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Antarctic notothenioid fishes as subjects for research in evolutionary biology

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DOI: 10.1017/S0954102000000341

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Antarctic Science 12 (3): 276-287 (2000) 0 British Antarctic Survey Printed in the United Kingdom

Antarctic notothenioid fishes as subjects for research in

evolutionary biology
JOSEPH T. EASTMAN
Department of Biomedical Sciences, Ohio University, Athens, OH 45701-2979, USA
eastman@ohiou edu

Abstract: Antarcticais a continental island and the waters of its shelfand upper slopeare an insular evolutionary
site. The shelf waters resemble a closed basin in the Southern Ocean, separated from other continents by
distance, current patterns and subzero temperatures. The benthc fish fauna of the shelf and upper slope of the
Antarctic Region includes 213 species with higher taxonomic diversity confined to 18 families. Ninety-six
notothenioids, 67 liparids and 23 zoarcids comprise 45%, 32% and 11% of the fauna, a combined total of 88%.
In high latitude (71-78”s) shelf areas notothenioids dominate abundance and biomass at levels of 90-95%.
Notothenioids are also morphologically and ecologically diverse. Although they lack a swim bladder, the
hallmark of the notothenioid radiation has been repeated diverslficationinto water column habitats. There are
pelagic, semipelagic,cryopelagc and epibenthic species. Notothenioidsexhbit the Qsproportionate speciosity
and high endemismcharacteristicoffish speciesflock. Antifreeze glycopeptidesoriginating from a transformed
trypsinogen gene are a key innovation. It is not known when the modem Antarcticshelffauna assumed its current
taxonomic composition. A late Eocene fossil fauna was taxonoinically diverse and cosmopolitan. There was
a subsequent faunal replacement with little carryover of families into the modem fauna. Basal notothenioid
cladesprobably diverged in Gondwananshelf locationsduring the early Tertiary. Dates inferred from molecular
sequences suggest that phyletically derived Antarctic clades arose 15-5 n1.y.a.
Received 5 October 1999, accepted 21 February 2000

Key words: adaptive radiation, Antarctic, evolution, fish fauna, Notothenioidei, species flock

Introduction
Evolution is the major unlfying principle of biology and
evidence of the evolutionary process pervades all levels of
biological organization from molecules to ecosystems.
Although the influenceof evolutionextends to the fauna of the
most isolated continent, Antarctica is not usually included
among notable evolutionary sites such as the Galapagos,
Hawaii, Australia,Madagascar, the East African Great Lakes
and Lake Baikal. The Scientific Committee on Antarctic
Research (SCAR) Workshop on “Evolutionary Biology of
Antarctic Organisms” has highlighted the potential of the
Antarctic fauna for evolutionarystudies. Topics dealing with
fishes were well represented among the papers given at the
workshop. Perhaps more than any other group of organisms,
the radation of notothenioids, a suborder of perciforms, has
served as a subject for research in Antarctic evolutionary
biology. After introductory comments on Antarctica as an
evolutionary site, I will provide an overview of the fish fauna
with a summary of the taxonomic composition, a basic
prerequisitefor evolutionarystudies. Sections will follow on
notothenioid biodiversity, the adaptive radiation of
notothenioids and the Cenozoic fossil fish faunas.
Antarctica as an evolutionary site
Studies of evolutionary radiations on islands are naturally
276
focussed on terrestrial faunas that evolved in isolation.
Antarctica is a continental-sized island, twice the size of
Australia, with the dominantfauna inhabiting the waters of the
adjacent continental shelf rather than the landmass. The
insular characteristicsof the shelfinclude geographicisolation
by distance, oceanographic isolation by currents and thermal
isolation by subzero temperature. Although the Antarctic is
not mentioned in the recent book Evalution an Islands, Grant
(1998, p. vi) notes that the attention ofevolutionarybiologists
is drawn to islands, as well as isolated lakes, by a number of
commonfeaturesofislandfaunasincludingtheir“strangeness”,
replicated evolutionand rapiQty of diverslfication.Strangeness
or uniquenesscertainlycharacterizesnotothenioidfishesliving
at subzero temperatures with antifreeze and without
haemoglobin; fishes that, although lacking a swim bladder,
have repeatedly diversified into water column niches; fishes
that are dominant at abundance and biomass levels of 90-95%
and fishes that have a history estimated in millions rather in
than tens of millions of years.
Ichthyologistshave had access to the Antarctic shelffauiia
for a century and therefore, unlike the deep-sea and large
tropical river systems, this fauna is well characterized
taxonomically (Gon & Heemstra 1990, Miller 1993,
Andriashev 1986, Andriashev & Stein 1998) and also from
otherbiologicalperspectives (Andriashev 1965,DeWitt 1971,
 ANTARCTIC FISH FAUNA 277

Balushkin 1984, Kock 1992, Eastman 1993, di Prisco et al.

Number of species
1991, 1998). As thebest example of an adaptive radiationof
marinefishes, the notothenioiddiverslficationhasbeen studied Fishes of the Southern Ocean (Gon & Heemstra 1990), the
at the organismal, organ system and molecular levels of definitive work on Antarctic fishes, inventoried the fauna of
organization (Eastman1993,Bargellonietal. 1994,Clarke & the Antarctic Region at 272 species representing 49 families.
