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ISSN 10630740, Russian Journal of Marine Biology, 2013, Vol. 39, No. 4, pp. 276–286. © Pleiades Publishing, Ltd., 2013.
Original Russian Text © I.A. Chereshnev, O.A. Radchenko, A.V. Petrovskaya, 2013, published in Biologiya Morya.
276
INTRODUCTION
The subfamily Xiphisterinae sensu Makushok [1] is
within the family Stichaeidae and includes todate six
genera and nine species:
Xiphister mucosus, X. atropur
pureus, Phytichthys chirus, Cebidichthys violaceus,
Esselenichthys carli, E. laurae, Dictyosoma burgeri,
D. rubrimaculatum
, and
Nivchia makushoki.
The dis
tribution of the subfamily is amphiPacific: species of
the genera
Xiphister, Phytichthys, Cebidichthys
, and
Esselenichthys
are found in coastal waters of the north
eastern Pacific (the southeastern Bering Sea, the Gulf
of Alaska, and southward along the Pacific coast to
Central California); species of the genera
Dictyosoma
and
Nivchia
occur in the northwestern Pacific (basins
of the northern Yellow Sea and the Sea of Japan,
Pacific side of Honshu Island); a fossil taxon of
Niv
chia
was described from the LateMiocene deposits of
Sakhalin Island [1, 4, 12, 14, 18, 25, 26].
The genera
Xiphister
and
Phytichthys
were origi
nally classified within the family Xiphisteridae and the
genus
Cebidichthys
was placed in the family Cebidich
thyidae within the order Blenniiformes (Jordan, 1923,
cited after: [16], [21]). In addition, the genera
Neozo
arces
and
Zoarchias
were assigned by Jordan [16] to
the latter family because of the similar structure of the
dorsal fin consisting of “spinous” (only spines) and
following “soft” (soft rays) portions. However, Jordan
retained the genus
Dictyosoma
, which possesses a sim
ilar combined dorsal fin in the family Pholidae
1
.
In a substantial revision of stichaeids and related
fish families of the superfamily Stichaeoidae,
Makushok [1] recognized the subfamily Xiphisterinae
with the genera
Xiphister, Phytichthys, Cebidichthys
,
and
Dictyosoma
within the family Stichaeidae. He
noted the significant morphological heterogeneity of
the subfamily represented by two groups of closely
related genera
Xiphister
and
Phytichthys, Cebidichthys
,
and
Dictyosoma
. In the opinion of Makushok [1], the
morphological differences between these groups are
attributable not to the polyphyletic origin of the sub
family, but to the “progressively increasing specializa
tion” in the series
Dictyosoma–Phytichthys–Xiphister
leading to serious morphological changes of different
directionality but within one phyletic group.
Makushok [1] remarked that among the taxa of the
family Stichaeidae the subfamily Alectriinae is the
closest to the subfamily Xiphisterinae, while the sub
family Azygopterinae is the least close (it is only close
to the genera
Phytichthys
and
Xiphister
).
In the following revision based on cladistic analy
sis, Yatsu [25] proposed that the subfamily Xiphisteri
1
Jordan [16] included in the family Pholidae several genera from
the family Stichaeidae (
Chirolophis, Opisthocentrus, Plectobran
chus, Plagiogrammus, Pholidapus, Eulophias, Askoldia, Gymno
clinus, Alectrias, Alectridium
), but he remarked that Pholidae is a
quite diverse group and needs further subdivision.
ICHTHYOLOGY
Relationships and Position of the Taxa of the Subfamily Xiphisterinae
in the System of the Suborder Zoarcoidei (Perciformes)
I. A. Chereshnev, O. A. Radchenko, and A. V. Petrovskaya
Institute of Biological Problems of the North, Far East Branch, Russian Academy of Sciences, Magadan, 685000 Russia
email: radchenko@ibpn.ru
Received June 20, 2012
Abstract
—Analysis of the nucleotide sequences of mitochondrial and nuclear DNA genes was used to exam
ine the relationships and position of the subfamily Xiphisterinae in the system of the suborder Zoarcoidei.
This study showed the genetic heterogeneity of Xiphisterinae and the propriety of its division into two sub
families: Xiphisterinae with the genera
Xiphister
and
Phytichthys
and Cebidichthyinae with the genera
Cebid
ichthys
,
Dictyosoma
,
Esselenichthys
, and
Nivchia
. The genetic differences between the two subfamilies were
not less, but in some cases even greater than the differences between families within the suborder; therefore,
they should be raised to the rank of a family, Xiphisteridae and Cebidichthyidae, and classified not within the
superfamily Stichaeoidae but rather as independent taxa of the suborder Zoarcoidei.
Keywords
: Suborder Zoarcoidei, subfamily Xiphisterinae, mitochondrial DNA, COI, cytochrome b, 16S
rRNA, nuclear DNA, RNF213 gene, genetic and morphological divergence, taxonomic structure, status in
Zoarcoidei system
DOI:
10.1134/S1063074013040032
RUSSIAN JOURNAL OF MARINE BIOLOGY Vol. 39 No. 4 2013
RELATIONSHIPS AND POSITION OF THE TAXA OF THE SUBFAMILY XIPHISTERINAE 277
nae (in the volume accepted by Makushok [1]) be
divided into two subfamilies: Xiphisterinae with the
genera
Xiphister, Phytichthys
, and
Ernogrammus
(from
the subfamily Stichaeinae) and Cebidichthyinae with
the genera
Dictyosoma
and
Cebidichthys
. Later, the
genera
Esselenichthys
and
Nivchia
, which are close to
the genera
Cebidichthys
and
Dictyosoma
, were
included in the subfamily Xiphisterinae sensu
Makushok, 1958 [4, 12, 14].
