Evolutionary diversification in freshwater sculpins (Cottoidea): a review of two major adaptive radiations

Abstract

Freshwater sculpins, grouped by their com-mon ecological characteristic of freshwater habitats, comprise the species from the genera Cottus, Trachidermus, Mesocottus and Myoxocephalus as well as the Baikal sculpins. These fishes are typically coldwater-adapted, having probably originated poly-phyletically from ancestral species of marine sculpins. Gottus, the most speciose taxonomic group, includes at least 64 species and is distributed throughout the fresh waters of the northern part of the Northern Hemisphere. Indinidual species have diverse life histories, such as fluvial, lacustrine, catadromous, and freshwater amphidromous. The second most abundant group, the Baikal sculpins, includes 33 species in 12 genera representing 3 families, and comprises many benthic, and a few bentho-pelagic and pelagic species. The freshwater sculpins belonging to Trachidermus, Mesocottus and Myoxocephalus include only one or two species in each genus. Recent molecular phyloge-netic analyses of Cottus species, Baikal sculpins and their relatives have demonstrated mainly that (1) Cottus kazika is a sister taxon to Trachidermus fasciatus (designated lineage A), (2) Cottus species, except for C. kazika, and the Baikal sculpins are monophyletic, (3) on the basis of (1) and (2), Cottus as presently recog-nized is not monophyletic, and (4) the Major monophy-letic lineages include 7 lineages: lineage B from Eurasia, lineages C and D from East Asia, the Cottopsis clade (sensu Copeia 2005:303–311, 2005) from the west coast of North America, the Cottus clade from the Circum-Arctic sea, the monophyletic Baikal sculpins, and the Uranidea clade. These findings suggested that the monophyletic freshwater sculpins that comprise the lin-eage A and the 7 other lineages may undergone two major radiations, one having occurred in the fresh water Cottus species in the northern part of the Northern Hemisphere, and the other in the Baikal sculpins in the Lake Baikal, the world's oldest freshwater lake. Through these adaptive radiations, a tremen-dous diversity of morphological, ecological, phys-iological and life historical traits now exists in the freshwater sculpins. Keywords Evolutionary history . Life-history diversification . Molecular phylogeny . Larval development . Adaptive radiation . Cottus species . Baikal sculpins

Full text

Evolutionary diversification in freshwater sculpins
(Cottoidea): a review of two major adaptive radiations
Akira Goto & Ryota Yokoyama & Valentina G. Sideleva
Received: 2 July 2013 /Accepted: 17 March 2014
#
Springer Science+Business Media Dordrecht 2014
Abstract Freshwater sculpins, grouped by their com-
mon ecological cha racteristic of freshwater habitats,
comprise the species from the genera Cottus,
Trachidermus, Mesocottus and Myoxocephalus as well
as the Baikal sculpins. These fishes are typically
coldwater-adapted, having probably originated poly-
phyletically from ancestral species of marine sculpins.
Gottus, the most speciose taxonomic group, includes at
least 64 species and is distributed throughout the fresh
waters of the northern part of the Northern Hemisphere.
Indinidual species have diverse life histories, such as
fluvial, lacustrine, catadromous, and freshwater
amphidromous. The second most abundant group, the
Baikal sculpins, includes 33 species in 12 genera
representing 3 families, and comprises many benthic,
and a few bentho-pelagic and pelagic species. The
freshwater sculpins belonging to Tra chi de rmu s,
Mesocottus and Myoxocephalus include only one or
two species in each genus. Recent molecular phyloge-
netic analyses of Cottus species, Baikal sculpins and
their relatives have demonstrated mainly that (1)
Cottus kazika is a sister taxon to Trachidermus fasciatus
(designated lineage A), (2) Cottus species, except for
C. kazika, and the Baikal sculpins are monophyletic, (3)
on the basis of (1) and (2), Cottus as presently recog-
nized is not monophyletic, and (4) the Major monophy-
letic lineages include 7 lineages: lineage B from Eurasia,
lineages C and D from East Asia, the Cottopsis clade
(sensu Copeia 2005:303–311, 2005) from the west coast
of North America, the Cottus clade from the Circum-
Arctic sea, the monophyletic Baikal sculpins, and the
Uranidea clade. These f indings suggested that the
monophyletic freshwater sculpins that comprise the lin-
eage A and the 7 other lineages may undergone two
major radiations, one having occurred in the fresh water
Cottus species in the northern part of the Northern
Hemisphere, and the other in the Baikal sculpins
in the Lake Baikal, the w orld’soldestfreshwater
lake. Through these adaptive radiations, a tremen-
dous diversity of morphological, ecological, phys-
iological and life hist ori cal traits now exists in the
freshwater sculpins.
Keywords Evolutionary history
.
Life-history
diversification
.
Molecular phylogeny
.
Larval
development
.
Adaptive radiation
.
Cottus species
.
Baikal sculpins
Environ Biol Fish
DOI 10.1007/s10641-014-0262-7
A. Goto (*)
:
R. Yokoyama
Field Science Center for Northern Biosphere, Hokkaido
University,
3-1-1 Minato-cho, Hakodate 041-8611, Japan
e-mail: akir@fish.hokudai.ac.jp
V. G. Sideleva
Zoological Institute, The Russian Academy of Science,
Universitetskaya Emb. no. 1, St. Petersburg 199034, Russia
Present Address:
A. Goto
Department of Science of Environmental Education,
Hokkaido University of Education,
1-2 Hachiman-cho, Hakodate, Hokkaido 040-8567, Japan
Present Address:
R. Yokoyama
Civil Engineering & Eco-Technology Consultants, Co., Ltd,
2-23-2 Higashi-IkebukuroToshimaTokyo 170-0013, Japan

Preface
Although more than 600 species of the superfamily
Cottoidea (cottoids) are distributed in marine environ-
ments, about 100 sculpin specie s inhabit Northern
Hemisphere freshwater habitats (Goto 1990; Sideleva
2003; Nelson 2006; Yabe 2011; Yokoyama and Goto
2011). Comprising species fr om the g enera Cottus,
Trachidermus, Mesocottus and Myoxocephalus as well
as the Baikal sculpins, these freshwater sculpins proba-
bly originated polyphyletically from ancestral species of
marine sculpins (Scott and Crossman 1973; Goto 1982,
1990, 2001b; Yabe 1985, 2011; Sideleva 1994, 2003;
Yokoyama and Goto 2011).
The most speciose group of freshwater sculpins be-
long to the genus Cottus, being highly suitable for
studies of the evolutionary biology, including adaptation
to fresh water, biogeography, local adaptations, life his-
tory evolution, and speciation in fishes derived from
marine environments. In addition, origins of the biodi-
versity in Cottus species are relevant to a general under-
standing of the evolution of coldwater adapted freshwa-
ter fishes in the Northern Hemisphere. In this review
paper, we will examine the evolutionary histories of
freshwater sculpins, especially the genus Cottus and its
relatives based on molecular genetic analyses and life
history diversity.
Freshwater sculpins as an ecological grouping
in cottoids
The superfamily Cottoidea (cottoids), which comprises
ca. 670 species and 149 genera in 11 families, is distrib-
uted widely in Northern Hemisphere waters. Although
most species are marine, many live in freshwater, being
generally termed freshwater sculpins (not a valid taxo-
nomic group). They include species of Cottus,
Trachiderm us, Mesocottus, Myoxocephalus, and the
Baikal sculpins, the first-mentioned being the most
speciose taxonomic group with 64 species (Berg 1949;
McAllister and Lindsey 1961; Scott and Crossman
1973; Chereshnev 1982; Lee et al. 1980; Goto 2001a;
Moyle 2002; Kottelat and Freyhof 2007; Sideleva and
Goto 2009; Eschmeyer and Fricke 2010; Yokoyama and
Goto 2011), although Kinziger and Wood (2010) num-
bered 68 species, including some undescribed. These
species represent a taxonomic group that has success-
fully adapted to various freshwater environments and
become morphologically, physiologically, ecologically
and behaviorally diverse. The second most abundant
group, the Baikal sculpins, includes 33 species in 12
genera representing 3 families (Sideleva 2003). The
remaining taxa include Trachidermus and Mesocottus
(each with a single species) and Myxocephalus (one
species with two subspecies: Goto 1990; Kontula and
Väinöla 2003; Yokoyama and Goto 2011).
Species diversity, distribution, and life histories
of freshwater sculpins
Species diversity and distribution of Cottus species
Fishes of the genus Cottus are distributed in freshwater
throughout most of Europe, Siberia, Central Asia, East
Asia (including the Japanese Archipelago), and North
America (Fig. 1). Cottus species are typical coldwater-
adapted fishes. Like salmonids and sticklebacks, they
are a major component of fish communities in rivers and
lakes distributed in the middle to high latitudinal regions
(Freeman et al. 1988; Goto and Nakano 1993; Miyasaka
and Nakano 1999). The species richness (64 species) of
Cottus is similar to those of the salmonids, Salvelinus
(56 species) and Coregonus (72 species) and well ex-
ceeds those of Gasterosteus (6 species), Phoxinus (25
species) and Thymallus (13 species), all of which share
Northern Hemisphere ranges similar to that of the
Cottus species (Eschmeyer and Fricke 2010).
Most individual Cottus species show regional speci-
ficity in their geographic distribution (Fig. 1), with 11
species in East Asia, 9 species in Siberia (considered
broadly), 16 species in Europe, 19 species on the Pacific
Ocean side of the North America, and 15 species in the
inland areas of the North America. It is generally true
that Cottus species are sedentary (McCleave 1964; Hill
and Grossman 1987; Goto 1998; Natsumeda 2007),
tending to be isolated to specific areas within eac h
habitat. In addition, because their populations often
adapt locally, a species may diverge both ecologically
and morphologically (Yokoyama and Goto 2002;
Kinziger and Wood 2003; Nolte et al. 2006). Such
divergent characteristics have contributed to the high
species richness in each local region.
Cottus species inhabit a variety of freshwater envi-
ronments that include lakes and the upper, middle and
lower courses of rivers (Goto and Nakano 1993; Petty
and Grossman 1996, 2010; Goto et al. 2013). Each
Environ Biol Fish