Johnston 1996,Klingenberg& Ekau 1996,Ritchie etal. 1996, In the interveningdecade this number has risen to 3 13 species
Chen et al. 1997a, 1997b, Cheng 1998a, di Prisco 1998, from 50 families. This is 1.2-1.3% of the world's fish fauna
Eastman & Clarke 1998, Ozouf-Costaz et al. 1997, Pisano of 24 618 (Nelson 1994) to 25 000 (Eschmeyer 1998) valid
et al. 1998). However, notothenioids arejust beginning to be species. While some of the 41 additions are new species,
appreciatedoutside the Antarctic scientificcommunity and to others are simply new records for the Southern Ocean. For
serve as exemplars of adaptive radiation (Smith 1996, p. 71, example, a completetreatment of the liparidgenus Careproctus
Givnish 1997, p. 21,30-31, Helfmanetal. 1997, p. 307-309, (Andnashev & Stein 1998) was not available for inclusion in
Johns & Avise 1998). Fishes of the Southern Ocean, With the publication of this
Perhaps the reason the Antarctic shelf waters and its fish monograph on Careproctus, the most noteworthy change in
fauna are under-appreciated in an evolutionary context is that the past decade has been an increase in the count of Southern
much research to date, with the encouragement of funding Ocean liparids from 31 to 67 species. This family has
agencies, has emphasized aspects of extreme biology rather surpassed the Nototheniidae as the most speciose family of
thanw i n g principlesof evolutionarybiology. This approach Antarctic fishes.
has yielded valuable information about molecular and organ Benthic fish are the major component of the fauna on the
system function at low temperature, but has not focussed shelfand upper slope of the Antarctic Region. There are 213
attention on aspects of organismal biology that the Antarctic benthic species and hlgher taxonomic diversity is confined to
fauna shares with faunas in other isolated habitats such as rift 18 families (Table I). In the high latitude (71-78"s)
lakes, postglacial lakes and islands. Even among biologists embayments of the Weddell and Ross seas, the fauna consists
there is little notoriety associated with a fauna that is remote of about 80 species (Hubold 1992,Eastman & Hubold 1999).
and difficult to access through ice-covered shelf waters. The T h s includesthe endemicshelfcomponent and a cosmopolitan
evidence for evolution is there, however, and research on the non-notothenioid mesopelagic component (not included in
fish fauna will provide insight into evolutionary processes in Table 1) - the latter consisting of less than 10 species in the
marine habitats as well as raising the visibility of Antarctic Weddell and Ross Seas (Hubold & Ekau 1987, Eastman &
evolutionary biology. Hubold 1999). Representatives of this cosmopolitan group
includebathylagids,paralepidds, myctophidsand macrourids.
The modern environment and fish fauna
The Southern Ocean is the expanse of cold sea-water south of Table I. Families of benthic fishes from the Antarctic Region.
the mean position of the Antarctic Polar Front (45-60°S), Taxona No of speciesb % fauna
includingthe Sub-Antarcticislands of the Indian Ocean sector
Myxinidae (hagfkhes) 1 0.5
(Gon & Heemstra 1990, p. 70). This is the Antarctic Petromyzontidae (lampreys) 1 0.5
Zoogeographic Region. The Southern Ocean encompasses Rajidae (skates) 8 3.7
about one-tenthof the world oceanand the Antarcticcontinental Carapidae (pearlfishes) 1 0.5
shelf,where most of the fishes are found, comprises 2 x 106km2 Moridae (deepsea cods) 4 1.8
Muraenolepididae (eel cods) 4 1.8
(Pakhomov 1997,p. 378), about 7-8%ofthe 27-29 x lo6km2
Gadidae (cods) 1 0.5
of total shelf area in the world (Kennett 1982). Unllke other Congiopodidae (horsefishes) 1 0.5
large marine ecosystems, the shelf and upper slope of the Bathylutichthyidae' 1 0.5
Antarctic Region resemble a closed basin, isolated from other Liparidae (snailfishes) 67 31.5
shelf areas by distance, current patterns and subzero Zoarcidae (eelpouts) 23 1 0 . 8 1 87.4
Notothenioidei (includes 5 Antarctic families)d 96 45.1
temperatures. Thus the ranges of many fish species, while
Tripterygiidae (triplefins) 1 0.5
large and frequently encompassing the entire continental Achiropsettidae (southern flounders) 4 1.8
shelf, are as circumscribed as those of lacustrine endemics
Totals 213 100%
elsewhere in the world. The fish fauna is also hghly endemic,
with 88% of the species confined to waters south of the "Arranged phylogenetically with sequencing according to Nelson (1 994).
AntarcticPolarFront(Andriashev 1987). Ifjust notothenioids bBased on Gon & Heemstra (1990) with notothenioids updated by
Eastman & Eakin (2000) and with these additions among non-
are considered, species endemism rises to 97% (Andriashev notothenioids: number of liparids from Andnashev & Stein (1998, p. 58,
1987). Comparative figures for endemism of near-shore table 3) plus three from Matallanas (1998, 1999) and number of zoarcids
ichthyofaunasin other isolated marine habitats include 9-16% from Anderson (1994).
for the Galapagos, 23% for Easter Island and 25% for Hawaii 'Balushkin & Voskoboynikova (1990).
(Grove & Lavenberg 1997, McCosker 1998). dSee Table 111.
