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Research Article
Resolving species boundaries in the Atlanta brunnea species group (Gastropoda, Pterotracheoidea)
expand article infoDeborah Wall-Palmer, Mona Hegmann§, Erica Goetze|, Katja T. C. A. Peijnenburg
‡ Naturalis Biodiversity Center, Leiden, Netherlands
§ University of Rostock, Rostock, Germany
| University of Hawaii at Manoa, Hawaii, United States of America
¶ University of Amsterdam, Amsterdam, Netherlands
Open Access

Abstract

Atlantid heteropods are a family of holoplanktonic marine gastropods that occur primarily in tropical and subtropical latitudes. Atlantids bear a delicate aragonitic shell (<14 mm) and live in the upper ocean, where ocean acidification and ocean warming have a pronounced effect. Therefore, atlantids are likely to be sensitive to these ocean changes. However, we lack sufficiently detailed information on atlantid taxonomy and biogeography, which is needed to gain a deeper understanding of the consequences of a changing ocean. To date, atlantid taxonomy has mainly relied on morphometrics and shell ornamentation, but recent molecular work has highlighted hidden diversity. This study uses an integrated approach in a global analysis of biogeography, variation in shell morphology and molecular phylogenies based on three genes (CO1, 28S and 18S) to resolve the species boundaries within the Atlanta brunnea group. Results identify a new species, Atlanta vanderspoeli, from the Equatorial and South Pacific Ocean, and suggest that individuals of A. brunnea living in the Atlantic Ocean are an incipient species. Our results provide an important advance in atlantid taxonomy and will enable identification of these species in future studies of living and fossil plankton.

Keywords

Atlantidae, biogeography, phylogenetic analysis, shell morphology, South Pacific Ocean

Introduction

The heteropods (Pterotracheoidea) are a superfamily of marine gastropods (Order Littorinimorpha) consisting of three families: Pterotracheidae, Carinariidae and Atlantidae (Lalli and Gilmer 1989; Bouchet et al. 2017). While most marine gastropods are benthic in habitat, heteropods are holoplanktonic and live entirely in the upper water column. This study focuses on the Atlantidae (atlantids), the most species-rich family of heteropods, including more than 60 % of all heteropod species recognised so far (Seapy 1990; Wall-Palmer et al. 2018b). Atlantids are widespread and occur primarily in the epipelagic zone between the surface and 250 m, in tropical and subtropical latitudes (Wall-Palmer et al. 2018a). They are highly modified for life in the open ocean with several striking morphological adaptions such as the development of complex image-forming eyes, a foot that has adapted into a single swimming fin, and the reduction in size (< 14 mm) and weight of the laterally compressed, thin-walled (3–40 µm) shell (Lalli and Gilmer 1989). The entire shell is moved back and forth rapidly during swimming, so that the swimming fin and shell work together as dissimilar paired swimming appendages (Karakas et al. 2018). This locomotory design means that a structurally sound shell is vital for the survival of atlantids because it is necessary for all swimming, including capturing prey and evading predators. The shell of most atlantids is composed of aragonite, an unstable polymorph of calcium carbonate that is 50 % more soluble in the oceans than calcite (Sun et al. 2015). The chemical composition of the shell and persistent exposure to increasingly acidified waters in the upper water column makes atlantids likely to be particularly sensitive to ocean acidification (Wall-Palmer et al. 2016). However, sensitivity to ocean change is known to be species-specific in holoplanktonic marine gastropods. Roberts et al. (2014) found that different forms of the shelled pteropod Limacina helicina (Phipps, 1774) show contrasting trends in shell weight when exposed to undersaturation of calcium carbonate. Therefore, to gain deeper understanding of the consequences of a changing ocean, it is extremely important to resolve the species boundaries of holoplanktonic gastropods accurately, so that species-resolved environmental sensitivities can be determined.

To date, the taxonomy of atlantid heteropods has mainly relied on morphometrics and shell ornamentation, even though it is hard to tell some species apart only by use of morphological characteristics (Richter 1973). In particular, identification within the genus Atlanta Lesueur, 1817 is difficult, due to the similarities in body and shell forms (Ossenbrügger 2010). Additionally, there can be variation in morphology and ornamentation within a single species (e.g. Atlanta selvagensis de Vera & Seapy, 2006, Wall-Palmer et al. 2018b). Consequently, Richter (1973) suggested that morphometrics alone were insufficient to describe a new species, and assumed that as a result the number of heteropod species was largely underestimated. This underestimated diversity was confirmed in the first molecular phylogenetic study to include all atlantid morphospecies which found 30 % more mitochondrial cytochrome c oxidase subunit 1 (CO1) clades than there are described morphospecies (Wall-Palmer et al. 2018b). These authors found at least 10 additional atlantid clades that may represent new species in addition to the 23 currently described present-day species. This study, as well as many others (Goetze 2010; Burridge et al. 2015, 2019; Barco et al. 2016; Bode et al. 2017; Cornils et al. 2017), highlights the importance of combining morphology (morphometrics), biogeography and molecular analyses when exploring species diversity in the open ocean.

Based on morphological characters (shell, eye type, radula, operculum), atlantid heteropods are divided into groups of closely related species (Tesch 1949). The Atlanta brunnea group was first described as the Atlanta turriculata group by Tesch (1908), and prior to this study contained two species: A. turriculata d’Orbigny, 1836 and A. brunnea Gray, 1850 (= Atlanta fusca Souleyet, 1852). Additional diversity within this group has been recognised in morphological studies (Souleyet 1852; Tesch 1906; Richter 1961; van der Spoel 1972, 1976) and a single molecular study (Wall-Palmer et al. 2018b); however, the taxonomy of this group has not been investigated in sufficient detail. Here we use a combination of the morphological, biological/biogeographical and phylogenetic species concepts (De Queiroz 2007) to investigate the species boundaries within the A. brunnea group. We formally describe the previously recognised A. turriculata form B (van der Spoel 1972, 1976), also previously named A. brunnea form B (Wall-Palmer et al. 2018b) as Atlanta vanderspoeli sp. nov. named after Professor Siebrecht van der Spoel who first recognised A. vanderspoeli but did not describe it as a new species (Van der Spoel 1972, 1976).

