RESEARCH ARTICLE
Phylogeny and New Classification of
Hydrothermal Vent and Seep Shrimps of the
Family Alvinocarididae (Decapoda)
Alexander L. Vereshchaka*, Dmitry N. Kulagin, Anastasia A. Lunina
P.P. Shirshov Institute of Oceanology of Russian Academy of Sciences, Moscow, 117997, Russia
* alv@ocean.ru
Abstract
OPEN ACCESS
Citation: Vereshchaka AL, Kulagin DN, Lunina AA
(2015) Phylogeny and New Classification of
Hydrothermal Vent and Seep Shrimps of the Family
Alvinocarididae (Decapoda). PLoS ONE 10(7):
e0129975. doi:10.1371/journal.pone.0129975
Academic Editor: Andreas Hejnol, Sars International
Centre for Marine Molecular Biology, NORWAY
Received: December 2, 2014
Accepted: May 14, 2015
Published: July 10, 2015
Copyright: © 2015 Vereshchaka et al. This is an
open access article distributed under the terms of the
Creative Commons Attribution License, which permits
unrestricted use, distribution, and reproduction in any
medium, provided the original author and source are
credited.
Data Availability Statement: All relevant data are
within the paper.
Funding: The studies were supported by the
Russian Foundation for Basic Research (grant
number 15-04-08228). The funders had no role in
study design, data collection and analysis, decision to
publish, or preparation of the manuscript.
Competing Interests: The authors have declared
that no competing interests exist.
The paper addresses the phylogeny and classification of the hydrothermal vent shrimp family Alvinocarididae. Two morphological cladistic analyses were carried out, which use all 31
recognized species of Alvinocarididae as terminal taxa. As outgroups, two species were
included, both representing major caridean clades: Acanthephyra purpurea (Acanthephyridae) and Alpheus echiurophilus (Alpheidae). For additional support of the clades we utilised
available data on mitochondrial Cytochrome c Oxidase I gene (CO1) and 16S ribosomal
markers. Both morphological and molecular methods resulted in similar tree topologies and
nearly identical clades. We consider these clades as evolutionary units and thus erect two
new subfamilies: Rimicaridinae (Alvinocaridinides, Manuscaris, Opaepele, Shinkaicaris,
Rimicaris), Alvinocaridinae (Alvinocaris), whilst recognising Mirocaridinae (with genera Mirocaris and Nautilocaris) at subfamily level. One genus, Keldyshicaris could not be assigned
to any subfamily and is thus left as incertae sedis. The monophyly of Alvinocardinae was
supported by morphological data, but not supported by molecular data (two analyses); the
monophyly of all subfamilies was supported both by morphological and molecular data.
Chorocaris is herein synonymized with Rimicaris, whilst Opaepele vavilovi is herein transferred to a new genus Keldyshicaris. Morphological trends within Alvinocarididae are discussed and short biogeographical remarks are given. We provide emended diagnoses for
all subfamilies and genera along with keys to all recognized species.
Introduction
Shrimps of the family Alvinocarididae inhabit deep-sea cold-seeps and hydrothermal vent
areas around the world, and have been found in the Atlantic, Pacific, and Indian Oceans [1]
within the depth range of 252 to 4960 m [2–3]. Most species of the family occur at hydrothermal vents, but a few are found in cold-seep areas [3]; one species, Alvinocaris longirostris, has
been reported from both vents and seeps [4–7]. The first record of the family was based on a
few specimens from the Galapagos Rift, which were described in 1982 as Alvinocaris lusca by
Austin Williams and Fenner Chace [8]. Later the first author described a further two species of
PLOS ONE | DOI:10.1371/journal.pone.0129975 July 10, 2015
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Phylogeny and New Classification of Alvinocarididae
a new genus, Rimicaris from the hydrothermal vent field TAG [9]. One of these species was
subsequently transferred to a new genus Chorocaris in 1990 [10]. In the middle of the 1990s,
Russian and American scientists described two further genera Opaepele [11] and Mirocaris
[12]; whilst more recently the genera Nautilocaris, Shinkaicaris, and Alvinocaridinides were
described by Japanese and French researchers [2], [13], [14].
Due to drastic metamorphosis in ontogeny, the history of the family systematics has not
been smooth and some taxa were later synonimised. For example, the genus Iorania [15] and
the species Rimicaris aurantiaca [16] are now considered to be juveniles of Rimicaris exoculata.
There was no consensus on the status of the new family Mirocarididae established for a single
genus Mirocaris [12]; phylogenetics showed a significant distance between this group and the
rest of Alvinocarididae [17–18], although taxonomists kept Mirocaris as a genus within Alvinocarididae [19]. Status for Opaepele vavilovi also remains unseratin [20].
Three new species and a new genus Manuscaris have recently been described from hydrothermal vents in the Pacific Ocean [21]. In this comprehensive study, partial sequences of mitochondrial COI were used, resulting in a minor change in the classification of Alvinocarididae,
the transfer of Opaepele susannae into Chorocaris [21].
At present, 9 genera and 31 species are known within the family and a comprehensive phylogenetic analysis is needed to disentangle existing problems and to elucidate the status of all
genera.
This task is eased by the presence of a significant amount of information on partial
sequences of mitochondrial COI gene in GenBank, unusually rich for decapods. Much of this
data was used in a previous comprehensive study [17], which confirmed three distinct clades
consistent with morphology at that time: (1) Rimicaris/Chorocaris/Opaepele, (2) Alvinocaris,
and (3) Mirocaris. Evolutionary relationships of vent-endemic shrimp species were shown to
correlate neither with their current biogeographic distribution nor with the history of sea-floor
spreading. Later studies have incorporated further molecular data for several recently described
species and enhanced information for the species studied in [3], [17], [18], [21–26]. However,
no attempt to carry out a complete phylogenetic analysis of the whole family Alvinocarididae
has been carried out to date.
Combining both morphological and molecular evidence should shed light on the complex
relationships in Alvinocarididae.
In this paper we summarize original and literature data about the composition, morphology,
and genetic diversity of the family Alvinocarididae. Further, we (1) find and describe morphological characters, (2) perform cladistic morphological analyses, (3) analyze molecular data, (4)
combine and compare morphological and molecular results, (5) discuss supported taxa, and
(6) provide a new classification, emended diagnoses, and identification keys for all subfamilies,
genera, and species.
Material and Methods
Material for morphological analysis
Material was collected along the Mid-Atlantic Ridge during six cruises of R/V “Akademik Mstislav Keldysh” with the use of two deep-sea manned submersibles "Mir–1" and "Mir–2" (34th
cruise, August-October 1994, 39th cruise, August-October 1996, 41st cruise, August-December
1998, 47th cruise, June-July 2002, 49th cruise August 2003, 50th cruise, August 2005). Seven
vent fields were investigated during 1994–2005, including Menez Gwen (37.8417 N 31.525 W),
Lucky Strike (37.2933 N 32.2733 W), Rainbow (36.23 N 33.902 W), Broken Spur (29.17 N
43.1717 W), TAG (26.1367 N 44.8267 W), Snake Pit (23.3683 N 44.95 W) and Logatchev
PLOS ONE | DOI:10.1371/journal.pone.0129975 July 10, 2015
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Phylogeny and New Classification of Alvinocarididae
(14.752 N 44.9785 W). No specific permission was required for field studies in any of these
locations. The field studies did not involve endangered or protected species.
Shrimps were collected using baited traps and suction samplers. Immediately after retrieval
all specimens were sorted, measured, and preserved in 80% alcohol. Measurements follow
established methods for shrimp morphological description [27]. Shrimp morphology and its
temporal/spatial variations were thoroughly investigated for this material on the basis of 5861
individuals [28], [29]. A detailed description of this material and discussion of the various species may be found in [20], [29], [30].
Analysis of the morphology of all species within the family was made with the use the above
original data and all other available literature data (Table 1).
Terminal taxa, outgroups, and characters used for morphological
analysis
All thirty-one recognized species of Alvinocarididae were included as terminals. Outgroup
selection was made on the basis of a comprehensive molecular study [31], which revealed two
major clades of Caridea: (1) Alpheidae, Hippolytidae, Crangonidae, Glyphocrangonidae, Barbouriidae, Pandalidae, Hymenoceridae, Gnathophyllidae, and Palaemonidae and (2) Rhynchocinetidae, Oplophoridae, Nematocarcinidae, Alvinocarididae, Campylonotidae, Pasiphaeidae
and Eugonatonotidae. The first outgroup species, Acanthephyra purpurea A. Milne-Edwards,
1881 [32], represents the first clade: Wong et al. [33] have shown that family Acanthephyridae
is sister to Oplophoridae and advocate combining both families as Oplophoridae. We chose A.
purpurea partly because this species is present in GenBank and could also be used as the outgroup in the molecular analysis. The second outgroup species, Alpheus echiurophilus Anker,
Komai and Marin 2015 [34], belongs to Alpheidae and represents the second major clade of
Caridea. Both species are ecologically very different (pelagic and burrowing) as well as morphologically and a comparison of cladograms is thus instructive.
Sixty-three morphological characters (ten multistate) were used in the analysis, and are
listed in Table 2, along with character states, brief descriptions, and references to figures (see
also Figs 1–3). The data matrix is presented in Table 3.