278 JOSEPH T. EASTMAN

Liparids, notothenioids and zoarcids are the most speciose swim bladders, they may have been unable to fill all water
fish taxa on the Antarctic shelf. In a large-scale summary column niches. In t h s respect, the notothenioidbody form has
(Table I), these groups account for 87.4% of the species. In proved to have more capacity for diversification than have
the most southerly shelf areas (Table II), this figure rises to those of liparids and zoarcids whlch are keyed to epibenthic
91.6%. Such restriction of higher taxonomic diversity is and benthic life, respectively. As will be seenbelow, however,
unusual among shelf faunas of the world. a count of taxa alone leads to an under appreciation of the
Although liparids are the most speciose family in a large- morphological and ecological diversity of notothenioids.
scale synopsisof the Antarctic Region (Table I), this does not
accuratelyportray aspects of dwersity and biomass. Liparids
Notothenioid taxonomy
are not morphologically or ecologically diverse compared
with notothenioids. While speciose, many liparid species are The suborderNotothenioideiincludeseightfamilies,43 genera
known from only a few specimens and are probably not with 122 species. As summarized in Table 111, five families
representedby large populations and biomass (Andriashev & and 96 species are Antarctic whereas three families and 26
Stein 1998). T h s is expected in a group inhabiting the deeper species are non-Antarctic (Eastman & Eakin 2000). Ninety-
portion of the water column where productivity is reduced. three Antarctic notothenioids were included in Fishes of the
Midwater (DeWitt 1970) and benthic @eWitt 1971, Ekau Southern Ocean (Gon & Heemstra 1990), with an additional
1990, Hubold 1992, Eastman & Hubold 1999) trawling in the 25 non-Antarctic species for a total of 118. The seeming
Ross and Weddell seas indicates that notothenioids always addition of only four species in the past decade is artifactual
hold overwhelmingdominancein speciesdiversity,abundance and d i s p s e s a period of considerableactivityin notothenioid
and biomass - the latter two at levels of 90-95% (Table I1 and taxonomy. While 1 1 new specieswere described, seven other
references above). T h s is an exceptional degree of habitat species were placed in synonymy, hence the net gain of only
saturationby a single higher taxonomicgroup. Notothenioids four (Eastman & Eakm 2000).
are dominant because they occupy niches filled by Another system of notothenioidtaxonomy recognizes more
taxonomicallydiversegroups offish in temperateand tropical genera and species, approximately 47 and 130, respectively
oceans, groups not represented on the Antarctic shelf. (Balushkin 1992, 1997a, 1997b). Miller (1993), following
The discrepancy between the large area of the Antarctic Balushkin's system, delineated 103 species of Antarctic
shelf and the low species richness may in part be attributable notothenioids. The differencein taxonomic approachbetween
to the absence of certain habitats in the high Antarctic; there
are no estuaries, intertidal zones, reefs or shallow shelves.
Since the shelfaverages 500 m deep, versus 130 m elsewhere Table 111. Species diversity and geographic distribution within
notothenioid families and among nototheniid genera.
in the world (Kennett 1982), the prime site for fish diversity
and abundance is missing in the Antarctic. There is also a Antarctic non-Antarctic Total
phylogenetic constraint that may have limited the size of Family" species species species
fauna. Since notothenioids, liparids and zoarcids all lack Bovichtidae 1 9 10
Pseudaphritidae 0 1 1
Eleginopidaeb 0 1 1
Table 11. Fish collected in nineteen bottom trawls at depths of Nototheniidae 33 15 48
107-1 191 m on the shelf of the south-westem Ross Sea (73-77"S), Patagonotothen 1 13
cruises 96-6 and 97-9 of the RV Nathaniel B. Palmerb Notothenia 3 2
Paranotothenia 2 0
Percentage by:
Lepidonotothen 4 0
Family no. of no. of weight
Gobionotothen 4 0
speciesb specimens' (Station 119 only)d
Trematomiis 11 0
Rajidae 6.4 0.7 Pagothenia 2 0
Muraenolepididae 2.1 1.6 Cryothenia 1 0
Liparidae 6.4 0.8 Aethotaxis 1 0
Zoarcidae 8.5 5.3 8.8 Dissostichiis 2 0
Nototheniidae Gvozdarus 1 0
Artedidraconidae Pleuragramma 1 0
76.6 91.6 91.2 Harpagiferidae 6 0 6
Bathydraconidae 19.1 18.9 Artedidraconidae 25 0 25
Channichthyidae 14.9 8.1 29.2 Bathydraconidae 16 0 16
Totals 100% 100% 100% Channichthyidae 15 0 15
Totals 96 26 122
'Data from Eastman & Hubold (1999).
bNumberof species is 47. "Familial nomenclature after Balushkin (1992) and phylogenetic
'Number of specimens is 979. sequencing of non-Antarctic families after Lecointre et al. (1997).
'%umber of specimem at Station 119 (77"19'S, 165'41'E; 900-910 m bDeWitt et al. (1990) rather than Balushkin (1992) is followed for the
deep) is 83. spelling of the stem-genus portion of the family name Eleginopidae.
 ANTARCTIC FISH FAUNA
splitting and lumping accounts for the disparity between
Balushkin’s and Miller’s counts and that of Gon & Heemstra
(1990). The latter is used in this paper and also serves as the
basis for the species list of Eastman & Eakin (2000). Most
differences between the two systems centre on the families
Nototheniidaeand Channichthyidae.
The Antarctic fish fauna is far from being completely
described. Collecting in accessible and presumably well-
stubed areas of the Antarctic shelf is still producing new
species. Recently 19 bottom trawls in the Ross Sea yielded
979 specimens including two new artedidraconid species
(Eakm & Eastman 1998, Eastman & Eakin 1999), a colour
morph of a known arteddraconid (Eastman & Eakin 1999)
and two new species of the liparid Paraliparis (Eastman,
unpublished data). The new artedidraconids were taken in
shallow water (100-300 m) on the tops of banks or in the
vicinity of sponge beds. One new liparid was captured less
than 50 km offshore, in an innershelf depression at 1200 m,
and the other was taken over a bottom that was 465 m deep.
Notothenioid phylogenetics
Much information on phyletic relationshps has appeared in
the past few years. This work has utilized DNA sequencedata
from mitochondria1 genes (Bargelloni et al. 1994, 1997,
Ritchie et al. 1996, 1997), nuclear genes (Lecointre et al.