Materials and methods

Specimen collection

A total of 22 A. brunnea, 14 A. vanderspoeli (based on the descriptions of van der Spoel 1976) and 55 A. turriculata were examined in this study. All specimens have biogeographical data and have been analysed in at least one additional way (molecular, morphological or both, Table 1, Figure 1). Specimens were collected during several research cruises (Table 1) using various plankton nets. Collection methods have been described for all research cruises (Schmidt 1932; Hirai et al. 2015; Burridge et al. 2017a; Wall-Palmer et al. 2018b; Wall-Palmer et al. in preparation). Specimens from the DANA cruise of 1921 (two A. brunnea, two A. vanderspoeli, and two A. turriculata) were kindly made available by the Natural History Museum of Denmark (NHMD). All biogeographical data have been visualised using the software QGIS (QGIS Development Team 2016).

Table 1.

Collection information for specimens examined in this study, with inclusion into each type of analysis as indicated at right. Specimens used for the combined gene phylogeny are indicated with +.

Species BOLD/GenBank accession number Museum accession number Ocean Cruise Station Biogeography Latitude/Longitude Morphological analysis Molecular analysis
CO1 28S 18S
Atlanta brunnea AGD001-17 RMNH.MOL.341299 Atlantic AMT24 05 34.75, -26.62
ATCP003-19 RMNH.MOL.341308 Atlantic AMT27 09 35.30, -26.28
ATCP008-19 RMNH.MOL.341314 Atlantic AMT27 11 32.87, -26.91
ATCP009-19 RMNH.MOL.341315 Atlantic AMT27 11 32.87, -26.91 ✓+ ✓+ ✓+
ATCP010-19 RMNH.MOL.341316 Atlantic AMT27 11 32.87, -26.91 ✓+ ✓+ ✓+
ATCP004-19 RMNH.MOL.341309 Atlantic AMT27 37 -6.87, -25.04
ATCP006-19 RMNH.MOL.341311 Atlantic AMT27 41 -12.63, -25.05
ATCP007-19 RMNH.MOL.341312 Atlantic AMT27 47 -24.01, -25.05 ✓+ ✓+ ✓+
ATCP011-19 RMNH.MOL.341317 Atlantic AMT27 47 -24.01, -25.05 ✓+ ✓+ ✓+
AGD008-17 RMNH.MOL.341304 Indian SN105 04 8.02, 67.08 ✓+ ✓+ ✓+
AGD009-17 RMNH.MOL.341305 Indian SN105 04 8.02, 67.08
AGD010-17 RMNH.MOL.341300 Indian SN105 08 4.38, 67.00
AGD011-17 RMNH.MOL.341301 Indian SN105 08 4.38, 67.00 ✓+ ✓+ ✓+
AGD012-17 RMNH.MOL.341302 Indian SN105 08 4.38, 67.00
AGD013-17 RMNH.MOL.341303 Indian SN105 08 4.38, 67.00
Indian SN105 08 4.38, 67.00
AGD002-17 RMNH.MOL.341313 Pacific KH1110 05 -23.00, 180.01
ATCP001-19 RMNH.MOL.341306 Pacific KOK1703 07 23.62, -157.61
ATCP002-19 RMNH.MOL.341307 Pacific KOK1703 07 23.62, -157.61
ATCP005-19 RMNH.MOL.341310 Pacific SO255 100 -28.52, 179.59
NHMD-232129 Pacific DANA 3556 VIII 2.87, -87.63
NHMD-232129 Pacific DANA 3556 VIII 2.87, -87.63
Atlanta vanderspoeli AGD003-17 RMNH.MOL.341320 Pacific KH1110 15 -23.00, -119.27
AGD004-17 RMNH.MOL.341321 Pacific KH1110 15 -23.00, -119.27
AGD005-17 RMNH.MOL.341322 Pacific KH1110 15 -23.00, -119.27
AGD006-17 RMNH.MOL.341323 Pacific KH1110 21 -23.00, -100.00
ATCP013-19 RMNH.MOL.341324 Pacific KH1110 21 -23.00, -100.00
AGD007-17 RMNH.MOL.341325 Pacific KH1110 21 -23.00, -100.00
ATCP012-19 RMNH.MOL.341319 Pacific SO255 057 -29.95, -178.73
ATCP014-19 RMNH.MOL.341326 Pacific SO255 057 -29.95, -178.73
Pacific SO255 073 -28.13, 179.02
ATCP015-19 RMNH.MOL.341327 Pacific SO255 073 -28.13, 179.02 ✓+ ✓+ ✓+
ATCP016-19 RMNH.MOL.341328 Pacific SO255 080 -29.10, -179.72 ✓+ ✓+ ✓+
ATCP017-19 RMNH.MOL.341329 Pacific SO255 080 -29.10, -179.72
NHMD-232153 Pacific DANA 3613 V -22.72, 166.10
NHMD-232154 Pacific DANA 3620 IV -24.78, 170.31
Atlanta helicinoidea ATCP052-19 RMNH.MOL.341459 Pacific KOK1703 06 23.52, -156.78 ✓+ ✓+ ✓+
ATCP049-19 RMNH.MOL.341456 Pacific KOK1703 08 23.62, -157.61 ✓+ ✓+ ✓+
ATCP047-19 RMNH.MOL.341454 Pacific KOK1703 08 23.62, -157.61 ✓+ ✓+ ✓+
Atlanta turriculata AGD372-17 RMNH.MOL.341775 Indian SN105 01 11.89, 66.97
AGD367-17 RMNH.MOL.341779 Indian SN105 01 11.89, 66.97
AGD368-17 RMNH.MOL.341780 Indian SN105 01 11.89, 66.97
AGD369-17 RMNH.MOL.341781 Indian SN105 01 11.89, 66.97
