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REVIEWS

Disaptation and recovery in the
evolution of Antarctic fishes
John Montgomery and Kendall Clements

T

and Victoria have evolved more
rapidly 6, thus generating a higher
species richness. These cichlid
radiations have also provided a
rich source of data against which
to debate issues of evolution and
adaptation, such as the relationships between microevolution and
macroevolution6, speciation processes7,8 and adaptive radiation9,10.
The intrinsic scientific interest of Antarctica and the multinational nature of Antarctic science has meant that surprising
progress has been made in underThe radiation of Antarctic
standing the biology and evolufishes
tion of Antarctic fishes. In the past
Recent reviews1,2 summarize our

five years there have been over 150
understanding of the origins of the
papers on Antarctic fishes: 30 on
John Montgomery and Kendall Clements are at the
evolutionary radiation, and how it
ecological questions; over 80 on
relates to the Antarctic environ- School of Biological Sciences, University of Auckland, anatomical, physiological and
Private Bag 92019, Auckland, New Zealand
ment past and present. The develomolecular adaptations to the
(j.montgomery@auckland.ac.nz;
ping consensus is that Antarctic
environment (particularly low
k.clements@auckland.ac.nz).
notothenioid success can be attemperature); 15 on systematics;
tributed to one key evolutionary
and 20 on evolution. From this
innovation – glycopeptide antiand previous work, the phylogenfreeze1 (Box 1). Protection from freezing is essential in shal- etic relationships of the group are relatively well known
low ice-covered sea, because teleost blood is less salty than and the timescale over which the radiation has occurred is
seawater and freezes at a correspondingly higher tempera- also well constrained. Thus, the monophyletic radiation of
ture. Thus, in shallow Antarctic habitats, freezing protec- Antarctic notothenioids is an excellent system with which

tion alone might be sufficient to explain the dominance of to explore issues of adaptation and evolutionary change,
notothenioid fishes and the virtual absence of competition comparable to and complementary with the cichlid radifrom other teleost fish groups. Elasmobranch fishes ations. The main thrust of this article is to single out the
employ an osmoregulatory strategy providing them with issue of adaptive loss and regain, which has recently
sufficient freezing protection; however, they are only become evident in the evolution of Antarctic fishes. Disappoorly represented in Antarctic waters. Eastman1 suggests tation and its partial reversal are apparent in the lateralthat there might be other habitat or trophic factors that line sensory systems of species that have become secondexplain their low representation in the Antarctic fish fauna. arily pelagic, and in the haemoglobinless channichthyids.
Recent molecular evidence has shown that the antifreeze glycoprotein evolved from pancreatic trypsinogen3,
Box 1. Glossary
thus providing an exciting and rare example of how an old
Allometry: the relationship between the sizes of various parts of an organism.
protein gene can be changed to generate a new gene for an
Antifreeze: Antarctic fishes have a glycopeptide antifreeze, which is secreted
entirely new protein with a new function. Indeed, if the
into the blood and other body fluids. The effect of the antifreeze is to lower
notothenioid antifreeze is the ‘key evolutionary innothe freezing point of the blood and prevent the build-up of ice crystals.
vation’ of the group, it presents us with a unique case of
Crista: a molecular layer that overlies the primary sensory nucleus of the
being able to directly relate an extensive radiation, and
lateral-line system. The eminentia and crista form part of an adaptive filter
faunal dominance of a group of fishes through organismal
that cancels self-generated noise in the mechanosensory lateral-line system.
adaptation, to protein evolution.

Eminentia: part of the brain associated with the cerebellum. The main cells in
this area are the granule cells whose axons form the parallel fibres of the crista.
Adaptive radiations are important case studies in evoluMyoglobin: an oxygen-binding pigment located in muscle cells.
tionary biology. However, within the fishes we have only a
Paedomorphic: retention of juvenile characters in adulthood owing to
few clear-cut examples. The best known is the radiation of
somatic development being slowed with respect to gonadal maturation.
cichlid fishes in the African Great Lakes; however, there is
Pleiotropy: a gene influencing more than one aspect of the phenotype.
4
also a significant radiation of cottid fishes in Lake Baikal . It is
Subcarangiform: fishes intermediate in locomotor ability between anguilliinteresting to briefly compare the notothenioid radiation
form and carangiform. Typically, subcarangiform fishes have a thickened
with the better known cichlid radiations. Like the nototheforebody and undulations are mainly confined to the posterior part of the
body, thus less than one wavelength is present.
nioids, the cichlids have evolved to play a wide variety of ecological roles5; however, the cichlid faunas of Lakes Malawi
he notothenioid fishes form a
monophyletic radiation that
dominates the fish fauna of
the Antarctic continental shelf. This

perciform suborder (Notothenioidei)
has about 95 species divided among
five families. Four of the families
are predominantly or exclusively
Antarctic; however, one family
(Bovichtidae) is only found outside
the Antarctic. Hence, the term
Antarctic notothenioids refers to
the suborder Notothenioidei minus
the family Bovichtidae.