species may utilize a particular habitat, those in rivers,
often preferring a gravel substrate with many flat rocks
on the riverbed, although some inhabit sandy or muddy
substrate in rivers or water deeper than 100 m in lakes
(McPhail and Lindsey 1970; Moyle 2002). A few un-
usual species, which inhabit freshwater caves in karst
landforms, are characterized by small eyes, large head
sensory canals, and sparse body pigmentation (Burr
et al. 2001). In addition, there are several species that
inhabit marine coastal areas for a short period of their
life history, although generally categorized as freshwater
amphidromous fishes (McDowall 2007). Clearly, Cottus
species can inhabit a variety of freshwater environments
and are “versatile and successful fish” as described by
Mills and Mann (1983). Additionally, Moyle (2002)
mused: “perhaps no group of fishes occurring in the
fresh water s of Califor nia have given biologists
(including this author) more identification headaches
than sculpins.” Such challenges are probably due to
the subtle interspecific morphological differences that
have likely arisen from small habitat differences driving
species divergence (Goto 1977, 1990; Yamazaki et al.
2003; Kinziger and Wood 2003, 2010).
Clearly, Cottus species present special taxonomic
challenges. The Cottus pollux species complex is an
especially complicated group, remains a source of con-
fusion in the taxonomy of Japanese Cottus species. To
date, a number of species, including C. kazika, C.
hangiongensis, C. nozawae, C. amblystomopsis,
C. reinii, the large-, medium-, and small-egg types of
C. pollux, and a few undescribed species exhibiting
substantial genetic divergence, have been recorded from
Japan (Fig. 2) (Goto 2001b; Goto et al. 2001; Yokoyama
2010; Yokoyama and Goto 2011). In the present paper,
Mesocottus
haitej
Myoxocephalus quadricornis quadricornis
Myoxocephalus q.
thompsoni
Europe
Cottus gobio
C. aturi
C. duranii
C. haemusi
C. hispaniolensis
C. koshewnikowi
C. metae
C. microstomus
C. perifretum
C. Petiti
*C. poecilopus
C. rhenanus
C. rondeleti
C. sabaudicus
C. scaturigo
C. transsilvaniae
Siberia East Asia
Pacific Ocean
Coast of North
America
North America
C. altaicus
*C. cognatus
C. dzungaricus
C. kuznetzovi
C. nasalis
*C. poecilopus
C. sibiricus
*C. szanaga
C. spinulosus
C. amblystomopsis
C. czerskii
C. hangiongensis
C. kazika
C. koreanus
C. nozawae
C. pollux (the middle-egged type)
C. pollux (the large-egged type)
C. reinii
C. pollux (the small-egged type)
*C. szanaga
C. volki
C. aleuticus
C. asper
C. asperrimus
*C. bairdii
C. beldingii
C. bendirei
*C. cognatus
C. confusus
C. greenei
C. gulosus
C. hubbsi
C. klamathensis
C. leiopomus
C. marginatus
C. perplexus
C. pitensis
C. princeps
C. rhotheus
C. tenuis
C. baileyi
*C. bairdii
C. caeruleomentum
C. carolinae
C. chattahoochae
*C. cognatus
C. echinatus
C. extensus
C. girardi
C. hypselurus
C. immaculatus
C. kanawhae
C. paulus
C. ricei
C. tallapoosae
Trachidermus fasciatus
Cottidae
Abyssocottidae
Comephoridae
Abyssocottus (3 spp.)
Asprocottus (6 spp.)
Cottinella (1 sp.)
Cyphocottus (2 spp.)
Limnocottus (4 spp.)
Neocottus (2 spp.)
Procottus (4 spp.)
Comephorus (2 spp.)
Batrachcottus (4 spp.)
Cottocomephorus (3 spp.)
Leocottus (1 sp.)
Paracottus (1 sp.)
Baikal sculpins (33 species and 12 genera in 3 families)
Fig. 1 Schematic diagram showing the geographic distribution of
the genus Cottus and its relatives (in grey areas), and species
richness in each of the geographic region Europe, Siberia, East
Asia, west coast of North America, and the northeast coast of
North America of the Northern Hemisphere (Eschmeyer and
Fricke 2010 ). A few species, Cottus bairdii, C. cognatus, C.
poecilopus and C. szanaga, which are distributed in multiple
geographic regions are numbered in each region. In addition, the
distributional ranges of Baikal sculpins and Mesocottus haitej and
the Myoxocephalus species group are represented in left and right
side boxes, respectively. Data for the distribution of each species
and species group followed Berg (1949), Scott and Crossman
(1973), Chereshnev (1982), Lee et al. (1980), Goto (2001a),
Moyle (2002), Kottelat and Freyhof (2007), Sideleva and Goto
(2009), Eschmeyer and Fricke (2010), and Kinziger and Wood
(2010)
Environ Biol Fish

for convenience, the small egg-type of C. pollux is
considered as a synonym of C. reinii due to their low
level of genetic differentiation (Yokoyama and Goto
2005;Tsukagoshi2012), although the fomer has a
freshwater amphidromous life history and is distributed
allopatrically to C. reinii (endemic to the Lake Biwa,
migrating between the lake and feeder rivers).
Life histories of Cottus species
Most Cottus species have fluvial or lacustrine life histo-
ries, living in fresh water throughout their lives (Fig. 2).
However, several Cottus species that have diadromous
life histories are distributed in the East Asia and on the
Pacific coast of North America. In East Asia including
Japan, catadromous, freshwater amphidromous (hereaf-
ter, referred to as amphidromous), lacustrine and fluvial
life histories are common (Fig. 2)(Goto1990;
Yokoyama and Goto 2011).
A unique catadromous species of Cottus, C. kazika,
inhabits fresh water during its juvenile and young
stages, adult subsequently migrating downstream to
the sea to spawn (Takeshita et al. 1999). Adult females
produce many small eggs [ca. 870–1,450/clutch and
1.4–1.6 mm in diameter (Goto 2001b)] from which
small pelagic larvae hatch. Such larvae remain in the
marine coastal waters for ca. 1–2 months, before mi-
grating to river mouths and settling upstream on the
riverbed. There they attain adultfood and the cycled is
repeated (Fig. 2).
Amphidromous Cottus species produce many small
eggs (ca. 400–3,600/clutch) in the lower reaches of
rivers (Goto 2001b), where they generally spawn on
the gravel substrate. The newly hatched larvae rise to
the surface of the river (a phototactic response) and then
drift downstream to the estuary (Goto 1977, 1981a,
1990). This strategy may contribute to high survival of
larvae (Goto 1977, 1988, 1993). The pelagic larvae
spend about one to 1 ½months in the marine coastal
areas before migrating to river mouths and settling on
the riverbed. In the rivers, they eventually attain matu-
rity as adults. In Japan, amphidromous life histories in
fishes are restricted to ayu (Plecoglossus altivelis) and a
number of gobiid fishes in the genera Gymnogobius and
Rhynogobius, and subfamily Sicydiinae, in addition to 4
Cottus species, including
C. amblystomopsis,
C. hangiongensis, C. reinii and the medium egg type
of C. pollux (Goto 1990; Shimize et al. 1994; Goto and
Arai 2003, 2006; Tsukagoshi et al. 2011; Yokoyama and
Goto 2011; Tsukagoshi 2012).
In addition to catadromous and amphidromous life
histories, a number of Cottus species have a lacustrine or
fluvial life history (Table 2). The former includes two
types: (1) migrating between a lake and its inlet rivers of
which the former is used for growth and the latter for
reproduction, as exhibited by the C. reinii population in
Lake Biwa, and (2) living exclusively in a lake (referred
to as lacustrine landlocked), as seen in populations of
Alaskan C. aleuticus (A. Goto unpubl. data) and
C. extensus (Neverman and Wurtsbaugh 1992;
Ruzycki et al. 1998). Mature females of lacustrine land-
locked species produce many small eggs [ca. 2,000–
3,000/clutch and 1.4–1.6 mm in diameter for C. reinii
(Goto 2001b)], the larvae living pelagically, as in the
North American C. extensis (Ruzycki et al. 1998).
Femailes of other lacustrine species produce a small
number of large eggs that give rise to benthic larvae,
as in the North American C. cognatus (Heard 1965;
Fig. 2). A lacustrine landlocked life history in Cottus
species is probably less common in Europe (Koli 1969;
Witkowski 1979; Kotusz et al. 2004), although common
in North America (Faber 1967; Krejsa 1967; Moyle
2002; Lindstrom 2005; Baumsteiger et al. 2012).
In contrast, fluvial species, which live in rivers for
their entire lives, utilize the latter for both growth and
reproduction, and usually produce a small number of
large eggs [ca. 100–200/clutch and 2.8–3.4 mm in di-
ameter for C. nozawae (Goto 1990, 2001b)]. Larvae
undergo direct development and are benthic immediate-
ly after hatching (Goto 1975, 1977, 1983, 1987, 1990,
2001b).
Life history evolution and speciation events in the genus
Cottus
Based on a number of studies on the diversity of life
histories in Cottus species, a hypothesis of speciation
has been proposed, viz “speciation from amphidromous
fishes to fluvial species resulting from land-locked pop-
ulations of the former” (Mizuno 1963; Goto 1977, 1990,
1994, 1996, 2001b). For instance, Goto (1981b, 1990,
1996, 2001b) speculated that in both the amphidromous
sculpin C. amblystomopsis and fluvial sculpin
C. nozawae, which are sister taxa, speciation occurred
from a common ancestor as a result of an opportunity for
life history divergence.
Environ Biol Fish

This speciation hypothesis is based upon the results
of comparative studies of early ontogenetic develop-
ment and a physiological trait shared between the two
species. Larvae of fluvial C. nozawae hatch after a two
prolonged developmental stage, compared with those of
amphidromous C. amblystomopsis. Consequently, the
C. nozawae larvae are larger and more advanced in
development than the latter. Because C. nozawae can
begin a benthic life just after hatching, the larvae are
well adapted to the upper reaches of rivers where
food availability is limited for less advanced larvae
(Greenberg 1964; Goto 1975, 1977, 1990; Maekawa
and Goto 1982). A speciation model based on an
opportunity for life history divergence that is accom-
panied by the relationship between egg size and
early ontogenetic development is also known for
the amphidromous and fluvial pair of sister taxa in
other aquatic animals such as ragworms (Hediste
spp.) (Sato 1999; 2001), freshwater shrimps
(Palaemon paucidens) (Nishino 1980; Chow et al.
1988), freshwater prawns (Macrobrachium
nipponensis) (Shokita 1975, 1979; Mashiko 1990,
2001)andgobiidfishes(Rhinogobius spp. and
R. flumineus) (Mizuno 1960, 1963; Nishida 1994,
1996, 2001).
The physiological similarity shared by larvae of both
C. amblystomopsis and C. nozawae include tolerance to
salinity and ability to survive in seawater (Goto 1981b),
suggesting that salinity tolerance in C. nozawae larvae
was probably inherited from an ancestral marine sculpin
species, and that freshwater adaptation was probably
acquired as the species became fluvial, and large eggs
evolving as a long-term consequence of freshwater ad-
aptation (Goto 1981b, 1990, 1994, 1996, 2001b; Goto
and Andoh 1990; Okumura and Goto 1996; Yokoyama
and Goto
2005, 2011). From these genetic, ecological,
and physiological data, a hypothesis of speciation has
been proposed as “speciation from an ancestral species
having an amphidromous life history to the fluvial
C. nozawae” (Goto 1996, 2001b; Yokoyama and Goto
2005, 2011).
The process by which diadromous fishes become
land-locked is well known in anadromous species such
as in many salmonids. However, land-locking in anad-
romous salmonids has not usually led to speciation,
although contributing to intraspecific life history varia-
tions (Foote et al. 1989, 1992; Wood and Foote 1990;
Taylor et al. 1996; Beacham et al. 2012). For conversion
from an amphidromo us to a fluvial life history, the
following life history traits would inevitably to change;
Lacustrine
Catadromous
Lacustrine
land-locked
(having pelagic larvae)
Amphidromous life
between a lake and river
Lacustrine
land-locked
(having benthic larvae)
Freshwater
amphidromous
River
Sea
S
PlL
BL
BL
PlL
S
S
S
S
S
S
BL
BL
BL
BL
BL
PlL
PlL
PlL
Fluvial
Fig. 2 Schematic diagram of life histories of the Cottus species.
Lines labelled “allow” indicate migration of fishes from one
habitat to another habitat. Classification of life histories followed
Goto (1987, 1990) and Tsukamoto (1994). The lacustrine life
history was subdivided into land-locked lacustrine, lacustrine
and fluvial life histories (see Text and Table 2). BL: benthic life,
PlL: pelagic larval life, S: spawning
Environ Biol Fish