Analytical method for cladistic analysis
Data were analyzed using a combination of programs by maximum parsimony: Winclada/
Nona, TNT, and Mesquite [35–37].
All characters were unordered (non-additive) and equally weighted, missing data were
scored as unknown. Characters were unordered, so the score given for each state (i.e., 0, l, 2)
implies nothing about order in a transformation series [38]. Trees were generated in TNT
under the implicit enumeration. Relative stability of clades was assessed by standard bootstrapping (sample with replacement) with 10000 pseudoreplicates and by Bremer support (algorithm TBR, saving up to 10000 trees up to 3 steps longer).
Molecular data
Both Mitochondrial Cytochrome c Oxidase I (CO1) and 16S ribosomal markers were selected
for phylogenetic analyses, as only these markers have been sequenced for a representative number of alvinocaridid species, with CO1 sequences for 20 (out of 31) species available (Table 4).
For the present phylogenetic analyses, we used all publicly available 271 CO1 sequences for
individuals identified to species-level. Partial 16S sequences are only available for 10 alvinocaridid species (Table 4). For the present phylogenetic analyses, we used all 29 sequences available
in the GeneBank.
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Phylogeny and New Classification of Alvinocarididae
Table 1. List of all valid species of the family Alvinocarididae, with remarks on their former and current status.
Genus
Species
Description, author and
year
Type locality, depth
Before (Komai,
Tsuchida, 2015)
After (Komai,
Tsuchida, 2015)
Here
Alvinocari-dinides
Alvinocari-dinides
Alvinocaridinides
formosa
Komai, Chan, 2010
Gueishandao, Yilan County, Taiwan, 24°51.231'N
0121°59.204'E, 252–275 m
Alvinocaris
Alvinocaris
Alvinocaris
alexander
Ahyong, 2009
Rumble V Seamount, 36°08.27–07.96'S 78°11.74–
11.70'E, 485–415 m
Alvinocaris
Alvinocaris
Alvinocaris
brevitelsonis
Kikuchi, Hashimoto, 2000
”Depression C” of the Minami-Ensei Knoll, 28°
23.35'N 127°38.38'E, 705 m
Alvinocaris
Alvinocaris
Alvinocaris
chelys
Komai, Chan, 2010
Gueishandao, Yilan County, Taiwan, 24°49.682'N
122°0.254'E, 300–276 m
Alvinocaris
Alvinocaris
Alvinocaris
dissimilis
Komai, Segonzac, 2005
Depression C, Minami-Ensei Knoll, 28°23.35'N 127°
38.38'E, 705 m
Alvinocaris
Alvinocaris
Alvinocaris
komaii
Zelnio, Hourdez, 2009
Kilo Moana, Eastern Lau Spreading Center, Lau
Basin, southwest Pacific,; 20°9'S 76°12'E, 2620 m
Alvinocaris
Alvinocaris
Alvinocaris
longi-rostris
Kikuchi, Ohta, 1995
Iheya Ridge, Clam Site, Okinawa Trough, 27°
32.70'N 126°58.20'E, 1360 m
Alvinocaris
Alvinocaris
Alvinocaris
lusca
Williams, Chace, 1982
Galapagos Rift Rose Garden area, 0°48.25'N 86°
13.48'W, maximum of 2450 m
Alvinocaris
Alvinocaris
Alvinocaris
markensis
Williams, 1988
Mid-Atlantic Rift Valley about 70 km south of Kane
Fracture Zone, 23°22.09'N 44°57.12'W, 3437 m
Alvinocaris
Alvinocaris
Alvinocaris
methanophila
Komai, Shank, Van
Dover, 2005
ODP site 996, Blake Ridge Diapir, 32°29.623'N 76°
11.467'W, 2155 m
Alvinocaris
Alvinocaris
Alvinocaris
muricola
Williams, 1988
West Florida Escarpment, 26°01'N 84°54.61'W,
3277 m
Alvinocaris
Alvinocaris
Alvinocaris
niwa
Webber, 2004
Rumble V, 36°8.63–8.57'S 178°11.77–11.50'E,
877–655 m
Alvinocaris
Alvinocaris
Alvinocaris
stactophila
Williams, 1988
north central Gulf of Mexico about 129 km S of
Louisiana, 27°46.94'N 91°30.34'W, 534 m
Alvinocaris
Alvinocaris
Alvinocaris
solitaire
Yahagi, Watanabe,
Kojima, Beedessee,
Komai, 2014
Central Indian Ridge, Solitaire hydrothermal vent
field,19°33.413’S, 65°50.888’E, 2606 m
Alvinocaris
Alvinocaris
Alvinocaris
williamsi
Shank, Martin, 2003
Menez Gwen hydrothermal field, North Atlantic
Ocean, 37°50.5'N 31°31.3'W, 850 m
Chorocaris
Chorocaris
Rimicaris
chacei
(Williams, Rona, 1986)
TAG Hydrothermal Field, Mid-Atlantic Ridge, 26°
08.3'N 44°49.6'W, 3620–3650 m
Chorocaris
Chorocaris
Rimicaris
paulexa
Martin, Shank, 2005
Homer Vent (347OC black smoker), 17°37.220'S
113°15.123'W, 2595 m, southern East Pacific Rise
-
Chorocaris
Rimicaris
parva
Komai, Tsuchida, 2015
Manus Basin, South Su, Wave Mercury 2007 (Luk
Luk) Campaign, 03°08.09’S, 152°10.5’E, 1310 m
Chorocaris
Chorocaris
Rimicaris
vandoverae
Martin, Hessler, 1990
Alice springs vent field, Mariana Back-Arc Basin,
18°12.599'N 144°42.431'E, 3640 m
-
Chorocaris
Rimicaris
variabilis
Komai, Tsuchida, 2015
Manus Basin, South Su, Wave Mercury 2007 (Luk
Luk) Campaign, 03°08.09’S, 152°10.5’E, 1310 m
Mirocaris
Mirocaris
Mirocaris
fortunata
(Martin, Christiansen,
1995)
Vent site 3, Lucky Strike hydrothermal vent, Azores,
37°17.6'N 32°16.5'W, 1624 m
Mirocaris
Mirocaris
Mirocaris
indica
Komai, Martin, Zala,
Tsuchida, Hashimoto,
2006
Central Indian Ridge, Kairei Field, 25°19.2'S 70°
02.4'E, 2422 m
-
Manuscaris
Manuscaris
acuminatus
Komai, Tsuchida, 2015
Manus Basin, South Su, Wave Mercury 2007
Campaign, 03°08.09’S, 152°10.5’E, 1310 m
Nautilocaris
Nautilocaris
Nautilocaris
saintlaurentae
Komai, Segonzac, 2004
North Fiji Basin, White Lady site, 16°59.50'S 173°
55.47'E, 2000 m
Opaepele
Opaepele
Opaepele
loihi
Williams, Dobbs, 1995
Loihi Seamount, Hawaii, 18°55'N 155°16'W, 980 m
(Continued)
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Phylogeny and New Classification of Alvinocarididae
Table 1. (Continued)
Genus
Species
Description, author and
year
Type locality, depth
Before (Komai,
Tsuchida, 2015)
After (Komai,
Tsuchida, 2015)
Here
Opaepele
Chorocaris
Rimicaris
susannae
Komai, Giere, Segonzac,
2007
Lilliput, southern Mid-Atlantic Ridge, 09°32.845'S
13°12.546'W, 1500 m, mussel field with diffuse vent
fluids
Opaepele
Opaepele
Keldyshicaris
vavilovi
Lunina, Vereshchaka,
2010
Mid-Atlantic Ridge, Broken Spur vent site, stn 4797
Rimicaris
Rimicaris
Rimicaris
exoculata
Williams, Rona, 1986
TAG Hydrothermal Field, Mid-Atlantic Ridge, 26°
08.3'N 44°49.6'W, 3620–3650 m
Rimicaris
Rimicaris
Rimicaris
hybisae
Nye, Copley, Plouviez,
2011
Mid-Cayman Spreading Centre, Caribbean, Von
Damm vent field, 18822.6050 N81847.8750 W; 2300
m
Rimicaris
Rimicaris
Rimicaris
kairei
Watabe, Hashimoto, 2002
The Central Indian ridge, Indian Ocean, the Kairei
Field, 25°19.16'S 70°02.40'E, 2454 m
Shinkaicaris
Shinkaicaris
Shinkaicaris
leurokolos
(Kikuchi, Hashimoto,
2000)
”Depression C” of the Minami- Ensei Knoll, 28°
23.35'N 127°38.38'E, 705 m
doi:10.1371/journal.pone.0129975.t001
Analysis of molecular data
Multiple alignments were made with the use of the Clustal W algorithm [39]. Six CO1
sequences were discarded after alignment, as they represented non-barcoding parts of the CO1
gene or were too short. The remaining 265 aligned sequences were trimmed according to the
shortest sequences (Accession Numbers: KC840928-KC840940, HM125910-HM125956) with
a total length of 471 bp. Amino acid sequences received from the nucleotide sequences had no
stop codons within the open reading frame using the invertebrate mitochondrial code. All 16S
sequences after alignment were trimmed according to the shortest sequences (Accession Numbers: AM087916- AM087925) with a total length of 286 bp.