AGD370-17 RMNH.MOL.341782 Indian SN105 01 11.89, 66.97
AGD371-17 RMNH.MOL.341783 Indian SN105 01 11.89, 66.97
AGD376-17 RMNH.MOL.341774 Indian SN105 04 8.02, 67.08
Atlanta turriculata AGD375-17 RMNH.MOL.341776 Indian SN105 04 8.02, 67.08
AGD373-17 RMNH.MOL.341784 Indian SN105 04 8.02, 67.08 ✓+ ✓+ ✓+
AGD374-17 RMNH.MOL.341785 Indian SN105 04 8.02, 67.08
AGD380-17 RMNH.MOL.341769 Indian SN105 08 4.38, 67.00
AGD378-17 RMNH.MOL.341777 Indian SN105 08 4.38, 67.00
AGD379-17 RMNH.MOL.341778 Indian SN105 08 4.38, 67.00
AGD377-17 RMNH.MOL.341786 Indian SN105 08 4.38, 67.00
ATCP123-19 RMNH.MOL.341814 Indian SN105 08 4.38, 67.00
AGD381-17 RMNH.MOL.341770 Indian SN105 19 -2.95, 66.99 ✓+ ✓+ ✓+
AGD382-17 RMNH.MOL.341771 Indian SN105 19 -2.95, 66.99
AGD383-17 RMNH.MOL.341772 Indian SN105 19 -2.95, 66.99
AGD384-17 RMNH.MOL.341773 Indian SN105 19 -2.95, 66.99
AGD363-17 RMNH.MOL.341797 Pacific KH1110 05 -23.00, 180.01
AGD361-17 RMNH.MOL.341801 Pacific KH1110 05 -23.00, 180.01
AGD362-17 RMNH.MOL.341802 Pacific KH1110 05 -23.00, 180.01
AGD365-17 RMNH.MOL.341798 Pacific KH1110 08 -22.79, -158.10
AGD364-17 RMNH.MOL.341799 Pacific KH1110 08 -22.79, -158.10
AGD366-17 RMNH.MOL.341800 Pacific KH1110 08 -22.79, -158.10
ATCP103-19 RMNH.MOL.341788 Pacific KOK1703 01 22.91, -157.72
ATCP112-19 RMNH.MOL.341803 Pacific KOK1703 01 22.91, -157.72
ATCP102-19 RMNH.MOL.341787 Pacific KOK1703 03 22.65, -157.69
ATCP116-19 RMNH.MOL.341807 Pacific KOK1703 03 22.65, -157.69
ATCP118-19 RMNH.MOL.341809 Pacific KOK1703 03 22.65, -157.69
ATCP120-19 RMNH.MOL.341811 Pacific KOK1703 03 22.65, -157.69 ✓+ ✓+ ✓+
ATCP122-19 RMNH.MOL.341813 Pacific KOK1703 03 22.65, -157.69
ATCP124-19 RMNH.MOL.341815 Pacific KOK1703 03 22.65, -157.69
ATCP104-19 RMNH.MOL.341789 Pacific KOK1703 05 22.65, -157.69
ATCP125-19 RMNH.MOL.341816 Pacific KOK1703 05 22.65, -157.69
ATCP127-19 RMNH.MOL.341818 Pacific KOK1703 05 22.65, -157.69
ATCP129-19 RMNH.MOL.341820 Pacific KOK1703 05 22.65, -157.69
ATCP113-19 RMNH.MOL.341804 Pacific KOK1703 06 23.52, -156.78
ATCP117-19 RMNH.MOL.341808 Pacific KOK1703 06 23.52, -156.78
ATCP119-19 RMNH.MOL.341810 Pacific KOK1703 07 23.62, -157.61
ATCP115-19 RMNH.MOL.341806 Pacific KOK1703 08 23.62, -157.61
ATCP121-19 RMNH.MOL.341812 Pacific KOK1703 08 23.62, -157.61 ✓+ ✓+ ✓+
ATCP105-19 RMNH.MOL.341790 Pacific SO255 057 -29.95, -178.73
ATCP106-19 RMNH.MOL.341791 Pacific SO255 073 -28.13, 179.02 ✓+ ✓+ ✓+
ATCP114-19 RMNH.MOL.341805 Pacific SO255 073 -28.13, 179.02
Pacific SO255 073 -28.13, 179.02
ATCP126-19 RMNH.MOL.341817 Pacific SO255 073 -28.13, 179.02 ✓+ ✓+ ✓+
ATCP128-19 RMNH.MOL.341819 Pacific SO255 073 -28.13, 179.02
ATCP107-19 RMNH.MOL.341792 Pacific SO255 080 -29.10, -179.72
ATCP108-19 RMNH.MOL.341793 Pacific SO255 080 -29.10, -179.72
ATCP109-19 RMNH.MOL.341794 Pacific SO255 080 -29.10, -179.72
ATCP110-19 RMNH.MOL.341795 Pacific SO255 080 -29.10, -179.72
ATCP111-19 RMNH.MOL.341796 Pacific SO255 100 -28.52, 179.59
NHMD-232140 Pacific DANA 3563 IV -7.76, -131.37
NHMD-232145 Pacific DANA 3586 VII -9.72, -170.67
Figure 1. 

Collection locations for A. brunnea group specimens analysed in this study. Members of this species group are known to inhabit all oceans from 40N to 30S (Wall-Palmer et al. 2018b).

Imaging and morphological analysis

Specimens were identified based on the species keys of Richter and Seapy (1999), Seapy et al. (2003) and van der Spoel (1976), and imaged using a Zeiss automated z-stage light microscope at Naturalis Biodiversity Center, Leiden. Specimen shells were destroyed during the process of DNA extraction, so archived images provide the opportunity to verify in cases of uncertainty between morphologically identified specimens and molecular results. All images are available through the Barcode of Life Data System (BOLD; http://www.boldsystems.org) and are linked to physical DNA extracts at Naturalis Biodiversity Center (Table 1).