Based on an unpublished work of Stoddard (1985)
(cited after [18]), Mecklenburg and Sheiko [18] sug
gested a different composition and structure of the
subfamily Xiphisterinae. They created two tribes:
Xiphisterini (genera
Xiphister, Phytichthys, Esselenich
thys, Dictyosoma, Cebidichthys
) and Alectriini (genera
Alectrias, Alectridium, Anoplarchus, Pseudalectrias
).
Nelson [19] agreed with the proposed system of the
Xiphisterinae; he included in it the nine listed genera
but without tribes until a more thorough taxonomic
treatment of the entire family Stichaeidae would be
performed along with obtaining evidence of the
monophyly of its subfamilies.
It should be noted that Mecklenburg and Sheiko
[18] reduced the number of subfamilies in the family
Stichaeidae from eight [1] to six. At the same time, a
new subfamily Neozoarcinae was introduced that
contained, along with the traditional genera
Neozo
arces
and
Zoarchias
[2], the genera
Azygopterus
and
Eulophias
, which Makushok [1] regarded as the type
for the monotypical subfamilies Azygopterinae and
Eulophiinae, while the subfamily Alectriinae was
placed in the subfamily Xiphisterinae in the rank of a
tribe.
The serious controversy concerning the taxonomic
structure and position of the subfamily Xiphisterinae
within the system of the family Stichaeidae [1, 18, 25]
necessitated the use of the moleculargenetic
approach. Analysis of the variability of the nucleotide
sequences of some mitochondrial and nuclear genes
has revealed the genetic heterogeneity of the subfamily
Xiphisterinae, thus justifying its subdivision into two
subfamilies, Xiphisterinae and Cebidichthyinae [10].
The level of genetic differences between Cebidichthy
inae and other subfamilies of the Stichaeidae is quite
significant. In this regard, the aim of the present study
is to elucidate the position, taxonomic status, and
relationships of the subfamilies Xiphisterinae and
Cebidichthyinae within the system of the suborder
Zoarcoidei.
MATERIALS AND METHODS
We used representatives of the families Stichaeidae,
Zoarcidae, Pholidae, Ptilichthyidae, Zaproridae,
Neozoarcidae, Cryptacanthodidae, Anarhichadidae,
and Bathymasteridae (Table 1). The Atlantic horse
mackerel
Trachurus trachurus
(family Carangidae,
Perciformes) was used as the outgroup [24].
Genomic DNA was isolated according to the stan
dard procedure [17]. Sequences of oligonucleotide
primers for the polymerase chain reaction and the
determination of nucleotide sequences of the mito
chondrial COI, cytochrome b, and 16S rRNA genes
and the nuclear RNF213 gene were given in previous
works [6–8].
Phylogenetic analysis of the nucleotide sequences
of the mitochondrial and nuclear genes was performed
separately. The data set for the mtDNA was formed of
six parts (the first nucleotide positions of the COI and
cytochrome b genes, the second nucleotide positions
of these genes, the third nucleotide positions com
bined, the 16S rRNA gene). For these parts, the fol
lowing optimal models of nucleotide substitutions
were selected using the Modeltest v3.7 [20] and Akaike
information criterion (AIC): GTR + G, TrNef + I +
G, F81, HKY, TIM + G, TVM + I + G. For the
RNF213 gene, the data set consisted of three parts
(the first, second, and third nucleotide positions), the
models selected were F81 + G, HKY + I, and K81.
The studied sample was enlarged by the GenBank data
for the nucleotide sequences of the mtDNA COI gene
of species of the subfamilies Xiphisterinae and Cebid
ichthyinae (Table 1). The nucleotide substitution
models used in the phylogenetic analysis of these data
were TIMef + G, F81, and TrN + G.
The analysis of phylogeny was performed using the
MrBayes v.3.1.2 program [22]. Three “heated” and
one “cold” chains were run for 10
6
generations and
every 100th tree was sampled. Out of 10001 generated
trees, the first 1001 were discarded. From the remain
ing trees that had stable estimates of the parameters of
nucleotide substitution models and likelihood (LnL),
we obtained consensus trees and estimates of the pos
terior probability of their branching.
RESULTS AND DISCUSSION
The nucleotide sequences of the COI, cytochrome
b, 16S rRNA, and RNF213 genes were placed in the
Genbank/NCBI database under the numbers listed in
Table 1. The length of the sequenced regions was 2044
base pairs (bp) for the mitochondrial genes and 630 bp
for the nuclear gene RNF213. In the studied mtDNA
genes, we found 632 variable and 532 phylogenetically
informative nucleotide positions, and 943 nucleotide
substitutions. The sequence of the RNF213 gene is
characterized by 91 polymorphic and 21 informative
nucleotide positions and 97 nucleotide substitutions.
The transition/transversion ratio was 2.7 : 1 for the
mtDNA genes and 1.9 : 1 for RNF213. Aminoacid
residue substitutions were found in the nucleotide
sequences of the mitochondrial and nuclear genes
coding for proteins: 11, 44, and 33 substitution muta
tions in the COI, cytochrome b, and RNF213 genes,
respectively.
278
RUSSIAN JOURNAL OF MARINE BIOLOGY Vol. 39 No. 4 2013
CHERESHNEV et al.
