![Comparisons in shell morphology between the oldest fossil heteropods and larval shells of extant members of the Atlantidae. a Juvenile Atlanta selvagensis collected live from the Atlantic Ocean in 2010, b Juvenile A. selvagensis, a recent fossil from Caribbean sediments, c-d The oldest potential heteropod, Coelodiscus minutus from the Early-Middle Jurassic (190.8-170.3 Ma). Specimens BSPG 2008 XXIX 42c and BSPG 2008 XXIX 56f, images from Teichert and Nützel [16], e-f Juvenile Oxygyrus inflatus collected live from the Atlantic Ocean in 2010, g-h The oldest potential Atlantidae, Belerophina minuta from the Early Cretaceous (~ 113-100.5 Ma). Bellerophina images courtesy of Steven Tracey [22]](https://www.researchgate.net/profile/Erica-Goetze/publication/344344173/figure/fig2/AS:938638804267009@1600800338181/Comparisons-in-shell-morphology-between-the-oldest-fossil-heteropods-and-larval-shells-of_Q320.jpg)
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R E S E A R C H A R T I C L E Open Access
Fossil-calibrated molecular phylogeny of
atlantid heteropods (Gastropoda,
Pterotracheoidea)
Deborah Wall-Palmer
1*
, Arie W. Janssen
1
, Erica Goetze
2
, Le Qin Choo
1,3
, Lisette Mekkes
1,3
and
Katja T. C. A. Peijnenburg
1,3
Abstract
Background: The aragonite shelled, planktonic gastropod family Atlantidae (shelled heteropods) is likely to be one
of the first groups to be impacted by imminent ocean changes, including ocean warming and ocean acidification.
With a fossil record spanning at least 100 Ma, atlantids have experienced and survived global-scale ocean changes
and extinction events in the past. However, the diversification patterns and tempo of evolution in this family are
largely unknown.
Results: Based on a concatenated maximum likelihood phylogeny of three genes (cytochrome coxidase subunit 1
mitochondrial DNA, 28S and 18S ribosomal rRNA) we show that the three extant genera of the family Atlantidae,
Atlanta, Protatlanta and Oxygyrus, form monophyletic groups. The genus Atlanta is split into two groups, one
exhibiting smaller, well ornamented shells, and the other having larger, less ornamented shells. The fossil record, in
combination with a fossil-calibrated phylogeny, suggests that large scale atlantid extinction was accompanied by
considerable and rapid diversification over the last 25 Ma, potentially driven by vicariance events.
Conclusions: Now confronted with a rapidly changing modern ocean, the ability of atlantids to survive past global
change crises gives some optimism that they may be able to persist through the Anthropocene.
Keywords: Atlantidae, Planktonic gastropods, Cytochrome coxidase subunit 1, 28S and 18S ribosomal rRNA, Ocean
change, Rapid diversification
Background
The Atlantidae is a family of small (< 14 mm) marine
predatory gastropods with a holoplanktonic mode of life
(Fig. 1). Atlantids fall within the superfamily Pterotra-
cheoidea, known commonly as heteropods, or sea ele-
phants. Unlike the other two heteropod families
(Carinariidae and Pterotracheidae), all three genera of the
Atlantidae (Atlanta, Protatlanta and Oxygyrus)havethin-
walled laterally compressed aragonite shells that are
broadened with a keel. A modified foot serves as a primary
swimming fin, and the broad shell is used as a secondary
swimming fin [1]. Together, the fin and the shell generate
rapid and directed movement for prey capture and preda-
tor evasion. Atlantids are able to fully withdraw into their
shell and seal the aperture with an operculum. They also
have well developed eyes, a sucker on their fin for securing
prey, and a proboscis, or trunk, which is used for reaching
into the shells of prey, such as shelled pteropods [2–4]. It
is clear that atlantids have remarkable and derived adapta-
tions for a holoplanktonic lifestyle, however, their evolu-
tionary history is largely unknown. Until now, hypotheses
about the evolution of atlantids (and heteropods in
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* Correspondence: dmwallpalmer@gmail.com
1
Plankton Diversity and Evolution, Nauralis Biodiversity Center, Leiden, The
Netherlands
Full list of author information is available at the end of the article
Wall-Palmer et al. BMC Evolutionary Biology (2020) 20:124
https://doi.org/10.1186/s12862-020-01682-9
general) have relied upon a fossil record with vast gaps
[5], due to a combination of the loss of delicate aragonite
shells during diagenetic processes, creating genuine gaps
in the fossil record, and a lack of research on fossil hetero-
pods as a whole, creating knowledge gaps. Despite these
gaps, the evolutionary history of this group is of interest in
understanding how these delicate aragonite shelled plank-
ton, and presently the only aragonite shelled predatory
holoplankton, have fared through past climate change and
ocean acidification events, since the Early Cretaceous. The
morphologically similar aragonite shelled pteropods are
known to have survived through both the Cretaceous-
Paleogene (KPg or KT) extinction event and the Paleocene
Eocene Thermal Maximum (PETM), which were both
times of extreme climate change and the closest analogues
to predicted ocean changes [6–8].
The thin-walled aragonite shells of the atlantids, and
their habitat in the upper ocean imply that they are
likely to be sensitive to ocean acidification and ocean
warming, in a similar way to the shelled pteropods [9].
The only study addressing the effects of ocean acidifica-
tion on atlantids found negative effects of reduced ocean
pH on shell growth and the down-regulation of biomi-
neralisation and growth genes [10]. Relatively recent
local extinctions have been reported for several atlantid
species. Atlanta plana Richter, 1972 and Atlanta turri-
culata d’Orbigny, 1836 are not found in the modern
Atlantic Ocean [11], however, fossils of both species
have been found in Late Pleistocene sediments of the
Caribbean Sea [12], and A. plana has also been found in
Pliocene rocks of southern France and southern Spain
[13,14]. These records suggest the local extinction of A.
turriculata at around 16 thousand years (ka), and A.
plana in the last 3.5–1 ka. Protatlanta sculpta Issel,
1911 is currently only known from the Atlantic Ocean,
but was present in Late Pleistocene sediments of the In-
dian Ocean 24–16 ka ago (D. Wall-Palmer personal ob-
servation) and in Pliocene rocks of Pangasinan,
Philippines [15]. Most of these local extinctions have oc-
curred within the warming period since the Last Glacial
Maximum, and may reflect sensitivity to a changing
ocean.