Due to the small size of atlantid shells it is difficult to orientate them in a reproducible way for reliable morphometric measurements. Therefore, micro-computed tomography (micro-CT) was used to generate 3D-models for a subset of specimens in order to create 2D-slices through the larval shell for reproducible morphological measurements. A total of five A. brunnea, seven A. vanderspoeli, and 19 A. turriculata were imaged using a SkyScan 1172 high resolution micro-CT scanner. In total 958 images were collected per specimen using the following parameters: no filter, medium resolution camera, an image pixel size of 1.31–2.23 µm, a source voltage of 57 kV, a source current of 177 µA and an exposure time 600–800 ms. The rotation pitch was 0.2°, with averaging frames of 4, and random movement of 10. The software Avizo 9.0 was used to generate a 3D-surface of each shell, and to make 2D-slices perpendicularly through the earliest part of the suture of the protoconch (Figure 2, protoconch pointing upwards) by setting landmarks on the larval shell. Morphological analysis of the 2D-slices was carried out using the software IMAGEJ (Schneider et al. 2012). The apical angle (Figure 2A), maximum larval shell height (Figure 2B), maximum larval shell width measured perpendicular to the spire axis (Figure 2C) and adult shell diameter excluding the keel (Figure 2D) were measured from the 2D-slice three times and the means were calculated. Additionally, the number of whorls in the larval shell and the total number of whorls in the shell were counted using the method of Seapy (1990). For statistical analyses of the morphological data, the software PAST v3.12 was used (Hammer et al. 2001). Normal distributions were tested using the Shapiro-Wilk test (Shapiro 1965). To determine the most important variables, a Principal Component Analysis (PCA) was carried out. T-tests were used to detect significant differences between the clades with regards to those informative variables.

Figure 2. 

Examples of shell parameters measured from 2D slices of micro-CT scans. Measurements include A apical angle B larval shell height C maximum larval shell width, and D maximum adult shell diameter. The position of the slice through the 3D model to create a 2D image is shown in E relative to the suture.

Scanning Electron Microscopy (SEM) images were also made on a subset of specimens to investigate the surface shell morphology and ornamentation for each clade. Two specimens of A. vanderspoeli and three specimens of A. turriculata were scanned using a JEOL JSM-7600F Field Emission SEM. For A. brunnea, images of two specimens from Wall-Palmer et al. (2018b) were used.

Molecular methods

DNA extraction was carried out on whole specimens using the NucleoMag 96 Tissue kit on a Thermo Scientific KingFisher Flex magnetic particle processor with a final elution volume of 75 µl. A ~920 bp fragment of the nuclear 18S rRNA gene was amplified using primers 18S-KP-F (Burridge et al. 2017b) and 1800R (Vonnemann et al. 2005). A ~868 bp fragment of the nuclear 28S rRNA gene was amplified using primers C1-F (Dayrat et al. 2001) and D3-R (Vonnemann et al. 2005). Additionally, a ~658 bp fragment of the mitochondrial cytochrome c oxidase subunit 1 gene (mtCO1) (Hebert et al. 2003) was amplified using primers jgLCO1490 and jgHCO2198 (Geller et al. 2013). All primers were tailed with M13F and M13R for Sanger sequencing (Messing 1983). PCR reactions contained 17.3 µl ultrapure water (milliQ), 2.5 µl Qiagen 10× PCR buffer CL, 0.5 µl 25 mM MgCl2, 1 µl 10 mg/ml Life BSA, 1.0 µl 10 pMol/µl of each primer, 0.5 µl 2.5 mM dNTPs, 0.25 µl 5U/µl Qiagen Taq and 1 µl of DNA extract (diluted either 5 or 10 times). For all three genes, PCR was carried out using a BIO-RAD Thermal Cycler and starting with an initial denaturation step of 3 min at 96 °C, followed by 40 cycles of denaturation of 15 s at 96 °C, annealing of 30 s at 50 °C, extension of 40 s at 72 °C and a final extension step of 5 min at 72 °C. PCR products were sequenced by BaseClear (Leiden). All sequences are publicly available through BOLD (see Table 1 for accession numbers). Molecular results have been previously published for some of the specimens (Wall-Palmer et al. 2018b, in preparation).

Phylogenetic analyses

Sequences (forward and reverse strands) were assembled, aligned and verified in Geneious R8 and multiple sequence alignment was performed using MEGA-X (Kumar et al. 2016a). The resulting length of sequence alignments for CO1, 28S and 18S were 658 bp, 868 bp and 920 bp respectively. Phylogenetic relationships were estimated based on single-gene Maximum Likelihood analyses performed in RAxML 8.2.9 (Stamatakis 2014) using the General Time Reversible (GTRCAT) model followed by bootstrap analyses of 1000 replicates (CO1) or 1500 replicates (18S, 28S). Phylogenetic analysis of the three genes combined (2447 bp, GTRCAT, partitioned, 3000 replicates) included) included a subset of 14 specimens (plus three specimens of A. helicinoidea), with two specimens per clade per region (in regions where clades are present). All three genes were available for all of the specimens (Table 1). CO1 Genetic distances between and within clades/species were calculated using a Kimura-2-parameter (KP2) substitution model with uniform rates in MEGA-X (Kumar et al. 2016b). Three specimens of Atlanta helicinoidea were used as an outgroup in all phylogenetic analyses.

Results

The phylogenetic, morphological and biogeographical analyses produced a congruent result, distinguishing three species within the A. brunnea species group. This includes the two previously known species, A. brunnea and A. turriculata. In addition, the previously described A. brunnea form B, (Wall-Palmer et al. 2018b) also known as A. turriculata form B (van der Spoel 1972, 1976) is a valid new species and is formally named here A. vanderspoeli sp. nov.