an increase in egg size by which large well-developed
larvae are produced, and the acquisition of freshwater
tolerance during the benthic larval period after hatching
(Mizuno 1963; Goto 1990, 1996, 2001b; Nishida 1996,
2001). Such changes in life history traits probably lead
to speciation from an amphidromous ancestral species to
a fluvial species, although the changes may be unlikely
to occur simultaneously.
Goto (1996, 2001b) proposed a hypothesis that spe-
ciation of fluvial C. nozawae may have occurred in
parallel in more than on e location, which he called
“polypatric speciation and parallel evolution of life his-
tory traits”.
Species diversity, distribution and life history
of other freshwater sculpins
The g enus Tra ch id er m us includes a single species,
T. fasciatus, which is restricted to the rivers flowing into
the Ariake Bay, Kyushu Island, Japan, and those
flowing into the Yellow and Bohai seas (Tsukahara
1952;TakeshitaandKimura1994;Takeshitaetal.
2004). The tidal ranges in those areas is significant,
tidewaters extending long distances up the rivers, which
have shallow gradients and extensive tidal flats
(Takeshita and Kimura 1994). Female T. fasciatus pro-
duce a large number of small eggs [ca. 288–6,050 and
1.4–1.9 mm in diameter (Goto 2001b)] from which
small pelagic larvae hatch. Genetic data suggest that
the populations in the Ariake Bay were isolated from
those in the Yellow and Bohai seas in the late
Pleistocene when those waters occupied distinct ocean
basins (Yokoyama and Goto unpubl. data). This species
has a catadromous life history, migrating to the sea to
spawn.
Mesocottus haiteji, the only known species in the
genus, is distributed in the lower to upper reaches of
the Amur River basin and to rivers flowing into the
Mamiya (Tatar) Strait between the northern Sakhalin
Island and the east coast of Siberia. The species appears
to be typical of the endemic freshwater fishes of the
Amur River basin (Berg 1949). However, there is little
known of its life history. Distribution records in the
Silka River, the uppermost river in the Amur River
basin, indicate a probable fluvial life history.
Although species of Myoxocephalus are predomi-
nantly marine, M. quadricornis (two subspecies) in-
habits freshwater lakes. Controversy exists as to whether
the subspecies should be treated as distinct species.
Furthermore, M. quadricornis that are distributed in
North America are always referred to the genus
Tri gl ops is (McAllister 1961;McAllisterand
Aniskowicz 1976; Eschmeyer and Fricke 2010). The
present paper follows Kontula and Väinölä (2003) for
the taxonomy of M. quadricornis based on the data on
genetic relat ionships betwee n the Palea rctic and
Newarctic fishes.
The fourhorn sculpin M. quadricornis quadricornis
includes a marine form that lives in shallow brackish
coastal waters along the Arctic Sea face of the Eurasian
and North American continents, as well as land-locked
populations in northern Europe (Fig. 2). In contrast, the
deepwater sculpin M. quadricornis thompsonii is dis-
tributed in North American lakes, adults usually
inhabiting depths greater than 50 m. In Lake Superior,
the sculpins live in the deepest zone (about 400 m) of the
lake (Selgeby 1988) and in lakes where M. quadricornis
thompsonii occurs with one or more other Cottus spe-
cies, it appears to inhabitat depths greater than the latter
(Selgeby 1988). The lacustrine populations of both
M. quadricornis subspecies, both characterized by pe-
lagic larvae, remain land-locked throughout life (Fig. 2)
(Nyman an d Westin 1968;Westin1969;Khanand
Faber 1974; Geffin and Nash 1992).
Baikal sculpins, endemic to Lake Baikal as their
common name suggests, are also a suitable group for
studying adaptive radiation. Like cichlid fishes in
African lakes and Darwin’s finches in the Galápagos
Islands, Baikal sculpins are extremely specialized in
their ecological and morphological characteristics.
They include 33 species in 12 genera representing 3
families (Table 1) (Sideleva 2002, 2003). The ecological
and life history diversity of Baikal sculpins is described
in detail latter in this review.
Molecular phylogeny of species in the genus Cottus
and its relatives
Acomprehensivehypothesisforthephylogenyof
Cottus species and their relatives, based on previous
studies of their molecular phylogeny, is presented here
with suggestions regarding their zoogeographic distri-
bution and discussion of their evolutionary history.
Previous studies of the molecular phylogeny and
population genetic structure of Cottus are listed in
Table 1. Many have examined inter- and intraspecific
relationships of the C. gobio species complex in Europe,
Environ Biol Fish

Ta b l e 1 References of studies on molecular phylogeny and genetic population structure for the freshwater sculpins
Main subject Preference Main region surveyed Object of taxon Molecular marker
Genetic relationships
among species within
Yokoy a ma a nd Goto (2005)
a
Eurasia, Lake Baikal and North
America
Eurasian Cottus and its relatives mtDNA 12S, CR
Within a genus Kinziger et al. (2005)
a
North America, Lake Baikal and
Eurasia
Cottus and Baikal sculpins mtDNA Cyt b, ATPase 8/6
Genetic relationships among Kontula et al. (2003)
a
Lake Baikal, Eurasia and North
America
Baikal sculpins and Cottus mtDNA Cyt b, ATPase 8/6, CR
Baikal sculpins Nishida et al. (1999)LakeBaikal Baikalsculpins mtDNA16S
Kiril’chik and Slobodyanyuk
(1997)
Lake Baikal Baikal sculpins and Cottus mtDNA Cyt b
Genetic relationships
among closely
Hunt et al. (1997)LakeBaikal Baikalsculpins ncDNArodopsin
Related species, and speciation Kiril’chik et al. (1995)LakeBaikal Baikalsculpins mtDNACytb
Slobodyanyuk et al. (1995)LakeBaikal Baikalsculpins mtDNACytb,ATPase8/6
Grachev et al. (1992)LakeBaikal Baikalsculpins mtDNACytb,ATPase8/6
Genetic relationships among
closely related species, and
speciation
Okumura and Goto (1996)Japan Cottus amblystomopsis and C. nozawae mtDNA-RFLP, allozyme
Goto and Andoh (1990)Japan Cottus amblystomopsis and C. nozawae allozyme
Okazaki (1997)Japan Cottus pollux species group mtDNA ND1, ND2•allozyme
Okazaki et al. (1994)Japan Cottus pollux species group allozyme
Okazaki and Kobayashi (1992)Japan Cottus pollux species group allozyme
Hybridazation between
closely
related species
Strauss (1986)NorthAmerica Cottus bardii and C. cognatus allozyme
Zimmerman and Wooten (1981)NorthAmerica Cottus cognatus and C. confusus allozyme
Taxonomy of polytypic
species
and genetic relationships
among them
Shedko and Miroshnichenko
(2007)
East Asia Cottus volki mtDNA CR
Kinziger et al. (2007)NorthAmerica Cottus carolinae species group mtDNA ATPase 8/6
Kinziger and Wood (2003)NorthAmerica Cottus hypselurus mtDNA Cyt b
Eppe et al. (1999)Europe
Cottus petiti (C. gobio species group) allozyme
Nyman and Westin (1968)Europe Myoxocephalus quadricornis species
group
allozyme
Genetic population structure
and phylogeny
Yokoy a ma e t a l . (2008)
a
Eurasia Cottus poecilopus species group mtDNA CR
Šlechtov á et al. (2004)Europe Cottus gobio species group mtDNA CR
Paśko and Maslak (2003)Europe Cottus poecilopus allozyme
Kontula and Väinölä (2004)Europe Cottus gobio species group mtDNA CR, allozyme
Kontula and Väinölä (2003)PanArcticSea Myoxocephalus quadricornis species
group
mtDNA Cyt b, ATPase 8/6
Vo l c k ae r t e t a l . ( 2002)Europe Cottus gobio species group mtDNA CR
Yokoy a ma a nd Goto (2002)Japan Cottus nozawae mtDNA CR
Kontula and Väinölä (2001)Europe Cottus gobio species group mtDNA CR, allozyme
Environ Biol Fish

the C. poecilopus species group in Eurasia, the C. pollux
species complex and the C. nozawae species group in
Japan and its neighboring areas, and both the
C. carolinae and C. hypselurus species groups in
North America. Unfortunately, a genetic-based hypoth-
esis for the interspecific phylogeny of Cottus has not yet
been presented for most of the species included in the
genus.
Phylogenetic analyses using regional Cottus species
groups and closely related genera
Phylogenetic relationships have been reported for
Cottus species and their relatives from eastern Eurasia
and East Asia (Yokoyama and Goto 2002; Yokoyama
et al. 2008), North America (Kinziger et al. 2005) and
the Baikal sculpins (Kontula et al. 2003) (Table 2). A re-
analysis of these results enabled two phylogenetic trees,
based on common mtDNA markers for as many Cottus
species as possible, to be constructed. From these, we
have hypothesized the most comprehensive and reliable
phylogeny of Cottus sp ecies and their r elatives
(Fig. 3a, b).
The first tree, estimating phylogenetic relationships
among Cottus species and their relatives from North
America, Lake Baikal, and a part of Eurasia, was based
on data from Kontula et al. (2003) and Kinziger et al.
(2005) (Fig. 3a). The second tree estimated the relation-
ships among most of the Cottus species from Eurasia
and East Asia, being based on data from Kontula et al.
(2003), Yokoyama and Goto (2005) and Yokoyama
et al. (2008) (Fig. 3b). In both phylogenetic analyses,
marine sculpins (families Cottidae or Psycholutidae)
were used as outgroups. Additionally, samples of
Myoxocephalus quodricornis quodricornis and
M. quodricornis thompthoni, both freshwater sculpins,
were also used as an outgroup, although they did not
appear to be closely related, at least in morphology, to
the Cottus species (Yabe 1985).
The two phylogenetic trees obtained (Fig. 3a, b) were
similar in that the Cottus species and their relatives
included several lineages. The species composition of
each lineage did not differ substantially between the
trees, the phylogeneti c relat ionships determined for
Cottus species and their relatives being as follows: (1)
agroupcomprisingCottus species (except for
C. kazika), Trachidermus fasciatus
, the Baikal sculpins,
and a euryhaline species Leptocottus armatus, from
North America appear to be a monophyletic lineage
Ta b l e 1 (continued)
Main subject Preference Main region surveyed Object of taxon Molecular marker
Englbrecht et al. (2000)Europe Cottus gobio species group mtDNA CR
Hänfling and Brandl (1998)Europe Cottus gobio species group allozyme
Riffel and Schreiber (1995)Europe Cottus gobio species group allozyme
Interfamilies and intergenera Smith and Wheeler (2004)ScorpaenisformesfishesmtDNA,ncDNA
mtDNA mitochondrial DNA, 12S 12S rRNA, 16S 16S rRNA, CR control region, Cyt b cytochrome b, ncDNA nuler DNA, RFLP restricted fragment lengthpolymorphismanalysis
a
Articles which were used for phylogenetic analysis in this study
Environ Biol Fish