Holoplanktonic gastropods are thought to have
evolved from benthic gastropods with planktotrophic
larvae, with likely progression to remain planktonic in
response to increasing hostility of the sea floor, including
anoxic bottom conditions [16] and/or an increase in
benthic shell destroying predators [17]. Holoplanktonic
gastropods first appear in the Jurassic, coinciding with
the Early Jurassic Anoxia Event [18]. Amongst the earli-
est holoplanktonic gastropods are several potential het-
eropod genera including Coelodiscus, Freboldia and
Tatediscus [16,19,20]. Coelodiscus minutus (Schübler,
1833) [16,21] from the Pliensbachian–Aalenian of the
Fig. 1 Adult representatives of the three extant Atlantidae genera. aProtatlanta souleyeti, bAtlanta gibbosa, cOxygyrus inflatus. All specimens
were collected and photographed during the AMT27 cruise from the Atlantic Ocean
Wall-Palmer et al. BMC Evolutionary Biology (2020) 20:124 Page 2 of 14
Early–Middle Jurassic (190.8–170.3 Ma) is the earliest
known holoplanktonic caenogastropod and probable
heteropod. Coelodiscus minutus has a shell morphology
remarkably similar to larval atlantid shells of the genus
Atlanta (Fig. 2a-d).It is thought that C. minutus does
represent an early heteropod [19], but only two ontogen-
etic stages can be identified from abundant fossil mater-
ial (compared to three in modern heteropods), and
therefore it is not a member of any of the extant families
[16]. The planktotrophic larval stage of C. minutus prob-
ably became the adult stage when transitioning to a
holoplanktonic mode of life, and the adult shell of the
modern atlantid heteropods developed later [16].
The oldest potential member of the family Atlantidae
does not appear in the fossil record until ~ 57 Ma later,
in the Early Cretaceous. Bellerophina minuta (Sowerby,
1812) [22,23], found in the Albian (~ 113–100.5 Ma),
has an involute, more rounded shell morphology with
clear ornamentation that is similar to larval shells of the
extant atlantid genus Oxygyrus (Fig. 2e-h).Destombes
[24] considered the relationship between B. minuta and
the genus Oxygyrus to be unclear, due to differences in
size and incompleteness of the aperture in B. minuta
fossils. He therefore placed B. minuta into a separate
family, Bellerophinidae, in which an older genus Frebol-
dia (163.5–157.3 Ma) is now also placed [18]. However,
the relationship between Oxygyrus and B. minuta re-
mains enigmatic [22], and here we consider B. minuta to
belong within the family Atlantidae, having a shell
morphology very similar to the extant genus Oxygyrus
[22]. Indeed, the World Register of Marine Species
places the genus Bellerophina within the Family Atlanti-
dae. Freboldia fluitans Nützel & Schneider, 2016 (163.5–
157.3 Ma) is thought to be holoplanktonic and its shell
morphology is involute and quite rounded in shape,
however, unlike B. minuta, the shell surface has little or
no ornamentation, and the coiling direction of F. fluitans
cannot be determined with certainty [18].
Through the Late Cretaceous, Paleocene and Eocene
there are no known atlantid fossils, creating a gap in the
record of ~ 73 Ma. The recent fossil record of the Atlan-
tidae, extending to the Piacenzian (3.6–0 Ma) is rela-
tively well known [5]. However, from the Piacenzian to
the Chattian of the Oligocene (~ 27.82–3.6 Ma) [25], di-
versity is much lower with only five atlantid species, and
two not determined to species level. There are eight
atlantid species known to have become extinct during
the Miocene and the Pliocene [5], and one extinct genus,
Atlantidea [26].
Although heteropods have almost certainly been alive
for the last ~ 190 Ma, nothing is known from these large
57 Ma and 73 Ma gaps in the fossil record, and so the
evolutionary diversification patterns and timing of this
group are unclear. It has been hypothesised that within
the family Atlantidae, the genus Atlanta, with an entirely
aragonite shell, is the earliest diverged, and that the
genus Oxygyrus, with a shell composed of both aragonite
and conchiolin (probably to improve buoyancy), is the
latest to diverge [2,27–30]. However, the shell of the
Early Cretaceous B. minuta is morphologically most
similar to Oxygyrus (Fig. 2), contradicting this hypothe-
sised evolutionary history of the atlantids.
Only a single large-scale study has previously explored
the molecular phylogeny of the atlantid heteropods [11].
Wall-Palmer et al. [11] revealed considerable hidden di-
versity using a global dataset of mitochondrial cyto-
chrome coxidase subunit 1 (CO1) sequences from
specimens of all known atlantid morphospecies.
Fig. 2 Comparisons in shell morphology between the oldest fossil heteropods and larval shells of extant members of the Atlantidae. aJuvenile
Atlanta selvagensis collected live from the Atlantic Ocean in 2010, bJuvenile A. selvagensis, a recent fossil from Caribbean sediments, c–dThe
oldest potential heteropod, Coelodiscus minutus from the Early-Middle Jurassic (190.8–170.3 Ma). Specimens BSPG 2008 XXIX 42c and BSPG 2008
XXIX 56f, images from Teichert and Nützel [16], e–fJuvenile Oxygyrus inflatus collected live from the Atlantic Ocean in 2010, g–hThe oldest
potential Atlantidae, Belerophina minuta from the Early Cretaceous (~ 113–100.5 Ma). Bellerophina images courtesy of Steven Tracey [22]
Wall-Palmer et al. BMC Evolutionary Biology (2020) 20:124 Page 3 of 14
However, deeper genus level relationships were not re-
solved in this study, and it provided few clues about the
longer-term evolutionary history of the family. In the
present study, an extended CO1 dataset is used in com-
bination with two nuclear genes, 28S and 18S, to pro-
duce a more complete molecular phylogeny with which
to compare previous morphology based hypotheses of
atlantid evolution. Through a fossil-calibration of this
phylogeny, the likely timing of diversification reveals the
persistence of this successful group of holoplankton
through past ocean changes.
Results and discussion
Phylogeny of the Atlantidae
Phylogenetic analysis of a concatenated (3-gene) align-
ment of CO1, 28S and 18S recovered species and genera,
with node supports of > 80% (100% for most) at most
levels of the atlantid tree (Fig. 3). For the first time, it
can be demonstrated that all three atlantid genera are
monophyletic with 100% bootstrap support, however, re-
lationships between the genera remain inconclusive.
Maximum likelihood analyses of individual genes recov-
ered species and genera with varying levels of success
(Figs. S1,S2,S3). While all 34 previously known putative
atlantid species [11] (including all 24 morphospecies)
were resolved by the CO1 phylogenetic tree (supports of
> 80, 100% for most), two additional putative species
were also detected and verified by ABGD analysis (one
within A. peronii C, and one within O. inflatus A). This
brings the total number of putative species to 36, of
which 24 are described as morphospecies and 12 are
undescribed putative species. However, the deeper rela-
tionships between atlantid genera were not supported
within the CO1 phylogenetic tree (< 60%, Fig. S1). Con-
versely, 28S and 18S trees did not always resolve
species-level relationships. The 28S phylogeny supported
13 of the described morphospecies and a further seven
of the undescribed putative species, whereas the 18S
phylogeny supported only four described morphospecies
and four undescribed putative species. The 28S and 18S
trees did, however, provide moderate support for rela-
tionships among the atlantid genera (> 60%, Figs. S2and
S3, respectively).