1997) or a combination of both (Bargelloni & Lecointre,
1998, Chen et al. 1998). Amino acid sequences of a-and B-
chains of haemoglobin have also been used (Stam et al. 1997,
1998). Notothenioid molecular phylogenetics has provided
answers to some questions whilst also opening additional
avenuesfor research. For example,the traditionalBovichtidae
was found to be paraphyleticand the newly definedBovichtidae
(Bovzchtusand Cottoperca)appears no more closely related
to other notothenioids than are several non-notothenioid
outgroups (Lecointre et al. 1997). Pseudaphritis urvillii
(Valenciennesin Cuvier& Valenciennes),formerlyconsidered
a bovichtid, has been reassigned to the monotypic family
Pseudaphritidae(Balushkin 1992),andmoleculardataindicate
that this species is the sister group of all non-bovichtid
notothenioids (Lecointre et al. 1997). Furthermore, it is
possible that the familiesNototheniidaeand Bathydraconidae
are paraphyletic and that three offour nototheniid subfamilies
are not natural groups (Eiargelloni et al. 1994, Bargelloni &
Lecointre 1998, Ritchie et al. 1997, Stam et al. 1997).
Obviously much work remains to be done.
The monophyly of notothenioids has not been firmly
establishedon morphologcal grounds. The presence of three
plate-like pectoral radials is a possible synapomorphy @akin
1981,Lecointre etal. 1997). The most recent molecular data
have not supported monophyly (Lecointre et al. 1997,
Bargelloni & Lecointre 1998), but amino acid sequences in
haemoglobin suggest that the Antarctic notothenioids are
monophyletic (Stam et al. 1997). Lecointre et al. (1997)
suggested that a possible reason for this finding is that early
279
cladogenesiswithin notothenioidswas simultaneouswith the
explosive diversification of perciforms, thus with little time
for differences to accumulatethe resolutionof outgroup nodes
is difficult. Below I discuss the possibility that antifreeze
glycopeptides are a synapomorpliy for the clade of Antarctic
notothenioids.
Nature of notothenioid biodiversity
Biodiversity is defined as the collection of genomes, species
and ecosystems occurring in a geographically defined region
(Committee on Biological Diversity in Marine Systems 1995,
p. 1). Biodiversitytherefore exists at three levels ofbiological
organization: genetic (intraspecific), organismal (specific)
and ecological (communities). My emphasis here is on
organismal biodiversity, although I will also mention
intraspecific variation.
One point that should be made initially is that the waters of
the Antarctic shelf are not a biodwersity hotspot with large
numbers of endemic species found in a relatively small area.
Just the oppositeis true -a relatively small number of endemic
species inhabit a large area. As describedpreviously,it is not
the numbers but the nature of the fish biodiversity that
dstinguishes the Antarctic from all other shelf areas in the
world. The fish fauna lacks the higher taxonomic dwersity
characteristicofmost inshoremarine habitats. On the Antarctic
shelf, notothenioids dominate the fauna in terms of species
diversity, abundance and biomass. Notothenioids have also
diversified into a number of life history types - they are
morphologically and ecologcally diverse.
Organismal biodiversity: morphological and ecological
components
In addition to phyletic &versification, and unlike many other
fish groups including some radiations (Brooks & McLennan
1991, p. 171-185, Mayden 1992, p. 870, 876), notothenioids
have also experiencedsubstantialmorphologicaland ecological
diverslfication. T h s can be summarized by saying that
notothenioidsunderwent a depth-related diversification, most
similar to that of the cottoids in Siberian Lake Baikal (Smith
&Todd 1984). The notothenioid diversificationwas keyed to
the utilization of unfilledniches in the water column,especially
pelagic or partially pelagic zooplanktivory and piscivory. In
the absence of competition from a taxonomically diverse
fauna, notothenioids were able to fill these niches as well as
remaining the dominant benthic group. Their diversification
centred on the evolutionary alteration of buoyancy and the
morphology associated with swimming and feedmg in the
water column. Although they lack swim bladders, in some
speciesdensityreductionto neutralbuoyancy hasbeen achieved
through a combination of reduced skeletal mineralizationand
lipid deposition. Best demonstrated in the family
Nototheniidae, about 50% of the Antarctic species inhabit the
water columnratherthan the ancestralbenthic habitat (Eastman
280 JOSEPH T. EASTMAN
 ANTARCTIC FISH FAUNA 281

1993). Referred to as pelagization, this evolutionary tailoring
of morphology for life in the water column has arisen
independentlyin dfferent nototheniid clades (Klingenberg&
Ekau 1996).
Figure 1provides a sample ofthe morphologd, ecological
and geographc dlversity among some of the 48 species in the
family Nototheniidae (Table 111). While about half of the
species are benthic as adults (Fig. la-b, d-g), others are
semipelagic(Fig. Ih), epibenthic (Fig. li), cryopelagic(Fig. Ij)
andpelagic (Fig. lk-I). With someexceptions,the arrangement
of the figure is based on weight in seawater (Eastman 1993)
from heaviest at 4.4% (Fig. la) to lightest at 0.6% (Fig. 11).
The adults in this sample range in size from 10cm TL and 30g
(Fig. Id) to 2 m TL and over 100 kg (Fig. Ik). Ecologml
diversityin this family is further enhanced by the ontogenetic
pelagichenthic habitat shifts, exemplified by juveniles of
Notothenia (Fig. lc). Species with complex life cycles
contributeextrabiodversity to a region (Harper &Hawkworth
1994, p. 10).
