia (Cnidaria: Anthozoa) based on mitochondrial protein-coding sequences (ND2, msh1). Molecular Phylogenetics and Evolution 41: 513-527

Despite their abundance and ecological importance in a wide variety of shallow and deep water marine communities, octocorals (soft corals, sea fans, and sea pens) are a group whose taxonomy and phylogenetic relationships remain poorly known and little studied. The group is currently divided into three orders (O: Alcyonacea, Pennatulacea, and Helioporacea); the large O. Alcyonacea (soft corals and sea fans) is further subdivided into six sub-ordinal groups on the basis of skeletal composition and colony growth form. We used 1429 bp of two mitochondrial protein-coding genes, ND2 and msh1 , to construct a phylogeny for 103 octocoral genera representing 28 families. In agreement with a previous 18S rDNA phylogeny, our results support a division of Octocorallia into two major clades plus a third, minor clade. We found one large clade (Holaxonia-Alcyoniina) comprising the sea fan sub-order Holaxonia and the majority of soft corals, and a second clade (Calcaxonia-Pennatulacea) comprising sea pens (O. Pennatulacea) and the sea fan sub-order Calcaxonia. Taxa belonging to the sea fan group Scleraxonia and the soft coral family Alcyoniidae were divided among the Holaxonia-Alcyoniina clade and a third, small clade ( Anthomastus-Corallium ) whose relationship to the two major clades was unresolved. In contrast to the previous studies, we found sea pens to be monophyletic but nested within Calcaxonia; our analyses support the sea fan family Ellisellidae as the sister taxon to the sea pens. We are unable to reject the hypothesis that the calcaxonian and holaxonian skeletal axes each arose once and suggest that the skeletal axis of sea pens is derived from that of Calcaxonia. Topology tests rejected the monophyly of sub-ordinal groups Alcyoniina, Scleraxonia, and Stolonifera, as well as 9 of 14 families for which we sampled multiple genera. The much broader taxon sampling and better phylogenetic resolution afforded by our study relative to the previous efforts greatly clarify the relationships among families and subordinal groups within each of the major clades. The failure of these mitochondrial genes as well as previous 18S rDNA studies to resolve many of the deeper nodes within the tree (including its root) suggest that octocorals underwent a rapid radiation and that large amounts of sequence data will be required in order to resolve the basal relationships within the clade.

2004 Smith, P. J. , S. M. McVeagh, J. T. Mingoia, and S. C. France. Mitochondrial DNA sequence variation in deep-sea bamboo coral (Keratoisidinae) species in the southwest and northwest Pacific Ocean. Marine Biology 144: 253-261

The Keratoisidinae are a poorly known, but phenotypically diverse group of deepwater corals. Recent developments in deepwater trawling in the southwest Pacific have provided many more specimens of bamboo corals. Two sub-regions of the mitochondrial genome were sequenced to test genetic relationships among specimens collected over a wide geographical range (27-50°S): a sub-region of the large-subunit rRNA (16S rRNA), characterized by a highly variable insertion/deletion (INDEL#2) region; and a non-coding region between COII and COI. Based on DNA haplotypes, 14 species of Keratoisidinae were recognized among 88 specimens from deep water in the southwest Pacific Ocean. The common haplotypes also appeared in specimens collected in the northwest Pacific Ocean and may indicate that some bamboo coral species are widespread in the Pacific, or that the mitochondrial markers are insensitive to recent speciation events. Many specimens were taken from flat bottom areas and, contrary to assumptions, the bamboo corals are not endemic to seamounts. The closure of some seamounts to trawling will protect bamboo corals from extinction, but not from local depletion.