Atlantids have long been divided into groups of closely
related species (Table 1) based on morphological charac-
ters. The 3-gene maximum likelihood (ML) phylogeny
largely supports these morphology based species groups
(Table 1), with only the Atlanta peronii Lesueur, 1817,
Atlanta gibbosa Souleyet, 1852 and Atlanta lesueurii
Gray, 1850 groups not resolved (Fig. 3). The A. lesueurii
group is monophyletic, but not supported (bootstrap
support 37%). The A. peronii and A. gibbosa groups are
not monophyletic due to the position of A. frontieri
Richter, 1993, which falls within the A. gibbosa group
(Fig. 3). As found in previous phylogenetic analysis of
CO1 [11], several atlantid morphospecies contain one or
more additional well-supported putative species (boot-
strap support > 80%). Here we find that six morphospe-
cies contain a total of 17 putative species. The majority
of these putative species (11 of 17) show some degree of
geographical separation, residing in different ocean ba-
sins, and seven of these putative species are also sup-
ported by the more slowly evolving, independently
inherited nuclear markers, demonstrating that they are
probably distinct species. However, further work in re-
solving the morphology and distributions of these new
species would be necessary to describe and validate each
one [32].
The 3-gene phylogeny demonstrates that the genus At-
lanta can be split into two broad groups: one of smaller-
shelled species generally with shell ornamentation, and
one of larger-shelled species generally lacking shell orna-
mentation (Fig. 3). The smaller ornamented species form
a well-supported monophyletic group containing the At-
lanta inflata Gray, 1850, A. brunnea Gray, 1850, A. gau-
dichaudi Gray, 1850 and A. lesueurii species groups
(95% supported). The larger and non-ornamented
shelled species are grouped together, but have low node
support (58% support). These two broad groups are also
supported by radula type (Table 1), with the smaller
ornamented group having a ‘type I radula’, in which the
number of tooth rows continually increases because
teeth are never cast off, and the larger non-ornamented
group having a ‘type II radula’, with a set number of
tooth rows per species because teeth are cast off the an-
terior end [33]. These results suggest that the genus At-
lanta has followed two evolutionary routes.
Previous morphology based studies that focussed on
the shell, eyes, radula and operculum [27–30], as well as
chromosomal studies [34], also support a lineage of
larger-shelled species generally lacking shell ornamenta-
tion. Richter [27–30] proposed an evolutionary route
where shells became flatter, shell walls became thinner
and the central spire became narrower and tilted over
evolutionary time. The lineage of larger, non-
ornamented species identified in the present study do
exhibit these shell features. Richter proposed that this
evolutionary path resulted from selective pressure to im-
prove swimming efficiency by providing a broad flat
shell to counteract the side-to-side swimming motion.
This may partly be true, however, we now know that the
shell is used as a secondary swimming fin by A. selvagen-
sis de Vera & Seapy, 2006, and likely by all atlantid spe-
cies [1] so a broadening of the shell may permit faster
swimming speeds.
Richter [27–30] proposed a second evolutionary route
within the genus Atlanta that involves the reduction of
shell mass, where shells gradually become composed of
Wall-Palmer et al. BMC Evolutionary Biology (2020) 20:124 Page 4 of 14
Fig. 3 Maximum likelihood phylogeny of the family Atlantidae based on a concatenated dataset of cytochrome coxidase subunit 1 mitochondrial
DNA (CO1), 28S and 18S ribosomal rRNA (total 2472 bp). Black squares represent bootstrap support >80%. Species groups based on morphology are
highlighted with coloured boxes (see Table 1)
Wall-Palmer et al. BMC Evolutionary Biology (2020) 20:124 Page 5 of 14
Table 1 A summary of the morphology based species groups, key morphological characters for each group [31], and the
phylogenetic support obtained for each group in our analyses
Species group Species Radula type Shell and keel composition Morphological characters of this group Is the group supported
by the 3-gene
phylogeny?
Atlanta
brunnea
Atlanta brunnea
Gray, 1850
I Both aragonite Small shell (< 2 mm) with a tall keel. Larval shell is tall,
conical, covered with ornamentation and with a
prominent carina slightly above mid-whorl height
Yes
Atlanta turriculata
d’Orbigny, 1836
I
Atlanta vanderspoeli
Wall-Palmer, Heg-
mann & Peijnenburg,
2019
I
Atlanta inflata Atlanta ariejansseni
Wall-Palmer, Bur-
ridge & Peijnenburg,
2016
I Both aragonite Small-medium sized shell (< 4 mm) with a short or tall
keel. Larval shell is flattened, or low conical and either
smooth, or ornamented with evenly spaced spiral
ridges or punctae.
Yes
Atlanta californiensis
Seapy & Richter,
1993
I
Atlanta helicinoidea
(A and B) Gray, 1850
I
Atlanta inflata Gray,
1850
I
Atlanta selvagensis
de Vera & Seapy,
2006
I
Atlanta
lesueurii
Atlanta lesueurii Gray,
1850
I Both aragonite The larval shell is very small, with only 2.5 whorls. Yes - species group
together but node
support is low (37%).
Atlanta oligogyra (A,
B and C) Tesch, 1906
I
Atlanta
gaudichaudi
Atlanta echinogyra
Richter, 1972
I Both aragonite Small-medium shell (< 4 mm). Larval shell flattened to
conical with varying numbers of spiral lines (only 1 in
A. gaudichaudi).
Yes, but node support is
moderate (75%).
Atlanta gaudichaudi
Gray, 1850
I
Atlanta plana
Richter, 1972
I
Atlanta peronii Atlanta fragilis
Richter, 1993
II Both aragonite Medium-large sized shell (< 10mm). Larval shell is
flattened or low conical with no ornamentation (except
A. frontieri).
No - species do not
group together. A.
frontieri groups with A.
gibbosa group.
Atlanta frontieri
Richter, 1993
II
Atlanta peronii (A, B
and C) Lesueur, 1817
II
Atlanta rosea (A, B
and C) Gray, 1850
II
Atlanta
inclinata
Atlanta inclinata
Gray, 1850
II Both aragonite Large shell (< 6 mm) with a tall keel. Larval shell large,
conical and globose, tilted relative to the adult shell.
Larval shell covered with small tubercula.