Table 1.
A list of the species that were used in this study
Systematic position Species (no. of specimen) Locality
No. in Genbank/NCBI
(genes COI/cyt. b/16S rRNA/RNF213)
Fam. Stichaeidae:
subfam. Stichaeinae
Stichaeuspunctatus
(1453) Sea of Okhotsk, Shantar Islands JN591552/JN591557/JN591562/JQ689662
subfam. Opisthocentrinae
Askoldia variegata
(1465) The same HQ873614/HQ873646/HQ873670/HQ873656
subfam. Lumpeninae
Leptoclinus maculatus
(1389) Western Kamchatka shelf HQ873611/HQ873643/HQ873667/HQ873652
Acantholumpenus mackayi
(1436) Sea of Okhotsk, Ulbanskiy Bay HQ873612/HQ873644/HQ873668/HQ873653
subfam. Chirolophinae
Chirolophis japonicus
(1258) Kunashir Island HQ873616/HQ873648/HQ896818/HQ873657
subfam. Alectriinae
Alectrias alectrolophus
(1440) Sea of Okhotsk, Shantar Islands JN591553/JN591558/JN591563/JQ417856
Anoplarchus insignis
(1481) USA, Washington State, San Juan Island JQ417843/JQ417847/JQ417851/JQ417857
subfam. Xiphisterinae
Xiphister atropurpureus
(1483) The same JN591554/JN591559/JN591564/JQ417858
Xiphister mucosus
* Canada, British Columbia FJ165467/–/–/–
subfam. Cebidichthyinae
Dictyosoma burgeri
(1492) Japan JQ417844/JQ417848/JQ417852/JQ417859
D. burgeri
* No data JF709889/–/–/–
D. rubrimaculatum
* No data JF709890/–/–/–
Cebidichthys violaceus
* USA, California GU440267/–/–/–
Esselenichthys carli
* The same GU440319/–/–/–
Fam. Zoarcidae:
subfam. Lycozoarcinae
Lycozoarces regani
(1323) Northern Sea of Japan FJ932601/FJ932613/FJ887743/HQ896821
subfam. Zoarcinae
Zoarces viviparus
(493) Gulf of Finland, Baltic Sea EF208062/FJ744403/FJ798756/JN209949
subfam. Lycodinae
Lycodes raridens
(202) Sea of Okhotsh, off Tauiskaya Bay EU380264/EU404178/EU741757/HQ896820
subfam. Gymnelinae
Hadropareia middendorffii
(300) Sea of Okhotsk, Nagaev Bay HM217160/HM217165/HM217169/HM217151
Leptostichaeus pumilus
(1375) Sea of Japan, Peter the Great Bay JN591551/JN591556/JN591561/JQ689661
Fam. Neozoarcidae
Neozoarces pulcher
(1187) The same F J932603/FJ932615/F J887745/ HQ896822
Fam. Anarhichadidae
Anarhichas lupus
(1384) Northern Sea, Sweden HQ873609/HQ873641/HQ873665/HQ896823
Fam. Zaproridae
Zaprora silenus
(1185) Western Kamchatka shelf FJ932606/FJ932618/FJ887748/HQ873659
Fam. Ptilichthyidae
Ptilichthys goodei
(1186) Sea of Okhotsk, Talan Island FJ932605/FJ932617/FJ887747/HQ873660
Fam. Pholidae
Pholis picta
(1281) Kunashir Island HM051084/HM051096/HM051097/JN816391
Apodichthysflavidus
(1475) USA, Washington State, San Juan Island JN591555/JN591560/JN591565/ JN816397
Rhodymenichthys dolichogaster
(471) Tauiskaya Bay, Nedorazumeniya Island HM051088/HM051091/HM051102/HM217158
Xererpes fucorum
(1477) USA, Washington State, San Juan Island JN816386/JN816388/JN816390/JN816399
Fam. Cryptacanthodidae
Cryptacanthodes bergi
(1468) Sea of Japan, Peter the Great Bay HQ873618/HQ873650/HQ873663/HQ873662
Fam. Bathymasteridae
Bathymaster derjugini
(331) The same EU741725/EU741751/EU741792/HM217159
Fam. Carangidae
Trachurus trachurus
* Ireland AB108498 (complete mt genome)/EU638269
Note: * Data on the gene nucleotide sequences were derived from GenBank.
