Species boundaries of Gulf of Mexico vestimentiferans (Polychaeta, Siboglinidae) inferred from mitochondrial genes

Abstract

At least six morphospecies of vestimentiferan tubeworms are associated with cold seeps in the Gulf of Mexico (GOM). The physiology and ecology of the two best-studied species from depths above 1000 m in the upper Louisiana slope (Lamellibrachia luymesi and Seepiophila jonesi) are relatively well understood. The biology of one rare species from the upper slope (escarpiid sp. nov.) and three morphospecies found at greater depths in the GOM (Lamellibrachia sp. 1, L. sp. 2, and Escarpia laminata) are not as well understood. Here we address species distributions and boundaries of cold-seep tubeworms using phylogenetic hypotheses based on two mitochondrial genes. Fragments of the mitochondrial large ribosomal subunit rDNA (16S) and cytochrome oxidase subunit I (COI) genes were sequenced for 167 vestimentiferans collected from the GOM and analyzed in the context of other seep vestimentiferans for which sequence data were available. The analysis supported five monophyletic clades of vestimentiferans in the GOM. Intra-clade variation in both genes was very low, and there was no apparent correlation between the within-clade diversity and collection depth or location. Two of the morphospecies of Lamellibrachia from different depths in the GOM could not be distinguished by either mitochondrial gene. Similarly, E. laminata could not be distinguished from other described species of Escarpia from either the west coast of Africa or the eastern Pacific using COI. We suggest that the mitochondrial COI and 16S genes have little utility as barcoding markers for seep vestimentiferan tubeworms.

Introduction

For the better part of the last century, marine biologists assumed oceans were largely interconnected by currents that enabled larvae and propagules to reach distant shores and assure gene flow even over great distances. More recently, the use of molecular tools has challenged assumptions regarding population structure and speciation in the ocean and demonstrated that marine animals often have genetically distinct populations despite geographic proximity (Palumbi and Warner, 2003). Although sharp genetic breaks between close populations have been recorded throughout the ocean, most of what is known about speciation patterns and phylogeography has been inferred from shallow-water and coastal systems, which represent only about 15% of the aquatic environment. Thus, our knowledge of processes that lead to population divergence and speciation in the open ocean is relatively limited (Thornhill et al., 2008, and references therein; Zardus et al., 2006).

Vestimentiferan tubeworms, which include 10 genera in the polychaete family Siboglinidae (Halanych et al., 2001, Kojima et al., 2002, McMullin et al., 2003, Rouse, 2001), are abundant at deep-sea hydrothermal vents and cold seeps at depths ranging from 80 to 9345 m (Cordes et al., 2007b, Mironov, 2000, Miura et al., 2002). In the deep Gulf of Mexico, six morphospecies have been reported (Cordes et al., 2009). Two described species, Lamellibrachia luymesi (van der Land and Narrevang, 1975) and Seepiophila jonesi (Gardiner et al., 2001), are relatively well studied, and their ecology and physiology are well understood (Bergquist et al., 2002, Cordes et al., 2007a, Cordes et al., 2007b). They occur on the upper Louisiana slope at between ∼500 and 950 m depth and occasionally co-occur with a rare undescribed species, escarpiid sp. nov. The three other morphological species are found on the lower Louisiana slope at depths greater than about 950 m (Lamellibrachia sp. 1, L. sp. 2, and Escarpia laminata).

In this paper, we present phylogenetic hypotheses based on the mitochondrial large ribosomal subunit rDNA gene (16S) and mitochondrial cytochrome oxidase 1 gene (COI) of over 200 vestimentiferans (sequenced for either or both genes) including 180 individuals from the six morphospecies that occur in the Gulf of Mexico. Phylogenetic trees are used to examine the distribution of vestimentiferans in the Gulf of Mexico and their relations to other vestimentiferans around the world. We examined the concordance between the morphological and phylogenetic data to identify differences between the genealogical and morphological species analyzed. Finally, we compared between- and within-species 16S and COI genetic distances and show that these two mitochondrial genes have little utility as “barcoding molecules” for vestimentiferans.