Yes
Atlanta tokiokai van
der Spoel & Troost,
1972
II
Atlanta
gibbosa
Atlanta gibbosa
Souleyet, 1852
II Both aragonite Medium shell (< 4mm) with a tall keel that is very thin
and transparent. Larval shell large, conical and globose,
tilted relative to the adult shell. Larval shell smooth.
No - species group
together with A. frontieri.
Low node support (32%).
Atlanta meteori (A
and B) Richter, 1972
II
Oxygyrus Oxygyrus inflatus (A,
B and C) Benson,
1835
I Inner shell aragonite, outer
shell and keel of conchiolin.
Large shell (< 14 mm) very rounded, almost spherical
and involute with a tall conchiolin keel. Larval shell
heavily ornamented with zig-zig spiral lines. The final
whorl of the adult shell is partially composed of
conchiolin.
Yes
Protatlanta Protatlanta sculpta
Issel, 1911
I Aragonite shell, conchiolin
keel
Small shell (< 2 mm) of aragonite with a tall conchiolin
keel. Larval shell is low conical with 2.5–3 whorls.
Yes
Protatlanta souleyeti
(Smith, 1888)
I
Wall-Palmer et al. BMC Evolutionary Biology (2020) 20:124 Page 6 of 14
less aragonite and more conchiolin. This route would in-
volve the direct evolution from the ornamented mem-
bers of the genus Atlanta (fully aragonite shell, Fig. 1b),
to Protatlanta (aragonite shell, conchiolin keel, Fig. 1a)
and terminating in Oxygyrus (shell largely composed of
conchiolin, Fig. 1c). The monophyletic group of smaller,
ornamented Atlanta species identified in the present
study does share the same radula ‘type I’with Prota-
tlanta and Oxygyrus. However, the relationships between
the three Atlantidae genera are not resolved, and there-
fore, this evolutionary hypothesis cannot be tested. A
broader dataset including information from the other
two heteropod families and more genetic information is
needed to resolve and inform these three deepest nodes
within the atlantid phylogeny.
Gaps in the fossil record
The fossil-calibrated Bayesian molecular phylogeny pre-
sented here (Fig. 4) supports an Early Cretaceous origin
for the family Atlantidae and implies that the gap in the
atlantid fossil record from the Early Cretaceous to the Oligo-
cene is likely due to poor shell preservation. The fossil record
of thin aragonitic holoplanktonic gastropod shells is affected
by both dissolution and by compaction during diagenesis
[35]. The euthecosome pteropods, of similar shell compos-
ition, thickness and size to the atlantids are also greatly af-
fected by diagenetic processes, and have a similar gap within
their fossil record, from the Late Cretaceous until the Eocene
[35], although recently, several potential shelled pteropods
from the Paleogene (Danian) and Late Cretaceous have been
described [36]. In modern oceans, pteropods are generally
much more abundant than atlantids and this difference in
abundance may explain why more pteropod fossils have
been found. The fossil record of both atlantids and eutheco-
some pteropods is more complete from the Eocene to the
present day [5,35]. It is very likely that there are Early Cret-
aceous to Oligocene atlantid fossils still to be found. Despite
the prodigious palaeontological research of Janssen (e.g. [15,
25,37]) and Nützel (e.g. [16,20]), there are few researchers
working in this field.
Fig. 4 The fossil-calibrated phylogeny of the family Atlantidae. Error bars shown in purple (95%) are presented for putative species with posterior
probabilities ≥85%. Calibration fossils are indicated with letters A-F (see legend and Table 3). Major geological events, including the Cretaceous-
Paleogene extinction event (KT), the Paleocene-Eocene Thermal Maximum (PETM), the Terminal Tethyan Event (TTE) and the uplift of the Isthmus
of Panama (IoP) are highlighted in orange
Wall-Palmer et al. BMC Evolutionary Biology (2020) 20:124 Page 7 of 14
Evolutionary history of the family Atlantidae
The fossil-calibrated Bayesian phylogeny (Fig. 4) has a
comparable topology to the 3-gene ML tree (Fig. 3), with
each genus of the Atlantidae a well-supported monophy-
letic group. The Bayesian phylogeny also confirms the
grouping of smaller ornamented, and larger less orna-
mented species of Atlanta (posterior probability > 99%).
The calibration fossil for the oldest member of the
superfamily Pterotracheoidea (heteropods) roots the mo-
lecular clock analyses within the Early Jurassic (Fig. 4).
The order Littorinimorpha, in which Pterotracheoidea
belongs, also originated in the Early Jurassic [38]. There-
fore, it is probable that little time transpired between the
origins of the Littorinimorpha and Pterotracheoidea
groups [16]. These gastropods likely adopted a holo-
planktonic lifestyle in response to several environmental
pressures that made the seafloor an unfavourable habi-
tat. During the Marine Mesozoic Revolution (251.9–
66.0 Ma) a re-shuffling of the marine realm took place
[17]. Throughout the Jurassic and Cretaceous, gastro-
pods underwent great diversification, with benthic gas-
tropods generally showing a strengthening of their shell
that is thought to have been caused by increased preda-
tion pressure [17]. Therefore, a move to a holoplank-
tonic lifestyle for gastropods such as Coelodiscus
minutus may have been an escape from benthic preda-
tors. Anoxic bottom waters are also known to have oc-
curred during the Jurassic [16]. Teichert and Nützel [16]
suggest that increasing frequency of dysoxic episodes
and hostile benthic conditions likely stimulated plankto-
trophic gastropod larvae to extend their planktonic
phase, eventually evolving into holoplanktonic species.
Elsewhere in the marine realm during the Jurassic there
was a clear expansion and diversification of marine mi-
croplankton with the appearance of the first plank-
tonic foraminifera and coccolithophores [17],
suggesting favourable conditions for calcifiers to col-
onise the upper ocean.
The molecular dating analyses propose a Mid-
Cretaceous Albian origin for the family Atlantidae (109–
101 Ma, Fig. 4, Table 2). This was a time of widespread
changes in the ocean climate system driven by tectonic
processes and volcanism. Sea levels rose, and increased
atmospheric CO
2
induced global warming, leading to
changes in ocean circulation and ocean stratification
[39]. With the continuation of the Marine Mesozoic
Revolution, there was a turnover of calcifying marine
plankton with high rates of extinction accompanied by a
dramatic increase in speciation and plankton diversity
[39]. In the Albian, ocean carbonate chemistry was al-
tered, potentially through hydrothermal activity, and
began to favour calcium carbonate producing plankton
[40]. There was a marked increase in marine productiv-
ity and calcification in planktonic foraminifera and
calcareous nanoplankton despite the rise in atmospheric
CO
2
. This was potentially made possible by nutrient
supply from submarine volcanism and a greater flux of
nutrients to the ocean from intensified terrestrial weath-
ering [39].