RUSSIAN JOURNAL OF MARINE BIOLOGY Vol. 39 No. 4 2013
RELATIONSHIPS AND POSITION OF THE TAXA OF THE SUBFAMILY XIPHISTERINAE 279
As was noted above, a previous study on the taxo
nomic structure and phylogenetic relationships of the
subfamily Xiphisterinae within the system of the
stichaeid fishes revealed quite significant genetic dif
ferences between the genera
Xiphister
and
Dictyosoma
(13.7% for mtDNA and 2.2% for nuclear DNA) that
are comparable with the differences between subfami
lies in the families Stichaeidae and Zoarcidae [10]. In
phylogenetic trees of stichaeid and zoarcid fishes
([10], Figs. 1–3),
Xiphister
and
Dictyosoma
formed no
shared clusters and, on the contrary, were highly sepa
rated topologically. The genus Xiphister is closer to the
family Stichaeidae than the genus
Dictyosoma
: the
genetic difference of the former genus from the
stichaeids is 9.9–13.2% (on average, 12%), while this
difference for the latter genus is markedly greater,
12.7–15.1 (14)%. These genera fairly significantly dif
fer from taxa of the subfamily Alectriinae:
Xiphister
,
12.1% for the mtDNA genes and 2% for the nuclear
gene RNF213;
Dictyosoma
, 14.8 and 2.8%, respec
Pholis picta
(1281)
Apodichthys flavidus
(1475)
Rhodymenichthys dolichogaster
(471)
Ptilichthys goodei
(1186)
Askoldia variegata
(1465)
Zaprora silenus
(1185)
Leptoclinus maculatus
(1389)
0.03
Trachurus trachurus
*
Bathymaster deriugini
(331)
Bathymasteride
Dictyosoma burgeri
(1492)
Cebidichthyidae
Anarhichadidae
Anarhichas lupus
(1384)
Neozoarces pulcher
(1187)
Leptostichaeus pumilus
(1375)
Hadropareia middendorffii
(300)
Neozoarcide
Zoarcidae
Zoarces viviparus
(493)
Lycozoarces regani
(1323)
Lycodes raridens
(1202)
Chirolophis japonicus
(1258)
Chirolophinae,
Stichaeidae
Pholidae
Xiphisterine
Stichaeidae
Xererpes fucorum
(1477)
Xiphister atropupureus
(1483)
Alectrias alectrolophus
(1440)
Stichaeus punctatus
(1453)
Alectriinae
Stichaeinae
Cryptacanthodidae
Cryptacantodes bergi
(1468)
Lumpeninae,
Stichaeidae
Zoproridae
Opisthocentrinae,
Stichaeidae
Ptilichthyidae
100
52
78
94
89
70
100
100
100
100
100
100
86
99
91
100
100
67
Pholidae
Fig. 1.
A Bayesian tree of haplotypes of the superfamily Stichaeoidae and the family Zoarcidae inferred from the nucleotide
sequences of the mitochondrial COI, cytochrome b, 16S rRNA genes. Tree parameters: LnL = –15680; A : C : G : T = 0.247 :
0.286 : 0.194 : 0.272;
α
parameter of gamma distribution is 0.147. The numerals at the base of clusters are estimates of the stability
of branching nodes in 50% Bayesian consensus trees (%).
280
RUSSIAN JOURNAL OF MARINE BIOLOGY Vol. 39 No. 4 2013
CHERESHNEV et al.
tively. The latter genus is in a basal position in the phy
logenetic trees ([10], Figs. 1 and 2), being distant from
both the subfamily Alectriinae and the genus
Xiphister
.
The above results and the analysis of a set of the most
informative morphological features confirmed the
Yatsu’s [25] scheme of division of the subfamily
Xiphisterinae into two subfamilies: Xiphisterinae with
the genera
Xiphister
and
Phytichthys
and Cebidichthy
inae with the genera
Cebidichthys
and
Dictyosoma
, to
which the genera
Esselenichthys
[12, 14] and
Nivchia
[4] were assigned later. The same genetic studies do
not allow the inclusion of the genus
Ernogrammus
in
the subfamily Xiphisterinae, because the genera
Xiphister
and
Ernogrammus
are distant in the phyloge
netic trees and the level of divergence between them is
comparable with the differences between subfamilies
in the family Stichaeidae [10].
MrBayes (v.3.12) phylogenetic trees inferred from
the nucleotide sequences of mitochondrial and
nuclear genome regions show the position of the stud
ied taxa of the suborder Zoarcoidei (Figs. 1–3).
The consensus tree built from the three mtDNA
genes (Fig. 1) consisted of three large clusters. The
external cluster is composed of the haplotypes of taxa
of the family Pholidae; the divergence values between
their mtDNA were not high, 9.6–11.2 (10.6)% (Table
2). Microclusters of the family Ptilichthyidae and the
subfamily Opisthocentrinae (genus
Askoldia
) adjoin
Zoares viviparus
(493)
Lycodes raridens
(202)
Lycozoarces regani
(1323)
Hadropareia middendorffii
(300)
Neozoarces pulchers
(1187)
87
94
92
71
89
76
Anarhichas lupus
(1384)
Pholis picta
(1281)
Apodichthys flavidus
(1475)
Rhodymenichthys dolichogaster
(471)
Leptostichaeus pumilus
(1375)
Zaprora silenus
(1185)
Ptilichthys goodei
(1186)
Stichaeus punctatus
(1453)
Askoldia variegata
(1465)
Leptoclinus maculatus
(1389)
Chirolophis japonicus
(1258)
Alectrias alectrolophus
(1440)
Xiphister atropurpureus
(1483)
Xererpes fucorum
(1477)
Cryptacantodes bergi
(1468)
Dictyosoma burgeri
(1492)
Bathymaster derjugini
(331)
Trachurus trachurus*
0.02
Fig. 2.
A Bayesian tree of the superfamily Stichaeoidae and the family Zoarcidae inferred from the nucleotide sequences of the
nuclear RNF213 gene. Tree parameters: LnL = –1913.866; A : C : G : T = 0.288 : 0.215 : 0.256 : 0.241; the
α
parameter of the
gamma distribution is 0.114.