2002 France, S. C., and L. L. Hoover. DNA sequences of the mitochondrial COI gene have low levels of divergence among deep-sea octocorals (Cnidaria: Anthozoa). Hydrobiologia 471: 149-155

Abstract. We are analyzing genetic diversity in deep-seamount octocorals with the ultimate goal of studying the effect of retention and dispersal of larvae on genetic population structure. Here we report on the sequence diversity of the mitochondrial cytochrome oxidase I (COI) gene among 11 species. Uncorrected pairwise sequence divergences ranged from 0.4% – 10.3% for comparisons among species spanning the intrageneric to interordinal levels. Relative to other invertebrates, these divergences are very low, suggesting that COI may not be useful as a genetic marker for studying dispersal among deep-sea octocoral populations. Possible explanations for the reduced rates of divergence observed include a lower rate of evolution for octocoral mitochondrial genomes and the presence of a gene, mtMSH, which may code for a mitochondrial DNA mismatch-repair system. We report the finding of mtMSH in three deep-sea octocorals (Acanthogorgia sp., Corallium ducale, and Paramuricea sp.), which brings the total published observations of this gene to six species, all in the subclass Octocorallia.

2001 France, S. C., and L. L. Hoover. Analysis of variation in mitochondrial DNA sequences (ND3, ND4L, MSH) among Octocorallia (=Alcyonaria) (Cnidaria: Anthozoa). Bulletin of the Biological Society of Washington 10:110-118

Abstract. We have sequenced a portion of the mitochondrial genome encompassing ND3, ND4L and mtMSH, and the two non-coding regions (NCRs) between the genes, from 15 species of Octocorallia. ND4L has a lower substitution rate than ND3, and mtMSH shows the highest rate of substitution, with approximately twice the percentage of variable sites as the NADH genes. There were no insertions or deletions in any of the protein-coding sequences, but the NCRs ranged from 4 bp to a maximum of 39 bp in length. In a limited sample, we observed no variation in NCR sequences among conspecific individuals, nor in some cases, in interspecific comparisons. This report now brings the total published observations of a mitochondrial mismatch repair gene homologue (mtMSH) to 18 species, all in the subclass Octocorallia (=Alcyonaria).

2001 Berntson, E. A., F. M. Bayer, A. G. Mcarthur, and S. C. France. Phylogenetic relationships within the Octocorallia (Cnidaria: Anthozoa) based on nuclear 18S rRNA sequences. Marine Biology 138:235-246.

Abstract. We determined the nuclear 18S rRNA sequences for 41 species of octocorals and used these to address the validity of the historical ordinal divisions and the current subordinal divisions within the Subclass Octocorallia. We also explored the phylogenetic affinities of the species Dendrobrachia paucispina, which was originally classified in the Order Antipatharia (subclass Ceriantipatharia) although polyp structure indicates it belongs in the Subclass Octocorallia. Trees constructed using maximum likelihood techniques are incongruent with the current and historical taxonomy of the Octocorallia. There appear to be three major clades of octocorals. The first clade included most but not all pennatulaceans as a monophyletic group. The second clade contained 21 species representing all major octocoral groups other than pennatulacenas. The third clade contained members from three suborders of the Alcyonacea and one member of the Pennatulacea. These data could not be used to distinguish the branching order of the three major clades. The species D. paucispina had a close affinity with the genera Corallium and Paragorgia (Alcyonacea: Scleraxonia) although its morphology suggests it is more similar to the genus Chrysogorgia (Alcyonacea: Calcaxonia). The morphological character of dimorphism (the presence of both autozooids and siphonozooids within a single colony) corresponded loosely with the topology of the most likely trees and a single origin of dimorphism could not be rejected. Despite sampling from the majority of families within the Octocorallia, many of the relationships within this group remain ambiguous.