Due to the limited atlantid fossil record, it is not pos-
sible to determine whether the atlantids diversified dur-
ing the Late Cretaceous, Paleocene or Eocene, only that
the ancestor of Protatlanta and Oxygyrus likely split
from the ancestor of Atlanta in the Mid-Cretaceous
(Albian, Fig. 4). However, both extant lineages of the
family Atlantidae do persist over the Cretaceous-
Paleogene (KPg or KT, ~ 66 Ma) extinction event and
the Paleocene-Eocene Thermal Maximum (PETM, ~ 56
Ma), both times of intense environmental change and
ocean acidification [7,8]. There are no known Paleocene
fossils for the Oxygyrus + Protatlanta lineage, the first
known fossil being Atlantidea rotundata (Gabb, 1873) in
the Oligocene. However, the partial replacement of ara-
gonite with conchiolin in the shells of this lineage may
have been a response to ocean acidification. This change
is particularly evident in Oxygyrus where conchiolin
covers the aragonite shell entirely, likely protecting it
from seawater chemistry in a similar way to the perios-
tracum in pteropods [41]. All major lineages of the ara-
gonite shelled pteropods also lived through these periods
[6,42], experiencing a reduction in surface ocean pH
during the PETM on the order of 0.3–0.4 units [43]. It is
thought that euthecosome pteropods even diversified
during the PETM [6], possibly in response to increased
nutrient levels and ocean warming [43].
Our analyses estimate that from ~ 28–23 Ma to the
Present day, considerable radiation of the Atlantidae lin-
eages that lead to Recent species occurred, including the
origin of all extant genera and species. In particular,
there has been rapid diversification in the genus Atlanta
during the last ~ 25 Ma (Fig. 4). Estimated times for the
common ancestor of the three atlantid genera were
25.46 Ma (28.46–23.42 Ma), 14.50 Ma (15.32–13.92 Ma)
and 8.11 Ma (13.04–3.66 Ma) for Atlanta, Protatlanta
and Oxygyrus, respectively (Table 2). This dating sup-
ports the morphology based hypothesis that a conchiolin
shell and conchiolin keel are more derived characters in
the family Atlantidae, and were likely not features of the
Late Cretaceous B. minuta, which shares a similar shell
morphology to the calcified juvenile shell of Recent
Oxygyrus.
Two important vicariance events occurred in the last
25 Ma, including the Terminal Tethyan Event (TTE) of
the Mid-Miocene at ~ 18–12 Ma [44] and the uplift of
the Isthmus of Panama (IoP) in the Pliocene at ~ 3 Ma
[45]. These geographical events had a pronounced effect
on the ocean and the evolution of marine organisms.
During the period of oceanographic and climate change
Wall-Palmer et al. BMC Evolutionary Biology (2020) 20:124 Page 8 of 14
surrounding the closure of the Miocene Tethys Sea,
which separated the Atlantic Ocean from the Indian
Ocean, lineages leading to Recent species of atlantid
underwent rapid diversification, with the appearance of
all of the modern species groups (except the Atlanta
inclinata Gray, 1850 group Fig. 4, Table 2). Diversifica-
tion of the euthecosome pteropods also occurred at this
time, with many of the extant genera originating in the
Mid-Miocene [42]. For the atlantids, this is also the first
extinction event detectable within the fossil record, with
three species becoming extinct at ~ 13.82 Ma [5]. Due to
the incomplete fossil record of atlantids, it is not pos-
sible to estimate what proportion of total atlantid diver-
sity became extinct at this time, however, only
Atlantidea rotundata and an unidentified Atlanta sp.
are known to have survived this event [5].
Molecular dating analyses indicate that most modern
species arose following the TTE in the Tortonian at ~ 12–
10 Ma (Fig. 4). Additionally, our results suggest that several
atlantid morphospecies also splitintomultipleputativespe-
cies within the last 5 Ma, including Atlanta peronii A, B,
C1 and C2, Atlanta rosea A and B Gray 1850, Atlanta
meteori A and B Richter, 1972, Atlanta oligogyra BandC
Tesch, 1906 (Fig. 4). This may have been a response to the
Pliocene uplift of the IoP at ~ 3 Ma, which closed the link
between the Atlantic Ocean and the Pacific Ocean [45]. All
of these putative species (apart from A. peronii AandB)
show clear geographical separation, with one putative spe-
cies being present in the Atlantic Ocean only, and the other
being present in the Pacific and Indian Oceans [11]. A sec-
ond large-scale and global (known from deposits in the
Caribbean Sea, Mediterranean Sea, Philippines and Japan
[5]) atlantid extinction event also took place during this
time, with 40% of known atlantid species becoming extinct;
five species at the Pliocene-Pleistocene boundary (~ 2.58
Ma) and Atlanta cordiformis Gabb, 1873 at ~ 5.33 Ma [5].
Therefore, the rapid diversification of the genus Atlanta at
this time was probably also accompanied with population
bottlenecks and (local) extinctions caused by ocean changes
related to the IoP. More recently, localised extinctions of
Atlanta turriculata and Atlanta plana in the Atlantic
Ocean, and Protatlanta sculpta in the Indian Ocean have
been detected in the Quaternary fossil record [12–14].
These extinctions have occurred over the last ~ 24 ka and
may reflect ocean changes during the period following the
Last Glacial Maximum.