Intraspecijc biodiversity
There is another aspect of nototheniid biodiversity that is not
conveyed by a count of species. The genus Trematomus,for
example, includes speciesexhibiting variability in head shape,
colour and karyology. Although widespread among some
species of boreal lacustrine fishes (Skulason & Smith 1995),
tlus phenomenon of morphism or phenotypic plasticity has
only recently been recognized in Antarctic fishes. I will cite
three examples.
The circum-Antarctic nototheniid Trematomus newnesi
Boulenger exists as two morphs in the Ross Sea - the typical
morph (Fig. lh), which served as the basis for the species
description (Boulenger 1902),anda large mouthlbroadheaded
morph comprising28% of the population (Eastman & DeVries
1997). These canbe separatedbyvisual inspection. The large
mouth morph has a wider and blunter head, longer upperjaw,
wider gape and darker coloration. However, a subsequent
sample from the same location contained a high percentage
(47%) of an intermediate morph (Eastman & DeVries,
unpublished data). Inference from morphology and
measurements suggests that the large mouth morph is more
benthic than the typical semipelagic morph, although
buoyancies have not been measured. This may be an example
of diversification along a depth gradient, and its dwovery
suggests that the bounds of the nototheniid adaptive radiation
may extend to the population level. With the finding of
intermediate morphs, other interpretations are also possible.
For example, the large mouth morph could be a cryptic or
sibling species, and the intermediate morphs are the result of
introgression,crossesbetween largemouth and typical morphs.
This hypothesis cannot be tested without data on genetic
dwerslfication.
In the only Antarctic example of morphism where genetic
information has been obtained, mitochondnal DNA sequences
ofthe 12s and 16s ribosomalregions indicatedthat thebrown
and white blotch colour morphs of Trematomus bernacchii
Boulengerwere not geneticallydifferent (Bernardi& Goswami
1997). As these mitochondrial regions are conserved, it is
possible that genetic differences could have accumulated in
more variable regions (Bernardi & Goswami 1997).
Finally, polymorphism in chromosome number and
morphologyhas been discovered in several widely dstributed
nototheniids includmg Trematomus eulepidotus Regan and
T. hansoni Boulenger (Ozouf-Costaz et al. 1997,Pisano et al.
1998). Although the systematicsignificanceofthesefindmgs
is not clear, intraspecificchromosomalrearrangementmay be
an initial stage in the attainment of reproductive isolationor it
may appear incidentally before or after species formation
(Ozouf-Costaz et al. 1997).
The notothenioid speciesjlock
The species flocks of fishes studied to date have lived in
freshwater, and most origmated in the past 3 m.y. (million
years) (Echelle & Kornfield 1984, McCune 1997). Eastman
& Clarke (1998) have drawn parallels between the high
Antarcticshelfand lacustrinehabitatsand, using the criteriaof
hbbink(1984, p. 22-23), havesuggestedthatthefivehtarctic
notothenioid families exhibit the dsproportionate speciosity

Fig. 1. (opposite) Adults and one juvenile (c) depicting the range of morphological, ecological and geographical diversity in the family
Nototheniidae. a. Notothenza angustata Hutton, heavy inshore benthic and rockpool species with a cold temperate and sub-Antarctic
distribution. b. Adult Notothenza rnicrolepidota Hutton, rocky reef dwelling benthic species with a Subantarctic distribution.
c . Pelagic juvenile (86 mm TL) of N. rnzcrolepidota with silvery colouring and forked caudal fin, frequently captured far from shore,
d. Patagonotothen eleguns (Giinther), small blenny-like species from southern South America. e. Gobionotothen gbberzfrons
(Lonnberg), benthic species common near the Antarctic Peninsula. f. Trematomus bernacchii Boulenger high Antarctic inshore benthic
species. g.Trernatomus scotti (Boulenger), high Antarctic offshore benthic species. h. Typical morph of Trematomus newnesi
Boulenger, a semipelagic Antarctic species. i. Trematomus loennbergii Regan, epibenthic Antarctic species living near the bottom at
depths of 663-1 191 m. j. Pagothenia borchgrevinh (Boulenger), cryopelagic Antarctic species living near the platelet layer underlying
fast sea ice. k. Drssostichus eleginoides Smitt, large Subantarctic piscivorous predator probably close to neutral buoyancy and living at
depths to 1500 m. 1. Pleuragramma antarcticum Boulenger, shoaling neutrally buoyant zooplanktivore, the dominant species in the
water column (0-900 m) of the high Antarctic shelf. [All illustrations, except a-c and g, are of the holotype for the species.
Illustrations from these sources: a from Waite (1909); b, c, f, h, j and 1 from Boulenger (1902); d from Gunther (1 880); e from Lonnberg
(1905); g from Regan (1914), i from Regan (1913) and k from Smitt (1898).]
282 JOSEPH T. EASTMAN
and endemism characteristic of a species flock.
Recently another approach has been made to this question
using molecular sequence data. Johns & Avise (1998)
attempted to identie phylogenetic footprints characterizing
an ancient species flock when viewed at the present time.
Usingmolecularphylogeneticdata, they testednull theoretical
models that assume random temporal placement of
phylogenetic nodes. The null model is rejected if speciation
is non-random and if there is significant clustering of
cladogenetic events in time. Their analysis detected an
ancient marine species flock, with an estimated age
8.5-3.6 m.y., among the 65 species of north-eastern Pacific
scorpaeniform rockfishes of the genus Sebastes. Johns &
Avise (1998) conducted a similar analysis using the
notothenioid molecular data of Bargelloni et al. (1994) and
Ritchieetal. (1996). Whenbovichtidswereexcluded,statistical
tests of nodal placements in the notothenioid phylogeny
suggested that speciation events were non-random, with
signifcant clustering of cladogenetic events in time - the
hallmark of a species flock. This was true for the Antarctic
notothenioid families in general and also for the nototheniid
trematomids in particular. The dates of these two rahations
hadbeenpreviouslyestimatedat 10-15 m.y. (Bargellonietal.