1999 Rosel, P.E.., S. C. France, J.Y. Wang and T. D. Kocher. Genetic structure of harbour porpoise Phocoena phocoena populations in the Northwest Atlantic based on mitochondrial and nuclear markers. Molecular Ecology 8: S41-S54

Abstract. The harbour porpoise, Phocoena phocoena, experiences high levels of non-natural mortality due to interactions with commercial fisheries throughout its range. To accurately evaluate the significance of this bycatch, information on population structure is needed. We have examined the population structure of this species in the Northwest Atlantic Ocean using mitochondrial DNA sequence and nuclear microsatellite data. Samples from four previously proposed summer breeding populations - Gulf of Maine, eastern Newfoundland, the Gulf of St. Lawrence, and West Greenland - were analyzed. Control region sequences revealed a significant partitioning of genetic variation among most of these summer populations, indicating that Northwest Atlantic harbour porpoises should not be considered one panmictic population. Analysis of females alone yielded the highest levels of population subdivision, suggesting females are more philopatric than males. At least three management units may be defined for harbour porpoises in the Northwest Atlantic based on these data. Analysis of six microsatellite loci failed to detect significant population subdivision. Male-mediated gene flow may maintain homogeneity among nuclear loci, while female philopatry is sufficient to produce a signal of population subdivision in the maternally inherited mtDNA genome. MtDNA analyses also indicate that winter aggregations of harbour porpoises along the U.S. mid-Atlantic states are comprised of animals from more than one summer breeding population.

1999 France, S.C., N. Tachino, T.F. Duda, Jr., R.A. Shleser and S.R. Palumbi. Intraspecific genetic diversity in the marine shrimp Penaeus vannamei: multiple polymorphic elongation factor-1alpha loci revealed by intron sequencing. Marine Biotechnology 1: 261-268

Abstract. Intron sequences from the elongation factor 1alpha (EF1a) gene from the marine shrimp Penaeus vannamei reveal extensive variation even among inbred populations of hatchery-raised shrimp. Among 44 individuals analyzed, we found 13 alleles varying by up to 7.5% sequence differences, and including several allele-diagnostic insertions and deletions. High heterozygosity contrasts with low genetic variation at allozyme loci, but we observed up to 4 alleles per individual, suggesting that we have identified two separate, polymorphic loci. We partitioned the observed alleles into two groups representing hypothetical duplicated loci. However, the alleles are so similar to one another that a phylogenetic analysis does not cluster them into monophyletic groupings. A possible explanation is that concerted evolution is acting to homogenize genetic variation among these two putative loci.

1999 Berntson, E. A., S. C. France and L. S. Mullineaux. Phylogenetic Relationships within the Class Anthozoa (Phylum Cnidaria) Based on Nuclear 18S rDNA Sequence Information. Molecular Phylogenetics and Evolution 13(2): 417-433

Abstract. Taxonomic relationships within the corals and anemones (Phylum Cnidaria: Class Anthozoa) are based upon few morphological characters. The significance of any given character is debatable, and there is little fossil record available for deriving evolutionary relationships. We analyzed complete 18S ribosomal sequences to examine subclass-level and ordinal-level organization within the Anthozoa. We suggest that the Subclass Ceriantipatharia is not an evolutionarily relevant grouping. The Order Corallimorpharia appears paraphyletic, and closely related to the Order Scleractinia. The 18S rRNA gene may be insufficient for establishing robust phylogenetic hypotheses concerning the specific relationships of the Corallimorpharia and the Ceriantharia, and the branching sequence for the orders within the Hexacorallia. The 18S rRNA gene has sufficient phylogenetic signal, however, to distinguish among the major groupings within the Class Anthozoa, and we use this information to suggest relationships for the enigmatic taxa Dactylanthus and Dendrobrachia.

1996 France, S. C. & T. D. Kocher. DNA sequencing of formalin-fixed crustaceans from archival research collections. Molecular Marine Biology and Biotechnology 5 (4): 304-313

Abstract. Marine invertebrate collections have historically been maintained in ethanol following fixation in formalin. These collections may represent rare or extinct species or populations, provide detailed time-series samples, or come from presently inaccessible or difficult-to-sample localities. We have tested the viability of obtaining DNA sequence data from formalin-fixed, ethanol-preserved (FFEP) deep-sea crustaceans, and found that nucleotide sequences for mitochondrial 16S rRNA and COI genes can be recovered from FFEP collections of varying age, and that these sequences are unmodified compared to those derived from frozen specimens. These results were repeatable among multiple specimens and collections for several species. Our results indicate that in the absence of fresh or frozen tissues, archived, FFEP specimens may prove a useful source of material for analysis of gene sequence data by PCR and direct sequencing.