TREE vol. 15, no. 7 July 2000

The radiation of notothenioid fishes provides an
excellent system to explore issues of evolution
and adaptation. Most studies emphasize
adaptation to the extreme Antarctic
environment; however, recent work provides
cogent examples of disaptation or evolutionary
loss of function. The nature and extent of

regressive change is revealed by subsequent
adaptive recovery. Ancestral notothenioids were
benthic but some became secondarily pelagic
through the retention of larval characters.
Paedomorphosis has produced detrimental
changes in lateral-line sensory systems that
have been made good by compensatory
adaptation. In the icefish family, compensatory
adaptation has followed the loss of the oxygenbinding pigments haemoglobin and myoglobin.

0169-5347/00/$ – see front matter © 2000 Elsevier Science Ltd. All rights reserved.

PII: S0169-5347(00)01896-6

267

REVIEWS
Secondary pelagicism
and paedomorphosis
Generally, it is agreed that

notothenioids are derived
from bottom-dwelling ances5.87 ± 0.17
Benthic
Bovichtus variegatus
tors without swimbladders1.
Typical
benthic fishes with
Pelagic
0.01 ± 0.01
Dissostichus mawsoni
no swimbladder and no
Notothenia angustata
4.43 ± 0.14
Benthic
special buoyancy adaptations in water weigh about
Trematomus pennellii
3.04 ± 0.11
Benthic
5% of their weight in air.
The thornfish (Bovichtus

Trematomus loennbergii
2.28 ± 0.17
Epibenthic
variegatus), often taken as a
2.62
Trematomus newnesi
Semipelagic
functional outgroup for the
Antarctic notothenioids, and
Trematomus bernacchii
3.37 ± 0.09
Benthic
the New Zealand black cod
2.91 ± 0.07
Trematomus hansoni
Benthic
(Notothenia angustata) weigh
in at close to that. By con3.13 ± 0.08
Trematomus nicolai
Benthic

trast, Antarctic notothenioids
all weigh considerably less
2.75 ± 0.08
Pagothenia borchgrevinki
Cryopelagic
than 5% of their weight in
Pleuragramma antarcticum
0.57 ± 0.07
Pelagic
water (Fig. 1). This is
especially true of the pelagic
Trends in Ecology & Evolution
Pagothenia
borchgrevinki,
Pleuragramma
antarcticum
Fig. 1. Phylogeny of selected notothenioid taxa. Dots on the cladogram show the multiple evolution of a pelagic
and Dissostichus mawsoni.
lifestyle. The cladogram is based on Klingenberg and Ekau13, and the character distribution is from Eastman11.
Eastman11 has detailed the

Habitat and buoyancy (weight in water) data are from Eastman1.
distinctive characters of
Pleuragramma,
including
those that relate to their pelagic lifestyle (Table 1). To his list,
we could also add silveryness and modest lateral compresTable 1. Distinctive characters of adult
sion – two characters also found in pelagic notothenioids and
a
Pleuragramma antarcticum
typical of many midwater teleosts. Both are persistent larval
characteristics that contribute to midwater camouflage.
Possibly
Convergent with
Character
paedomorphic nototheniids
The suite of characters associated with secondary
pelagicism make an interesting case study for understanding evolutionary processes. As Eastman11 has noted, many
Permanently pelagic
✓
✓

of these characters are paedomorphic (Box 1), a view rePelagic eggs and spawningb
–
–
inforced by osteological studies12. In general, notothenioids
Near neutral buoyancy
✓
✓
have pelagic larval stages and it appears that secondary
Delayed skeletal ossification
✓
✓
pelagicism has evolved from the retention of larval characLow mineral content of skeleton
✓
✓
ters. The mechanism underlying paedomorphosis is
Persistent notochordb
✓
✓
thought to be a change in the timing of developmental
Red-fibred lateralis superficialis

✓
–
events11,13. Changes at such a fundamental level will impact
b
muscle
on a large interrelated character set, with the result that it
Subcarangiform locomotion (Box 1)
✓
–
makes little sense to try to tease apart individual traits as
Large intermuscular lipid sacsb
–
–
adaptations. In addition, only a subset of these characters
Habitat