Phylogenetic analyses

Phylogenetic analyses of CO1 (Figure 3) and combined genes (Figure 4) recover these three species with moderate to high bootstrap support. The single gene phylogenies of 18S and 28S resolve deeper relationships, but do not resolve the more recent divergences at the species level within the A. brunnea species group (Suppl. material 1: Figures S1–S2). All of the single and combined gene phylogenetic analyses support the A. brunnea species group as being monophyletic with 100 % node support. In the combined gene phylogeny (Figure 4), A. vanderspoeli forms a monophyletic group with 97% node support, supporting inference that this is a valid species. Atlanta brunnea also forms a well-supported (80 % for the combined genes) monophyletic group, but this is further split into two clades. Atlanta turriculata forms a monophyletic group (Indian and Pacific Oceans), but this is only moderately supported (68% node support).

Figure 3. 

A Distribution maps showing the collection locations for each clade identified in B. The collection location of specimens of A. turriculata forma B identified by van der Spoel (1976) from offshore of Ternate Island is marked with a white triangle B maximum likelihood phylogeny based on the mitochondrial cytochrome c oxidase subunit 1 gene, with strong bootstrap support for four clades within the A. brunnea group. Atlanta vanderspoeli is supported as a valid species, and A. brunnea is formed of two geographically isolated clades. Bootstrap support (%) for nodes is displayed and branch lengths are proportional to the amount of inferred change, as indicated by the scale bar (mean number of nucleotide substitutions per site).

Figure 4. 

Maximum likelihood phylogeny of the A. brunnea species group based on analysis of the combined genes CO1, 28S and 18S with a total alignment of 2447 bp. All four clades within the A. brunnea species group are monophyletic with strong bootstrap support. Bootstrap support (%) for nodes is displayed and branch lengths are proportional to the amount of inferred change, as indicated by the scale bar (mean number of nucleotide substitutions per site).

Genetic distances for CO1 support the position of A. vanderspoeli as a valid new species. Atlanta brunnea and A. vanderspoeli are separated by a CO1 genetic distance of 13–16% (Table 2). These genetic distances are comparable to the CO1 genetic distances between the previously described species within this species group, A. brunnea and A. turriculata (18–20 %). CO1 genetic distances between A. brunnea, A. vanderspoeli, A. turriculata and the outgroup species A. helicinoidea are 22–25%, 23–24% and 21–22%, respectively (Table 2).

Table 2.

Mean values (in bold) and ranges for genetic distances among members of the A. brunnea species group, based on a 658 bp fragment of the mitochondrial cytochrome c oxidase subunit 1 gene calculated using a Kimura 2-parameter substitution model with uniform rates.

CO1 A. brunnea Atlantic A. brunnea Indian & Pacific A. vanderspoeli Pacific A. turriculata Indian & Pacific A. helicinoidea Pacific
A. brunnea Atlantic 0
0
A. brunnea Indian & Pacific 6 1
6–7 0–1
A. vanderspoeli Pacific 16 14 0
15 –16 13–15 0–1
A. turriculata Indian & Pacific 2 19 19 0
19–20 18–20 18–20 0–1
A. helicinoidea Pacific 24 23 24 21 0
24–25 22–24 23–24 21–22 0

Within A. brunnea, the molecular data identify a further separation into two well supported geographic clades, one containing the Indian and Pacific Ocean population and one containing the Atlantic Ocean population (Figure 4, node support of 75% and 99% respectively for the combined genes). There is a CO1 genetic distance of 6–7% between specimens from the Atlantic Ocean and specimens from the Indian and Pacific oceans. This genetic distance is less than distances between other species within the A. brunnea group, and therefore, one of these two populations is likely to be an incipient species. However, the type locality of A. brunnea is not known for certain, Gray (1850) having written only ‘A. brunnea, Eydoux’ to accompany his drawing of this species. Here we accept the lectotype locality because we assume that Gray illustrated the same specimens that Souleyet (1852) named A. fusca (originally given the vernacular name “Atlanta brune”), as they both originated from specimens collected by Eydoux on the “Bonite” expedition and the illustrations are almost identical (Suppl. material 1: Figure S3). The type locality for A. fusca is the Indian Ocean and so we assume here that the type locality of A. brunnea is also the Indian Ocean. Therefore, the newly detected Atlantic Ocean population should be considered as the incipient species.

Shell morphology

Principal Component Analysis (PCA) identifies the apical angle of the protoconch and the number of whorls in the larval shell as the most informative morphological characters to distinguish between A. brunnea, A. vanderspoeli, and A. turriculata (Figure 5). The apical angle of A. brunnea is the widest (58.7°–71.0°), followed by A. vanderspoeli (35.9°–45.8°) and A. turriculata (17.4°–32.2°, Suppl. material 2: Table S1, Figure 6). The difference in apical angle between A. brunnea and A. vanderspoeli, and between A. turriculata and A. vanderspoeli is significant (t-test, p=<0.001 for both; Figure 6). Differences in the number of whorls in the larval shell are also identified by the data. Atlanta brunnea has 3.75–4.25 whorls, A. vanderspoeli has 3.25–4.00 whorls and A. turriculata has 4.00–4.50 whorls in the larval shell (Suppl. material 2: Table S1). The height to width ratio of the larval shell, maximum number of whorls (in the whole shell) and adult shell diameter overlap for the three clades and cannot be used as reliable identifying features (Suppl. material 2: Table S1). The low number of specimens does not allow an assessment of morphological differences between the Atlantic Ocean and the Pacific and Indian Ocean specimens of A. brunnea.

Figure 5. 

Principal Component Analysis (PCA) performed on apical angle, height: width ratio and the number of whorls in the larval shell. Species identity confirmed for most specimens (N = 25) using DNA barcoding (CO1). Two specimens of each species (total N = 6) derive from the DANA collection, and could not be DNA barcoded (formalin-fixed). Morphometric data are reported in Suppl. material 2:Table S1.

Figure 6. 

Shell apical angles of A. brunnea (Atlantic, Pacific and Indian oceans), A. vanderspoeli (Pacific Ocean) and A. turriculata (Pacific and Indian oceans) are significantly different and do not overlap.