1994) and 3.4 m.y. mtchie et al. 1996), respectively.
A key innovation
A key innovation is a uniquely derived novel feature, or
synapomorphy, characteristic of a clade and correlated with
theradiationofthat clade(Brooks&McLennan 1 9 9 1 , ~181). .
The innovation must also aid entry to a new ecological habitat
(Grant 1998,p. 3 13-3 14). Key innovationsare the exception
rather than the rule among flocks of fishes. The five different
varieties of peptide and glycopeptideantifreezeshave evolved
from pre-existing proteins by gene duplication followed by
sequence hvergence (Davies et al. 1993, Chen et al. 1997a,
1997b, Cheng 1998a). This has occurred independently at
least nine times amongphyletically diverse cold water teleosts
(Davies et al. 1993, Cheng 1998b). Antifreeze glycopeptides
ofhtarcticnotothenioids meet the criteriafor a key innovation.
When mapped on the notothenioid cladogram, they have a
single origin at the node for the Antarctic clade - the sister
group of the non-Antarctic Eleginopidae (Eastman & Clarke
1998). Given their orign from a transformed trypsinogen
gene, they are uniquely derived and distinct from all other
antifreezes including the antifreeze glycopeptides of Arctic
gadidswhich have a differentbut unidentified genomic origin
(Chen et al. 1997a, 1997b, Cheng 1998a). The contribution
of antifreeze glycopeptides to survival in new habitat is
obvious since diversification into subzero ice-laden water
would have been impossible without them @eVries 1988).
There has been considerably more Qverslfication in the
Antarctic component of the suborder (95 species) than in the
non-Antarctic (26 species). Based on the 14-5 m.y. age
inferredfrom the divergenceof molecular sequencesbetween
trypsinogenandantifreeze(Chen etaE. 1997a),the acquisition
of genes responsible for the synthesis of antifreeze in the
nototheniid Dissostichusmawsoni Norman is coincident with
the cooling and appearance of ice in the Southern Ocean.
Radiations within the radiation
Repeated diversification into water column habitats has been
the hallmark of the notothenioid radiation. Althoughthe most
thoroughly studied cases are in the family Nototheniidae
(DeVries & Eastman 1978, Eastman & DeVries 1981,1982,
Klingenberg & Ekau 1996), there may also be examples
among icefish of the family Channichthyidae. A molecular
phylogeny is available for channichthyids and mapping of
lifestyle data suggests there have been benthic-pelagic
&versificationsat most nodes in the cladogram (Chen et al.
1998). This hypothesis is based on existing life history
information, whch is scant for some species, and buoyancies
have not been measured. Some species do have a morphology
associated with habitation of the water column. Dacodraco
hunteri Waite, for example, has a weakly ossified skeleton
with considerable cartilagein the skull (Eastman 1999). It has
a partially persistent notochord and reduced amounts of bone
in the vertebral column since the centra are incompletely
constricted. Since their weight in seawater averages only
1.3% of weight in air, Dacodraco are among the lightest
notothenioids. It is likely that other channichthyidspossess
similar morphology since heterochrony is thought to have
been important in the &versification of several notothenioid
lineages into water column habitats (Balushkin 1984,
p. 127-128, Iwami 1994, Voskoboinikova 1994). Delayed
ossification is a paedoniorphic trait, most pronounced in the
phyletically derived channichthyid species (Voskoboinikova
1997).
The fossil record and the evolution of notothenioids
Does information from the fossil record contribute to
understanhng the nature of modern Antarctic fish fauna, with
greatly restricted higher taxonomic diversityunlike that of any
other shelf area in the world? T h s question is an attempt to
understand a faunal replacement that took place sometime
over the past 40 m.y. in the waters of the Gondwanan shelf.
The null hypothesis is that there would be some taxonomic
carryover from the Eocene to the modern Antarctic fauna, as
was true in the case ofother southern continentslike Australia
(Long 1982). The Cenozoic fossil record provides a starting
point, but beyond this speculation predominates.
Eocene fauna
As is the case with many extant groups, there is no fossil fauna
that is immediately ancestral to the modern Antarctic fish
fauna. There is, however, a late Eocene (-40 Ma) fauna.
These fossil fish from the La Meseta Formation on Seymour
 ANTARCTIC FISH FAUNA
Island, near the tip ofthe AntarcticPeninsula, are representative
of a high latitude (z6OoS) shelffauna at this time. Seymour
Island had a taxonomically diverse fish fauna that was cool
temperate in character (Eastman 1993). As biogeographic
provinciality was less evident at high latitudes in the Eocene,
this fauna was cosmopolitan rather than endemic to the
Antarctic component of Gondwana.
Chondrichthyes - cartilaginousflshes
The Eocene fish fauna from Seymour Island consists of about
26 taxa-20 chondrichthyans(Case 1992,Long 1992a, Cione
& Reguero 1998) and 6-7 actinopterygians (Eastman 1993,
Long 1992b,Cioneetd. 1995). Therangeofchondrichthyans
includes chimaeras, large predatory sharks, sedentarybenthlc
sharks, saw sharks, skates and eagle rays. However the 70%
dominance by chondrichthyans is artifactual, attributable to
the durabilityand distinctivenessof their dentitionin the fossil
record. Their teeth are frequently identfiable to species, but
this is not the case with most actinopterygian remains from
SeymourIslandoranywhereelse (Grandelk Chatterjee 1987).