Table 2 Overview of calibrated node ages resulting from two independent runs of 10
8
generations (for nodes with a fossil calibration),
and derived node ages either resulting from independent runs that did not include a calibration for that node (for nodes with a fossil
calibration), or derived from two independent runs using all calibrations (all nodes without a fossil calibration). A derived age was not
possible for the node calibrated by Atlantidea rotundata because the tree topology changed when this fossil was removed
Node Calibration type Calibration age
(Ma)
Calibrated or derived
age
Age of crown (95% confidence intervals,
Ma)
Earliest heteropod Fossil: Coelodiscus
minutus
190.8–170.3 Calibrated 185.39 (189.76–182.86)
Derived 113.68 (138.62–100.83)
Family Atlantidae Fossil: Bellerophina
minuta
113–100.5 Calibrated 103.44 (109.19–100.59)
Derived 46.71 (75.23–27.10)
Genus Atlanta Fossil: Atlanta sp. 28.1–23.03 Calibrated 25.46 (28.46–23.42)
Derived 35.88 (58.41–16.17)
Clade Oxygyrus+
Protatlanta
Fossil: Atlantidea
rotundata
15.97–13.82 Calibrated 19.18 (24.22–15.47)
Derived N/A
Genus Protatlanta Fossil: Protatlanta
kbiraensis
15.97–13.82 Calibrated 14.50 (15.32–13.92)
Derived 8.08 (12.53–3.59)
Genus Oxygyrus Derived 8.11 (13.04–3.66)
Atlanta brunnea group Derived 10.92 (15.95–5.84)
Atlanta inflata group Derived 15.69 (21.41–9.88)
Atlanta lesueurii group Derived 16.48 (21.50–11.62)
Atlanta peronii group Derived 15.32 (20.62–9.80)
Atlanta gaudichaudi
group
Derived 13.35 (19.34–7.56)
Atlanta inclinata group Derived 4.75 (9.78–1.10)
Atlanta gibbosa group Derived 11.78 (17.64–6.31)
Clade Atlanta peronii Fossil: Atlanta peronii 3.6–2.58 Calibrated 3.24 (3.98–2.72)
Derived 9.38 (15.27–4.03)
Wall-Palmer et al. BMC Evolutionary Biology (2020) 20:124 Page 9 of 14
Conclusions - implications for a changing ocean
Calcifying plankton are widely accepted to be amongst
the most sensitive and first affected by current and pre-
dicted future warming and acidification of the world
oceans [46]. The results of this study show that the
upper ocean inhabiting, aragonite shell bearing atlantid
heteropods were able to persist through past climate cri-
ses, including the C-Pg (KT) extinction event, and the
PETM. The PETM is of particular interest, as it is con-
sidered the most analogous geological event to the
current Anthropogene climate crisis. However, the
current rates of change are unprecedented, even in com-
parison to the PETM [47] and there is really no analo-
gous climatic event with which to compare the predicted
future conditions [7]. Many marine organisms are un-
likely to have sufficient time to adapt at the current rate
of change.
The present study shows that although global-scale
environmental changes over the last 25 Ma have likely
caused large scale extinction of atlantids, they have
also resulted in periods of exceptional diversification.
Past ocean changes, largely resulting from vicarance
events, provided opportunities for speciation and have
driven evolution within this family. Vermeij [48]
hypothesised that when raw materials (e.g. from sub-
marine volcanism) and energy (e.g. CO
2
induced glo-
bal warming) become available to organisms at
unusually high rates, there are increased opportunities
for evolution and diversification. Planktonic organisms
have high evolutionary potential and are considered
to be well poised for evolutionary responses to global
change [49]. Therefore, if atlantids are able to keep
up with the rate of anthropogenic ocean changes,
they may be able to not only survive, but even diver-
sify in the changing ocean.
Methods
Specimen collection
A total of 588 specimens from all 34 known putative
atlantid species [11], including all 24 currently de-
scribed atlantid morphospecies, and 15 specimens of
one carinarid species were analysed in this study (591
CO1, 240 28S and 234 18S sequences, Table S1,Fig.
S4). For the concatenated gene phylogeny, a subset of
102 specimens was selected to provide good geo-
graphical coverage for each known putative species
(Fig. S4). Of these specimens, 36 were collected from
18 stations in the Atlantic Ocean during the Atlantic
Meridional Transect cruises in 2014 (AMT24, N= 28)
and 2017 (AMT27, N= 8). A total of 24 specimens
were collected from nine stations in the Indian Ocean
during oceanographic cruises SN105 (N=18) and
VANC10MV (N= 6). In the Pacific Ocean, 42 speci-
mens were collected from 23 stations during cruises
ACE-ASIA (N = 1), DRFT (N = 2), KH1110 (N= 16),
KM1109 (N = 2), KOK1703 (N= 3), S226 (N=4),
SO255 (N= 13) and WCOA16 (N = 1). In addition,
for the concatenated gene phylogeny, two specimens
of the partially shelled heteropod genus Carinaria,
collected during the oceanographic cruise SN105
(N = 2), were used as outgroup taxa.
Collection methods included the use of a variety of
plankton nets (e.g. ring, bongo, midwater trawl). These
have been previously described for most of the oceano-
graphic cruises listed here [11,50–54]. Collection tech-
niques for cruises SO255, KOK1703 and AMT27 have
not been previously published and we describe them
here. Cruise SO255 took place on board the RV Sonne
to the north east of New Zealand between March and
April 2017. Specimens were collected using a ring net
with an aperture of 1 m diameter, a mesh size of 350 μm
and a maximum sampling time of 30 min. At stations
SO255_041 and SO255_057, vertical net hauls were car-
ried out from 200 m water depth to the surface. At all
other stations, oblique tows were made in the upper 100
m. Cruise KOK1703 took place offshore of Hawaii,
around station ALOHA, on board the RV Ka’imikai-O-
Kanaloa in March 2017. Sampling was carried out using
either a 0.71 m diameter CalBOBL bongo net with a
mesh size of 200 μm, or a ring net with a 2 m diameter
and mesh size 505 μm. For all stations, oblique tows
were conducted in the upper 200 m for a maximum of
44 min. During cruise AMT27, specimens were collected
using a 0.71 m diameter bongo net and a 1 m diameter
ring net, both with a mesh size of 200 μm. Oblique
bongo net tows sampled a range of maximum depths
from 233 to 388 m and ring net tows sampled a range of
maximum depths from 56 to 99 m.
DNA extraction and amplification
Prior to DNA extraction, all specimens were imaged using
stacking microscopy on a Zeiss Discovery V20 or V12
microscope (images for previously unpublished specimens
deposited in the Barcode of Life Data System, BOLD, ac-
cession numbers in Table S1). DNA was extracted from
whole specimens using two methods. For most specimens,
the NucleoMag 96 Tissue kit (Macherey-Nagel) was used
on a Thermo Scientific KingFisher Flex magnetic particle
processor, with a final elution volume of 75 μl. For smaller
batches of specimens, DNA was extracted using the
DNeasy Blood and Tissue spin-column protocol with a
final elution volume of 100 μL. Both methods were suc-
cessful. An archive of DNA extracts, collection informa-
tion and images for all specimens is stored at Naturalis
Biodiversity Center, Leiden under the accession numbers
in Supplementary Table 1.
Three commonly used gene fragments were amplified. A
~ 570 bp fragment of the mitochondrial cytochrome c
Wall-Palmer et al. BMC Evolutionary Biology (2020) 20:124 Page 10 of 14
oxidase subunit 1 gene (CO1) was amplified using primers
jgLCO1490 (5′–TITCIACIAAYCAYAARGAYATTGG–3′)
and jgHCO2198 (5′–TAIACYTCIGGRTGICCRAAR-
AAYCA–3′)[55]. A ~ 1000 bp fragment of nuclear 28S
rRNA was amplified using primers C1-F (5′-ACCCGC
TGAATTTAAGCAT-3′)[56]andD3-R(5′-GACGATCG
ATTTGCACGTCA-3′)[57]. A ~ 970 bp fragment of nuclear
18S rRNA was amplified using primers 18S-KP-F (5′-
TGGAGGGCAAGTCTGGTG-3′)[42] and 1800R (5′-
GATCCTTCCGCAGGTTCACCTACG-3′)[57]. Primers
were tailed with M13F and M13R for sequencing [58].