RUSSIAN JOURNAL OF MARINE BIOLOGY Vol. 39 No. 4 2013
RELATIONSHIPS AND POSITION OF THE TAXA OF THE SUBFAMILY XIPHISTERINAE 281
Lycodes raridens
(202)
Lucozoarces regani
(1323)
Hadropareia middendorffii
(300)
Zoarces viviparus
(493)
Neozoarces pulcher
(1187)
Leptostichaeus pumilus
(1375)
Anarhichas lupus
(1384)
Alectrias alectrolophus
(1440)
Anoplarchus insignis
(1481)
Chirolophis japonicus
(1258)
Stichaeus punctatus
(1453)
Xererpes fucorum
(1477)
Xiphister atropurpureus
(1483)
63
55
54
100
67
96
97
53
100
99
100
100
100
100
100
100
Xiphister mucosus
*
80
Cebidichthys violaceus
*
Pholis picta
(1281)
Rhodymenichthys dolichogaster
(471)
Apodichthys flavidus
(1475)
Ptilichthys goodei
(1186)
Askildia variegata
(1465)
Leptoclinus maculatus
(1389)
Acantholumpenus mackayi
(1436)
Zaprora silenus
(1185)
Cryptacantodes bergi
(1468)
Dictyosoma burgeri
(1492)
Dictyosoma burgeri
*
Dictyosoma rubrimaculatum
*
Esselenichthys carli
*
Bathymaster derjugini
(331)
Trachurus trachurus*
0.02
Fig. 3.
A Bayesian tree of haplotypes of the superfamily Stichaeoidae and the family Zoarcidae inferred from the nucleotide
sequence of the mitochondrial COI gene. Tree parameters: LnL = –5279.935; A : C : G : T = 0.234 : 0.283 : 0.172 : 0.311; the
α
parameter of the gamma distribution is 0.151. *Data on gene nucleotide sequences were derived from GenBank.
this group. The genetic differences between the taxa in
these microclusters vary in the range of 9.6–11.9
(10.9)%. A somewhat lower level of divergence is
observed in the next microcluster, which combined
species of distant families such as Zaproridae,
Stichaeidae (subfamily Lumpeninae), and Cryptacan
thodidae, 9.3–10.3 (9.6)%. In the central cluster,
which only includes taxa of the families Stichaeidae
(subfamilies Stichaeinae, Alectriinae, Xiphisterinae,
and Chirolophinae) and Pholidae (genus
Xererpes
),
the degree of genetic differences is the greatest, 11.2–
12.7 (12.1)%. Remarkably, the subfamily Chirolophi
nae, which Makushok [1] considers to be close to the
subfamily Stichaeinae, is in an external position and
shows the greatest differences from other taxa within
this cluster, 12.5%.
It is significant that the two clusters form a macro
cluster with a fairly high support (89%), whose taxo
nomic volume corresponds to the superfamily
282
RUSSIAN JOURNAL OF MARINE BIOLOGY Vol. 39 No. 4 2013
CHERESHNEV et al.
Table 2.
Divergence values (in %) between the nucleotide sequences of the mtDNA genes (below the diagonal) and the RNF213 gene (above the diagonal)
Species 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23
1.
Leptostichaeus pumilus
(1375) – 3.4 3.2 2.7 2.3 2.9 1.8 2.3 1.9 1.8 1.9 1.8 2.1 2.8 2.6 2.4 2.1 2.1 2.1 2.6 1.9 3.2 12.6
2.
Zoarces viviparus
(493) 12.5 – 2.3 2.3 1.9 3.3 2.3 2.8 2.4 2.6 3.1 2.8 3.1 3.4 3.2 3.2 2.6 2.6 2.6 3.1 2.7 3.7 12.8
3.
Lycodes raridens
(202) 11.8 10.4 – 2.6 1.9 3.2 2.3 2.8 2.4 2.4 3.1 2.6 2.8 2.8 2.9 3.2 2.6 2.6 2.6 3.1 2.7 3.4 12.4
4.
Lycozoarces regani
(1323) 12.6 9.8 8.9 – 1.6 2.6 1.6 2.4 2.1 2.3 2.4 2.4 2.8 3.1 2.9 2.4 2.3 2.3 2.3 2.1 2.4 3.1 12.2
5.
Hadropareia middendorffii
(300) 12.6 10.5 10.2 10.0 – 2.3 1.1 1.8 1.4 1.6 2.2 1.6 2.1 2.4 2.3 2.3 1.6 1.6 1.6 2.1 1.6 2.7 11.8
6.
Neozoarces pulcher
(1187) 12.4 11.0 11.6 12.5 11.6 – 1.6 2.3 1.9 2.1 2.6 2.3 2.6 3.3 2.8 2.8 2.1 2.1 2.1 2.6 2.3 3.1 12.2
7.
Anarhichas lupus
(1384) 11.4 10.8 9.2 9.6 10.6 10.8 – 1.5 1.1 1.3 1.8 1.4 1.8 2.3 1.9 1.9 1.3 1.3 1.3 1.8 1.3 2.4 11.7
8.
Zaprora silenus
(1185) 13.6 13.7 13.2 13.1 13.9 12.0 11.4 – 1.0 1.1 1.6 1.3 1.6 2.3 1.8 1.8 1.1 1.1 1.1 1.9 1.3 2.3 11.1
9.
Ptilichthys goodei
(1186) 13.6 12.9 13.3 12.9 13.3 14.1 11.9 13.3 – 0.8 1.3 1.0 1.3 1.9 1.4 1.4 0.8 0.8 0.8 1.6 1.0 1.9 11.0
10.
Stichaeuspunctatus
(1453) 14.1 13.4 14.3 13.9 14.8 13.6 11.9 12.1 13.7 – 1.1 0.5 1.0 1.6 1.1 1.6 1.0 1.0 0.6 1.4 1.1 2.1 10.9
11.
