Unexpected molecular and morphological diversity of hemichordate larvae from the Neotropics

Abstract

The diversity of tropical marine invertebrates is poorly documented, especially those groups for which collecting adults is difficult. We collected the planktonic tornaria larvae of hemichordates (acorn worms) to assess their hidden diversity in the Neotropics. Larvae were retrieved in plankton tows from waters of the Pacific and Caribbean coasts of Panama, followed by DNA barcoding of mitochondrial cytochrome c oxidase subunit I (COI) and 16S ribosomal DNA to estimate their diversity in the region. With moderate sampling efforts, we discovered six operational taxonomic units (OTUs) in the Bay of Panama on the Pacific coast, in contrast to the single species previously recorded for the entire Tropical Eastern Pacific. We found eight OTUs in Bocas del Toro province on the Caribbean coast, compared to seven species documented from adults in the entire Caribbean. All OTUs differed from each other and from named acorn worm sequences in GenBank by >10% pairwise distance in COI and >2% in 16S. Two of our OTUs matched 16S hemichordate sequences in GenBank: one was an unidentified or unnamed Balanoglossus from the Caribbean of Panama, and the other was an unidentified ptychoderid larva from the Bahamas. The species accumulation curves suggest that nearly all the species have been collected and only one more species might still remain undetected in the Pacific. In contrast, the Caribbean species accumulation curve suggests that further sampling could yield more than 10 additional OTUs. Tornaria from the 14 OTUs exhibited typical planktotrophic morphologies, and, in some cases, may be distinguished by differences in pigmentation and by the number of telotrochal ciliary bands, but in general, few diagnostic differences were detected.

Knots, spoons, and cloches: DNA barcoding unusual larval forms helps document the diversity of Neotropical marine annelids

“…Sequences are not available for A. panamensis and the available sequence for A. belyaevi is for an animal collected from near South Orkney Islands (Goto et al., 2020), which brings into question the veracity of the record of this species in Panama. Such significant increases in species diversity are typical of barcoding studies focusing on larvae from poorly studied groups of invertebrates (Barber & Boyce, 2006; Collin, Venera‐Pontón, Driskell, Chan, et al, 2019; Collin, Venera‐Pontón, Driskell, MacDonald, et al., 2019; Mahon et al., 2010).…”

Sampling multiple life stages significantly increases estimates of marine biodiversity

“…In a pioneering study, Barber and Boyce [7] found that only 50% of the gonodactyloid stomatopod larval operational taxonomic units (OTUs) collected in the Coral Triangle could be matched to adults, despite having reference sequences for more than 90% of the known species from the region. Studies focused on planktonic stages in less well-studied regions, or of understudied groups like hemichordates, phoronids or certain families of polychaetes, report similar or greater match discrepancies, likely due to poor sampling of the adult fauna [8][9][10][11][12]. However, even studies that include both life stages report larvae for which the adult forms have not been detected [13,14] or were not sampled at the same site [15].…”

How I wonder what you are: Can DNA barcoding identify the larval asteroids of Panama?

“…Surveys of marine invertebrate larvae are a powerful tool for the detection of hidden diversity (Barber & Boyce, 2006; Collin, et al., 2019; Collin et al, 2019a, 2019b; Mahon et al., 2010). They may be particularly effective at capturing deep‐water, small, or infaunal species that are difficult to collect as adults by use of standard sampling techniques, and thus provide an independent assessment of diversity that complements species lists based solely on studies of adults (Collin, et al., 2020; Mahon et al., 2010; Sewell & Jury, 2011).…”