Chondrichthyansprobably composed a greater percentage of
the Eocene fauna than the 4% in the modern Antarctic fauna
(Gon&Heemstra 1990),but theexact figure isuncertain. The
majority of chondrichthyan species in the modern fauna are
skates of the genera Bathyraja and Raja. The modern cool
temperate Tasmanian fauna includes 15% chondrichthyans
(Last et al. 1983). Case (1992) suggests that during the late
Eocene the east coast of the Antarctic Peninsula was an area
of upwelling and therefore capable of supporting a high
biomass of prey necessary for maintenance of a diverse shark
fauna. The recent report of a fossilized gill raker from the
basking shark Cetorhinus (Cione & Reguero 1998), a
specialized filter feeder on zooplankton, supports this
hypothesis. The filter feeding strategy is not represented
among chondrichthyans or actinopterygians in the modern
Antarctic fauna.
Isit possible that skateshave continuouslyoccupiedAntarctic
coastal waters since the early Tertiary, or are they Quaternary
immigrants? Skates of the genera Bathyraja and Raja are the
only fisheswith familial and generic representation inboth the
Eocene and modern faunas (Long 1994). Althoughfavouring
persistence, Long (1994) objectively summarizes both sides
of the issue. This question should be answerable using
molecular techniques to infer phylogenetic relationships and
divergence times among rajids of the Southern Hemisphere.
Actinopterygii - ray-flnnedjshes
The actinopterygian fossils from Seymour Island include
clupeoids(herrings),silunforms(catfish),gaMorms (codfish),
oplegnathids (knifejaws), labrids (wrasses) and trichiurids
(cutlassfish). The teeth and durophagous diet of oplegnathids
and labrids suggest hard shelled invertebrate prey was then
abundant. With the exception of gadiforms, these taxa are not
283
representedin the modem Antarcticfauna. The representation
of notothenioids in the fossil fish fauna from Seymour Island
is debatable. A partial cranium has been identified as either a
gadiform (Eastman & Grande 1991) or a representative of the
basal notothenioid family Eleginopidae, Proeleginops
grandeastmanorum (Balushkin 1994).
With reference to the perciform fossil record elsewhere in
the world, 40 millionyears is a reasonabledate for the possible
existence of a basal notothenioid group on the Gondwanan
sheK. Thereare no indisputableperciformfossilsin Cretaceous
deposits, but by the early Middle Eocene (z50 Ma) most
perciform families were represented to the extent that
subsequent diverslfication was “mere tinkering” (Patterson
1993,p. 53). For example,theEocene Monte Bolca coral reef
assemblage from northern Italy, deposited in what was then
the Tethys Sea, is broadly similar in familial composition to
modern reef assemblages (Bellwood 1996). This suggests
that the evolution of perciforms was rapid, with basic body
plans and familial lineages establishedby 50 Ma followed by
a period of stasis. Perciforms dominated shallow tropical
marine communities at this time. It is not surprising that the
versatile perciform body plan was also suitable for benthic
habitats in high southern latitudes.
Pliocene fauna
With little ice-free rock exposed in Antarctica, there is scant
information about any transitional or intermedate faunas
spanning the gap between the late Eocene and modern faunas.
Pliocene (4.2-3.5 Ma) invertebrate and cetacean fossils from
Marine Plain in the Vestfold Hills indicate that the inshore
fauna, which also includes one unidentlfiablefish, was unlike
the modern fauna (Quilty 1994). For example, decapod
crustaceans have a long fossil history in Antarctica but are
unknown in the modern fauna. A Pliocene decapod from the
Marine Plain verifies that this group was still represented in
coastal waters at this time (Feldmann & Quilty 1997), as the
result of either persistence or re-invasion. The diversity of
cetaceans from the Marine Plain deposits is also noteworthy
and unlike the modern coastal fauna. Five species have been
discovered to date, includmg an 8.5 m-long squid-eating
dolphin (Quilty 1994).
The Cenozoic paleoenvironment and the divers$cation of
notothenioids
During the early Miocene (25-22 Ma) the Antarctic shelf was
subject to a series of tectonic and oceanographic events that
probably altered faunal composition. For example, seafloor
spreading and the opening of the Drake Passage to deep water
began to separate Antarctica from other Gondwanan
landmasses (Kennett 1982). The development of the
unrestricted Antarctic Circumpolar Current and initial
formationofthe AntarcticPolar Front, with increasingbiogenic
productivity and somewhat lower temperatures to the south
284 JOSEPH T. EASTMAN
sennett 1982), began to define the Southern Ocean and
Antarctic Zoogeographic Region. These events isolated
Antarctica and initiated climatic changes that eventually
eliminatedsome habitats availableto the late Eocene Seymour
Island fish fauna. After the middle Miocene (016 Ma),
expansion of the ice sheet led to destruction of inshore habitat
by ice, with repeated grounlngs of parts of the sheet as far as
the shelf break (Anderson 1999, p. 229-230). Invertebrate
faunas and trophic conltions changed as well. Emigration,
regional extirpationand/or extinction reduced the diversity of
the fish fauna, and its taxonomic composition was altered
through geologic time. There was a post-Eocene faunal
replacement with little carryover of families into the modern
fauna.