Low levels of typical notothenioid
AFGPb,c
Possession of a novel AFGPb,c
Three haemoglobin componentsb
Photoreceptors dominated by single
cones
Large superficial neuromasts
Hypertrophied eminentia and crista
of brainb
Three pyloric cecab
Silver coloration
Laterally compressed body form
aExcept

–

–

–
–
✓

–
–
✓

✓
–

✓
–

–
✓
✓

–
✓
✓

for large superficial neuromasts, all characters are apomorphic when
polarized relative to Trematomus bernacchii. Check marks indicate characters that
might be paedomorphic in Pleuragramma and also characters that are convergent
in other water column clades of nototheniids.
bAutapomorphic (unique derived or diagnostic) characters for Pleuragramma.
cAFGP, antifreeze glycopeptide.

268

Wt in H2O/
wt in air
100 ( SE)

Box 2. Definitions
Adaptation: an organismal character produced by natural selection for a particular biological role33–35.
Aptation: an organismal character that confers use to the organism,
regardless of whether its phylogenetic origin featured natural
selection33,34.
Disaptation: an organismal character whose use to the organism
is demonstrably inferior to that of a phylogenetically antecedent
character33,35.
Exaptation: an organismal character that has been coopted for
use unrelated to its origin. Originally, an exaptive character might
have been an adaptation for a different use or a nonadaptation33,34.
Nonaptation: an organismal character that confers no use for
organismal survival or reproduction relative to phylogenetically
antecedent characters. A primary nonaptation is one whose origin
cannot be ascribed to the direct action of natural selection. Nonaptation might also arise secondarily by loss of the use of a character33–35.
Readaptation: an organismal character produced by natural
selection that reverses, or partially reverses, a disaptation.

TREE vol. 15, no. 7 July 2000

REVIEWS
will contribute to performance enhancement within the
defined ‘selection regime’ (sensu Lauder et al.14).
Certain character changes might be correlated with the
paedomorphic change, but be functionally neutral or even
disadvantageous; this evolutionary loss of function is termed
disaptation (Box 2). For example, incomplete canal formation
in the lateral line can be caused by an early arrest of development. This leaves canal neuromasts exposed on the surface of
the body without the benefit of the front-end mechanical filter
that the canals usually provide15 (Fig. 2). In essence, the
boundary layer generated within the canals protects the
sense organ from low-frequency self-generated noise. The loss
of the canals is an example of a change induced by an altered
developmental programme with potentially detrimental functional implications16. It is interesting that Pleuragramma
behaves as a sit-and-wait predator11, and that the eminentia
and crista of the brain are hypertrophied (Box 1; Table 1).
Fig. 2. Lateral view of the head of Trematomus hansoni showing the pore
These characteristics would, to some extent, compensate for
openings of the lateral-line system. Trematomus hansoni is a benthic
the loss of canals. Sit-and-wait predatory behaviour reduces
notothenioid with an adult body length of approximately 200 mm. The trunk
self-induced noise at the level of the receptor, and the
lateral-line system is visible, as are the pore openings of the infraorbital
eminentia and crista form part of a sophisticated adaptive filcanal line (below the eye) and other head lines. The pores open into canals
within which are the sensory neuromasts. The canals act as a mechanical
ter that cancels self-induced noise17. It would appear that loss
filter, attenuating low frequency noise. If the canals are lost by the early
of the lateral-line canals, incidental to paedomorphic change,
arrestment of development, as happens particularly in the trunk system of
might have been compensated for by changes in behaviour
pelagic species, then this front-end filter is lost.
and central sensory processing mechanisms.
Mapping the occurrence of secondary pelagicism on a
notothenioid cladogram indicates that it has evolved at Loss of respiratory pigments in the icefish
least three times across the group1,11,13 (Fig. 1). Thus, on Loss of haemoglobin and myoglobin (Box 1) in the family
the basis of multiple independent evolutionary origins it is Channichthyidae also provides compelling examples of
reasonable to talk of the retention of larval characters in disaptation and recovery. Loss of haemoglobin is an
notothenioids as an adaptation to the pelagic habitat. One autapomorphy (unique derived or diagnostic character) for
of these secondarily pelagic groups includes the genus Channichthyidae. The cold temperature of Antarctic waters
Dissostichus. What is remarkable about the two increases oxygen solubility, such that haemoglobin loss is
Dissostichus species is their
large size in comparison with
other notothenioids (Fig. 3).
One interpretation is that the
changes in development leading to paedomorphosis have
resulted in an altered growth
profile. Whatever the developmental mechanism, the
increased size of D. mawsoni
has functional implications
for certain organ systems.
The mechanosensory lateral
line again provides an example. The mechanical filtering
effect of lateral-line canals
depends on canal diameter –
a large canal loses the ability
to act as a filter. Allometric
(Box 1) growth of lateralline canals in D. mawsoni
would produce wide canals
with little or no attenuation
of low-frequency noise. Compensatory adaptation again
appears to have occurred
with the incorporation of
Fig. 3. Four Antarctic fish species illustrating secondary pelagicism, giantism and the haemoglobinless icefishes.
(a) The benthic Trematomus bernacchii has an adult body length of approximately 200 mm, which can be cona narrow section of canal in
sidered close to the ancestral benthic condition and size. (b) The cryopelagic Pagothenia borchgrevinki is one of
the region of the receptor
the secondarily pelagic species, with an adult body length of approximately 200 mm. (c) The giant Antarctic cod
that reasserts the lowDissostichus mawsoni was caught long-line fishing through the fast-ice in McMurdo Sound. (b) and (c) are
frequency attenuation and
approximately to the same scale – the size of the fish is evident from the diameter of the hole through the ice
(approximately 1.2 m). (d) One of the haemoglobinless Antarctic fish species Chionodraco hamatus; this specihas the added benefit of
men has a head length of approximately 80 mm.
producing a high-frequency
amplification15.
TREE vol. 15, no. 7 July 2000