Phylogenetic analysis was performed using both Maximum Likelihood (ML) and Bayesian
analyses. To root the resultant trees, Acanthephyra purpurea Awas used (also see section 2.2).
The best-fit model selected using jModelTest 2.1.7 [40] was the Tamura-Nei model with a
gamma distribution and invariable sites (TrN+G+I) for CO1 and the Hasegawa-Kishino-Yano
model with a gamma distribution (HKY+G) for 16S data set. These models were used to generate ML gene trees in MEGA 5. Support for branches was assessed using bootstrap analyses with
1,000 replicates [41]. Bayesian phylogenetic analysis was made with the use of MrBayes v3.2.1
[42]. A general time-reversible model (GTR) of sequence evolution with a gamma distribution
and invariable sites for CO1 data set was chosen as it represents the closest approximation of
the Tamura—Nei model in MrBayes. HKY+G model was used for 16S data set. The Markov
Chain Monte Carlo (MCMC) analysis was further used with the following settings: (1) for
CO1–18 million generations, trees sampled every 5000 generation, and the first 900 trees discarded; (2) for 16S–1.5 million generations, trees sampled every 1000 generation, and the first
375 trees discarded. The average standard deviation of split frequencies between two runs of
MCMC was less than 1% for each analysis, thus indicating convergence.
Estimation of clade robustness
For morphological analyses, we considered the clades robust if they received simultaneous Bremer support 3 after both analyses. For molecular analyses, we considered the clades robust if
they received Bayesian posterior probability value 75%.
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Phylogeny and New Classification of Alvinocarididae
Table 2. List of morphological characters and their states.
No
Character
0
Rostrum
Character state
State No
Figure
absent
0
1A
present
1
1B
1B
CARAPACE
1
2
3
Rostrum
Rostrum,
Rostrum
4
Rostrum
5
Rostrum
6
Rostrum
7
8
9
10
11
12
13
14
Rostrum, minimal number of dorsal teeth or notches
Rostrum, maximal number of dorsal teeth or notches
Rostrum
Rostrum
Rostrum, minimal number of ventral teeth or notches
Rostrum, maximal number of ventral teeth or notches
Rostrum, minimal number of teeth or notches on carapace
Rostrum, maximal number of teeth or notches on carapace
15
Carapace, postrostral dorsal carina extending beyond the midlength
16
Carapace, antennal angle
17
Carapace, acute pterygostomial tooth
st
not reaching end of 1 antennular segment
0
reaching end of 1st antennular segment
1
1C
overreaching end of 2nd antennular segment
2
1D
tip acute
0
1C
tip obtuse
1
1B
laterally compressed
0
1C
not laterally compressed
1
1B
not dorsoventrally compressed
0
1C
dorsoventrally compressed
1
1B
dorsally carinate
0
1C
not dorsally carinate
1
1B
dorsally smooth
0
1E
dorsally notched
1
1F
dorsally toothed
2
1C,D
0
0
5–10
1
11–15
2
16 or more
3
0
0
4–10
1
11–15
2
16 or more
3
ventrally carinate
0
1C
not ventrally carinate
1
1B
ventrally smooth
0
1E
ventrally notched
1
1F
ventrally toothed
2
1D
0
0
1–2
1
3–6
2
0
0
1–2
1
6–11
2
0
0
1–5
1
6–10
2
0
0
1–5
1
6–10
2
absent
0
present
1
blunt
0
acute
1
absent
0
(Continued)
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Phylogeny and New Classification of Alvinocarididae
Table 2. (Continued)
No
Character
18
Dorsal organ under carapace
19
20
Dorsal organ under carapace
Dorsal organ
Character state
State No
present
1
absent or inconspicuous
0
conspicuous
1
restricted to postorbital region
0
extended beyond the postorbital region
1
nearly entire
0
four-lobed, without pores
1
four-lobed, with a pore
2
Figure
ABDOMEN AND TELSON
21
22
23
24
25
26
Third abdominal segment, posterior margin of pleura
Telson, long linear row of movable dorsolateral spines (5 in row)
Telson, long sinuous row of movable dorsolateral spines (5 in row)
Telson, number of strong spines on posterior margin
Telson, posterior margin
Telson, posterior concave margin
smooth
0
2A
serrated
1
2B
absent
0
present
1
absent
0
present
1
2–4
0
2C
6 or more
1
2D
convex
0
2C
concave
1
2D
with shallow incision
0
2D
nearly bilobed
1
THORACIC APPENDAGES
27
28
29
Eyestalks
Eyestalks
Eyes, anterior margin
30
Antenna II
31
Maxilla II, plumose bacteriophorous setae on scaphognathite
32
Maxilliped III, epipod
33
Maxilliped III, epipod
34
Maxilliped III, merus
35
Pereopod I, epipod
36
Pereopod I, epipod
37
Pereopod I, grooming apparatus
38
Pereopod II, epipod
39
Pereopod II, epipod
not fused partly
0
fused partly, mould seam present
1
not fused entirely
0
fused entirely, without mould seam
1
entire
0
with conspicuous tubercle
1
not operculiform
0
operculiform
1
1C
absent
0
2E
present
1
2F
subtriangular
0
strap-like
1
not terminated in hook
0
terminated in hook
1
unarmed
0
with 1–2 distal spines
1
absent or rudimentary
0
strap-like
1
not terminated in hook
0
terminated in hook
1
absent or inconspicuous
0
conspicuous
1
absent or rudimentary
0
strap-like
1
not terminated in hook
0
3A
3A
3A
3A
3A
(Continued)
PLOS ONE | DOI:10.1371/journal.pone.0129975 July 10, 2015
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Phylogeny and New Classification of Alvinocarididae
Table 2. (Continued)
No
Character
40
Pereopod II, movable spines on ischium
41
Pereopod III, epipod
42
Pereopod III, epipod
43
Pereopod III, strong movable spines on ischium
44
Pereopod III, proximal strong movable spines on merus
45
Pereopod III, distal movable spines on merus
46
47
Pereopod III, dactyl
Pereopod III, dactyl
48
Pereopod IV, epipod
49
Pereopod IV, epipod
50
Pereopod IV, strong movable spines on ischium
51
Pereopod IV, proximal strong movable spines on merus
52
Pereopod IV, distal movable spines on merus
53
Pereopod IV, dactyl
54
55
Pereopod IV, dactyl
Pereopod V, strong movable spines on ischium
56
Pereopod V, dactyl
57
Pereopod V, dactyl
Character state
State No
Figure
terminated in hook
1
3A
absent
0
present
1
absent or rudimentary
0
strap-like
1
not terminated in hook
0
terminated in hook
1
absent
0
present
1
absent
0
present
1
absent
0
present
1
single row of accessory spinules absent
0
single row of accessory spinules present
1
two or more rows of accessory spinules absent
0
two or more rows of accessory spinules present
1
absent or rudimentary
0
strap-like
1
not terminated in hook
0
terminated in hook
1
absent
0
present
1
absent
0
present
1
absent
0
present
1
single row of accessory spinules absent
0
single row of accessory spinules present
1
two or more rows of accessory spinules absent
0
two or more rows of accessory spinules present
1
absent
0
present
1
single row of accessory spinules absent
0
single row of accessory spinules present
1
two or more rows of accessory spinules absent
0
3A
3A
3B
3B
3B
3A
3A
3C
3C
3C
3D
ABDOMINAL APPENDAGES
58
59
60
61
62
Pleopod II, appendix interna
Pleopod III, appendix interna
Pleopod IV, appendix interna
Uropodal exopod, a single movable spine mesial to posterolateral tooth
Uropodal exopod, two movable spines mesial to posterolateral tooth
developed
0
-
much reduced
1
3E
developed
0
-
much reduced
1
3E
developed
0
-
much reduced
1
3E
absent
0
-
present
1
-
absent
0
-
present
1
-
doi:10.1371/journal.pone.0129975.t002
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Phylogeny and New Classification of Alvinocarididae
Fig 1. Morphological characters used for phylogenetic analysis. Anterior part of body. (A)-(E) after [13], (F) after [20], (G) after [70].
doi:10.1371/journal.pone.0129975.g001
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Phylogeny and New Classification of Alvinocarididae
Fig 2. Morphological characters used for phylogenetic analysis. Posterior part of body and maxilla. (A), (C)-(E) after [13], (B) after [70], (F) after [9].
doi:10.1371/journal.pone.0129975.g002
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Phylogeny and New Classification of Alvinocarididae
Fig 3. Morphological characters used for phylogenetic analysis. Thoracic and pleonic appendages. (A), (E) after [12], (B)-(D) after [13].
doi:10.1371/journal.pone.0129975.g003
The electronic edition of this article conforms to the requirements of the amended International Code of Zoological Nomenclature, and hence the new names contained herein are available under that Code from the electronic edition of this article. This published work and the
nomenclatural acts it contains have been registered in ZooBank, the online registration system
for the ICZN. The ZooBank LSIDs (Life Science Identifiers) can be resolved and the associated
information viewed through any standard web browser by appending the LSID to the prefix
"http://zoobank.org/". The LSID for this publication is: urn:lsid:zoobank.org:pub: XXXXXXX.
The electronic edition of this work was published in a journal with an ISSN, and has been
archived and is available from the following digital repositories: PubMed Central, LOCKSS.