Diversificationof notothenioidswas probably facilitatedby
the thermal isolation of Antarctica, by the increasing
productivity of the Southern Ocean beginning about 22 Ma
(Kennett 1982) and by the absence of competition from non-
notothenioids. Niches were available and, as a generalized
benthic group, notothenioids were able to adapt to new
conditions. There was also probably an element of chance in
the emergence of the notothenioid stock - being in the right
place at the right time. The notothenioid diversificationmay
have been protracted through much of the Tertiary, with
cladogenetic events separated by long periods of stasis. For
example, the divergence of some of the basal non-Antarctic
clades,the Pseudaphritidaein Australia and the Eleginopidae
in South America, may have taken place by vicariance during
the fragmentation of Gondwana when stocks became
established on the coasts of isolated continental blocks
(Eastman 1993). The separation of the eleginopid clade,
represented by the extant Eleginops maclovinus (Cuvier in
Cuvier & Valenciennes), from the rest of the non-bovichtid
notothenioids is estimated at 23-22 m.y. (Bargelloni &
Lecointre 1998). T h s coincideswith the opening oftheDrake
Passage and formation of the Antarctic Polar Front.
The phyletically derived Antarctic clades appeared later.
Inferred dates for the age of the radiation of the five Antarctic
notothenioid families, those with antifreeze glycopeptides,
are in the range of 15-5 m.y. For example, inference from
mitochondria1 DNA sequences implies that the radiation of
this group took place within the last 15 m.y. (Bargelloni et al.
1994) or 16-10 m.y. (Bargelloni & Lecointre 1998). The
small sequence divergence between notothenioid antifreeze
glycopeptide and trypsinogen genes provides a similar age,
14-5 m.y., for the radiation of the Antarctic families. The
inferred date for this gene conversionencompassesthe time of
appearance of ice in the Southern Ocean (Chen et al. 1997a).
In the family Nototheniidae,the averageage of the trematoniid
radiation is only 3.4 m.y. or late Pliocene (ktchie et al. 1996).
Trematomids are lugh latitude inshore fish with high levels of
antifreeze. Although controversial, the late Pliocene
(3.5-1.8Ma) may have been a time of climatic and glacial
instability at high Antarctic latitudes (Quilty 1996). If
Antarctica was partially deglaciated and a rise in sea level
increased the area of the shelf, these warm-dominatedvicarant
events could also have provided new habitat suitable for
diversification of some notothenioids (Eastman 1993,
p. 143-144).
Finally, why is the modernAntarcticfaunadistinctlydifferent
from those of other southern continents when all shared a
common early Tertiary fish fauna? The answer probably lies
in the regional historical processes mentioned previously,
especiallytectonic, oceanographicand climatic events. These
processes are important in establishingpatterns of diversityin
polar marine organisms (Brey et al. 1994). With the breakup
of Gondwana, each southern landmass and its shelf fauna
became independent and influenced by lfferent hstorical
processes. As the Tertiary progressed, Antarctic shelf waters
became increasingly isolated and subject to current patterns,
glacial scour, changing temperatures, marked seasonalityand
altered trophic conditions. By the late Miocene-late Pliocene
(6.5-2 Ma), low water temperatures, extreme geographc
isolation and lack of south flowing surface currents limited
immigration of many Southern Hemisphere epipelagic and
inesopelagic groups into waters south of the Antarctic Polar
Front. The shelf fauna became increasingly endemic and
distinctive, but it is not known when it became modern in
taxonomic composition.
Future research
The development of Antarctic evolutionary biology has
benefited greatlyfromwork on notothenioidfish. IfAntarctica
is to gainvisibility as adistinctiveevolutionary site, additional
work on fish in this unique ecosystemwill be necessary. Ship-
based collecting as well as basic taxonomic and ecological
research should continue. The shelf waters are still yielding
new species and presenting challenging problems, such as
intraspecific variation and morphisni, in the delimitation of
species. The application of phylogenetic systematics has
allowed formulation of testablehypothesesof historicaldescent
amongnotothenioid lineages. This methodologyalsoprovides
a framework for tracing character acquisition during
diversification and thus opens up new approaches to
longstanding evolutionary mysteries. The most valuable
research in this area has answeredbroad organismal questions
by employingthe techniques of molecularbiology to track the
acquisition of a key innovation via gene conversion (Chen
et al. 1997a, 1997b,Cheng 1998a). The questionsin this case:
where did notothenioid antifreezes come from, when did they
appear and do they have aunique origin amongfish antifreezes?
The surprisingly direct answers were mentioned above in the
section on key innovations. It is hoped that work along these
lines will continue.
The exploration of remote islands has proved to be far more
valuable than merely documenting the existence of unusual
faunas. Discoveriesmade at the Galapagosstimulated Charles
Darwin to begin erecting the framework for evolutionary
thought. Darwin’svoyageintheHMS Beagle(l83 1-36), and
 ANTARCTIC FISH FAUNA
subsequent research by numerous scientists, has made the
Galapagos the premier evolutionary site in the world. At
about the same time (1839-43), James Clark Ross took HMS
Erebus and Terror into the h g h latitudes of Antarctic coastal
waters (Ross 1982). During the course of the voyage many
distinctive species were discovered including an endemic
tribe of four seals, six species of penguins and about a dozen
species of notothenioid fish, nine of which are still valid.
However, a comprehensive picture of the fauna did not
emerge and Antarcticaremainedunappreciatedas a continental
island with an endemic marine fauna. Antarctica has now
joined the Galapagos as a destination of tourist ships and
fishingvessels,but unlike the Galapagos, it still does not have
name recognition as a centre of evolution. This SCAR
Workshop inQcatesthat scientistsare now tappingthe potential
of the Antarctic for evolutionary studies.
Acknowledgements
I thank Bruno Battaglia and the SCAR Subcommitteeon the
EvolutionaryBiology ofAntarcticOrganismsfor the invitation
to speak at the workshop. I am also grateful to Edith Fanta for
her efforts in arranging the meeting and for her hospitality in
Curitiba, Brazil. The manuscript benefited greatly from the
reviews of Richard Eakin and Ofer Gon. Supportedby NSF
grant OPP94-16870 and by funds from an Ohio University
Presidential Research Scholar Award.
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