Ta b l e 2 Life history styles in freshwater sculpins
Species Lineage group
a
Life history style Spawning ground
b
Type of larvae
b
Reference
Myoxocephalus quadricornis quadricornis M/E/Lp coasta l marine/brackish/lake pelagic Westin (1969), Khan and Faber (1974)
Myoxocephalus quadricornis thompsoni Lp lake pelagic Khan and Faber (1974), Selgeby (1988),
Geffin and Nash (1992)
Mesocottus haitej – (F) (river) ? Berg (1949)
Leptocottus armatus unknown E coastal marine pelagic Jones (1962)
Trachidermus f a s c i a t u s Lineage A C coastal marine pelagic Takeshita et al. (1997), Onikura et al. (2002)
Cottus kazika Lineage A C coastal marine pelagic Kinoshita et al. (1999), Harada et al. (1999)
C. amblystomopsis Lineage C A river pelagic Goto (1975), Goto and Arai (2006)
C. nozawae Lineage C F river benthic Goto (1975), Goto and Arai (2006)
C. hangiongensis Lineage C A river pelagic Goto (1981a), Goto and Arai (2006)
C. koreanus Lineage C F river benthic Byeon et al. (1995), Fujii et al. (2005)
C. czerskii Lineage D A river (pelagic) Kolpakov (2009)
C. pollux (small-egged type) Lineage D A river pelagic Mizuno and Niwa (1961), Mizuno (1963),
Goto and Arai (2003)
C. reinii Lineage D La river/lake pelagic Watanabe (1958), Kurawaka (1992)
C. pollux (middle-egged type) Lineage D A river pelagic Shimizu et al. (1994), Goto and Arai (2003)
C. pollux (large-egged type) Lineage D F river benthic Mizuno and Niwa (1961), Mizuno (1963),
Goto and Arai (2003)
C. poecilopus Lineage B F/Lb ri ver/la ke benthic Starmach (
1962), Przybylski and
Borowska (1998)
C. altaicus Lineage B F (river) (benthic) Sideleva and Goto (2009)
C. dzungaricus – F(river) (benthic)Kottelat(2006)
C. kuznetzovi – F(river) (benthic)SidelevaandGoto(2009)
C. szanaga Lineage B F (river) (benthic) Sideleva and Goto (2009)
C. volki Lineage B F (river) (benthic)ShedkoandMiroshnichenko(2007),
Sideleva and Goto (2009)
C. aleuticus Cottopsis lineage A/Lp river/lake/river mouth pelagic Heard (1965), Brown et al. (1995)
,Moyle(2002)
C. asper Cottopsis lineage A/Lp/F river/lake/river mouth pelagic Sinclair (1968), Brown et al. (1995),
Moyle (2002), Baumsteiger et al. (2012)
C. asperrimus Cottopsis lineage F/Lb river/lake benthic Daniels and Moyle (1978), Moyle (2002)
C. gulosus Cottopsis lineage F river benthic Lee et al. (1980), Moyle (2002)
C. klamathensis Cottopsis lineage F/Lb river benthic Moyle (2002)
C. marginatus Cottopsis lineage F (river)(benthic)Leeetal.(1980)
C. perplexus Cottopsis lineage F river benthic Mo yle (2002)
Environ Biol Fish

Ta b l e 2 (continued)
Species Lineage group
a
Life history style Spawning ground
b
Type of larvae
b
Reference
C. pitensis Cottopsis lineage F river benthic Moyle (2002)
C. princeps Cottopsis lineage (Lb)/F (lake) ? Robins and Miller (1957)
C. beldingii unknown F/Lb river/lake benthic Ebert and Summerfelt (1969),
Moyle (2002)
C. confusus unknown F river (benthic) Gasser et al. (1981)
C. gr eenei unknown F (river) (benthic) Lee et al. (1980)
C. leiopomus unknown F (river) (benthic) Meyer et al. (2008)
C. rhotheus Uranidea lineage F/Lb river/lake (benthic) Lindstrom (2005)
C. tenuis Uranidea lineage F/Lb river/lake (benthic) Robins and Miller (1957)
C. bairdii Uranidea lineage F/Lb/Lp river/la ke benthic/pelagic Faber (1967), Scott and Crossman
(1973), Grossman et al. (2002)
C. cognatus Uranidea lineage F/Lb river/lake benthic Heard (1965), Scott and Crossman (1973)
C. baileyi Uranidea lineage F river (benthic) Lee et al. 1980
C. bendirei Uranidea lineage F (river) (benthic) Markle and Hill (2000)
C. caeruleomentum Uranidea lineage F (river) (benthic) Kinziger et al. (2000)
C. car olinae Uranidea lineage F river (benthic) Lee et al. (1980)
C. chattahoochae – Friver (benthic)Neelyetal.(2007)
C. echinatus (extincted) – Lp (lake) ? Lee et al. (1980)
C. extensus Uranidea lineage Lp lake pelagic Ruzycki et al. (1998), Ruzycki
and Wurtsbaugh (1999)
C. girardi Uranidea lineage F (river) (benthic) Lee et al. (1980)
C. hypselurus Uranidea lineage F (river) (benthic) Kinziger and Wood (2010)
C. hubbsi Uranidea lineage F river (benthic) Markle and Hill (2000)
C. immaculeatus – F(river) (benthic)KinzigerandWood(2010
)
C. kanawhae Uranidea lineage F (river) (benthic) Robins (2005)
C. paulus Uranidea lineage F river (benthi c ) Lee et al. (1980)
C. tallapoosae – Friver (benthic)Neelyetal.(2007)
C. ricei Cottus lineage Lp/F river/lake pelagic Snyder and Ochman (1985),
Oyadomari and Auer (2004)
C. sibiricus Cottus lineage F (river) (benthic) Berg (1949)
C. gobio Cottus lineage F/Lp/Lb river/lake benthic/pelagic Smyly (1957), Witkowski (1979),
Wanzenböck et al. (2000)
C. aturi – F(river) (benthic)KottelatandFreyhof(2007)
C. duranii – F(river) (benthic)KottelatandFreyhof(2007)
C. haemusi – F(river) (benthic)KottelatandFreyhof(2007)
Environ Biol Fish

Ta b l e 2 (continued)
Species Lineage group
a
Life history style Spawning ground
b
Type of larvae
b
Reference
C. hispaniolensis – F(river) (benthic)KottelatandFreyhof(2007)
C. koshewnikowi – F/(Lb) (river/lake) (benthic) Kottelat and Freyhof (2007)
C. metae – F(river) (benthic)KottelatandFreyhof(2007)
C. microstomus – F/(Lb) (river/lake) (benthic) Kottelat and Freyhof (2007)
C. perifretum – F(river) benthicKottelatandFreyhof(2007)
C. petiti – F(river) benthicPersatetal.(1996), Kottelat
and Freyhof (2007)
C. rhenanus – F(river) benthicKottelatandFreyhof(2007)
C. rondeleti – F(river) (benthic)KottelatandFreyhof(2007)
C. sabaudicus – F(river) (benthic)Sideleva(2009)
C. scaturigo – F(river) (benthic)KottelatandFreyhof(2007)
C. transsilvaniae – F(river) (benthic)KottelatandFreyhof(2007)
C. nasalis – F(river) (benthic)Berg(1949)
C. spinulosus – F(river) (benthic)Berg(1949)
M marine, E euryhaline, C catadromous, F fluvial, La lacustrine-fluvial, Lb lake land-locked(be nthic larvae), Lp lake land-locked (pelagic larvae), A freshwater amphidromous
a
See Fig. 3 for lineage group and its name
b
The traits of spawning ground and type of larvae in parenthese are inferred from each reference cited
Environ Biol Fish

(designated the Major lineage), when marine species are
used as the outgroup; (2) the monophyletic
Myoxocephalus quadricornis group that includes only
a single species (two subspecies) differs substantially
both morphologically and genetically from the Major
lineage; (3) Cottus kazika is a sister taxon to
Trachidermus fasciatus (designated lineage A); (4) al-
though Leptocottus armatus ap pear es to be cl osel y
related to the lineage A, its phylogenetic status was not
determined; (5) Cottus species (except C. kazika) and
the Baikal sculpins are monophyletic; 6) Judging from
3) and 5), the genus Cottus as presently understood is
not monophyletic; (7) the monophyletic Major lineage
includes 7 further lineages: lineage B from Eurasia,
lineages C and D from East Asia, the Cottopsis clade
(sensu Kinziger et al. 2005) from the west coast of North
Fig. 3 Molecular phylogenetic trees of the genus Cottus and its
relatives. The maximum likelihood tree representing mitochondri-
al DNA phylogeny: (a) based on the cyt b + ATPase 8/6 dataset
(Kontula et al. 2003; Kinziger et al. 2005)), and (b) that based on
CR data (Kontula et al. 2003;YokoyamaandGoto2005;
Yokoyama et al. 2008). Nodes marked with a black diamond (♦)
indicate >50 % bootstrap statistical support. Lineages and names
follow Yokoyama and Goto (2005) and Kinziger et al. (2005). The
same lineages in the (a) and (b) trees were repeated to simplify
understanding of the relationships. For North American, Eurasian
and Baikalian cottoids (a), cytochrome b and ATPase 8/6 se-
quences (Cytb AF549104-AF549162, AY116340-AY116371,
AY833327-AY8333369; ATPa se8/6 AY116308- AY116339,
AY833272-AY833326), reported by Kontula et al. (2003) and
Kinziger et al. (2005) were obtained from DDBJ/EMBL/Genbank.
For the freshwater sculpins from Eurasia including the Baikal
cottoids (b), the hom ologous control re gion sequences
(AB059335-AB059350, AB188157-AB188173, AY116372-
AY116403, AB308477-AB308531, Kontula et al. 2003;
Yokoyama and Goto 2005; Yokoyama et al. 2008) were retrieved
from the database. CR and Cy tb-ATPase8/6 sequences were
aligned using Clustal X (Thompson et al. 1997) with default
settings and were checked by eye, respectively. Phylogenetic trees
were constructed using maximum likelihood (ML) methods with
RaxML v.7.0.4 (Stamatakis et al. 2008). The Akaike information
criterion implemented in ModelTest 3.7 (Posad and Crandall
1998) was used to determine the best-fit model of molecular
evolution. For each data set, the general time reversible (GTR)
model with proportion of sites assumed to be invariable and
variable sites assumed to follow a discrete gamma distribution
was selected as the best fit model. The reliability of the internal
branches was assessed by 1,000 bootstrap replicates
Environ Biol Fish