All PCR reactions contained 17.30 μl ultra pure water
(mQ), 2.50 μl 10x Qiagen PCR buffer, 0.50 μl25mM
MgCl2, 1.00 μl 100 mM BSA, 1.00 μl 10 mM of each pri-
mer, 0.50 μl 2.5 mM dNTPs and 0.25 μl 5 U Qiagen Taq,
with 1.00 μl of template DNA, which was diluted up to
100 times for some samples. The same PCR steps were
performed for all three genes using an initial denatur-
ation step of 180 s at 96 °C, followed by 40 cycles of 15 s
at 96 °C, 30 s at 50 °C and 40 s at 72 °C, and finishing
with a final extension of 300 s at 72 °C. Sequencing of
forward and reverse strands was carried out by either
Macrogen Europe (Amsterdam), or Baseclear (Leiden).
Phylogenetic analyses
For individual gene phylogenies, a total of 237 new 28S
sequences, 230 new 18S sequences, and 99 new and 477
previously published [11,59,60] CO1 sequences of
atlantids were included (Table S1). The genus Carinaria
from the closely related heteropod family Carinariidae
was used as an outgroup with 14 CO1, three 28S and
four 18S sequences included from 15 specimens col-
lected in the Indian Ocean. Here, we consider a ‘putative
species’to be a well-supported monophyletic group
(bootstrap support > 80%) in our CO1 phylogenetic tree,
with interspecific genetic distances of > 6.95% (Jukes-
Cantor). We verified our selection of putative species
using Automatic Barcode Gap Discovery (ABGD) per-
formed on the entire CO1 dataset using Jukes-Cantor
genetic distances with default settings [61]. Similar to
previous ABGD analysis of atlantid CO1 sequences [11],
Atlanta inclinata and Atlanta tokiokai van der Spoel &
Troost, 1972 were grouped together due to high intra-
specific genetic diversity. However, here we consider
them to be two separate species because of clear
morphological differences. All other previously identified
putative species [11] were recognised by the ABGD ana-
lysis. Two additional putative species were also con-
firmed, one within A. peronii C, and one within O.
inflatus A, bringing the total number of putative species
to 36.
For the concatenated gene (3-gene) phylogeny, at least
one specimen from each atlantid putative species was in-
cluded from each ocean basin in which that putative
species resides. As far as possible, all three genes were
combined from a single specimen. In two cases, for At-
lanta plana and Atlanta selvagensis, it was necessary to
combine genes from different specimens at the same sta-
tion (A. plana SN105 station 19, A. selvagensis AMT24
station 16), in order to obtain complete taxon sampling
for all genes. Where records have been combined, speci-
mens were confirmed to be conspecific using CO1,
which was available for all specimens. All three markers
were obtained for each putative species in each region,
except for Atlanta gaudichaudi, which was only success-
ful for CO1 and 18S, and Atlanta californiensis for
which only CO1 was sequenced. A total of 102 CO1,
100 28S and 101 18S sequences are included in the
concatenated gene phylogeny.
New sequences were verified and edited using Gen-
eious R8 and all sequences were aligned using MEGA 7
[62]. All gaps in the alignments of 28S and 18S were
trimmed resulting in final alignments of 851 bp for 28S
and 964 bp for 18S. The alignment of CO1 was checked
for stop codons and then all 657 sites were included in
the analyses. The concatenated gene alignment was a
total of 2472 bp.
Single gene and 3-gene phylogenetic relationships
were resolved using maximum likelihood analyses in
RaxmlGUI 1.5b2 [63]. Using jModelTest, the most ap-
propriate evolutionary model was determined to be the
General Time Reversible (GTR) model with a proportion
of invariable sites (+I) and gamma distributed rate vari-
ation among sites (+G) independently for each gene as
well as for the 3-gene alignment. For the single gene
phylogenies, a maximum likelihood search was per-
formed with thorough bootstrapping analysis of 1000
replicates applied for CO1, and 1500 replicates applied
for 28S and 18S. The same analysis was carried out for
the concatenated gene analysis, but with the three genes
partitioned and 3000 replicates applied.
Fossil-calibrated phylogeny
A subset of 34 atlantid and one Carinaria concatenated
gene sequences were included in the fossil-calibrated
phylogeny, including a single representative of each pu-
tative species identified in previous CO1 phylogenies
[11] (35 CO1, 33 28S, 34 18S). Fossil-calibrated analysis
was carried out using BEAST 2.5.0 [64]. A GTR site
model and relaxed log-normal molecular clock were ap-
plied in BEAUti 2.5.0. A Yule model was calibrated using
log-normal distributions of several fossil dates (sum-
marised in Table 3). The crown node of the superfamily
Pterotracheoidea was calibrated using the earliest poten-
tial heteropod, Coelodiscus minutus [16] from the Pliens-
bachian of the Early Jurassic (190.8–182.7 Ma). For the
remaining calibration, the oldest known fossils for the
family Atlantidae (Bellerophina minuta [23]) and the
Wall-Palmer et al. BMC Evolutionary Biology (2020) 20:124 Page 11 of 14
genera Atlanta (Atlanta sp. [25]) and Protatlanta (Pro-
tatlanta kbiraensis [25]) were used as crown calibrations
(Table 3). The Eocene genus Eoatlanta and the species
Eoatlanta spiruloides were not included in the calibra-
tions because E. spiruloides is now thought to be a ben-
thic gastropod in the superfamily Vanikoroidea [65,66].
Based on careful consideration of morphology, the ex-
tinct species Atlantidea rotundata [26] was used to cali-
brate the node Oxygyrus + Protatlanta. This species
exhibits morphological characters in common with both
genera, having larval shell ornamentation similar to Oxy-
gyrus, but an adult shell similar to Protatlanta, and a
smooth periphery suggesting a conchiolin keel (common
to Oxygyrus and Protatlanta).Running the Bayesian ana-
lysis without the Atlantidea rotundata calibration chan-
ged the topology of the tree, grouping Atlanta with
Oxygyrus. This placement is not in agreement with the
topology of the concatenated ML phylogeny, which
shows that relationships between the three genera are
not well resolved with the current molecular dataset. Fi-
nally, the morphospecies Atlanta peronii, which is made
up of four putative species, was used to calibrate more
recent speciation [15]. The fossil genus Freboldia
(163.5–157.3 Ma) was not included in the calibrations
because, unlike B. minuta, this species does not show
morphological similarity to the Atlantidae and we are
unconfident in its current placement [18]. Two inde-
pendent MCMC chains were run with 10
8
generations
each and checked for convergence with a burnin of 10%
in Tracer 1.6.0 [67] before being combined using Log-
Combiner 2.5.0 [64]. Trees and log-likelihood values
were sampled at every 10
4
generations. Maximum clade
credibility trees were selected using TreeAnnotator 2.5.0
[64]. Calibration points were checked by running mul-
tiple analyses and leaving out one calibration fossil each
time (Table 2).