Results
Morphological clades
Analysis 1 with Acanthephyra purpurea as the outgroup retrieved 36 minimal length trees of
length 145 (Fig 4A). The basal clade Alvinocaris (pink in Fig 4A) forms a sister clade to the rest
of the family and is followed by Keldyshicaris and two sister clades: Nautilocaris+ Mirocaris
(blue) and Opaepele+Alvinocaridinides+Manuscaris+Shinkaicaris+Rimicaris (light green).
Within the clade Alvinocaris, Alvinocaris niwa is the most basal, followed by the other species
of Alvinocaris. Within the light green clade, there are three clades: Opaepele, Alvinocaridinides
PLOS ONE | DOI:10.1371/journal.pone.0129975 July 10, 2015
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Phylogeny and New Classification of Alvinocarididae
Table 3. The data matrix of morphological characters of Alvinocarididae.
Species
States of characters
Acanthephyra purpurea
120101 2 111 2 22000100–0000 0–0000010110110110 1 111010 1 111011000000
Alpheus echiurophilus
100111 0 001 0 00000000–0000 0–0010011011011111 1 000000 1 000010000010
Alvinocaris alexander
110000 2 130 2 11121110–0100 0–1010000100100100 [01]111000 1 111001000010
Alvinocaris brevitelsonis
120000 2 220 2 12111110–0100 0–1010000100100100 1 111000 1 111001000010
Alvinocaris chelis
110000 2 230 2 01121110–0100 0–1010000100100100 0 111000 0 111001000010
Alvinocaris dissimilis
120000 2 230 2 11121110–0100 0–1010000100100100 1 111000 1 1110?1000010
Alvinocaris komaii
120000 2 120 2 12121110–0101 1 11000000100100100 1 110100 1 110110100010
Alvinocaris longirostris
120000 2 120 2 22121110–0100 0–1010000100100100 1 111000 1 111001000010
Alvinocaris lusca
110000 2 120 2 12111110–0101 0–1010000100100100 1 111000 1 111011000010
Alvinocaris markensis
110000 2 230 2 22121110–1101 1 01010000100100100 1 111000 1 111011000010
Alvinocaris methanophila
110000 2 230 2 22121110–0100 0–1010000100100100 1 111000 1 111001000010
Alvinocaris muricola
120000 2 130 2 22121110–0100 0–1010000100100100 1 111000 1 111011000010
Alvinocaris niwa
110000 2 110 [02]11001110–1100 [01]01010000100100100 1 111000 1 1110?1000010
Alvinocaris williamsi
110000 2 120 0 00121110–0101 0–1010000100100100 1 111000 1 1110?1000010
Alvinocaris solitaire
120000 2 330 2 11221110–1101 1 01010000100100100 1 111000 1 111011000010
Alvinocaris stactophila
110000 2 230 2 11221110–0101 0–1010000100100100 1 111000 1 1110?1000010
Alvinocaridinides formosa
100111 2 231 0 00000111–0010 0–0100000100100000 [01]000100 [01]000100100010
Rimicaris chacei
101111 0 001 0 00000001100010 0–0100000100100000 0 000100 0 000100100001
Rimicaris paulexa
101111 0 001 0 00000011100010 0–0100000100100000 0 000100 0 000100100001
Rimicaris vandoverae
101111 0 001 0 00000011100010 0–0100000100100000 0 000100 0 000100100001
Rimicaris parva
101111 0 001 0 00000101100010 0–0100000100100000 0 000100 0 000100100001
Rimicaris variabilis
101111 0 001 0 00000111100010 0–0100000100100000 0 000100 0 000100100001
Rimicaris susannae
101111 0 001 0 00000101100010 0–0100000100100000 0 000100 [01]000100100001
Rimicaris exoculata
0–1111 0 001 0 00000001110010 0–0101100000000000 0 000100 0 000100100001
Rimicaris kairei
0–1111 0 001 0 00000001110010 0–0101100000000000 0 000100 0 000100100001
Rimicaris hybisae
101111 0 001 0 00000001120010 0–0100100100100000 0 000100 0 000100100001
Rimicaris loihi
101111 [01]011 1 01000111001010 0–0100000100100000 0 000100 0 000100100010
Shinkaicaris leurokolos
110100 2 111 0 00110111000010 0–0100000100100000 0 000100 0 000100100010
Manuscaris acuminata
110100 2 221 0 00110111001100 0–0100000100100100 1 000100 0 000100100010
Mirocaris fortunata
101111 0 001 0 00000111000011 0–1000011111111111 1 001011 [01]001001011110
Mirocaris indica
101111 0 001 0 00000111000011 0–1000011111111111 1 001011 [01]001001011110
Nautilocaris saintlaurentae
110111 2 011 0 01000111001011 0–1000011111111111 1 001011 1 001001011110
Keldyshicaris vavilovi
101111 1 111 1 01000111001101 0–1010000100100100 1 001000 1 001011000010
Missing data indicated by question marks (?); inapplicable data by hyphens (-); polymorphism indicated by brackets [01]
doi:10.1371/journal.pone.0129975.t003
+Manuscaris+Shinkaicaris, and Rimicaris (green). After discard of all unsupported clades with
Bremer support <3, all considered coloured clades persist (Fig 5A).
Analysis 2 with Alpheus echiurophilus as the outgroup retrieved 437 minimal length trees of
length 146; the tree topology slightly differs from that in Analysis 1, but the principal clades are
the same (Fig 4B, same colours). The clade Nautilocaris+ Mirocaris is basal and followed by
three clades: (1) Opaepele+Alvinocaridinides+Manuscaris+Shinkaicaris+Rimicaris, (2) Keldyshicaris, and (3) Alvinocaris. After discard of all unsupported clades with Bremer support <3,
all considered coloured clades persist (Fig 5B).
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Phylogeny and New Classification of Alvinocarididae
Table 4. GenBank accession numbers for COI and 16S sequences of species used for phylogenetic analyses.
Species
NCBI GenBank Accession number, Locality
Reference
Alvinocaris dissimilis
AB779491–AB779494
[72],[73]
Alvinocaris komaii
EU031816 Eastern Lau Spreading Center, southwest Pacific
[18]
Alvinocaris longirostris
AB222050, AB222051 Hatoma Knoll, Okinawa Trough
[73], [22]
NC020313, JQ035659 Hatoma Knoll, Okinawa Trough
[25]
AB821296 Hatoma Knoll, Okinawa Trough
[72]
GQ131897
[74]
Alvinocaris lusca
AF125404-AF125407 Galapagos hydrothermal vent field; 9°50’N hydrothermal vent field
[17]
Alvinocaris markensis
KC840879-KC840886, KC840893 Logatchev, Mid-Atlantic Ridge (MAR)
[44]
AF125408, AF125409 Snake Pit, MAR
[17]
KC840887-KC840892, KC840894-KC840927 Gulf of Mexico, GC852 site; Regab, West
Africa
[45]
Alvinocaris muricola (including Alvinocaris aff.
muricola)
EU031814, EU031815 Gulf of Mexico
[75]
EU868627, EU868628
[76]
Alvinocaris solitaire
LC007114 Solitaire hydrothermal vent field, Central Indian Ridge
[69]
Alvinocaris stactophila
AF125410, AF125411 Louisiana Slope, Gulf of Mexico
[17]
Alvinocaris chelys
NC 018778, JX184903 vent field off Gueishandao (or Kueishan Island), Yilan County,
northeastern Taiwan
[77]
Alvinocaris methanophila
AY163260 the Blake Ridge Diapir, Caribbean
[45],[69]
Chorocaris chacei
AF125395-AF125397, AF125414, AF125415 Snake Pit, TAG, MAR
[17]
KC840928-KC840940 Logatchev, Lucky Strike, MAR
[45]
AM076957, Lucky Strike, MAR
[78]
AM087920- AM087922
[79]
Chorocaris parva
AB772278, AB772282 PACMANUS, Manus Basin, South West Pacific
[21]
Chorocaris vandoverae
AF125417, AF125418 Alice Springs, Mariana Back-Arc Basin
[17]
Chorocaris variabilis
AB772279-AB772281, AB7722 PACMANUS, Manus Basin, South West Pacific
[21]
Mirocaris fortunate (including Mirocaris
keldyshi)
AF125424-AF125429, AF125430-AF125433 Lucky Strike, Broken Spur, Menez Gwen,
TAG, Logatchev, MAR
[17]
FJ769225, FJ769226 Menez Gwen, MAR
[23]
AM076959, Lucky Strike, MAR
[78]
AM087916- AM087919
[79]
Nautilocaris saintlaurentae
NC021971, KF226726 vent the Tofua Arc (Tonga)
[80]
Opaepele loihi
DQ328819-DQ328838 Marianca Arc
[81]
Rimicaris exoculata
Rimicaris kairei
Rimicaris hybisae
Acanthephyra purpurea
AF125436, AF125437 Loihi Seamount
[17]
NC020311, JQ035657 Nikko Seamount, Philippine Sea Plate
[25]
AF125398-AF125403, AF125419, AF125420, AF125440 TAG, Lucky Strike, Broken Spur,
Rainbow
[17]
AF044057 MAR
[82]
FN392996-FN393005 Rainbow, TAG, Logatchev, South MAR
[24]
HM125910-HM125956 Rainbow, TAG, Logatchev, Ashadze, South MAR
[83]
AF035459, TAG, South MAR
[82]
AM087923-AM087925
[79]
AM076958, Lucky Strike, MAR
[78]
AB813087-AB813108 Dodo, Solitaire, Edmond and Kairei fields
[84]
NC020310, JQ035656 Kairei Field (Rodriguez Triple Junction)
[25]
JN850606, JN850607 Beebe and Von Damm vent fields (Caribbean)
[3]
KJ566968-KJ5678003 Beebe and Von Damm vent fields (Caribbean)
[85]
GU183787, GU183788
[86]
KP075887, KP075899
[87]
doi:10.1371/journal.pone.0129975.t004
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Phylogeny and New Classification of Alvinocarididae
Fig 4. Strict consensus trees of Alvinocarididae and synapomorphies (numbers in circles). A, analysis 1 with Acanthephyra purpurea as the outgroup.