America, the Cottus clade from the Circum-Arctic sea,
the monophyletic Baikal sculpins (Kontula et al. 2003),
and the Uranidea clade. The phylogenetic status of four
Cottus species, C. beldingii, C. confuses, C. greenei and
C. leiopomus, was unable to be determined.
Species richness, distribution and life history
in each of the lineages proposed for the genus
Cottus and i ts relatives
Lineage A (East Asia)
Lineage A, including Cottus kazika and Trachidermus
fasciatus, was the first to diverge from the ancestral
Major lineage (Fig. 3a, b). The high probability exists
that the above two species are sister taxa, both because
of their genetic similarity (Fig. 3b) and their shared
catadromous life history. Both C. kazika and
T. f a s c i a t u s are distributed in East Asia, including
Japan. C. kazika is endemic to Japan, and T. faciatus
inhabits the rivers flowing into Ariake Bay of Kyushu
Island, Japan, and the Yellow Sea and rivers on the
southeastern part of the Korean Peninsula (Fig. 4).
Trachidermus fasciatus and C. kazika spawn in the
coastal waters of salinity concentrations of 20 ppt or
higher and 30 ppt or higher, respectively (Onikura et al.
1999; Takeshita et al. 1999). Their larvae do not develop
well in salinities below 20 ppt for the former species or
10 ppt for the latter (Takeshita et al. 1995, 1999).
Although both species can grow and reproduce in fresh-
water, their zygotes, embryos and larvae are not adapted
to fresh water or water with low salinity. Consequently,
lineage A species requires marine environments for
spawning and early ontogenetic development.
As shown in Fig. 3b, Trachidermus fasciatus has a
sister relationship with Cottus kazika which is presently
included in the genus Cottus. This result is strongly
supported by their common catadromous life history in
which adult fishes spawn in the sea, catadromy occur-
ring only in the above two species of about 100 species
of freshwater sculpins (Fig. 2, Table 2).
In one of the phylogenetic trees (Fig. 3a), a sister
taxon relationship between C. kazika and a euryhaline
species Leptocottus armatus was strongly supported. In
contrast, in the other tree (Fig. 3b), the relationship
between lineage A (C. kazika and Tr ach id erm us
fasciatus
) and L. armatus was not strongly supported.
Because the tree shown in Fig. 3a did not include
T. fasciatus, the sister relationship between C. kazika
and L. armatus shown the rein may be unreliable.
Consequently, the phylogenetic status of L. armatus
remains unresolved and although a relationship between
lineage A and L. armatus may exist, further studies are
necessary to clarify the phylogenetic status of
L. armatus. Significantly, perhaps, L. armatus is not a
freshwater species, inhabiting brackish waters through-
out its life (Jones 1962), although spaw ning in the
coastal seas and estuaries that exceed salinities of
10 ppt. The larvae are not adapted to fresh water
(Jones 19 62;Moyle2002), similar to those of
C. kazika and T. fasciatus.
Lineage B (northern Eurasia)
Lineage B includes the Cottus poecilopus species group
and is distributed in northern Eurasia from Primorskii to
the Siberian region in Russia, and in central Asia and
Linage A Linage B
Linage C
C. hangiongensis
- C. koreanus
C. amblystomopsis
- C. nozawae
Linage D
Cottopsis clade Cottus clade Uranidae clade
Baikal sculpins
Fig. 4 Geographic distribution indicated by black areas. Ranges
of lineages C and D drawn in high magnification. Distribution of
each lineage follows the references shown in Fig. 1
Environ Biol Fish

Europe (Figs. 3b and 4). Six sub-lineages are distributed
in (1) Europe (C. poecilopus), (2) the Irtysh River
(C. altaicus), (3) the Lena River (probably
C. kuznetzovi), (4) Eastern Siberia [C. kolymensis, re-
cently described as a new species of Cottus by Sideleva
and Goto (2012)], (5) the Amur River, Primorskii and
Sakhalin Island in Russia (C. szanaga), and (6) southern
Primorye, Russia, and the eastern Korean Peninsula
(C. volki)(ShedkoandMiroshnichenko2007;
Yokoyama et al. 2008; Sideleva and Goto 2009, 2012).
The life histories of speciesandpopulationsincluded
in lineage B are fluvial and lacustrine, and do not include
diadromous life histories (Witkowski 1979;Sidelevaand
Goto 2009, 2012). Those of C. poecilopus produce a
small number of large eggs, the larvae adopting a benthic
habit immediately after hatching (Starmach 1962;Jurajda
1992;PrzylskiandBorowska19 98). To date, no lac us-
trine species or populations have been reported. Larval
ecological characteristics of these species have not been
reported and pelagic larvae for this lineage are unknown
(Paśko and Maślak 2003).
Lineage C (East Asia)
Lineage C includes two sister taxon pairs: Cottus
amblystomopsis- C. nozawae and C. hangiongensis-
C. koreanus (Fig. 3a, b), the first species of each pair
being amphidromous and the second, fluvial. The
amphidromous species of each pair of sister taxa pro-
duce many small eggs from which pelagic larvae hatch,
and the fluvial species, a small number of large eggs
from which benthic larvae development directly.
Cottus amblystomopsis is distributed in Hokkaido
Island, Japan, and Sakhalin Isla nd and Primorye in
Russia, whereas C. nozawae is endemic to northern
Japan (Fig. 4)(Gotoetal.2001). Similarly,
C. hangiongensis is distributed in northern Japan and
the eastern Korean Peninsula, whereas C. koreanus is
restricted to the Korean Peninsula (Fig. 4). Thus, for
each pair of sister taxa, the amphidromous species are
distributed in both Japan and the eastern coast of
Eurasia, and the fluvial species are restricted to Japan
or the Korean Peninsula.
Lineage D (East Asia)
This lineage includes the Cottus pollux-C. reinii species
group (C. reinii with both amphidromous and lacustrine
life histories, and the amphidromous and medium-egg
type and the fluvial and large-egg types of C. pollux)
and C. czerskii, which is distributed along the eastern
coast of the Korean Peninsula to southern Primorskii,
Russia (Fig. 3b). Each of the large-egg and medium-egg
types of C. pollux is recognized here as a distinct spe-
cies, whereas the amphidromous small-egg type of
C. pollux and land-locked lacustrine C. reinii popula-
tions have been recently reaffirmed as a single species
C. reinii (Goto 2001b;YokoyamaandGoto2005;
Tsukagoshi 2012). The distributions of the species in
lineage D do not broadly overlap with those of lineage
C, although the fomer are distributed in Japan and along
the eastern coast of Asia (Fig. 4). The fluvial, large-egg
type of C. pollux and amphidromous medium-egg type
of C. pollux appear to be sister taxa (Fig. 3b), the third
such species pair observed in the genus Cottus, in addi-
tion to the two pairs of sister taxa in lineage C.
The C. pollux-C. reinii species group, which inspired
the model for speciation accompanying life history di-
vergence proposed by Mizuno (1963) and Goto (1977,
1990, 1996, 2001b), is a sister taxon related to
C. czerskii, which occurs in the Primorskii, Russia
(Fig. 3b) (Yokoyama and Goto 2005). The life history
of C. czerskii, which is important for interpreting life
history evolution in the C. pollux-C. reinii species
group, was recently reported to be amphidromous
and characterized by many small eggs (Kolpakov
2009). Thus, the lineage D species have life his-
tories that are common to amphidromous or lacus-
trine species and characterized by many small eggs
from which pelagic larvae are produced, except for
the large-egg type of C. pollux,whichisfluvial
and has a small number of large eggs from which
benthic larvae hatch (Table 3).
Lineage E (North America, the Pan-Arctic, and Lake
Baikal)
Lineage E corresponds to the sculpin group comprising
Cottus species from Europe, Siberia and North America
as well as the Baikal sculpins (Fig. 3b
) (Yokoyama and
Goto 2005). Furthermore, Kinziger et al. (2005) dem-
onstrated that lineage E included 4 divergent clades: (1)
the Cottopsis clade, (2) the Cottus clade, (3) the
Uranidea cl ad e, a nd (4 ) th e B aik al s cul pin s
(Fig. 3a). In this section, we follow the taxonomy
and names assigned to these species groups by
Kinziger et al. (2005).
Environ Biol Fish

The Cottopsis clade (western North America)
The Cottopsis clade of lineage E, being the first diver-
gent branch, includes 9 Cottus species that are distrib-
uted in rivers in western North America (Fig. 3a), only
C. asper occurring east of the Rocky Mountains
(Dennenmoser et al. 2013). Seven species have fluvial
and lacustrine life histories, and are characterized by
many small eggs and pelagic larvae (Table 3). The
remaining species, Cottus asper and C. aleuticus, are
both amphidromous and fluvial or lacustrine, the
amphidromous populations also having many small
eggs that produce pelagic larvae (Table 3). In Cottus,
the amphidromous life history occurs only in the west-
ern North American reprentatives of lineage E and in
lineages C and D from East Asia.
In C. asper and C. aleuticus, the coastal populations
are amphidromous and generally estuary-dependent for
part of their early life history (Mason and Machidori
1976; Brown et al. 1995), whereas the inland popula-
tions may be either fluvial or lacustrine (Moyle 2002).
The larvae of inland, lacustrine populations inhabit lakes
Table 3 Species richness of Baikal sculpins with reference to the ecological group and habitat zone
Family Species Ecologixal group Habitat zone
Cottidae Batrachocottus baicalensis Benthic Shallow water zone
(4 genera 9 spp.) Batrachocottus nikolskii Benthic Deep water zone
Batrachocottus talievi Benthic Wide water range
Batrachocottus maltiradiatus Benthic Deep water zone
Cottocomephorus grewingkii Benthopelagic Pelagic zone
Cottocomephorus alexandrae Benthopelagic Pelagic zone
Cottocomephorus inermis Benthopelagic Pelagic zone
Paracottus knerii Benthic Shallow water zone
Leocottus kesslerii Benthic Shallow water zone
Comephoridae Comephorus baicalensis Pelagic Pelagic zone
(1 genus 2 spp.) Comephorus dybowski Palagic Pelagic zone
Abyssocottidae Abyssocottus elochini Benthic ?
(7 genera 22 spp.) Abyssocottus gibbosus Benthic Deep water zone
Abyssocottus korotneffi Benthic Deep water zone
Asprocottus abyssalis Benthic Wide water range
Asprocottus herzensteini Benthic Wide water range
Asprocottus korjakovi Benthic Wide water range
Asprocottus korjakovi minor Benthic Wide water range
Asprocottus parmiferus Benthic Wide water rabge
Asprocottus platycephalus Benthic Wide water range
Asprocottus pulcher Benthic Wide water range
Cyphocottus megalops Benthic Wide water range
Cyphocottus eurystomus Benthic Wide water range
Cottinella boulengeri Benthic Deep water zone
Limnocottus bergianus Benthic Wide water range
Limnocottus godlewskii Benthic Wide water range
Limnocottus griseus Benthic Wide water rabge
Limnocottus pallidus Benthic Wide water range
Neocottus werestschagini Benthic Deep water zone
Neocottus thermalis Benthic Hydrothermal vent
Procottus jeittelesii Benthic Shallow water zone
Procottus gotoi Benthic Shallow water zone
Procottus gurwici Benthic Shallow water zone
Procottus major Benthic Wide water range
Environ Biol Fish