Ornamentation is limited in its use as an identifying feature for this species group, and the fine micro-ornamentation is only really visible with the use of SEM. All three species have a prominent ridge, or carina that runs slightly above mid-whorl height of the larval shell. The larval shell of A. brunnea is easily identified by the heavy zig-zag, and in places, net-like reticulate spiral lines covering the surface (Figure 7B). However, the ornamentation of A. vanderspoeli is more difficult to tell apart from A. turriculata. In both, the larval shell is more sparsely ornamented than in A. brunnea. In A. vanderspoeli, interrupted spiral lines and small projections roughly arranged in lines are found above the carina of each whorl, and zig-zag ornamentation is found below the carina of each whorl (Figure 7E, Figure 8). In A. turriculata, there is generally little or no ornamentation above the carina of each whorl, but in common with the other two species, zig-zag ornamentation is found below it (Figure 7H).

Figure 7. 

Scanning Electron Microscopy (SEM) and stacked light microscopy images of representative specimens of A. brunnea: A, B DANA_3929VIII C SN105_08, A. vanderspoeli: D–E DANA_3558VII (Holotype, NHMD-232132) F KH1110_15 and A. turriculata: G, H DANA_3929VIII I SN105_19. Apical angle is the most useful morphological feature for distinguishing between the species (B–C, E–F, H–I). The shell of A. brunnea is always brown (C); however, the colour of A. vanderspoeli and A. turriculata shell and soft tissues (F, I) can vary and these are not reliable features for identification.

Figure 8. 

SEM images of the A. vanderspoeli holotype from station DANA_3558VII (NHMD-232132) A apical view of the entire shell showing the rapid inflation of the shell B magnified view of the micro-ornamentation C magnified apical view showing the extent of the carina.

Biogeography

Data gathered in this study expand the known distribution of the A. brunnea group (Wall-Palmer et al. 2016, 2018b). Atlanta brunnea was found to have the broadest distribution, in the Atlantic Ocean (north and south subtropical gyres), in the Indian Ocean and in the Pacific Ocean (Figure 3). Atlanta brunnea was not found in the central southern Pacific Ocean, although this is based upon limited sampling coverage in this region. Conversely, A. vanderspoeli was only found in the equatorial and southern Pacific Ocean (0.80N–29.95S, 127.28E–100.00W). The two species only overlap in the south west and the east Pacific Ocean (Figure 3). The molecular results presented here show that the Atlantic Ocean population of A. brunnea is a geographically divergent species. Atlanta turriculata was found throughout the Pacific and Indian oceans, overlapping with the distribution of A. vanderspoeli in the equatorial and South Pacific Ocean. In agreement with previous studies, A. turriculata was not found in the Atlantic Ocean (Figure 3).

Discussion

A note on Atlanta turriculata d’Orbigny, 1836

Atlanta turriculata was described by d’Orbigny (1836) from the South Pacific Ocean. This is the region in which the distributions of A. turriculata and A. vanderspoeli overlap and so it is necessary to check that d’Orbigny described and illustrated specimens of A. turriculata and not the morphologically similar A. vanderspoeli. Unfortunately, type material of A. turriculata could not be found at either the Natural History Museum, London (NHMUK), or the Muséum National d’Histoire Naturelle, Paris (MNHN), where it should be present (syntype material located at NHMUK was discovered to be mislabeled specimens of Oxygyrus). In addition, the illustrations of A. turriculata made by d’Orbigny are not sufficiently detailed to determine which species he actually drew. Although the more widely geographically distributed, narrow-turreted spired species is now well known as A. turriculata, we find it necessary to solve this potential confusion by depositing a neotype specimen of (what is now widely known as) A. turriculata (see Systematics section for details, Figure 9).

Figure 9. 

Atlanta turriculata neotype RMNH.MOL.342213, housed at the Naturalis Biodiversity Center.

The validity of A. vanderspoeli sp. nov

Additional diversity within the A. brunnea species group has long been recognised, but, until now, this has not been thoroughly investigated. Van der Spoel (1972) first noticed A. vanderspoeli when he remarked on an atlantid form similar to A. turriculata, calling it A. turriculata forma B. Initially recognised from the soft tissues, van der Spoel described A. turriculata forma B as generally having a lack of tubercules on the operculum, which were present in A. turriculata. Later, van der Spoel (1976: 146–147) described the shell as having ‘whorls in the spire [that] increase more rapidly in width so that the spire in relation to the body whorl is larger than in [A. turriculata]’. Van der Spoel deposited specimens of this forma, which are now in the collection of the Naturalis Biodiversity Center, Leiden (Figure 10). More recently, Wall-Palmer et al. (2018b) detected an additional clade within the A. brunnea group using a CO1 phylogeny of a global collection of specimens. This clade was more closely related to A. brunnea, and was referred to as A. brunnea form B. Here we considered three species concepts to determine whether this new clade, referred to in this study as A. vanderspoeli, was a valid species; the morphological species concept, the biological isolation (biogeographical) species concept and the phylogenetic species concept (De Queiroz 2007). Under each of these concepts, our results verify that A. vanderspoeli is different from the two most closely related species, A. brunnea and A. turriculata. Although there were only a relatively small number of specimens available for morphological analysis, A. vanderspoeli shells were found to be morphologically distinct, having an apical angle that does not overlap with its two closest relatives. The combined three gene phylogeny supports A. vanderspoeli to be genetically distinct from A. brunnea and A. turriculata, with genetic distances comparable to other species within the group. Atlanta vanderspoeli also appears to have a relatively restricted distribution, only being found (thus far) in the equatorial and South Pacific Ocean. The pteropod species Cuvierina tsudai Burridge, Janssen & Peijnenburg, 2016 has a very similar geographical distribution (Burridge et al. 2015, 2016). The known distribution of A. vanderspoeli only overlaps with A. brunnea and A. turriculata at the very edges of their populations. Relatively poor spatial resolution of molecular data in the Pacific Ocean means it is possible that the distribution of A. vanderspoeli is also wider (e.g. in the north Pacific). The species is therefore not strongly geographically isolated from its two most closely related species. However, these results are compatible with the phylogenetic species concept, because even though the species overlap geographically and likely do meet in nature, there must be no interbreeding as evidenced by the combined gene phylogeny (and 28S, Suppl. material 1: Figure S1).