B, analysis 2 with Alpheus echiurophilus as the outgroup. Supported clades are marked by different colors: Mirocaridinae (blue), Alvinocaridinae (pink),
Rimicaridinae (light green), Rimicaris (green).
doi:10.1371/journal.pone.0129975.g004
Molecular clades
The molecular phylogenetic Analysis 1 with use of CO1 gene resulted in a tree (Fig 6A), which
resembles the morphological tree except the branching of Alvinocaris (Fig 5B). In the morpho
analysis Alvinocaris forms a single clade (not internally resolved), but in the genetic analysis
three (COI) or two (16S) clades occur.
The clade Mirocaris+Nautilocaris (Fig 6A, coloured in blue) is supported both by ML bootstrap (98) and Bayesian posterior probability (100). This clade comprises two genera: Mirocaris
(M. fortunata) and Nautilocaris (N. saintlaurentae). Genetic difference between the genera
Fig 5. Statistically robust clades of Alvinocarididae with bootstrap support (numbers above the clade) and Bremer support (numbers below the
clade in circles). A, analysis 1 with Acanthephyra purpurea as outgroup. B, analysis 2 with Alpheus echiurophilus as outgroup. Supported clades are
marked by different colors: Mirocaridinae (blue), Alvinocaridinae (pink), Rimicaridinae (light green), Rimicaris (green).
doi:10.1371/journal.pone.0129975.g005
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Phylogeny and New Classification of Alvinocarididae
Fig 6. Bayesian phylogenetic trees of the family Alvinocarididae based on COI gene (A) and 16 S gene (B) sequences. The horizontal scale bar marks
the number of expected substitutions per site. Statistical support indicated as Bayesian posterior probabilities (left values) and bootstrap analysis with 1,000
replicates (right values) and. Supported clades are marked by different colors: Mirocaridinae (blue), Alvinocaridinae (pink), Rimicaridinae (light green),
Rimicaris (green).
doi:10.1371/journal.pone.0129975.g006
reaches 5.1%. This clade is identical to the clade Nautilocaris+ Mirocaris revealed by both morphological analyses. The basal clade is followed by four clades.
The clade Alvinocaris komaii (Fig 6A, pink) comprises only one species of Alvinocaris.
Position of this on the tree topology is unresolved and thus requires further research.
The clade Alvinocaris solitaire+Alvinocaris markensis+Alvinocaris muricola+ Alvinocaris
lusca+Alvinocaris longirostris (Fig 6A, pink) is supported by ML bootstrap (81) and Bayesian
posterior probability (100). This clade comprises a significant part of the genus Alvinocaris (Fig
6A, coloured in pink). Alvinocaris solitaire is basal and followed by A. markensis, A. muricola
and Alvinocaris lusca+Alvinocaris longirostris. Genetic differences between three terminal subclades range from 5 to 6.7%.
The clade Alvinocaris dissimilis +Alvinocaris stactophila +Alvinocaris chelis (Fig 6A,
pink) is supported by ML bootstrap (99) and Bayesian posterior probability (100). This clade
comprises the rest of Alvinocaris used in Analysis 1 (Fig 6A, coloured in pink). The former two
species are genetically identical, while the genetic distance (p-distance) between them and A.
chelys reaches 0.5%.
The clade Rimicaris variabilis + Rimicaris parva + Rimicaris vandoverae + Rimicaris
exoculata + Rimicaris chacei + Rimicaris kairei + Alvinocaris methanophila + Rimicaris
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Phylogeny and New Classification of Alvinocarididae
hybisae+ Opaepele loihi (Fig 6A, light green) is supported by Bayesian posterior probability
(100). This clade comprises a part of the genus Rimicaris (Fig 6A, coloured in green) and two
other genera: Alvinocaris (a single sequence) and Opaepele. Specimens of C. chacei are divided
into two distant groups with genetic differences 7.9%.
The molecular phylogenetic Analysis 2 with use of 16S gene resulted in a tree with similar
clades (Fig 6B). The monophyly of the clades Mirocaris+Nautilocaris and Rimicaris exoculata
+ Rimicaris chacei + Rimicaris kairei + Rimicaris hybisae+ was supported (Bayesian posterior probability (100 and 76, respectively). Alvinocaris created two clades Alvinocaris longirostris+Alvinocaris muricola and Alvinocaris chelis (Bayesian posterior probability 85 and 99,
respectively), which agree with two clades of Analysis 1
Discussion
Both morphological analyses revealed three major robust monophyletic clades, herein assign to
them subfamiliar status, as Mirocaridinae, Rimicaridinae subfam. nov. and Alvinocaridinae
subfam. nov.
The clades
The clade/subfamily Mirocaridinae (Fig 5A and 5B, blue) comprises three species and two
genera: Nautilocaris and Mirocaris. This clade is supported by the following synapomorphies
common for both morpho analyses (starting from the character number):
(48–49) presence of strap-like epipods terminating in a hook, on the fourth pereopod,
(58–60) much reduced appendix interna in second to fourth pleopods
The clade is well supported by molecular data (Fig 6A).
The clade/subfamily Rimicaridinae (Fig 5A and 5B, light green) comprises thirteen species
and five genera: Opaepele, Alvinocaridinides, Manuscaris, Shinkaicaris, and Rimicaris. This
clade is also supported by the following synapomorphies common for both morpho analyses:
(28) entirely fused eyestalks without mould seam,
(47, 54, 57) presence of two or more rows of accessory spinules on the dactyls of the third to
fifth pereopods.
The clade is supported by molecular data (Fig 6A). The position of A. methanophila within
Rimicaridinae is worthy of comment. This result is based on a single specimen of A. methanophila, which was collected at the Blake Ridge Diapir site, sequenced and deposited in GenBank
(Accession No AY163260) under the name «Alvinocaris sp. TMS-2002». The shrimp was originally named «Blake Ridge shrimp» [43]. Later this specimen along with 33 other adult specimens was described as a new species A. methanophila [44]. Texeira et al [45] used the same
sequence and included this in their clade “ESU 2” which comprised specimens from three genera. We feel that the resulting position of A. methanophila in a common clade with R. chacei
and R. hybisae is a result of incorrect identification or processing the material.
Molecular analyses indicate close relation between Opaepele (O. loihi) and Rimicaris, however morphologically they are quite distinct and for now we keep both genera as valid. Both
morphological analyses supported validity of remaining genera of the clade Rimicaridinae:
Alvinocaridinides, Shinkaicaris, and Manuscaris.
The clade Rimicaris is nested within the clade Rimicaridinae and comprises all species of
the currently recognised genera Chorocaris and Rimicaris (Fig 5A and 5B, green). This clade
received very high support during morphological and molecular analyses and is also supported
by the synapomorphies common for both morpho analyses:
(19) dorsal organ under carapace extended beyond the postorbital region,
(61–62) presence of two movable spines mesial to posterolateral tooth on uropodal exopod.
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Phylogeny and New Classification of Alvinocarididae
As this is a robust monophyletic clade (except terminal R. exoculata+R. kairei), we herein
synonymize Chorocaris with Rimicaris, with Rimicaris being the older name. We note that the
type species of Chorocaris, Chorocaris chacei, was initially described as Rimicaris [9]. Our analyses also show that the former Opaepele susannae was correctly removed from the genus Opaepele (and transferred to Chorocaris) [21].
Recent molecular studies by Texeira et al [45] based on studies from the Tropical Atlantic
have previously showed a common clade for Rimicaris and Chorocaris. “These showed very
low genetic divergence at levels similar to divergence between individuals of the same species.
We posit that these taxa belong to the same genus, possibly even the same species” [45].
The clade is well supported by our molecular data (Fig 6A). A chequerwise arrangement of
the species belonging to the former Rimicaris and Chorocaris within Rimicaridinae gives additional evidence for their genetic similarity and thus synonimising both genera.
One of the unexpected results of our molecular analyses is the position of specimens of R.
chacei in two different and well supported clades (distance 7.9%). Those specimens which are
closer to R. exoculata, were identified and sequenced by T.M. Shank (NN AF125395-397,
AF125414-415 from Snake Pit and TAG [17]. The specimens closer to Opaepele loihi (NN
KC840928-KC840940 from Logatchev and Lucky Strike) are from Teixeira et al. [45]. This
division of R. chacei into two groups may be caused by various factors:
• mitochondrial introgression in which mitochondrial DNA of R. exoculata may have been
incorporated in the populations of C. chacei at Snake Pit and TAG. Similar effects were
found in other marine Malacostraca [46], [47] and also in vent Bivalvia [48], [49],
• existence of cryptic species of C. chacei recognized as a single morphological species.