(rather than the sea) and are pelagic (Heard 1965;
Sinclair 1968). Inland populations of both C. asper
and C. aleuticus produce small to middle-sized eggs
that hatch into pelagic larvae (Krejsa 1967; Brown
et al. 1995; Moyle 2002; A. Goto unpubl. data), subse-
quently inhabiting pools and slow-moving regions of
rivers, although spawned in the upper reaches of the
same (Krejsa 1967; Brown et al. 1995; Moyle 2002).
Both the amphidromous coastal and inland fluvial or
lacustrine populations, despite their life history differ-
ences, have some ecological similarities with Cottus
species from East Asia.
The Cottus clade (sub Arctic areas)
The Cottus clade represents the second divergent branch
of lineage E (Fig. 3a) and includes Cottus gobio, type
species of the genus Cottus. The species in this clade
have a Holarctic distribution, being found throughout
the Eurasian and North American continents (Fig. 4).
Cottus gobio, distributed throughout Europe, appears
to include at least 7 sub-lineages, which are divergent
from each other among regions or river basins
(Engelbrecht et al. 2000;Volckaertetal.2002;
Šlechtova et al. 2004). The original species described
as Cottus gobio has since been reclassified into 16
species (Fig. 1) (Freyhof et al. 2005; Sideleva 2009).
Although our phylogenetic analysis did not include all
of the latter, with the exception of C. gobio, all probably
belong to the Cottus gobio species group.
Species in the Cottus gobio group are fluvial or
lacustrine, with no evidence of amphidromous popula-
tions (Table 3). The fluvial species or populations pro-
duce a small number of large eggs from which benthic
larvae hatch (Smyly 1957; Fox 1978). In contrast, the
lacustrine populations from the Hallstättersee Lake in
Austria produce pelagic larvae (Wanzenböck et al.
2000). In general, however, members of the Cottus
gobio species group appear to produce a small number
of large eggs, but have the potential to adapt to diverse
environments, having variable larval morphologies and
developmental patterns.
Cottus sibircus is distributed in the rivers of the
Siberian region (the Ob, Yenisei, and Lena river basins),
its geographic range paralleling that of the C. gobio
species group across the Ural Mountains. It is fluvial
(Berg 1949), producing a small number of large eggs
(126–664 eggs/clutch) from which benthic larvae hatch,
as observed for fluvial populations of C. gobio.
Also included in this clade, the North American
species C. ricei is broadly distributed from the
Laurentian Great Lakes across the Mississippi River
basin to the Mackenzie River basin and to rivers on
the coast of Hudson Bay. It has both fluvial and lacus-
trine populations (McPhail and Lindsey 1970; Lee et al.
1980), the latter appearing to produce larvae that are
pelagic for about 25 days (Snyder and Ochman 1985;
Oyadomari and Auer 2004).
The Uranidea clade (North America)
This Uranidea clade includes Cottus species that are
distributed in the regions abutting the Bering Sea,
Arctic Sea and Hudson Bay, and the rivers flowing into
the Atlantic Ocean and Gulf of Mexico that are
located to the east and north of the Rocky
Mountains in North Americ a (Figs. 3a and 4).
Five Cottus species from this lineage are also
distributed in the upper reaches of the Colombia
River basin, on the western side of the Roc ky
Mountains. Those species differ sub stantially f rom
the other members of the clade.
All of the species in the Uranidea lineage are fluvial
or lacustrine, there having been no diadromous species
reported for the group, although lineages A, C and D in
East Asia and the North American Cottopsis include
amphidromous species (Table 3). The fluvial species in
the Uranidea clade appear to produce benthic larvae
with direct development, whereas the lacustrine species
C. extensus spawns in the near shore area of lakes, the
pelagic larvae settling to the benthos as juveniles, as do
the larvae of many other Cottus species (Ruzycki
et al. 1998). In addition, lacustrine populations of
C. bairdii,whicharedistributedwidelyinNorth
America, appear to produce pelagic larvae (Faber
1967), whereas fluvial populations of that species
produce benthic l arvae (Table 3).
In summary, species in the Uranidea clade inhabit
rivers or lakes and generally produce a small number of
large eggs from which well-developed benthic larvae
are produced, although some lacustrine species or pop-
ulations produce many small eggs from which pelagic
larvae hatch.
Baikal sculpins
The remarkably specialized, and morphologically and
ecologically diverse Baikal sculpins have been recently
Environ Biol Fish

reconfirmed as monophyletic on the basis of molecular
phylogenetic studies (Fig. 3a, b) (Kontula et al. 2003;
Yokoyama an d Goto 2005:Kinzigeretal.2005),
appearing to be most closely related to lineage E, which
includes several North American Cottus species
(Fig. 3a, b). Furthermore, mtDNA analysis that included
most of the North American Cottus species indicated
that the Baikal sculpins plus the Uranidea clade and the
several as yet undescribed Cottus species are monophy-
letic (Fig. 3a). Since sim ilar results can be seen in
Fig. 3b, it is likely that the Baikal sculpins are members
of lineage E, although previously assigned to three
different families [Cottidae, Abyssocottidae and
Comephoridae sensu Sideleva (1982, 2001, 2003)].
Present evidence indicates that the Baikal sculpins
should be reassigned to a single family. It is also clear
that the Baikal sculpins, which have diverged
morphologically and ecologically to the extent of that
they have been classified into 12 genera (in the afore-
mentioned 3 families), appear to be closely related to
Cottus species such as C. bairdii, C. extensus and
C. cognatus, which are included in lineage Uranidea
sensu Kinziger et al. (2005) (Fig. 3a).
Non-determined lineages of four North American
species
Although the lineages of four North American Cottus
species (C. beldingii, C. confuses, C. greeni and
C. leiopomus), restricted to the upper reaches and trib-
utaries of the Colombia River basin, could not be deter-
mined, largely due to molecular markers providing too
little information for the analysis, it is likely that they
1. Spawning ground
freshwater
marine / brackishwater
2. Life history style
fluvial / lacustrine
amphidromous
catadromous
marine life (euryhaline)
3. Early developmental stage
of larvae
benthic
pelagic
benthic / pelagic
fluvial / lacustrine /
amphidromous (polymorphism)
Trait Trait
Baikal sculpins
Reproduction
in freshwater
Reproduction
in freshwater
LeT of C. pollux
MeT of C. pollux
C. reinii
SeT of C. pollux
C. czerski
C. nozawae
C. koreanus
C. hangiongensis
C. amblystomopsis
C. kazika
C. fasciatus
C. kazika
Linage A
Linage B
Linage C
Linage D
Linage E
Leptocottus
Comephorus baicalensis
Comephorus dybowskii
Cottocomephorus grewingkii
Cottocomephorus inermis
Leocottus kesslerii
C. aleuticus
C. asper
C. gobio
C. ricei
C. extensus
C. bairdii
C. gobio
C. bairdii
C. aleuticus
Uranidae
Cottus
Cottopsis
Fig. 5 Schematic diagram of life history evolution in the genus
Cottus and its relatives reconstructed on the phylogenetic trees [(a)
and (b)]. Node length does not indicate evolutionary distance
between sculpin species. The same lineages in (a) and (b) trees
were repeated to simplify understanding of the relationships. Three
life history related traits: spawning ground, life history and eco-
logical type of larvae, are indicated on the termini of the phyloge-
netic trees. The data of lifehistory-related traits follows references
shown in Table 2
Environ Biol Fish

belong to lineage E and the Cottopsis clade or Cottus or
Baikal sculpins (Fig. 3a).
Evolution of life histories in the genus Cottus
In this section, we attempt to correlate the evolution of
life history diversification in the Cottus species and their
relatives, primarily from information represented in the
phylogenetic trees (Fig. 5, Table 3).
Spawning grounds
The catadromous species T. fasciatus and C. kazika, and
the euryhaline species L. armatus, utilize marine and
brackish waters (>10–20 ppt in salinity) for reproduc-
tion (Onikura et al. 1999; Takeshita et al. 1999). While it
is believed that a seawater requirement is a phylogenetic
constraint, as it is for marine sculpin species, the former
two species shift their habitats to fresh water for part of
their lives.
In contrast, Cottus species except for C. kazika, and
the Baikal sculpins reproduce in fresh water in spite of
their geographic ranges and life histories (Trait 1 shown
in Fig. 5). These results suggest that the existing species
and life history diversities in Cottus and its relatives
have evolved from a common ancestor that had acquired
the traits necessary for reproducing in fresh water, in-
cluding freshwater tolerance of gametes, embryos and
larvae. The prior acquisition of traits such as freshwater
tolerance, larger egg size and strength of parental care
for embryos and larvae necessary for reproduction in
fresh water has probably played an important role in
adaptation to freshw ater environ ments in the genus
Cottus and its relatives.
Life history traits in the early developmental stages
Considering the evolution of life histories in the Cottus
species and their relatives, an outstanding feature is that
catadromous species exist only in lineage A, which is
distributed in East Asia (Trait 2 shown in Fig. 5). In
contrast, fluvial, lacustrine, and amphidromous life his-
tories are represented in each lineage divergent from
lineage A, although the life history of their common
ancestor has not yet been elucidated. The
amphidromous species which arose in lineages C and
D from East Asia and the Cottopsis clade from the North
American west coast are not monophyletic, as shown in
Figs. 3 and 5, and may have evolved independently in
each region. In addition, three pairs of sister taxa that
each has an amphidromous and fluvial species exist in
lineages C and D, su ggesting that such life history
divergence occurred separately within each pair, i.e.
parallel events (Yokoyama and Goto 2005).
Why does an amphidromous life history occur often
in East Asia and on the west coast of the North
America? In general, freshwater amphidromy is thought
to have evolved frequently in oceanic island environ-
ments in which there are short steep rivers and where
regional extinctions of endemic organisms have likely
occurred (McDowall 2004; Watanabe et al. 2013). In
East Asia, numerous oceanic island settings exist, for
example, Japan. In western North America, on the other
hand, distinct coastal regions may have resembled oce-
anic island settings in their effects. In both regions of
such environmental similality, amphidromous species
use the sea during their larval stage before inhabiting
the lower reaches of rivers (Goto 1990, 1996, 2001b).
Small steep rivers assist the downstream migration of
larvae of ayu, galaxiids, sculpins and gobiid fishes,
whereas large and low incline rivers present risks due
to exhaustion of larval energy reserves before feeding
can begin in coastal waters and to an extended period of
exposure to predation (Iguchi and Mizuno 1990;
Tsukamoto 1991; McDowall 2004, 2007, 2009, 2010;
Watanabe et al. 2013). Thus, it is likely that these similar
environmental features have promoted independent
evolution of amphidromous life histories in East Asia
and western North America.
Ecological and physiological traits in the larval stage
Traits that have ecological implications for the life his-
tories of Cottus species, hence significant implications
for speciation events, include egg size and the extent of
development of newly hatched larvae (Mizuno 1963;
Goto 1977, 1990, 1996, 2001b). Fluvial species usually
produce a small number of large eggs in the upper
reaches of rivers, from which large well-developed lar-
vae hatch through direct development of embryos.
Immediately after hatching they assume a benthic life.
Such ecological and morphological traits in egg size and
larval development are thought to be necessary for
adaption to the middle and upper reaches of rivers where
food availability for the larvae is low but predation
pressure is also low (Greenberg 1964; Goto 1981b,
1990). On the other hand, amphidromous and lacustrine
Environ Biol Fish

