Biogeography and genetic diversity of the atlantid heteropods.

The atlantid heteropods are regularly encountered, but rarely studied marine planktonic gastropods. Relying on a small (<14 mm), delicate aragonite shell and living in the upper ocean means that, in common with pteropods, atlantids are likely to be affected by imminent ocean changes. Variable shell morphology and widespread distributions indicate that the family is more diverse than the 23 currently known species. Uncovering this diversity is fundamental to determining the distribution of atlantids and to understanding their environmental tolerances. Here we present phylogenetic analyses of all described species of the family Atlantidae using 437 new and 52 previously published cytochrome c oxidase subunit 1 mitochondrial DNA (mtCO1) sequences. Specimens and published sequences were gathered from 32 Atlantic Ocean stations, 14 Indian Ocean stations and 21 Pacific Ocean stations between 35°N and 43°S. DNA barcoding and Automatic Barcode Gap Discovery (ABGD) proved to be valuable tools for the identification of described atlantid species, and also revealed ten additional distinct clades, suggesting that the diversity within this family has been underestimated. Only two of these clades displayed obvious morphological characteristics, demonstrating that much of the newly discovered diversity is hidden from morphology-based identification techniques. Investigation of six large atlantid collections demonstrated that 61% of previously described (morpho) species have a circumglobal distribution. Of the remaining 39%, two species were restricted to the Atlantic Ocean, five occurred in the Indian and Pacific oceans, one species was only found in the northeast Pacific Ocean, and one occurred only in the Southern Subtropical Convergence Zone. Molecular analysis showed that seven of the species with wide distributions were comprised of two or more clades that occupied distinct oceanographic regions. These distributions may suggest narrower environmental tolerances than the described morphospecies. Results provide an updated biogeography and mtCO1 reference dataset of the Atlantidae that may be used to identify atlantid species and provide a first step in understanding their evolutionary history and accurate distribution, encouraging the inclusion of this family in future plankton research.

Global biogeography and evolution of Cuvierina pteropods.

BACKGROUND: Shelled pteropods are planktonic gastropods that are potentially good indicators of the effects of ocean acidification. They also have high potential for the study of zooplankton evolution because they are metazoan plankton with a good fossil record. We investigated phenotypic and genetic variation in pteropods belonging to the genus Cuvierina in relation to their biogeographic distribution across the world's oceans. We aimed to assess species boundaries and to reconstruct their evolutionary history. RESULTS: We distinguished six morphotypes based on geometric morphometric analyses of shells from 926 museum and 113 fresh specimens. These morphotypes have distinct geographic distributions across the Atlantic, Pacific and Indian oceans, and belong to three major genetic clades based on COI and 28S DNA sequence data. Using a fossil-calibrated phylogeny, we estimated that these clades separated in the Late Oligocene and Early to Middle Miocene. We found evidence for ecological differentiation among all morphotypes based on ecological niche modelling with sea surface temperature, salinity and phytoplankton biomass as primary determinants. Across all analyses, we found highly congruent patterns of differentiation suggesting species level divergences between morphotypes. However, we also found distinct morphotypes (e.g. in the Atlantic Ocean) that were ecologically, but not genetically differentiated. CONCLUSIONS: Given the distinct ecological and phenotypic specializations found among both described and undescribed Cuvierina taxa, they may not respond equally to future ocean changes and may not be equally sensitive to ocean acidification. Our findings support the view that ecological differentiation may be an important driving force in the speciation of zooplankton.

Time-calibrated molecular phylogeny of pteropods.