Figure 10. 

Five specimens of Atlanta turriculata forma B identified by van der Spoel and held in the collection at the Naturalis Biodiversity Center. These specimens are now designated as paratypes of Atlanta vanderspoeli RMNH.MOL.342212.

An Atlantic Ocean incipient species

Results of the phylogenetic analysis also highlight a probable incipient species. The morphospecies A. brunnea was found to have two genetically different populations, one in the Indian and Pacific Oceans, and one in the Atlantic Ocean. The genetic distance between the two populations is relatively small, but suggests that the populations of A. brunnea in the Atlantic Ocean must be isolated and becoming a new species. This result agrees with Wall-Palmer et al. (2018b) who suggested the existence of an additional genetic lineage but due to insufficient data this could not be confirmed as a distinct species. Richter (1961) also noted differences in the Atlantic population of A. fusca (= A. brunnea), describing them as having smaller, more pigmented shells when compared to specimens in the Indian Ocean. Differences in the operculum and radula were also reported by Richter (1961). We did not detect any morphological differences between the two populations of A. brunnea, however, only shell ornamentation and the measurements of the larval shell have been analysed here.

Systematics

Phylum Mollusca

Class Gastropoda Cuvier, 1797

Subclass Caenogastropoda Cox, 1960

Order Littorinimorpha Golikov & Starobogatov, 1975

Superfamily Pterotracheoidea Rafinesque, 1814

Family Atlantidae Rang, 1829

Genus Atlanta Lesueur, 1817

Atlanta vanderspoeli Wall-Palmer, Hegmann & Peijnenburg, sp. nov.

Figures 7, 8

Atlanta turriculata forma B – van der Spoel 1972: 550

Atlanta turriculata forma B – van der Spoel 1976: 146–147

Atlanta brunneaQuesquén Liza 2017: 265

Atlanta brunnea form B – Wall-Palmer et al. 2018b: 10, Fig. 3

Type locality

DANA expedition (1928–1930) station 3558VII, South Pacific 0.30S, 99.12W. Specimen collected on the 18h September 1928 at 19:00 from 200–300 m water depth.

Holotype. Figure 7D–E, NHMD-232132, Housed at the Natural History Museum of Denmark, Copenhagen.

Paratypes. NHMD-232153. DANA_3613V, South Pacific 22.72S, 166.10E. Specimen collected on 28 April 1928 at 03:15 from 100–200 m water depth. Housed at the Natural History Museum of Denmark, Copenhagen. RMNH.MOL.342212. Type material of A. turriculata forma B (Figure 10) was deposited by van der Spoel in the collections of the Zoological Museum of Amsterdam (now housed at the Naturalis Biodiversity Center, Leiden, RMNH). We designate these specimens as paratypes of A. vanderspoeli. They were collected during the “Siboga” Expedition at station 136 in the equatorial Pacific 0.80N, 127.28E.

Diagnosis

Atlanta species with a larval shell of 3 ¼ to 4 whorls. The larval shell is much higher than wide, conical with an apical angle of 35–46°. The larval shell has a prominent carina slightly above mid-whorl height. The whorls of the larval shell are further covered in a micro-ornamentation of interrupted spiral lines and small projections roughly arranged in spiral lines (approximately five lines in total) above this carina, and zig-zagged ornamentation below it (Figs 7D–F, 8).

Description

The shell is small and fresh specimens vary in colour from brown to pink-purple. The adult shell is on average 1000 μm in diameter without the keel (Suppl. material 2: Table S1). The shell begins to inflate on the boundary of teleoconch and protoconch at 3¼ to 4 whorls and has a total of 4¾ to 5 whorls in adults. The keel begins after 3¾ to 4 whorls and inserts between the final whorl and the preceding in larger specimens (filling the space between the whorls). The keel is tall (~400 μm), thin and transparent, and gradually truncates towards the aperture (after ca. ¾ of a whorl). The soft tissues of the foot/fin and sucker can be mottled black (see Suppl. material 3: video clip). The last whorl of the larval shell is ca. 262 to 372 μm in diameter (Suppl. material 2: Table S1). The larval shell is high and conical, with heavy ornamentation covering the surface. A prominent carina is situated slightly above mid-whorl height and is visible with light microscopy. The spiral lines and zig-zag ornamentation is more clearly visible using SEM. The operculum is type a (macro-oligogyre) and the eyes are of type a, with no transverse slit (Seapy et al. 2003).

Discussion

The shape of the larval shell, shell size, colouration, operculum and eye type demonstrate that A. vanderspoeli belongs within the A. brunnea species group. This is supported by the molecular analysis presented within this study and by Wall-Palmer et al. (2018b). Molecular data finds A. vanderspoeli to be most closely related to A. brunnea, followed by A. turriculata. These are also morphologically the most similar species. Atlanta vanderspoeli can be distinguished from these two species using the apical angle, which is more narrow than in A. brunnea, but wider than in A. turriculata. Van der Spoel (1972) noted that the operculum of (A. turriculata forma B) A. vanderspoeli generally does not have tubercles/spines, or that these are less developed (van der Spoel 1976) compared to the operculum of A. turriculata. Due to a lack of adult specimens, we were unable to extract an operculum to confirm this.

Distribution

All specimens were found in the equatorial and south Pacific Ocean from 0.80N to 29.95S, and from 127.28E to 100.00W (Figure 3). Specimens were collected from the upper 600 m using oblique and vertical plankton tows. During this study we only found specimens of A. vanderspoeli in the south Pacific Ocean. However, specimens identified as A. turriculata forma B by van der Spoel (1976) were collected at ‘Ternate Anchorage’ in the Indomalayan Archipelago (“Siboga” Expedition station 136, equatorial Pacific 0.80N, 127.28E. Figure 10).