Askoldia variegata
(1465) 13.5 13.1 13.5 13.9 14.4 12.2 12.7 11.4 11.9 11.5 – 1.3 1.3 1.6 1.8 1.8 1.4 1.4 1.1 1.9 1.6 2.6 11.3
12.
Leptoclinus maculatus
(1389) 14.0 12.9 12.8 12.9 13.5 13.2 11.6 9.3 12.7 12.3 11.6 – 1.1 1.6 1.3 1.8 1.1 1.1 0.8 1.6 1.1 2.3 11.1
13.
Chirolophisjaponicus
(1258) 13.8 14.2 14.6 14.3 15.1 14.6 12.1 12.6 13.1 12.5 13.8 12.9 – 1.6 1.4 2.1 1.4 1.4 1.1 1.9 1.6 2.6 11.3
14.
Alectrias alectrolophus
(1440) 14.1 14.8 14.0 14.7 14.7 14.0 12.9 12.4 14.7 11.2 12.6 12.7 12.5 2.1 2.6 2.1 2.1 1.8 2.6 2.3 2.9 11.9
15.
Xiphister atropurpureus
(1483) 13.8 13.7 13.4 12.5 13.1 13.7 11.4 11.6 14.0 11.9 13.1 12.5 12.4 12.7 – 2.3 1.6 1.6 1.3 2.1 1.8 2.7 11.7
16.
Dictyosoma burgeri
(1492) 14.9 14.6 14.0 14.9 15.1 14.0 13.4 13.9 14.9 14.1 13.3 13.4 15.0 14.5 13.7 – 1.6 1.6 1.5 2.4 1.8 2.6 11.7
17.
Pholis picta
(1281) 14.6 14.3 14.7 14.5 14.5 14.4 13.6 13.0 11.3 14.1 11.8 12.9 14.0 13.7 14.2 15.0 – 0.3 0.6 1.8 0.8 1.9 10.7
18.
Apodichthysflavidus
(1475) 15.4 15.5 15.6 16.3 16.0 14.0 14.3 13.6 13.9 14.7 13.5 14.5 14.5 15.4 14.2 13.9 11.2 – 0.6 1.8 1.1 1.9 10.9
19.
Rhodymenichthys dolichogaster
(471) 13.8 14.0 13.4 13.5 13.6 13.0 11.7 10.1 12.0 12.3 11.2 10.7 12.9 13.0 12.9 14.0 9.6 11.0 – 1.5 1.1 2.1 10.6
20.
Xererpes fucorum
(1477) 13.8 14.5 14.2 14.3 13.6 14.9 12.4 13.5 13.8 12.1 13.3 12.8 12.5 12.4 11.1 15.4 14.5 14.9 13.0 – 1.9 2.9 10.9
21.
Cryptacanthodes bergi
(1468) 13.3 12.6 13.7 13.0 13.4 12.6 11.3 9.6 12.3 11.6 10.7 10.3 13.0 12.6 12.0 13.2 13.0 14.0 11.9 12.5 – 2.3 11.3
22.
Bathymaster derjugini
(331) 13.3 14.5 13.5 13.6 13.8 14.0 11.4 11.6 12.8 13.0 12.1 12.2 13.1 12.7 13.1 14.3 13.8 14.1 11.3 13.4 11.2 – 10.9
23.
Trachurus trachurus
22.5 22.0 22.0 24.4 20.9 20.1 22.5 21.0 22.8 22.4 21.2 22.0 22.4 21.7 21.4 21.9 21.4 23.1 22.1 22.2 20.8 20.9 –
RUSSIAN JOURNAL OF MARINE BIOLOGY Vol. 39 No. 4 2013
RELATIONSHIPS AND POSITION OF THE TAXA OF THE SUBFAMILY XIPHISTERINAE 283
Stichaeoidae sensu Makushok [1]. The exceptions are
the families Zaproridae and Cryptacanthodidae
(present in the macrocluster), which are currently
considered to be independent families in the suborder
Zoarcoidei [11, 13], and the family Anarhichadidae
(absent in the macrocluster), which was placed by
Makushok [1] in the superfamily Stichaeoidae.
The third cluster of haplotypes is in an external
position with respect to the first two clusters and con
sists of the subfamilies of the family Zoarcidae and
groups close to them, viz., the genera
Leptostichaeus,
Neozoarces
, and
Anarhichas
. The values of divergence
between the mtDNA of the subfamilies of the Zoar
cidae were the smallest in all the compared groups,
8.9–10.4 (9.7)%. The overall level of genetic differ
ences in this cluster that includes the families Zoar
cidae, Neozoarcidae, Anarhichadidae, and the genus
Leptostichaeus
was 8.9–12.6 (10.8)%.
The haplotype of
Dictyosoma burger
is external to
all three clusters; it differs greatly from the rest, viz., by
13.2–15.4 (14.3)%, but most significantly from
Xerer
pes fucorum
(Pholidae),
Ptilichthys goodie
(Ptilichthy
idae),
Leptostichaeus pumilus, Alectrias alectrolophus
(Alectriinae), and from the family Zoarcidae as a
whole (Table 2).
Interestingly, the taxa of the Zoarcoidei that have
the combined dorsal fin of “spinous” and “soft” por
tions (genera
Neozoarces, Ptilichthys
, and
Dictyo
soma
), genetically differ from one another to a greater
extent than most families in the suborder, 14.0–14.9
(14.3)% for mtDNA. The genetic differences suggest
that the combined dorsal fin in the zoarcoid taxa
appeared independently (convergently) and on a dif
ferent genetic basis. We probably should agree with
Makushok [1] in that such a structure of the dorsal fin
is a primitive state in the superfamily Stichaeoidae.