1996 France, S. C. & T. D. Kocher. Geographic and bathymetric patterns of mitochondrial 16S rRNA sequence divergence among deep-sea amphipods, Eurythenes gryllus. Marine Biology 126: 633-644

Abstract. The physical uniformity of the deep sea suggests a lack of absolute barriers to faunal dispersal and thus genetic homogeneity in broadly-distributed species is expected. The deep-sea amphipod Eurythenes gryllus Lichtenstein (Lysianassoidea, Crustacea) is considered a panoceanic, cold-water stenotherm, with a vertical depth distribution from 184 to 6500 m. We surveyed mtDNA sequence diversity in E. gryllus to assess genetic diversity and population structure in different oceans and across traditionally defined bathyal and abyssal zones. DNA sequences (437 nucleotides length) from the mitochondrial large-subunit ribosomal RNA gene (16S rRNA) of 95 individuals, collected between 1982 to 1990 from 14 locations in the central North Pacific (including multiple samples on the slope of a seamount), eastern and western North Atlantic, and the Arctic Ocean, were obtained. Our analysis of DNA sequence diversity indicates 1) genetic homogeneity among sites within the same depth zone at the scale of ocean basins; and 2) genetically-divergent, cryptic taxa distributed at different depths, with the greatest diversity in the bathyal zone. These observations suggest that ecological and physical conditions are important isolating mechanisms that may lead to speciation in this group.

1996 France, S. C., P. E. Rosel, J. E. Agenbroad, L.S. Mullineaux, & T. D. Kocher. DNA sequence variation of mitochondrial large-subunit rRNA provides support for a two subclass organization of the Anthozoa (Cnidaria). Molecular Marine Biology and Biotechnology 5 (1): 15-28

Abstract. We have sequenced a portion of the mitochondrial 16S rRNA gene from 29 species of Anthozoa, representing six orders of the subclasses Ceriantipatharia, Hexacorallia, and Octocorallia, with the focus on deep-seamount corals ( 500 meters depth). We have detected significant length variation in the gene, with homologous gene fragments ranging from 545 base pairs (bp) in a shallow-water scleractinian coral to 911 bp in a deep-sea antipatharian black coral. The aligned sequences were divided into five regions: three high-identity sequence blocks (HSBs) and two highly variable blocks (INDELs). Most of the length variation among species occurred as varying numbers of nucleotides in the two INDELs. Little or no intraspecific sequence variation was detected over spatial scales of up to Ĺ150 km. Interspecific sequence variation was lowest among the octocorals and greatest among the ceriantipatharians. Our data indicate that the orders Ceriantharia and Antipatharia are highly divergent, and a phylogenetic reconstruction provides support for the two subclass system of the Class Anthozoa (Hexacorallia and Octocorallia).

1994 France, S. C. Genetic population structure and gene flow among deep-sea amphipods, Abyssorchomene spp., from six California Continental Borderland basins. Marine Biology 118: 67-77