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REVIEWS
not lethal but is detrimental. This point is made in studies of
red-blooded notothenioids, which can successfully survive
haemoglobin poisoning with carbon monoxide18, but presumably with a reduced scope for activity. Further evidence
that the loss of haemoglobin is detrimental comes from molecular studies that provide evidence for positive selection of
haemoglobin in red-blooded Antarctic fishes19. For example,
Gymnodraco acuticeps (Bathydraconidae, sister taxa to
Channichthyidae) has a higher rate of nonsynonymous
substitutions than synonymous substitutions in the DNA
sequences of its betaglobin gene. This is taken as evidence
of positive selection on the haemoglobin gene with its associated corollary that loss would represent a disaptation.
Recent molecular evidence suggests that the abrogation of haemoglobin synthesis in icefishes probably
resulted from a single mutational event in the ancestral
channichthyids that deleted the entire betaglobin gene and
the 59 end of the linked alphaglobin gene20–22. The strongest
evidence that this loss represented a disaptation comes
from the compensatory adaptive changes that have subsequently occurred in icefishes. For example, compared with
red-blooded notothenioids, the relative mass of the saclike
ventricle is about three times larger and blood volume is
about two to four times larger than that of other teleosts1,23.
In addition, systemic resistance is estimated as being less
than 10% that of rainbow trout24. These compensatory
changes mean that the heart functions as a volume, rather
than a pressure, pump, and that large volumes of blood are
circulated at high flow rates and low pressures to meet the
metabolic demands of the tissues25,26.
Myoglobin is a respiratory pigment found in muscle,
which enhances oxygen delivery to the tissue. Recent evidence27–29 shows that myoglobin in icefishes is expressed
only in the cardiac ventricle and that this expression
occurs in many, but not all, icefish species. Phylogenetic
and molecular analysis demonstrates that mutations
resulting in the loss of myoglobin expression have occurred independently at least three times, and by two distinctly different mechanisms. In Chaenocephalus aceratus
and Pagetopsis macropterus, mature messenger RNA
(mRNA) encoding myoglobin is apparently not produced,
despite the presence of the myoglobin gene in the DNA of
these species. In Champsocephalus gunnari, mature myoglobin mRNA is detectable but this message is not translated to produce myoglobin protein at detectable levels.
Multiple loss might be expected if the myoglobin was
nonfunctional. However, Sidell and co-workers have recently
presented molecular30 and physiological28,31 evidence indicating that retention of myoglobin is under positive selection
pressure, and that it does play a functional role in the icefish
heart. For example, in myoglobin-expressing species myoglobin cDNA sequences are highly conserved. By comparison,
the two species expressing mutant myoglobin RNA exhibited
a high degree of sequence variation.
The performance of isolated perfused hearts from myoglobin-containing and myoglobinless icefishes provides the
best demonstration of the functional role of myoglobin in the
icefish heart. Myoglobin-containing hearts of Chionodraco
rastrospinosus are capable of maintaining cardiac output
at higher after-load challenges than the myoglobinless
hearts of C. aceratus. However, poisoning the myoglobin of
C. rastrospinosus hearts dropped their performance to well
below that of C. aceratus, which provides evidence not only
that myoglobin is functional where it occurs in icefish hearts,
but also that compensatory adaptive changes have occurred
in the hearts of myoglobinless species. The nature of these
compensatory adaptive changes is yet to be determined.