The clade/subfamily Alvinocaridinae (Fig 5A and 5B, pink) comprises fourteen species of
the genus Alvinocaris. This clade is also supported by the following synapomorphies common
for both morpho analyses:
(3, 9) laterally compressed and ventrally carinate rostrum,
(15) presence of postrostral dorsal carina extending beyond the midlength of carapace.
Molecular analyses indicate presence of three supported clades of Alvinocaris (Fig 6A). Here
we consider the genus and the subfamily as monophyletic on the basis of the two morphological analyses and leave the possibility of a polyphyletic origin of the clade to be resolved by more
data in the future.
The clade Keldyshicaris comprises a single species, Keldyshicaris vavilovi. Both morphological analyses did not support monophyly of the former genus Opaepele and we suggest division
of this genus into two monotypic genera, Opaepele with O. loihi (subfamily Rimicaridinae) and
Keldyshicaris gen.n. with K. vavilovi n. comb. The status of this genus may be further clarified
after receiving molecular data.
Morphological trends in Alvinocarididae
Mirocaridinae and Rimicaridinae share a degenerate rostrum, reduced external spines and the
presence of the dorsal organ. This type of rostrum may be advantageous in the vicinity of shimmering waters and vent fluids where Mirocaridinae and Rimicaridinae occur. Predators are
rare in these extreme biotopes where sulphides, heavy metals, and methane are actively leaching from surrounding rocks [50]. A shorter unarmed rostrum along with reduced spines
reduces impact of strong turbulent water fluxes, which are common in the microbiotopes
where the shrimps thrive [51].
The dorsal organ has been described inside the carapaces of all recent genera of Mirocaridinae and Rimicaridinae [2], [20], [52–53]. These spot-like organs are believed to be homologous
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Phylogeny and New Classification of Alvinocarididae
to the ‘dorsal eye’ found in R. exoculata [2], [54–55], but are smaller and do not comprise four
lobes. The dorsal organ, also called ‘dorsal eye’, is an extremely efficient photoreceptor, used
for detecting light emitted from the vents [56–58].
Mirocaridinae further differ from other Alvinocarididae in having strap-like epipods terminating in a hook and in much reduced appendix interna in second to fourth pleopods. The
strap-like pereopodal epipods are common for many caridean families and these characters
may be retained from the ancestor. Modification in pleopodal characters may be related to specific traits in movement or copulation, which may be adaptive in the shimmering waters where
Mirocaridinae thrive.
Rimicaridinae possess entirely fused eyestalks and presence of two or more rows of accessory spinules on the dactyls of the third to fifth pereopods—adaptations favouring anchoring
close to the strong currents hydrothermal fluids. Within the clade Rimicaridinae, the genus
Rimicaris shows further modification of external structures on the rostrum and frontal part of
carapace, further development of the dorsal organ, and elaboration of uropodal exopod. The
polarization of the characters 19 along with inflation of carapace and extension of scaphognathite shows deeper association of Rimicaris with vent fluids than any of other genera of the
subfamily [51],[59], [60]. Presence of two strong movable spines instead of one (the polarization of characters 61–62) may indicate importance of the tail fan, which is used in the escape
behaviour of shrimps ([61]. The presence of additional spines may make this behaviour more
efficient when high-temperature turbulent water fluxes can suddenly erupt from the rocks and
damage shrimps [51].
Alvinocaridinae are characterized by a well-developed instead of reduced rostrum and postrostral carina, by a frontal ocular tubercle, and by the spination of the fourth-fifth pereopods.
These traits are plausibly accounted for by their habitat at the periphery of hydrothermal vent
fields [60]. In these habitats, predatory fish do occur and frontal armature may partly protect
the shrimps from attacks. The frontal ocular tubercle indicates that the eyes may have additional chemo- or mechanosensory function facilitating orientation at the vent field by means of
the frontal tubercle. If so, the tubercle may represent a sensory mechanism alternative to the
photoreceptory dorsal organ of other Alvinocarididae. Distal movable spines on the merus of
third and fourth pereopods (characters 45 and 51) are present in Alvinocaridinae, potentially
enabling more efficient prey catching and sorting and processing the organic particles which
the species live on.
Classification of Alvinocarididae
Subfamily Mirocaridinae, subfam. nov
urn:lsid:zoobank.org:act:1383E6D1-E57C-4EA0-8CD2-F0CDE9767A97
Diagnosis. Carapace dorsally smooth, without postrostral carina; dorsal organ conspicuous; telson bearing 12–19 strong spines. Eyes partly fused, anterior margin of cornea without
developed tubercle; epipods of first to fourth pereopods strap-like, terminating in a hook; meri
of third and fourth pereopods without movable spines; appendix interna in pleopods II-V
much reduced.
Type genus. Mirocaris Vereshchaka, 1997 [12], by original designation.
Genera included. Mirocaris Vereshchaka, 1997 [12], Nautilocaris Komai, Segonzac,
2004 [14].
Remarks. The type species of the genus Mirocaris is M. keldyshi, a junior subjective synonym of Chorocaris fortunata. Although the generic status of Mirocaris has largely been supported, the family Mirocarididae Vereshchaka, 1997 has not been recognized, but is herein
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Phylogeny and New Classification of Alvinocarididae
resurrected at subfamily level [19]. Molecular data have been previously indicating high status
of Mirocaris [17].
Genus Mirocaris Vereshchaka, 1997 [12]
Diagnosis. Rostrum dorsoventrally compressed, not reaching end of first antennular segment, apically obtuse, dorsally and ventrally not carinate, smooth; carapace with antennal
angle acute, pterygostomial tooth present; dorsal organ restricted to postorbital region; third
abdominal segment not serrated; telson with sinuous row of movable dorsolateral spines. Anterior margin of cornea without tubercle; scaphognathite not much expanded, without heavily
plumose bacteriophore setae; third maxilliped with distal movable spine on antepenultimate
segment; first pereopod with grooming apparatus; second pereopod with a distal movable
spine on ischium; ischia of third to fifth pereopods with or without movable spines; dactyli of
third to fifth pereopods with a single row of accessory spinules; uropodal exopod with a single
movable spine mesial to posterolateral tooth.
Type species. Mirocaris keldyshi Vereshchaka, 1997 (junior subjective synonym of Chorocaris fortunata Martin & Christiansen, 1995) [62].
Species included. Mirocaris fortunata (Martin, Christiansen, 1995) [62], Mirocaris indica
Komai, Martin, Zala, Tsuchida, Hashimoto, 2006 [63].
Remarks. The genus includes 2 species, one from the Atlantic, and the other from the
Indian Ocean. Both species are so similar in morphology that supporting molecular data are
necessary to prove the validity of M. indica. We keep here, however, a conservative approach
and recognize both species.
Genus Nautilocaris Komai, Segonzac, 2004[14]
Diagnosis. Rostrum dorsoventrally compressed, overreaching end of first antennular segment, apically acute, dorsally not carinate, toothed, ventrally smooth; carapace with antennal
angle acute, pterygostomial tooth present; dorsal organ restricted to postorbital region; third
abdominal segment serrated; telson with sinuous row of movable dorsolateral spines. Anterior
margin of cornea without tubercle; scaphognathite not much expanded, without heavily plumose bacteriophore setae; third maxilliped with a distal movable spine on antepenultimate segment; first pereopod with grooming apparatus; second pereopod with distal movable spine on
ischium; ischia of third to fifth pereopods with or without movable spines; dactyli of third to
fifth pereopods with a single row of accessory spinules; uropodal exopod with a single movable
spine mesial to posterolateral tooth.
Type species. Nautilocaris saintlaurentae Komai & Segonzac, 2004 [14], by monotypy.
Species included. Nautilocaris saintlaurentae Komai & Segonzac, 2004 [14].
Remarks. Nautilocaris differs from the closely related genus Mirocaris in having a longer
and denticulate rostrum and in the serrated pleura of the third abdominal somite.
Subfamily Rimicaridinae, subfam.nov
urn:lsid:zoobank.org:act:1E84ACE4-B031-43BA-8B91-CD0AFB4DBF77
Diagnosis. Carapace dorsally smooth, without postrostral carina; dorsal organ conspicuous; telson bearing 12–19 strong spines. Eyes fused entirely, anterior margin of cornea without
developed tubercle; epipods of first to fourth pereopods rudimentary; meri of third and fourth
pereopods without movable spines; appendix interna in pleopods II-V developed.
Type genus. Rimicaris Williams & Rona, 1986 [9], by present designation.
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Phylogeny and New Classification of Alvinocarididae
Genera included. Alvinocaridinides Komai & Chan, 2010 [2], Manuscaris Komai & Tsuchida, 2015 [21], Opaepele Williams & Dobbs, 1995 [11], Rimicaris Williams & Rona, 1986 [9],
and Shinkaicaris Komai & Segonzac, 2005 [13].