Pteropods are a widespread group of holoplanktonic gastropod molluscs and are uniquely suitable for study of long-term evolutionary processes in the open ocean because they are the only living metazoan plankton with a good fossil record. Pteropods have been proposed as bioindicators to monitor the impacts of ocean acidification and in consequence have attracted considerable research interest, however, a robust evolutionary framework for the group is still lacking. Here we reconstruct their phylogenetic relationships and examine the evolutionary history of pteropods based on combined analyses of Cytochrome Oxidase I, 28S, and 18S ribosomal rRNA sequences and a molecular clock calibrated using fossils and the estimated timing of the formation of the Isthmus of Panama. Euthecosomes with uncoiled shells were monophyletic with Creseis as the earliest diverging lineage, estimated at 41-38 million years ago (mya). The coiled euthecosomes (Limacina, Heliconoides, Thielea) were not monophyletic contrary to the accepted morphology-based taxonomy; however, due to their high rate heterogeneity no firm conclusions can be drawn. We found strong support for monophyly of most euthecosome genera, but Clio appeared as a polyphyletic group, and Diacavolinia grouped within Cavolinia, making the latter genus paraphyletic. The highest evolutionary rates were observed in Heliconoides inflatus and Limacina bulimoides for both 28S and 18S partitions. Using a fossil-calibrated phylogeny that sets the first occurrence of coiled euthecosomes at 79-66 mya, we estimate that uncoiled euthecosomes evolved 51-42 mya and that most extant uncoiled genera originated 40-15 mya. These findings are congruent with a molecular clock analysis using the Isthmus of Panama formation as an independent calibration. Although not all phylogenetic relationships could be resolved based on three molecular markers, this study provides a useful resource to study pteropod diversity and provides general insight into the processes that generate and maintain their diversity in the open ocean.

Revision of the genus Cuvierina Boas, 1886 based on integrative taxonomic data, including the description of a new species from the Pacific Ocean (Gastropoda, Thecosomata).

Shelled pteropods (Gastropoda, Thecosomata, Euthecosomata) are a group of holoplanktonic gastropods that occur predominantly in the surface layers of the world's oceans. Accurate species identifications are essential for tracking changes in species assemblages of planktonic gastropods, because different species are expected to have different sensitivities to ocean changes. The genus Cuvierina has a worldwide warm water distribution pattern between ~36°N and ~39°S. Based on an integrative taxonomic approach combining morphometric, genetic, and biogeographic information, the two subgenera of Cuvierina, Cuvierinas. str. and Urceolarica, are rejected. A new species is introduced: Cuvierina tsudaisp. n., which has to date been considered the same species as Cuvierina pacifica. Cuvierina tsudaisp. n. is endemic to the Pacific Ocean and is characterised by a shell height of 7.2-8.0 mm, a moderately cylindrical shell shape, the absence of micro-ornamentation and a triangular aperture. Cuvierina pacifica is restricted to the centre of the oligotrophic southern Pacific gyre, has a shell height of 6.6-8.5 mm, a more cylindrical shell shape, no micro-ornamentation and a less triangular aperture than Cuvierina tsudaisp. n.

Atlanta ariejansseni, a new species of shelled heteropod from the Southern Subtropical Convergence Zone (Gastropoda, Pterotracheoidea).

The Atlantidae (shelled heteropods) is a family of microscopic aragonite shelled holoplanktonic gastropods with a wide biogeographical distribution in tropical, sub-tropical and temperate waters. The aragonite shell and surface ocean habitat of the atlantids makes them particularly susceptible to ocean acidification and ocean warming, and atlantids are likely to be useful indicators of these changes. However, we still lack fundamental information on their taxonomy and biogeography, which is essential for monitoring the effects of a changing ocean. Integrated morphological and molecular approaches to taxonomy have been employed to improve the assessment of species boundaries, which give a more accurate picture of species distributions. Here a new species of atlantid heteropod is described based on shell morphology, DNA barcoding of the Cytochrome Oxidase I gene, and biogeography. All specimens of Atlanta ariejansseni sp. n. were collected from the Southern Subtropical Convergence Zone of the Atlantic and Indo-Pacific oceans suggesting that this species has a very narrow latitudinal distribution (37-48°S). Atlanta ariejansseni sp. n. was found to be relatively abundant (up to 2.3 specimens per 1000 m(3) water) within this narrow latitudinal range, implying that this species has adapted to the specific conditions of the Southern Subtropical Convergence Zone and has a high tolerance to the varying ocean parameters in this region.