species usually reproduce in the lower reaches of rivers,
spawning many small eggs from which small and poorly
developed pelagic larvae hatch. After hatching, the
amphidromous larvae drift to the sea, whereas the lacus-
trine species spend a pelagic life in lakes. The habitat in
which both larval types occur are locations where food
availability is high but the risk of predation is also high
(Goto 1981b, 1990). Accordingly, a trade off between
environmental factors and reproductive features is ap-
parent between the latter species and the fluvial ones.
Clearly, it is important to focus on the distribution of
important ecologica l and physiological traits, b eing
linked to the life history characteristics of the larvae of
Cottus species and their relatives (Trait 3 shown in
Fig. 5, Table 3).
Pelagic larvae occur in all lineages except lineage B
from Eurasia (Fig. 5). Although lacustrine species that
inhabit still water environments generally produce pe-
lagic larvae, as do marine sculpin species that inhabit the
shallow coastal areas (Goto 1990, 2001b), benthic lar-
vae occur in species in each lineage, except for lineage
A and L. armatus (Fig. 5). This demonstrates that most
of the lineages have acquired the ability to spawn in
freshwater and can produce both the pelagic and benthic
larvae as a result of their adaptation to various freshwa-
ter environments. Several species, such as C. gobio and
C. bairdii, have intraspecific polymorphism and can
produce both pelagic and benthic larvae (Table 3). The
variability of the early developmental patterns in the
lineages that are able to spawn in freshwater may have
made possible the spread of Cottus species into a variety
of freshwater environments.
Evolutionary history and life history diversification
in the genus Cottus and its relatives
The phylogenetic trees (Fig. 3a, b) showed that the 2
subspecies of Myoxocephalus quadricornis are distantly
related to other freshwater sculpins considered in the
present study. However, the M. quadricornis species
group is justifiably included within the diversity of the
genus Myoxocephalus, which includes the marine scul-
pins (Kontula and Väinölä 2003). Therefore, it is rea-
sonable to consider that the adaptation to fresh water
seen in the M. quadricornis species group has occurred
independently and in a different way from that of Cottus
species and their relatives.
Following is a recons truction of the evolutionary
histories of Cottus species and their relatives, which
have greater species diversity and have adapted to a
wider variety of freshwater environments than those in
the genus Myoxocephalus, based on their molecular
phylogeny, patterns of geographic distribution of each
lineage and the evolution of observed life history
patterns.
Origin and life history evolution in the genus Cottus
and its relatives
Three stages have been identified in the evolutionary of
Cottus and related species that underlie the broad spe-
cies diversity of the group; the occurrence of a lineage
that lives in freshwater (Stage I), the occurrence of a
lineage that spawns in freshwaters (Stage II) and the
invasion from eastern coastal areas of Asia to inland
areas of Eurasia and North America (Stage III).
Stage I Invasion of a freshwater habitat by an ancestral
sculpin species: derivation of lineage A
This stage required an ancestral, euryhaline sculpin
species, which was probably derived from a marine
species that inhabited the shallow coastal areas of the
northern Pacific Ocean. Subsequently, lineage A, in-
cluding the catadromous species, T. f a s c i a t u s and
C. kazika, apparently originated in the eastern coastal
areas of East Asia. Because their gametes, embryos and
larvae were not adapted to fresh water (probably a
physiological constraint of osmoregulation), it was nec-
essary that lineage A inhabited marine environments
during reproduction. Eventually, they successfully in-
vaded freshwaters in East Asia.
The monophyletic Trac hi de rm us fa sci a tu s and
C. kazika share a catadromous life history, but are ge-
netically divergent (Fig. 3b), and differ substantially in
larval morphological and ecological traits (Takeshita
et al. 1997; Kinoshita et al. 1999). Juvenile C. kazika
shift from a pelagic to a benthic life just after ossification
of their cartilaginous skeleton is complete. This transi-
tion is correlated with swimming ability. In contrast, and
a clear indication of the importance of examining not
only the similarity but also the heterogeneity of life
history characteristics between species within a leneage,
T. fasciatus individuals have a longer pelagic period
because of delayed skeletal ossification (Takeshita
et al. 2004). Consequently, it is likely that T. fasciatus
Environ Biol Fish

developed the ability to utilize the tidal flat habitats that
are influenced by large tidal ranges in Ariake Bay,
southern Japan and the Yellow Sea, eastern China
(Takeshita et al. 2004).
In this study, we were unable to deduce the phyloge-
netic position of L. armatus, although the species ap-
pears somewhat similar genetically to lineage A.
Ultimately, the phylogenetic placement of L. armatus
is critical for a full understanding of the evolutionary
history of Cottus species and their relatives, including
T. fasciatus, Mesocottus haiteji and the Baikal sculpins.
Stage II Evolution and subsequent dispersal into di-
verse freshwater habitats of a freshwater-
spawning species
Lineage A and the monophyletic lineage of the Cottus
species, except for C. kazika and the Baikal sculpins,
diverged from a common ancestor (Yokoyama and Goto
201 1). The geographical origin of the latter is unknown,
although it is believ ed to have been in coastal freshwater
areas of the northern Pacific Ocean (Yokoyama and Goto
2005, 2011).
Regardless of this, the ancestral species presumably
spread into freshwater habitats due to its acquisition of
the ability to spawn in freshwater (gametes, embryos
and larvae freshwater tolerant). The ancestral lineage
probably became distributed in most freshwater areas
of the northern Pacific Ocean coast and has diverged
into different regional lineages.
Divergence of life histories and speciation in Cottus
lineages C and D in East Asia
The phylogenetic trees (Fig. 3a, b)indicatethatlineagesC
and D originated in the coastal areas of East Asia. In these
areas, speciation from a common ancesto r was accompa-
nied by divergence into amphidromous and fluvial life
histories (Goto 1981b, 1990, 1996, 2001b). This speciation
pattern, “speciation accompanying with life history diver-
gence” occurred in parallel in three regions: the Korean
Peninsula in eastern Asia (amphidromous
C. hangiongensia and fluvial C. koreanus), the Japanese
Archipelago (amphidromous medium-egg typ e of
C. po llux and large egg type of C. pollux), and Japan and
Sakhalin Island, Russia (amphidromous
C. amblystomopsis and fluvial C. nozawae) (Fig. 5,
Yokoyama an d Goto 2005). The time of divergence for
each of the three spec ies pairs has been estimated as 1.7–
4.0 Mya, 0.9–2.2 Mya, and 0.7–1.6 Mya, respectively ,
dating back to Plioc ene to Plio-Pleistocene eras (Fig. 3b)
(Yokoyama and Goto 2005). It is notab le that these speci-
ation events, which were accompanied by life history
divergences into both amphidromous and fluvial forms,
appear to have occurred in the three different regions and at
different times.
A caveat for this interpretation is that the close rela-
tionships between the species pairs are remarkably com-
plex, and that the estimation of divergence times was
difficult. For example, the fluvial species C. nozawae
(lineage C) was genetically divergent in each region and
included at least three local sub-lineages that diverged
from each other about 0.9–1.5 Mya (Fig. 3b, Yokoyama
and Goto 2002, 2005). In addition, the three local sub-
lineages of C. nozawae did not have a bifurcate rela-
tionship with the amphidromous species,
C. amblystomopsis (Fig. 3b, Okumura and Goto 1996;
Yokoyama and Goto 2005). An explanation for these
observations is that the local sub-lineages of C. nozawae
diverged i nde pen dently from the ancestral sto ck of
C. amblystomopsis on several occasions (Okumura
and Goto 1996; Goto 1990, 1996, 2001b).
Following the emergence of sibling species by diver-
gence from a common ancestor or from hybrids between
two closely related species (M. Uranishi and A. Goto
unpubl. data), the gene phylogeny (especially mitochon-
drial gene phylogeny) may differ from the species phy-
logeny (e.g. Avise 2004). Consequently, for recently
emerged species, it may be difficult to determine the
reasons why monophyletic relationships cannot be de-
tected between sister taxa, e.g. C. amblystomopsis and
C. nozawae. To elucidate both the complex and close
relationship between the latter two species and their
evolutionary histories, an extension of the present study
will include additional mitochondrial makers plus nu-
clear markers. In the near future, it should be possible to
improve estimates of the relationship between life his-
tory divergence and speciation, as well as determining
the time of species divergence of the two species.
Furthermore, by contrasting patterns of divergence for
each of the three pairs of sister taxa, it may also be
possible to deduce the relationships between speciation
and geohistorical events.
Dispersal of lineage B into inland areas of Asia
Lineage B dispersed into the Eurasian Continent from
the coastal areas of the Pacific Ocean, subsequently
Environ Biol Fish

extending its range to each region of the continent. The
lineage appears to have spread initially into the inland
areas of northern Eurasia from the old Amur River basin
in East Asia, and then through connections between the
old Amur River and other major Siberian rivers (such as
the Lena, Yenisei and Ob Rivers). Judging from the
distribution of several sub-lineages in rivers of the
Primorye and the Amur River basin, multiple speciation
events occurred between C. szanaga and C. altaicus,
and C. poecilopus and C. volki at that time, although
they did not extend into the rivers facing the Bering
Strait or on Kamchatka Peninsula (Fig. 3b, Yokoyama
and Goto 2005; Shedko and Miroshnichenko 2007).
The geographic range and degree of genetic differenti-
ation among the species suggest that lineage B has
maintained its geographic isolation among the regions
and river systems after the lineage had spread through-
out northern Eurasia, even in the late Pleistocene when
drastic changes occurred in the natural environments.
Notwithstanding, because the ice-sheet did not extend
into the Siberian region during the glacial advances in
the Pleistocene, as o ccurred in Europe and Nor th
America (Hewitt 2004; Spielhagen et al. 2004), the
connections among river basins appear to have promot-
ed dispersal mixing of species of this lineage among the
rivers (Yokoyama et al. 2008).
Derivation of species in the Cottopsis clade
along the Pacific coast of North America
These species diverged from a common ancestor on the
Pacific coast of North America, the latter having acquired
the ecoph ysiological traits necessary for reproduction in
fresh water (Figs. 3 and 5,YokoyamaandGoto201 1).
From the phylogenetic tree (Fig. 3a), the Cottopsis
clade appears to have been distributed in North America
before the dispersal of the Uranidae and Cottus clades in
that region, although the distribution of all species,
except C. asper (Baumsteiger et al. 2012;
Dennenmoser et al. 2013) in the fo rmer linage was
restricted to the coastal areas and did not extend across
the Rocky Mountains.
Within the Cottopsis clade, C. asper and C. aleuticus
both exhibit an amphidromous life history, the remain-
ing species being freshwater residents (Baumsteiger
et al. 2012). A number of short, steep rivers existing
from mountains along the coast appear to have provided
natural environments similar to those in East Asia,
where the sister related Cottus species pairs are
distributed. In contrast, however, no pairs of sister taxa
exist within the Cottopsis clade (Fig. 5a). Individuals of
inland populations of C. asper and C. aleuticus produce
many small eggs from which pelagic larvae hatch, and
have a fluvial life history (Heard 1965; Krejsa 1967;
Sinclair 1968; Brown et al. 1995), life history charac-
teristics that differ the fluvial
Cottus species in East
Asia, such as C. nozawae and C. pollus LE both of
which have large eggs and well-developed larvae. An
interesting discrepancy exists between the polymorphic
life histories (amphidromous and lacustrine landlocked)
found in C. asper and C. aleuticus, and the monomor-
phic life history (fluvial) foun d in C. nozawae and
C. pollux LE.
Stage III Further species diversification following es-
tablishment of the Bering Strait and subse-
quent dispersal of Cottus species into the
inland areas of Eurasia and North America
Lineages A, B, C and D and the Cottopsis clade all
diverged in each region along the coasts of the northern
Pacific Ocean. It is notable, however, that except for
lineage B, they did not disperse across coastal mountains
into inland areas (Fig. 4). In this regard, dispersal into
inland areas of the Eurasian and North American conti-
nents from the northern coastal regions of the Pacific
Ocean may have been blocked by the Bering land bridge,
which formed during several glacial maxima. After the
recession of the glaciers and formation of the Bering Strait,
dispersal would have been possible for lineages other than
lineage B. North America and Eurasia were first isolated
by the Bering Strait ca. 5.5–4.8 Mya (Marincovich and
Gladenkov 1999). At that time, the lineages had success-
fully spread into inland areas and were probably able to
invade a broad range of freshwater environments.
Consequently, the lineage ranges extended and the biodi-
versity in each region increased.
The time of emergence of the Cottopsis and Uranidae
clades, and the Baikal sculpins was approximately 3.3–
8.0 Mya (Yokoyama and Goto 2005), a large time frame
that makes difficult any corre lation of phyloge netic
divergence with the formation of the Bering Strait.
Dispersal of the Cottus clade into inland areas
of Siberia, Europe and North America
It is likely that later dispersal of the Cottus clade into the
inland areas of Eurasia later followed a different route
Environ Biol Fish