270

Disaptation and recovery
Readaptation implies an adaptive change that compensates for an earlier detrimental loss (Box 2). In the case of
paedomorphic change or other macroevolutionary change
involving developmental mechanisms, it is easy to understand how other interrelated structures could be impacted, at times negatively. Paedomorphic change is not
an uncommon occurrence in evolution. There are several
other fish examples where members of benthic taxa have
reradiated into the pelagic habitat by the retention of larval characters. For example, the pelagic New Zealand
blennioid triplefin Obliquichthys is thought to be paedomorphic32. The Baikal radiation of cottid fishes might also
provide examples. It will be instructive to study these
other paedomorphic groups with respect to associated
loss and regain of particular functional attributes.
In the case of the repeated loss of single functional proteins, such as myoglobin, it is less obvious how these detrimental changes could become fixed in the population,
although genetic drift in small populations is a possible suggestion. Whatever the mechanism of detrimental change, be
it pleiotropy (Box 1) or genetic drift, the Antarctic fish radiation provides explicit examples of the nature and extent of
regressive change or disaptation in evolution. The best evidence of loss is the subsequent adaptive recovery, where
the compensatory adaptive change both illuminates the
loss and demonstrates the propensity of adaptive evolution.
Conclusions
It is possible to argue that the low competitive environment under which the notothenioid radiation has occurred
has allowed a tolerance of disaptation, and that this phenomenon might be higher in this radiation than elsewhere.
However, it could equally well be argued that disaptation
can only be adequately studied where there is a good phylogeny on which to map both the disaptation and the recovery. A study of other such radiations is required to address
the issue of the extent to which disaptation, then recovery,
is a general phenomenon in evolution.
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Environment, Academic Press
2 Clarke, A. and Johnston, I.A. (1996) Evolution and adaptive radiation of
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3 Chen, L. et al. (1997) Evolution of antifreeze glycoprotein gene from a
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radiations of Antarctic fish with those of nonAntarctic fish. In Fishes of
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Persistence of selfish genetic elements:
population structure and conflict
Melanie J. Hatcher

S

elf-promoting or selfish genSelfish genetic elements are vertically
disastrous consequences for the
etic elements (SGEs) have
transmitted factors that spread by obtaining a
host population. For instance, sex
long been of interest to evolutransmission advantage relative to the rest of
ratio distorters at fixation should
tionary biologists, because their the genome of their host organism, often with a cause population (and thus their
existence emphasizes the imporcost to overall host fitness. In many cases,
own) extinction owing to the
tance of a gene level perspective
conventional population genetics theory
absence of one sex. Other SGEs,
when interpreting selection and
predicts them spreading through populations,
such as those causing autosomal
adaptation. They spread because reaching fixation and becoming undetectable or meiotic drive or CI, will lose their
they encode traits beneficial to
sometimes driving the population extinct.
effect at fixation and, therefore,
their own transmission, even if However, in several well studied systems, these might become impossible to dethey impart costs to the organgenetic elements are known to persist at
tect. Although this has almost
isms carrying them1,2. They inrelatively low, stable frequencies. Recent
certainly happened in some
research suggests that several processes might
instances2, many empirical studclude ‘ultracompetitive’ alleles,
supernumerary B chromosomes, explain these observations, including population ies suggest that polymorphism
organelles and intracellular para- structure, intragenomic conflict and coevolution. for SGEs is widespread in natural
sites1–5. These factors manipulate
populations and that SGEs are
gametogenesis or host reproducmaintained at relatively low freMelanie Hatcher is at the School of Biology, Miall
tion by a variety of means to
quencies (Table 1). Recent emBuilding, University of Leeds, Leeds, UK LS2 9JT
enhance their own transmission;
pirical and theoretical studies are
(m.j.hatcher@leeds.ac.uk).
for instance, by inducing meiotic
now beginning to shed light on
drive (Box 1) or cytoplasmic inthis problem.
compatibility (CI; Box 1), and by
feminizing, killing or sterilizing males (Box 2). Early popu- Selection for suppressors
lation genetic models predicted that, in the absence of sup- Because the spread of SGEs creates genetic conflict with
pression, many such elements should spread through other elements of the host genome, selection should
populations to high frequency or fixation, sometimes with favour genes that modify or resist their action2. Generally,
TREE vol. 15, no. 7 July 2000

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