This is confirmed by an analogous structure of the dor
sal fin in the fossil genus
Nivchia
[4]. Evidently, such a
prominent morphological feature as the longitudinal
skin ridge on the head top in species of the subfamily
Alectriinae and the genera
Neozoarces, Cebidichthys
,
and
Dictyosoma
is also of a convergent origin. It is
quite possible that the above morphological peculiarity
was determined by the directional evolution of these
fish groups that appeared in the coastal emergent zone
of seas of the northern Pacific [1, 2].
In the consensus phylogenetic tree inferred from
the data on the nuclear RNF213 gene nucleotide
sequences (Fig. 2), clusters formed by taxa of the fam
ily Zoarcidae and close groups are noteworthy (
Neozo
arces, Anarhichas
), as well as the family Pholidae,
which repeat the “mitochondrial” clusters with the
same fish groups (Fig. 1). This is indicative of the high
stability and significance of the clustering of these
taxa. Other fish groups do not form any clusters and
are equally distant topologically from one another.
However, by the level of genetic differences (Table 2),
Bathymaster derjugini
, which belongs to the most
primitive zoarcoid family Bathymasteridae [11], dif
fered most significantly from all (2.6%, on average).
Taxa of the family Zoarcidae and the genus
Neozoarces
(on average, 2.5%), the genera
Leptostichaeus
(2.4%)
and
Alectrias
(2.3%) also differed fairly greatly. The
lowest values of genetic divergence in the RNF213
gene were found for the genus
Ptilichthys
(1.4%),
which is the most morphologically specialized among
the Zoarcoidei [13]. The highly specialized groups
Anarhichas, Zaprora
, and
Cryptacanthodes
showed, on
an average, no more than 1.8% differences; however,
in less specialized Stichaeidae and Pholidae the value
of genetic differences was still lower, 1.6%.
The phylogenetic tree that was inferred from the
nucleotide sequences of the COI gene and the Gen
Bankderived data for other species showed more
clearly the phylogenetic relationships between the taxa
(Fig. 3). A still high level of stability is exhibited by the
haplotype clusters of the Zoarcidae taxa and groups
close to them, as well as the taxa of the family Phol
idae, although in the former cluster the relationships
of the genera
Hadropareia
and
Zoarces
changed
towards
Neozoarces
and
Leptostichaeus
, while in the
latter cluster there was a change in the position of the
genera
Rhodymenichthys
and
Apodichthys
.
Microclus
ters of closely related species and genera were formed:
Alectrias
and
Anoplarchus
from the subfamily Alectrii
nae,
Xiphister atropurpureus
and
X. mucosus
from the
subfamily Xiphisterinae, and
Leptoclinus
and
Acan
tholumpenus
from the subfamily Lumpeninae.
The separation of the taxa of the subfamily Cebid
ichthyinae is most marked. They formed their own
cluster that is markedly far from Xiphisterinae,
Stichaeidae, Pholidae, and Zoarcidae. In the Cebid
ichthyinae cluster, species of the genus
Dictyosoma
that live at the Asiatic coast of the Pacific are closer to
one another than to the North American
Cebidichthys
violaceus
and
Esselenichthys carli
, which agrees with
morphological data. Thus, the genus
Dictyosoma
has a
fairly complicated system of body sensory canals, in
which the longitudinal canals of the upper and lower
sides of the body are connected by transverse anasto
moses that pass onto the canal of the ventral side ([3],
Figs. 6, 7; [25], Fig. 1; [15], p. 1049).
Cebidichthys
and
Esselenichthys
have one (in the former) or two to three
(in the latter) simple canals that are not connected by
anastomoses ([3], Figs. 6, 7; [25], Fig. 1; [14], Figs. 1,
2, 5). Since the body canals in fossil
Nivchia
are
arranged in a similar way to
Dictyosoma
, i.e., there is
an anastomotic network [4], this structure of the body
canals can be regarded as an ancestor state. In con
trast, their reduction and simplification, as in
Cebid
ichthys
and
Esselenichthys
, should be considered as a
derivative state that emerged in the course of evolution
of the subfamily in the ancestral form of these genera,
which is close to
Dictyosoma
and
Nivchia
, during their
expansion from the Sea of Japan area toward the
shores of North America. A similar process also
occurred in some head canals of the sensory system: in
284
RUSSIAN JOURNAL OF MARINE BIOLOGY Vol. 39 No. 4 2013
CHERESHNEV et al.
Cebidichthys
and
Esselenichthys
the occipital commis
sure is not connected with the upper body canal via a
firstorder canal (in Neelov’s [5] terminology); in
Esselenichthys
the number of pores in the inner rows of
the suborbital and postorbital canals is reduced; in
Cebidichthys
the inner pores disappear altogether ([1,
3], Fig. 6; [26], Fig. 2; [25], Fig. 3; [14], Fig. 2).
The paleontological and morphological data defi
nitely suggest that the genus
Dictyosoma
is the most
ancient in the subfamily Cebidichthyinae and the sub
family itself is a welldefined group of zoarcoid fish
taxa. In this regard, the subfamily should be elevated in
rank to a family, Cebidichthyidae, within the suborder
Zoarcoidei but not within the superfamily Stichae
oidae. Nazarkin [4] proposed that some morphologi
cal peculiarities of the “soft rayed” members of
Xiphisterinae (= Cebidichthyidae) be considered as
synapomorphies. These are the combined structure of
the dorsal fin, as well as the connection of the termi
nation of the dorsal and anal fins with the caudal fin
(unique to the superfamily Stichaeoidae), in which the
lengthened rays of these unpaired fins reach to and
overlap the middle of the marginal rays of the caudal
fin, while the fairly deep notches are retained ([1],
(a) (b)
(c) (d)
Fig. 4.