Supplementary information
Supplementary information accompanies this paper at https://doi.org/10.
1186/s12862-020-01682-9.
Additional file 1: Supplementary Table 1. Specimens included in this
study.
Additional file 2: Supplementary Figure 1. Maximum likelihood
phylogeny of the family Atlantidae based on cytochrome coxidase
subunit 1 mitochondrial DNA (CO1). Black squares represent bootstrap
support > 80%. Species groups based on morphology are highlighted
with coloured boxes (See Table 1).
Additional file 3: Supplementary Figure 2. Maximum likelihood
phylogeny of the family Atlantidae based on the nuclear gene 28S.
Poorly supported branches (< 60%) have been collapsed to simplify the
phylogeny. Black squares represent bootstrap support > 80%. Species
groups based on morphology are highlighted with coloured boxes (See
Table 1).
Additional file 4: Supplementary Figure 3. Maximum likelihood
phylogeny of the family Atlantidae based on the nuclear gene 18S.
Poorly supported branches (< 60%) have been collapsed to simplify the
phylogeny. Black squares represent bootstrap support > 80%. Species
groups based on morphology are highlighted with coloured boxes (See
Table 1).
Additional file 5 : Supplementary Figure 4. The distribution of all
specimens used in this study demonstrates the global coverage of the
dataset. Filled circles represent specimens used for the concatenated
gene phylogeny. Data were visualised using the software QGIS v2.8
(https://www.qgis.org/en/site/).
Abbreviations
ABGD: Automatic Barcode Gap Discovery; AMT24 and AMT27: Atlantic
Meridional Transect cruises for the years 2014 and 2017; BOLD or
BOLDSYSTEMS: Barcode of Life data system; CO1: cytochrome coxidase
subunit 1; CO
2
: carbon dioxide; DNA: deoxyribonucleic acid; GTR: General
Time Reversible; IoP: the uplift of the Isthmus of Panama; KPg or
KT: Cretaceous-Paleogene extinction event; PETM: Paleocene Eocene Thermal
Maximum; rRNA: ribosomal ribonucleic acid; TTE: Terminal Tethyan Event of
the M id-Miocene at ~ 18–12 Ma
Acknowledgements
We thank Atsushi Tsuda from the University of Tokyo for contributing
atlantid specimens and Thijs M.P. Bal from Nord University, Norway and
Frank Stokvis from Naturalis for help with developing molecular methods.
We would like to acknowledge the scientists, captain and crew who took
Table 3 Settings for the molecular clock calibration using a Yule model
Calibrated node Calibration type Age Oldest age
(Ma)
Youngest age
(Ma)
M S Offset Prior
dist.
Reference
Superfamily
Pterotracheoidea
Fossil: Coelodiscus
minutus
Pliensbachian 190.8 170.3 3.00 0.80 182.7 Log-
normal
[8]
Family Atlantidae Fossil: Bellerophina
minuta
Albian 113 100.5 4.00 1.00 100.5 Log-
normal
[14]
Genus Atlanta Fossil: Atlanta sp. Chattian 28.1 23.03 2.40 0.55 23.03 Log-
normal
[16]
Clade
Oxygyrus+
Protatlanta
Fossil: Atlantidea
rotundata
Langhian 15.97 13.82 0.90 0.65 13.82 Log-
normal
[17]
Genus Protatlanta Fossil: Protatlanta
kbiraensis
Langhian 15.97 13.82 0.90 0.65 13.82 Log-
normal
[16]
Clade Atlanta peronii Fossil: Atlanta peronii Piacenzian 3.6 2.58 0.51 0.50 2.58 Log-
normal
[11]
Wall-Palmer et al. BMC Evolutionary Biology (2020) 20:124 Page 12 of 14
part in cruises SO255, KOK1703 and AMT27 (DY084/085), as well as the
Atlantic Meridional Transect (AMT) programme.
Authors’contributions
DW-P and KTCAP designed the study, DW-P, KTCAP, EG, LM collected speci-
mens, DW-P carried out sample preparation and analysis. DW-P, LQC and
AWJ carried out data analysis. All authors contributed to manuscript prepar-
ation, and all authors have read and approved the manuscript.
Funding
This project was funded by the European Union’s Horizon 2020 research and
innovation programme under the Marie Sklodowska-Curie grant agreement
No 746186 [POSEIDoN, DWP]. KTCAP and fieldwork were supported by a Vidi
grant 016.161351 from the Netherlands Organisation of Scientific Research
(NWO). The R/V Sonne cruise SO255 was funded by the German Federal Min-
istry of Education and Research (BMBF; grant 03G0255A). Fieldwork on sev-
eral cruises was supported by US National Science Foundation grants OCE-
1029478 and OCE-1338959 to EG. The Atlantic Meridional Transect (AMT22,
AMT24, AMT27) 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 336 of the AMT programme. Funding agencies played no role in
study design, sample and data collection, analysis or interpretation, or in
writing the manuscript.
Availability of data and materials
The molecular dataset supporting the results of this article, including specimen
images and collection information, is available from the Barcode of Life Data
System (BOLDSYSTEMS) repository [68]doi:https://doi.org/10.5883/DS-
ATLANTID. Individual specimen accession numbers can be found in
Supplementary Table 1. Single gene and concatenated alignments are available
from Figshare [69]doi:https://doi.org/10.6084/m9.figshare.12420365.Voucher
DNA extracts are held at the Naturalis Biodiversity Center (bioportal.naturalis.nl)
under museum accession numbers presented in Supplementary Table 1.
Ethics approval and consent to participate
Not applicable.
Consent for publication
Not applicable.
Competing interests
The authors declare that they have no competing interests.
Author details
1
Plankton Diversity and Evolution, Nauralis Biodiversity Center, Leiden, The
Netherlands.
2
Department of Oceanography, University of Hawai’iatMānoa,
Honolulu, USA.
3
Institute for Biodiversity and Ecosystem Dynamics (IBED),
University of Amsterdam, Amsterdam, The Netherlands.
Received: 5 March 2020 Accepted: 6 September 2020
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