Abstract. Studies of geographic population variation needed to estimate gene flow are lacking in deep-sea biology. Using allozyme electrophoresis, I have studied population-level geographic variation among scavenging lysianassoid amphipod populations (Abyssorchomene spp.) inhabiting deep-water basins of the Southern California Continental Borderland. Samples were collected from November, 1987 to November, 1990, using baited traps, from 6 basins whose bottom depths ranged from ~1000 - 2100 m. Five basins (San Diego Trough, Santa Catalina, San Nicolas, Santa Cruz, Tanner Basins) could be grouped together as "shallow-sill" basins, with physical conditions distinctly different from a single "deep-sill" basin (San Clemente Basin). Amphipods tentatively identified as Abyssorchomene sp. 1 collected from the shallow-sill basins were morphologically discriminated from those collected in the San Clemente Basin, which were identified as Abyssorchomene sp. 2. Results from 8 enzyme loci revealed significant genetic differentiation [Nei's genetic distance (D) > 0.155] of deep-sill basin-dwelling Abyssorchomene sp. 2 vs. Abyssorchomene sp. 1 from the shallow-sill basins and low levels of gene flow (migration rate, M < 1). Comparisons of benthic fauna suggest the presence of an abyssal-related assemblage in the deep-sill basin isolated from the northern shallow-sill basins. Genetic distance among the 5 shallow-sill basin populations of Abyssorchomene sp. 1 was very low (D < 0.003). Estimates of gene flow among these populations were very high (M ~ 24 - 170) and suggested weak isolation by distance.

1993 France, S. C. Geographic variation among three isolated populations of the hadal amphipod Hirondellea gigas (Crustacea: Amphipoda: Lysianassoidea). Marine Ecology Progress Series 92:277-287

Abstract. The relative homogeneity and continuity of the deep sea may provide a habitat in which species can maintain widespread, genetically homogeneous populations. This study examines the lysianassoid amphipod Hirondellea gigas (Birstein and Vinogradov 1955) to determine whether populations from spatially-disjunct habitats in the deep-sea maintain genetic homogeneity. H. gigas is a scavenger which rapidly responds to and consumes experimental baitfalls at depths of 10000 meters. It appears to be endemic to western Pacific trenches, having been collected only within the Kurile-Kamchatka, Japan, Izu-Bonin, Volcano, Yap, Mariana, Palau, and Philippine Trenches. To estimate the degree of isolation of populations from the last three trenches, morphological variation was quantified through a discriminant analysis of surficial morphometric characters. Discriminant classification results were compared to "null-populations," generated using a bootstrap randomization procedure, to determine the significance of the discrimination. Variation was sufficient to allow 68.4 - 84.5 % of individuals to be correctly reclassified into their population using discriminant functions. Bootstrapped randomizations of the data indicate that the classification success was significantly greater than random. The results indicate that these geographically-isolated trench populations may have reduced levels of gene flow between them, causing them to diverge morphologically.

1992 France, S. C., R. C. Vrijenhoek & R. R. Hessler. Genetic differentiation between spatially-disjunct populations of the deep-sea, hydrothermal vent-endemic amphipod Ventiella sulfuris. Marine Biology 114: 551-559

Abstract. Species endemic to deep-sea hydrothermal vent ecosystems have disjunct distributions imposed by the island-like arrangement of their specialized habitats. Using allozyme electrophoresis, we examined genetic population structure of the hydrothermal vent amphipod Ventiella sulfuris Barnard & Ingram, 1990. Samples from five sites along the East Pacific Rise (EPR) and two along the Galapagos Rift were collected in 1990 and 1988 respectively. Variability, based on 12 enzyme loci, was relatively high (P95 = 41.6%; H = 0.158) compared with shallow-water marine and freshwater amphipods, and similar to the deep-sea lysianassid Eurythenes gryllus. Genetic divergence among populations spread along a contiguous rift axis (i.e. EPR) was low (Nei's D ranged from > 0.001 - 0.018). Genetic structure analysis suggests that along a contiguous ridge axis migration occurs in a stepping stone manner and is unconstrained by distances as great as 1200 km (migration rate, M, ranged from 1.9 - 67.8 individuals per generation). However, genetic divergence between populations on disjunct ridge axes was extremely high (D ranged from 0.438 - 0.476). Most of the variance in gene frequencies was due to the differences between the major subpopulations inhabiting the two distinct ridge axes, EPR and Galapagos Rift. Apparently, very little migration and gene flow occur between these major subpopulations (M << 1). This level of genetic divergence may be sufficient to justify separation of EPR and Galapagos Rift populations at the species level. Further analyses of morphological characters is required before taxonomic status can be assigned.

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