The head sensory canals in
Bathymaster caeruleofasciatus
((a), view from top and side),
Xiphister mucosus
((b), view from
top and side),
Cebidichthys violaceus
(c) and
Dictyosoma burger
(d). (a), from [23], Fig. 8; (b–d), from [25], Fig. 3.
RUSSIAN JOURNAL OF MARINE BIOLOGY Vol. 39 No. 4 2013
RELATIONSHIPS AND POSITION OF THE TAXA OF THE SUBFAMILY XIPHISTERINAE 285
Fig. 20d). It should be noted that in the genera
Xiphis
ter
and
Phytichthys
(the subfamily Xiphisterinae) the
membranes of the dorsal and anal fins are continuous
with the base of the caudal fin, without notches,
reaching to the beginning of its marginal rays, which is
also characteristic of some Stichaeinae, Alectriinae,
and most Pholidae ([1], Fig. 20
е–h
).
The genera
Phytichthys
and
Xiphister
also have a
number of synapomorphies. In particular, these are
the unique structure of the head canals of the sensory
system, in which the suborbital canal gives rise to three
(
Xiphister
) or four (
Phytichthys
) long firstorder cheek
canals surrounded throughout their length by ringlike
scales; and as the presence of a very long central pos
terior firstorder canal of the occipital commissure
with several secondorder canals (Fig. 4) ([1], Figs. 48,
49; [25], Figs. 3, 5). This type of structure of the ceph
alic sensory system is not found in the superfamily
Stichaeoidae, in the families Zoarcidae, Neozoar
cidae, Cryptacanthodidae, and Scytalinidae, i.e., in
virtually no taxa of the suborder Zoarcoidei [1–3, 11,
14, 25, and others]. Only representatives of the subor
der’s most primitive family Bathymasteridae have
cheek branches of the suborbital canal, which are
developed to varying degrees (but less than in
Phytich
thys
and
Xiphister
), and the lengthened central poste
rior firstorder canal of the occipital commissure with
short secondorder canals (Fig. 4a) [9, 23]. However,
in contrast to
Phytichthys
and
Xiphister
, these canals in
bathymasterids are skin tubes devoid of scales. We note
that the structure plan of the head sensory system in
the taxa of the family Cebidichthyidae is typical of the
family Stichaeidae (Fig. 4c, 4d) ([1], Fig. 48; [25],
Figs. 3, 5; [14], Fig. 2). The unique structural pecu
liarities of the head canals in
Phytichthys
and
Xiphister
should most likely be regarded as a plesiomorphic state
convergent to that in Bathymasteridae and inherited
by them from different ancestral forms. Another syna
pomorphy in Xiphisterinae is the joining of strongly
developed chewing muscles of both sides of the head
on the root of the skull ([1], Fig. 67; [25]), which
among other taxa of the stichaeoid and zoarcoid fishes
is only found in the highly morphologically specialized
monotypic subfamily Azigopterinae (family
Stichaeidae). However, as was noted by Makushok [1],
this anatomical feature developed independently in
Xiphisterinae and Azygopterinae.
Unlike the genus
Dictyosoma
, the genus
Xiphister
in
all phylogenetic trees is either within or in the direct
vicinity of the cluster of taxa of the superfamily
Stichaeoidae. In connection with this, the subfamily
Xiphisterinae can be elevated to the rank of a family
but within the superfamily Stichaeoidae. This is also
supported by the comparative morphological data that
fairly definitely indicate the phylogenetic separation
of this group of stichaeoid fishes [1–3, 10, 14, 25].
However, another taxonomic solution can exist, such
as a revision of the existing system of the superfamily
Stichaeoidae proposed by Makushok [1]. Judging
from the position of taxa in the phylogenetic trees
(Fig. 1, 3), members of the superfamily form no stable
groupings strictly relating to particular subfamilies and
families of the Stichaeoidae (unlike, for example, the
families Zoarcidae and Pholidae). The clusters can
include taxa from different phylogenetically distant
subfamilies and even families. At the same time, the
family Anarhichadidae, which was included by
Makushok [1] in the superfamily Stichaeoidae, is con
sistently present in the cluster of the families Zoar
cidae and Neozoarcidae, while the family Zaproridae
is clustered with the subfamily Lumpeninae (family
Stichaeidae) and the family Cryptacanthodidae
(Fig. 1). The superfamily Stichaeoidae should proba
bly be abandoned and its constituent families should
be regarded as independent taxa of the suborder Zoar
coidei [11, 13, 19].
ACKNOWLEDGMENTS
This work was supported by grants from the Rus
sian Foundation for Basic Research (no. 1104
00004) and from the RFBR/FEB RAS (no. 1104
98504). The authors are sincerely grateful to Prof.
Theodor Pietsch (University of Washington, United
States) for help with the materials for the genetic study
of the genera
Anoplarchus
and
Xiphister
and to
M.V. Nazarkin (Zoological Institute, Russian Acad
emy of Sciences) who kindly helped with the materials
of the genus
Dictyosoma
.
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Translated by E. Shvetsov