Etymology

Named after Professor emeritus Siebrecht van der Spoel, who first noticed A. vanderspoeli, but described it only as A. turriculata forma B due to a lack of specimens (van der Spoel 1976). Professor van der Spoel spent many years working on holoplanktonic gastropods and made important contributions to our understanding of their taxonomy and distributions.

Atlanta turriculata d’Orbigny, 1836

Figure 9

Original type locality

The great Austral Ocean between 30 and 34S.

Holotype. We have been unable to locate any type material for A. turriculata (thought to have been deposited in NHMUK or MNHN).

Neotype. RMNH.MOL.342213. SN105_08, Indian Ocean 4.38N, 67.00E. Specimen collected during the SN105 expedition of the ORV Sagar Nidhi, on the 10th December 2015 at 04:40 from 67 m water depth. Housed at the Naturalis Biodiversity Center, Leiden.

Two additional specimens have been deposited at the Natural History Museum, London. NHMUK20191155 and NHMUK20191156, from station KOK1703_06, Pacific Ocean 23.52N, 156.77W. Specimens collected during the KOK1703 expedition of the RV “Ka’Imikai-O-Kanaloa” on the 3rd September 2017 at 03:59 from 0–250 m water depth.

The holotype of Atlanta vanderspoeli is the property of the Natural History Museum of Denmark, Copenhagen. The neotype of Atlanta turriculata is the property of the Naturalis Biodiversity Center, Leiden. Both institutes maintain a research collection with proper facilities for preserving name-bearing types and these types are made accessible for study.

Conclusions

Using an integrated species concept, this study demonstrates that the A. brunnea group contains three valid species, A. brunnea, A. turriculata, and A. vanderspoeli sp. nov. A further incipient species that is restricted to the Atlantic Ocean should also be considered in future research, in particular during ecological or experimental studies. We hope that the integrated approach to species validation reported here will facilitate other workers in identifying A. vanderspoeli in their studies. Increased spatial coverage is now needed to fully understand the current distributions and environmental tolerances of this new species. Only with a larger and more complete dataset, including collection depths and concurrently collected environmental data, will it be possible to understand the responses of these atlantids to a changing ocean.

Acknowledgements

We are grateful to Atsushi Tsuda (University of Tokyo), Alice K. Burridge and Lisette Mekkes (Naturalis Biodiversity Center) for providing specimens and/or helping with specimen collection. We thank Arie W. Janssen and María Moreno-Alcántara for comments and suggestions on our manuscript, and particularly for help with the systematic section. We would also like to thank Yamell Kuen (University of Amsterdam) for sorting specimens from AMT27 material, Dirk van der Marel and Rob Langelaan for assistance with SEM and micro-CT and Tom Schiøtte and Martin Vinther Sørensen (Natural History Museum of Denmark, Copenhagen), Jeroen Goud and Bram van der Bijl (Naturalis Biodiversity Center, Leiden) and Andreia Salvador and Jon Todd (Natural History Museum, London) for facilitating access to collections in their care and for making specimens available to us. We would like to acknowledge the scientists and crew who took part in cruises AMT24, AMT27, DANA 1928–1930, KH1110, SN105, SO255, and KOK1703, and the Atlantic Meridional Transect (AMT) programme. The Atlantic Meridional Transect is funded by the UK Natural Environment Research Council through its National Capability Long-term Single Centre Science Programme, Climate Linked Atlantic Sector Science (grant number NE/R015953/1). This study contributes to the international IMBeR project and is contribution number 334 of the AMT programme. The SN105 expedition is part of IIOE-2 and was funded by the Indian National Centre for Ocean Information Services (INCOIS), Ministry of Earth Sciences, Govt. of India. The RV “Sonne”’ cruise SO255 was funded by the German Federal Ministry of Education and Research (BMBF; grant 03G0255A). This project has received funding from the European Union’s Horizon 2020 research and innovation programme under the Marie Skłodowska-Curie grant agreement No. 746186 (POSEIDoN, D.W-P.).

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Supplementary materials

Supplementary material 1 

Figures S1–S3

Deborah Wall-Palmer, Mona Hegmann, Erica Goetze3 Katja T.C.A. Peijnenburg

Data type: multimedia

Explanation note: Figure S1. Maximum likelihood phylogeny of the A. brunnea group based on 28S. Figure S2. Maximum likelihood phylogeny of the A. brunnea group based on 18S. Figure S3. The original illustration of (A) Atlanta brunnea by Gray (1850) is clearly copied from the original illustration by Eydoux and Souleyet (1841) of (B) Atlanta brune (vernacular name) later formally named A. fusca (Souleyet, 1852).

This dataset is made available under the Open Database License (http://opendatacommons.org/licenses/odbl/1.0/). The Open Database License (ODbL) is a license agreement intended to allow users to freely share, modify, and use this Dataset while maintaining this same freedom for others, provided that the original source and author(s) are credited.
Download file (10.52 MB)
Supplementary material 2 

Table S1. Morphometric data for A. brunnea, A. vanderspoeli and A. turriculata

Deborah Wall-Palmer, Mona Hegmann, Erica Goetze3 Katja T.C.A. Peijnenburg

Data type: measurement

This dataset is made available under the Open Database License (http://opendatacommons.org/licenses/odbl/1.0/). The Open Database License (ODbL) is a license agreement intended to allow users to freely share, modify, and use this Dataset while maintaining this same freedom for others, provided that the original source and author(s) are credited.
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Supplementary material 3 

Atlanta vanderspoeli video clip

Deborah Wall-Palmer, Mona Hegmann, Erica Goetze3 Katja T.C.A. Peijnenburg

Data type: multimedia

Explanation note: Atlanta vanderspoeli specimen (male) collected during cruise SO255 station 80 at 29.10S, 179.72W.

This dataset is made available under the Open Database License (http://opendatacommons.org/licenses/odbl/1.0/). The Open Database License (ODbL) is a license agreement intended to allow users to freely share, modify, and use this Dataset while maintaining this same freedom for others, provided that the original source and author(s) are credited.
Download file (39.00 MB)
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