Genus Alvinocaridinides Komai & Chan, 2010 [2]
Diagnosis. Rostrum dorsoventrally compressed, not reaching end of first antennular segment, apically blunt, dorsally toothed, ventrally smooth; carapace dorsally smooth, antennal
angle acute, pterygostomial tooth present; dorsal organ restricted to postorbital region; third
abdominal segment not serrated; telson with sinuous row of movable dorsolateral spines, posterior margin bearing 4 strong spines. Anterior margin of cornea without tubercle; scaphognathite not much expanded, without heavily plumose bacteriophore setae; third maxilliped
with 1 distal movable spine on antepenultimate segment; epipods of first to fourth pereopods
rudimentary; first pereopod with grooming apparatus; second pereopod without distal movable spine on ischium; ischia of third to fifth pereopods with or without movable spines; dactyli
of third to fifth pereopods with two or more rows of accessory spinules; appendix interna in
pleopods II-V developed; uropodal exopod with a single movable spine mesial to posterolateral
tooth.
Type species. Alvinocaridinides formosa Komai & Chan, 2010 [2], by original designation
and monotypy.
Species included. Alvinocaridinides formosa Komai & Chan, 2010.
Remarks. Komai and Chan [2] established this genus for a single new species, A. formosa.
Our analyses support the validity of this genus.
Manuscaris Komai & Tsuchida, 2015 [21]
Diagnosis. Rostrum laterally compressed, reaching end of first antennular segment, apically acute, dorsally carinate, toothed, ventrally smooth; carapace dorsally toothed, pterygostomial tooth present; third abdominal segment serrated; telson with linear row of movable
dorsolateral spines, posterior margin bearing 2–4 strong spines. Anterior margin of cornea
without tubercle; scaphognathite not much expanded, without heavily plumose bacteriophore
setae; third maxilliped with a distal movable spine on antepenultimate segment; epipods of first
to fourth pereopods rudimentary; first pereopod with grooming apparatus; second pereopod
with distal movable spine on ischium; ischia of third to fifth pereopods with or without movable spines; dactyli of third to fifth pereopods with two or more rows of accessory spinules;
appendix interna in pleopods II-V developed; uropodal exopod with a single movable spine
mesial to posterolateral tooth.
Type species. Manuscaris acuminata Komai and Tsuchida, 2015, by monotypy.
Species included. Manuscaris acuminata Komai and Tsuchida, 2015 [21].
Remarks. This genus was recently erected [21] and our analyses support its validity.
Opaepele Williams and Dobbs, 1995 [11]
Diagnosis. Rostrum dorsoventrally compressed, not reaching end of first antennular segment, apically blunt, dorsally and ventrally not carinate, notched or smooth; carapace dorsally
smooth, antennal angle acute, pterygostomial tooth present; dorsal organ restricted to postorbital region; third abdominal segment serrated; telson with sinuous row of movable dorsolateral spines, posterior margin bearing 2–4 strong spines. Anterior margin of cornea without
tubercle; scaphognathite not much expanded, without heavily plumose bacteriophore setae;
third maxilliped with a distal movable spine on antepenultimate segment; epipods of first to
fourth pereopods rudimentary; first pereopod with grooming apparatus; second pereopod
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Phylogeny and New Classification of Alvinocarididae
without distal movable spine on ischium; ischia of third to fifth pereopods without movable
spines; dactyli of third to fifth pereopods with two or more rows of accessory spinules; appendix interna in pleopods II-V developed; uropodal exopod with a single movable spine mesial to
posterolateral tooth.
Type species. Opaepele loihi Williams, Dobbs, by monotypy.
Species included. Opaepele loihi Williams, Dobbs, 1995 [11]
Remarks. Opaepele is herein restricted to the type species only, O. loihi. Opaepele susannae
has been recently transferred to Chorocaris [21] and our analyses confirm this decision. Opaepele vavilovi is transferred to a new genus, Keldyshicaris (see below).
Genus Rimicaris Williams & Rona, 1986 [9]
Diagnosis. Rostrum if present dorsoventrally compressed, not reaching end of first antennular segment, apically obtuse, dorsally and ventrally not carinate, smooth; carapace dorsally
smooth, antennal angle blunt or acute, pterygostomial tooth present or absent; dorsal organ
extending beyond the postorbital region; third abdominal segment smooth or serrated; telson
with sinuous row of movable dorsolateral spines, posterior margin bearing 2–4 strong spines.
Eyes fused entirely, anterior margin of cornea without developed tubercle; scaphognathite
expanded, with or without heavily plumose bacteriophore setae; third maxilliped with 0–2 distal movable spines on antepenultimate segment; epipods of first to fourth pereopods rudimentary; first pereopod with or without grooming apparatus; second pereopod without distal
movable spine on ischium; ischia of third to fifth pereopods with or without movable spines;
dactyli of third to fifth pereopods with two or more rows of accessory spinules; appendix
interna in pleopods II-V developed; uropodal exopod with two movable spines mesial to posterolateral tooth.
Type species. Rimicaris exoculata Williams & Rona, 1986 [9], by original designation.
Species included. Rimicaris chacei (Williams, Rona, 1986) [9], Rimicaris exoculata Williams, Rona, 1986, Rimicaris hybisae Nye, Copley, Plouviez, 2012 [3], Rimicaris kairei Watabe,
Hashimoto, 2002 [64], Rimicaris parva (Komai, Tsuchida) [21], Rimicaris paulexa (Martin,
Shank, 2005) [65], Rimicaris susannae (Komai, Giere, Segonzac, 2007) [66], Rimicaris vandoverae (Martin, Hessler, 1990) [10], and Rimicaris variabilis (Komai, Tsuchida) [21].
Remarks. The genus includes all species of the former genera Chorocaris sensu Komai and
Tsuchida [21] and Rimicaris.
Rimicaris exoculata from the Atlantic and R. kairei from the Indian Ocean are very similar
in morphology and are not statistically distinct on the molecular tree (Fig 6A). We keep a conservative approach and recognize both species, while pointing out a need of additional research
to confirm their validity.
Rimicaris vandoverae and R. paulexa are so similar morphologically that it is impossible to
articulate sharp distinctions between them. The species are geographically isolated and the
minor morphological distinctions may refer to an inter-population difference rather than to an
inter-specific variability. Molecular data (now missing for R. paulexa) will help in understanding the status of these species.
As stated above, R. chacei may include at least two cryptic species. New sequences are desirable to clarify this situation.
Genus Shinkaicaris Komai & Segonzac, 2005 [13]
Diagnosis. Rostrum laterally compressed, overreaching end of first antennular segment,
apically acute, dorsally carinate, toothed, ventrally smooth; carapace dorsally toothed, antennal
angle acute, pterygostomial tooth present; dorsal organ restricted to postorbital region; third
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Phylogeny and New Classification of Alvinocarididae
abdominal segment not serrated; telson with sinuous row of movable dorsolateral spines, posterior margin bearing 2–4 strong spines. Anterior margin of cornea without tubercle; scaphognathite not much expanded, without heavily plumose bacteriophore setae; third maxilliped
with a distal movable spine on antepenultimate segment; epipods of first to fourth pereopods
rudimentary; first pereopod with grooming apparatus; second pereopod without distal movable spine on ischium; ischia of third to fifth pereopods without movable spines; dactyli of
third to fifth pereopods with two or more rows of accessory spinules; appendix interna in pleopods II-V developed; uropodal exopod with a single movable spine mesial to posterolateral
tooth.
Type species. Alvinocaris leurokolos Kikuchi & Hashimoto, 2000 [67], by monotypy.
Genera included. Shinkaicaris leurokolos Kikuchi, Hashimoto, 2000.
Remarks. Our analyses support the validity of the genus.
Subfamily Alvinocaridinae, subfam. nov
urn:lsid:zoobank.org:act:87404656-6EDE-490E-A8E5-0F2464B370A7
Diagnosis. Rostrum laterally compressed, overreaching end of first antennular segment,
apically acute, dorsally carinate and toothed, ventrally carinate, toothed or smooth; carapace
dorsally toothed or smooth, with postrostral carina extending beyond midlength of carapace,
antennal angle acute, pterygostomial tooth present; dorsal organ inconspicuous; third abdominal segment smooth or serrated; telson with linear row of movable dorsolateral spines, posterior margin convex or concave, bearing 4–18 strong spines. Eye partly fused, anterior margin
of cornea with developed tubercle; scaphognathite not much expanded, without heavily plumose bacteriophore setae; third maxilliped with 1–2 distal movable spines on antepenultimate
segment; epipods of first to fourth pereopods rudimentary; first pereopod with grooming apparatus; second pereopod with distal movable spines on ischium; meri of third and fourth pereopods with movable spines; ischia of third to fifth pereopods with movable spines; dactyli of
third to fifth pereopods with a single row of accessory spinules; appendix interna in pleopods
II-V developed; uropodal exopod with a single movable spine mesial to posterolateral tooth.
Type genus. Alvinocaris Williams, Chace, 1982 [8], by present designation
Genera included. Alvinocaris Williams, Chace, 1982 [8].
Genus Alvinocaris Williams, Chace, 1982 [8]
Diagnosis. As in subfamily.
Type species. Alvinocaris lusca Williams, Chace, 1982 [8], by monotypy.