than the dispersal of lineage B, which probably spread
via freshwater connections among the inland rivers of
Eurasia that faced the Bering and Arctic seas. The
C. gobio species group and C. sibiricus diverged from
a common ancestor in Europe and Siberia, respectively.
Furthermore, because C. ricei in North America is ge-
netically similar to both the C. gobio species group and
to C. sibiricus (about 2 % sequence difference in
mtDNA; Fig. 3b), it is likely that the former diverged
from an ancestral stock that had dispersed into North
America from the Eurasian continent.
The recent determination that the C. gobio species
group that diversified in Europe and C. sibiricus were
not monophyletic, although having a complex phyloge-
netic relationship (R. Yokoyama, A. Goto and V. G.
Sideleva unpubl. data), suggests that they should be
treated as members of a spe cies group as has been done
with Arctic charr Salvelinus alpinus (Brunner et al. 2001),
in order to better understand their evolutionary history.
Adaptive radiation of the Baikal sculpins
Ancestral species of the genus Cottus spread into the
inland areas of the Eurasian Continent. Subsequently,
the ancestral stock of species such as C. gobio,
C. sibiricus or C. cognatus invaded Lake Baikal and
diverged to produce the diverse Baikal sculpins. Recent
molecular phylogenetic studies suggested that the
Baikal sculpins are monophyletic and have diversified
at the species level since approximately 1.2–3.1 Mya
(Kontula et al. 2003). They are presently included in the
genus Cottus and form a single lineage (Yokoyama and
Goto 2005; Kinziger et al. 2005).
In this enormous and ancient lake, the extraordinary
radiation of cottoid fishes from a single common ances-
tor, with species differentially adapted to the deeper
benthic and open pelagic habitats, might represent an
irrefutable example of divergent natural selection as a
major cause of their reproducti ve isolation (Fig. 6)
(Sideleva 1982, 1994, 2003; Goto 1994, 2000; Goto
et al. 2013). However, there remain a number of ques-
tions about the Baikal sculpins: (1) which species was
the progenitor? (2) how many species became adapted
to pelagic life despite not having an air bladder? (3) how
did they adapt to the depths with significant hydrostatic
pressure (ca. 140–160 atm) and no light? (4) how close
are the relationships among the species (species phylog-
eny), and (5) how did the present species richness (33
species) evolve (Table 3, Fig. 3a, b) (Sideleva 2003,
2011; Yokoyama and Goto
2011)?
Widespread dispersal of the Uranidea clade
from the Bering area into the inland areas of North
America
It is likely that the Uranidea clade diverged from an
ancestral species, which had dispersed into the inland
areas of North America via connections between rivers
facing the Bering Sea or Arctic coast (Fig. 3a). This
clade has adapted to the vast inland freshwater area of
North America, the species diversity illustrated by the
clade probably having resulted from its filling vacant
ecological niches in various freshwater environments
with little competition from other benthic fishes.
A number of the North American Cottus species,
such as C. asper, C. aleuticus and C. gulosus,are
lacustrine land-locked forms that utilize the diverse hab-
itats in lakes and ponds (Brown et al. 1995; Moyle 2002;
Baumsteiger et al. 2012). This may be a result of the
spread of fluvial species into lacustrine environments.
For example, lacustrine land-locked species or popula-
tions, such as C. extensis (Ruzycki et al. 1998), which
produce pelagic larvae, are found in a few lakes
(Table 3). The Uranidea species appear to be better
adapted for lakes due to their pelagic larvae. It is
1000m
1500m
(1 f., 1 genus, 3 spp.)
(1 f., 1 genus,
2 spp.)
Benthic
(2f., 10 genera,
28 spp.)
An ancestral benthic species of Cottus
Bentho-pelagic
Pelagic
Leocottus
Paracottus
Batrachocottus
Procottus
Limnocottus
Asprocottus
Batrachocottus
Limnocottus
Abyssocottidae
Cottinella
Abyssocottus
Fig. 6 Schematic diagram of hypothesis for adaptive radiation in
Baikal sculpins. The origin of Baikal sculpins is inferred as an
ancestral benthic species of the genus Cottus
Environ Biol Fish

probable that this life history was derived secondarily
from the fluvial species in this lineage.
In southeastern North America, more than ten
undescribed Cottus species, including cavefishes, have
been discovered (Kinziger et al. 2007). This region was
a refuge for freshwater animals during the glacial ad-
vances of the Pleistocene (Soltis et al. 2006), which
severely influenced North American habitats. A number
of fluvial Cottus species emerged as a result of long-
term geographic isolation among the regions and river
tributaries. Another fish group in the same region, the
benthic darters of the family Percidae, also became
highly diversified at both species and population levels
at that time (Lee et al. 1980; Near et al. 2001, 2011;
Keck and Near 2008; Keck and Etnier 2011; Harrington
and Edgar 2013).
In essence, the present study suggests that the mono-
phyletic freshwater sculpins that comprise lineage A and
7 other lineages may have undergone two periods of
adaptive radiation, one involving freshwater Cottus spe-
cies in the northern part of the Northern Hemisphere,
and the other, the Baikal sculpins, most of which are
endemic to Lake Baikal, the oldest and deepest fresh-
water lake in the world.
Conclusion and perspectives of the evolutionary
study of freshwater sculpins
This paper described the successful evolution of fresh-
water sculpins of the genus Cottus and its close relatives
including the Baikal sculpins that led to their extraordi-
nary biodiversity. Their evolutionary histories are be-
lieved to have originated in coastal areas of the Pacific
Ocean, from the time when sculpin species became able
to utilize freshwater habitats. Subsequently, adaptation
to f resh water and continuing speciation ac celerate d
when a lineage emerged that had acquired the physio-
logical and ecological ability to reproduce in fresh water.
During this evolutionary process, speciation occurred
in parallel wit h divergence in li fe history patterns.
Furthermore, speciation events may have been acceler-
ated by dispersal into the vast freshwater areas of the
inland regions of the Eurasian and North American
continents. During this diversification process, species
bacame adapted to a variety of freshwater environments,
primarily as a result of increasing variability in larval
development. The Baikal sculpins are included in this
group because of their genetic similarity, despite
possessing diverse morphological and ecological traits.
Even though many aspects of the evolutionary history
of the freshwater sculpins have been resolved, a few areas
remain elusive. In particular, a highly reliable molecular
phylogenetic tree that seamlessly covered all of the species
diversity of Cottus and its relatives could not be construct-
ed. The following areas of inquiry are emphasized, as their
resoluion will not only strengthen an overall phylogenetic
tree, but will also adva nce of our overall understanding of
the evolutionary history:
1) A single species of Mesocottus, M. haiteji, is en-
demic to the Amur River basin. Although it was not
included in the present molecular phylogenetic
analyses, other studies have indicated that it is dis-
tantly related to Cottus and its relatives. It is rea-
sonable to assume that species of this genus dis-
persed into the old Amur River basin by a different
route and at a different time than the Cottus species.
Because a greater understanding of M. haiteji may
assist in reconstructing the invasion of freshwater
by ancestors of freshwater sculpins, including a
major genus Cottus, a genetic analysis of Cottus
species plus M. haiteji is a likely first step.
2) It is desirable to selectively use marine sculpin
species as outgroups and to increase the number
of genes analyzed in order to obtain a more reliable
phylogenetic tree of the Cottus
species and their
relatives. The inclusion of species such as
Leptocottus armatus, for which the phylogenetic
status was inconclusive in this study, would im-
prove the molecular phylogenetic analyses and con-
struct a more robust phylogenetic tree. In addition
to a phylogenetic study, an exa mination of the
evolution of life history traits should be conducted
for all of the freshwater sculpins, except for the
Myoxocephalus quadricornis species group.
3) It is crucial to determine the origin of the Baikal
sculpins and the processes by which their adaptive
radiation and speciation eve nts occurred. This
would require construction of more reliable molec-
ular p hylog enetic trees that included sequences
from both mitochondrial and nuclear genes.
4) Finally, it will be important to obtain reliable and
improved estimates of the divergent times of each
lineage described in this study and to correlate those
times with well documented geological events that
coincide with formation (or removal) of barriers to
Environ Biol Fish

dispersal, such as the formation of the Bering land
bridge.
Acknowledgments We are grateful to A. J. Gharrett, D. L. G.
Noakes and G. S. Hardy for their invaluable comments and
correcting the English of our manuscript, and to T. Andoh, N.
Okumura, N. Kuramoto, M. Uranishi, H. Tsukagoshi, H. Shiraka-
wa, Y. Takahashi, Y. Yamazaki, K. Takata and H. Sakai for their
invaluable support of ecological field surveys and comments to an
early draft of this paper, and t o H-K. Byeon, K. Iguchi, I.
Irnazarow, S-R. Jeon, J. Kotusz, K.D. Louie, L. Pasko, D. Pitruk,
S.V. Shedko, N. Takeshita, K. Watanabe, S. Zolotukhin, and the
late S. Nakano for their providing fish samples. The field surveys
and fish collections carried out in this study complied with local
by-laws and regulations.
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