Species included. Alvinocaris alexander Ahyong, 2009 [38], A. brevitelsonis Kikuchi,
Hashimoto, 2000 [67], A. chelys Komai, Chan, 2010 [2], A. dissimilis Komai, Segonzac, 2005
[13], A. komaii Zelnio, Hourdez, 2009 [18], A. longirostris Kikuchi, Ohta, 1995 [7], A. lusca
Williams, Chace, 1982 [8], A. markensis Williams, 1988 [68], A. methanophila Komai, Shank,
Van Dover, 2005 [69], A. muricola Williams, 1988 [68], A. niwa Webber, 2004 [70], A. solitaire
Yahagi, Watanabe, Kojima, Beedessee, Komai, 2014 [71], A. stactophila Williams, 1988 [68], A.
williamsi Shank, Martin, 2003 [70].
Remarks. Molecular data indicate a presence of three species groups at least: (1) A. komaii,
(2) A. solitaire, A. markensis, A. muricola, A. lusca, A. longirostris, and (3) A. dissimilis, A.
stactophila, Alvinocaris chelis. Morphological analyses do not provide robust clades within
Alvinocaris.
Keldyshicaris gen.nov
urn:lsid:zoobank.org:act:4D7D81BC-2C9A-45A0-93EC-D276E33FA174
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Phylogeny and New Classification of Alvinocarididae
Diagnosis. Rostrum dorsoventrally compressed, not reaching end of first antennular segment, apically blunt, dorsally not carinate, dorsally and ventrally notched; carapace dorsally
smooth, antennal angle acute, pterygostomial tooth present; dorsal organ restricted to postorbital region; third abdominal segment serrated; telson with linear row of movable dorsolateral
spines, posterior margin bearing 2–4 strong spines. Anterior margin of cornea with rudimentary tubercle; scaphognathite not much expanded, without heavily plumose bacteriophore
setae; third maxilliped with a distal movable spine on antepenultimate segment; epipods of first
to fourth pereopods rudimentary; first pereopod with grooming apparatus; second pereopod
with distal movable spine on ischium; dactyli of third to fifth pereopods with two or more rows
of accessory spinules; appendix interna in pleopods II-V developed; uropodal exopod with a
single movable spine mesial to posterolateral tooth.
Type species. Opaepele vavilovi Lunina and Vereshchaka, 2010.
Species included. Keldyshicaris vavilovi (Lunina and Vereshchaka, 2010) [20].
Etymology. Named after the Russian R/V "Akademik Mstislav Keldysh" which significantly contributed to the studies of vent fauna.
Remarks. The proper position and status of Keldyshicaris within Alvinocarididae remains
uncertain.
Key to subfamilies, genera, and species of Alvinocarididae (Table 5)
Table 5.
1. Carapace with conspicuous postrostral carina extending beyond the midlength; no
conspicuous dorsal organ. Meri of pereopods III-IV with strong movable spines
- Carapace without conspicuous postrostral carina extending beyond the midlength;
dorsal organ conspicuous; Meri of pereopods III-IV without strong movable spines
2. Dorsal teeth present only on rostrum
2 (subfamily Alvinocaridinae, Alvinocaris)
13
Alvinocaris niwa
- Dorsal teeth both on rostrum and on carapace
3
3. Telson with 2–4 strong spines on posterior margin
4
- Telson with 6 or more strong spines on posterior margin
4. No strong movable spines on ischium of fourth pereopods
- Ischium of fourth pereopod with strong movable spines
5. Rostrum not reaching end of second antennular segment
- Rostrum overreaching end of second antennular segment
6. Ventral margin of rostrum with 1–2 small subdistal teeth
- Ventral margin of rostrum with 3 or more teeth
7. Posterior margin of telson with >2 pairs of spines
- Posterior margin of telson with 2 pairs of spines at lateral corners and 12–14 plumose
setae
8. Posterior margin of telson concave
- Posterior margin of telson convex
8
Alvinocaris chelys
5
A. methanophyla in the Atlantic and A. alexander in the Pacific
Ocean
6
Alvinocaris dissimilis
7
Alvinocaris brevitelsonis
A. muricola in the Atlantic and A. longirostris in the Pacific
Ocean.
9
11
9. Pleura of third abdominal somite smooth; posterior margin of telson bilobed; dactyli
of third to fifth pereopods with two or more rows of accessory spinules
Alvinocaris komaii
- Pleura of third abdominal somite serated; posterior margin of telson slightly concave;
dactyli of third to fifth pereopods with a single row of accessory spinules
10
10. Rostrum not reaching end of second antennular segment, with 3 or more ventral
teeth
- Rostrum overreaching end of second antennular segment, with 1–2 ventral teeth
11. Rostrum with ventral teeth
Alvinocaris markensis
Alvinocaris solitaire
12
(Continued)
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Phylogeny and New Classification of Alvinocarididae
Table 5. (Continued)
- No ventral teeth on rostrum
12. Rostrum with a single ventral tooth. Carapace with 6–10 dorsal teeth
- Rostrum with 2–6 ventral teeth. Carapace with 1–5 dorsal teeth
Alvinocaris williamsi
Alvinocaris stactophyla
Alvinocaris lusca
13. Epipods of first to fourth pereopods developed, strap-like, ending in hook;
appendices internae of second to fourth pleopods rudimentary
14 (subfamily Mirocaridinae)
- Epipods of first to fourth pereopods rudimentary, not strap-like, not ending in hook;
appendices internae of second to fourth pleopods normally developed
15 (subfamily Rimicaridinae)
14. Rostrum not reaching end of first antennular segment, dorsally smooth. Pleura of
third abdominal somite smooth
- Rostrum overreaching end of first antennular segment, with dorsal teeth. Pleura of
third abdominal somite serrate
15. Rostrum overreaching end of 1st antennular segment, carapace with dorsal teeth
- Rostrum not reaching end of 1st antennular segment, carapace without dorsal teeth
16. Rostrum and carapace bearing a total of 11 or more dorsal teeth; pleura of third
abdominal somite serrate; row of dorsolateral spines on telson linear; ischia of third and
fourth pereopods with movable spines
Rostrum and carapace bearing a total of 10 or less dorsal teeth; pleura of third
abdominal somite not serrate; row of dorsolateral spines on telson sinuous; ischia of
third and fourth pereopods without movable spines
17. Rostrum with dorsal teeth or notches; dorsal organ restricted to postorbital region;
uropodal exopod with a single movable spine mesial to posterolateral tooth.
- Rostrum without dorsal teeth or notches; dorsal organ extending beyond postorbital
region; uropodal exopod with two movable spines mesial to posterolateral tooth
Mirocaris (M. fortunata in the Atlantic, M. indica in the Indian
Ocean)
Nautilocaris, the only species N. saintlaurentae
16
17
genus Manuscaris, the only species Manuscaris acuminata
Shinkaicaris, the only species Shinkaicaris leurokolos
18
20 (genus Rimicaris)
18. Rostrum with acute tip, bearing >10 dorsal teeth, ventrally unarmed; pleura of third
abdominal somite not serrate
Alvinocaridinides, the only species Alvinocaridinides formosa.
- Rostrum with blunt tip, bearing <10 dorsal notches, ventrally armed with 1–2 notches;
pleura of third abdominal somite serrate
19
19. Telson with sinuous row of dorsolateral spines and 2–4 spines on posterior margin;
cornea without anterior tubercle; ischia of third and fifth pereopods without strong
movable spines; dactyli of third to fifth pereopods with two or more rows of accessory
spinules
Opaepele, the only species Opaepele loihi.
- Telson with linear row of dorsolateral spines and >10 spines on posterior margin;
cornea with anterior tubercle; ischia of third and fifth pereopods with strong movable
spines; dactyli of third to fifth pereopods with a single row of accessory spinules
Keldyshicaris, the only species Keldyshicaris vavilovi
20. Carapace width not exceeding carapace height in adults; dorsal organ nearly
entire; scaphognathite without heavily plumose bacteriophore setae
21
- Carapace width exceeding carapace height in adults; dorsal organ four-lobed;
scaphognathite with heavily plumose bacteriophore setae
25
21. Dactyli of third to fifth pereopods with two rows of accessory spinules
22
- Dactyli of third to fifth pereopods with 3–4 rows of accessory spinules
23
22. Pleura of fourth and fifth abdominal somites not serrated
- Pleura of fourth and fifth abdominal somites serrated
23. Pterigostomial tooth absent
- Pterigostomial tooth present
24. Pleura of fourth and fifth abdominal somites serrated
- Pleura of fourth and fifth abdominal somites not serrated
25. Rostrum short but conspicuous; dorsal organ with a pore; antepenultimate segment
of third maxilliped with 1–2 distal movable spines
- Rostrum absent; dorsal organ without pores; antepenultimate segment of third
maxilliped without distal movable spines
Chorocaris parva
Chorocaris susannae
Chorocaris chacei
24
Chorocaris variabilis
Chorocaris vandoverae from the Mariana Back Arc Basin and
Chorocaris paulexa from the East Pacific Rise
Rimicaris hybisae
R. exoculata-R. kairei complex (R. exoculata in the Atlantic, R.
kairei in the Indian Ocean)
doi:10.1371/journal.pone.0129975.t005
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Phylogeny and New Classification of Alvinocarididae
Acknowledgments
The authors are grateful to Dr. Sammy De Grave (Oxford) for the help and valuable comments.
The studies were supported by the Russian Foundation for Basic Research (grant number 1504-08228).
Author Contributions
Analyzed the data: AV DK AL. Wrote the paper: AV DK.
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