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Coelacanths placed in the sarcopterygian lineage.

Sarcopterygians, also known as
story of evolution. The obstacles for an
invasion of the land by fish, exquisitely
lobe-finned vertebrates, comprise adapted for life in the water as they
Mark Robinson1 coelacanths, lungfish and tetrapods. are, stretch the imagination. A body
and Chris T. Amemiya1,2,* The coelacanth lineage diverged previously supported by the water
from the tetrapods roughly 400 column must now be able to support
What are coelacanths? Coelacanths million years ago, making them a key itself in air, necessitating limbs with
are a curious group of fish, represented resource for comparative genomics. strong skeletal elements rather than
by only two extant species: the African Lungfish are located at an equally the delicate fin rays of bony fish;
coelacanth (Latimeria chalumnae) and propitious phylogenetic position as gills that efficiently extracted oxygen
the Indonesian coelacanth (Latimeria coelacanths but have intractably dissolved in water must be replaced
menadoensis). These large, lobe-finned large genomes, effectively ruling them with lungs for extracting oxygen
fish live in and around deep-water out as candidates for whole genome from the air; and as water becomes
caves off the coasts of southeastern sequencing. This particular window a precious commodity that must be
Africa and Indonesia. Around two of evolutionary time is especially conserved, more efficient ways to
meters in length, the coelacanth looks notable because a large number of key excrete waste products that don’t rely
like no other fish alive. In addition tetrapod innovations arose during that on an unlimited water supply need
to its fleshy limb-like fins with their period. to be found. Even the senses must
skeletal supporting structures, it has be significantly overhauled to match
a unique bicaudal tail and a hinge on I hear the coelacanth genome has the unique demands of the terrestrial
the top of its skull which allows it to now been sequenced... Yes, the environment.
expand its gape. When hunting they coelacanth genome makes it possible
orient themselves vertically, allowing to identify, with greatly increased Don’t the coelacanth’s fins look
an electrosensitive rostral organ in their resolution, genomic changes that may almost like limbs already? Yes, sort
snout to assist in the detection of prey. underlie the various adaptations that of. But as with all lobe-finned fishes,
Coelacanths are ovoviviparous, with accompanied the transition from life in they don’t have the proper digit field
their eggs developing and hatching in water to a life on land. For example, we (autopod) and they possess fin rays,
the oviduct before birth. can now distinguish between genomic or dermal bone, at their distal ends; an
gains or losses that were specific to the arrangement that is good for swimming
Only two species? So, why the hype? tetrapods and those that were shared but not walking on land. Rather, the
A number of factors contributed to the with the entire sarcopterygian lineage. coelacanth’s fins might be thought of as
fame of what might seem like a rather containing the rudiments of the autopod
obscure fish. For one, this fish had So, was a coelacanth relative the structure. Loss of the fin rays occurred
been playing an epic 70 million year first fish to crawl out of the water? in this evolutionary transition and an
game of hide-and-seek. Coelacanths The idea of the first fish to crawl onto inkling of how this could have taken
were a more abundant and diverse the land is one that captures people’s place can still be found by comparing
group prior to the extinction event imaginations. Identification of the the genomes of the coelacanth and
at the end of the cretaceous period closest living relative of the tetrapod other fishes with those of tetrapods.
(yes, the one that killed the dinosaurs); ancestor has long vexed evolutionary Genetic antecedents for building the
coelacanth fossils are well represented biologists. The lobe-finned fishes, of autopod proper have been found in
worldwide, yet conspicuously absent in which the coelacanth is a member, with the coelacanth genome in the form of
any rocks after that time. When a living their distinctive fins supported by limb- regulatory regions (enhancer elements).
coelacanth specimen was caught off like bony arrangements were proposed In particular, the HOX-D cluster of genes
the coast of South Africa and identified early on, and the discussion moved plays a key role in patterning digits in
in 1938 by Marjorie Courtenay- on to establishing which lineage was the tetrapod limb. It was possible to
Latimer and J.L.B. Smith, it was as the sister group to the tetrapods. find regulatory regions upstream of
surprising and unexpected as finding The discovery of extant coelacanths the HOX-D cluster that were shared
a T-rex, albeit perhaps slightly less made it possible to use molecular between tetrapods and coelacanths,
intimidating. However, it was more than phylogenetic analysis in addition to but which could not be found in teleost
just the surprise factor that made the morphological data. A number of fish. When such a coelacanth regulatory
discovery of the coelacanth perhaps studies tended to support the lungfish sequence was placed in a transgenic
the most notable zoological find of the as our closest living relative, but prior mouse, it was shown to drive reporter
last century. The existence of living to the publication of the coelacanth expression in an autopod-specific
coelacanths offered the possibility genome, no one had been able to rule pattern. This strongly suggests that the
of significant insights into the early out the possibility that both lungfish developmental program driving limb
origins of the tetrapods (Figure 1), and the coelacanth were equally patterning and formation in modern
the group comprising amphibians, related to the tetrapods. We now know tetrapods was indeed co-opted
reptiles, birds and mammals, which is that the lungfish is definitively the from a more ancient sarcopterygian
to say, ultimately, insights into our own closest living relative of the tetrapods developmental program.
evolutionary origins. (Figure 1).
Is the coelacanth a ‘living fossil’?
How so? Coelacanths emerged How do you make a fish into a There has been some push-back
during a critical stage of vertebrate land animal? The rise of terrestrial concerning the oft-used phrase, living
evolution, and are phylogenetically vertebrates is a fascinating success fossil, with regard to the coelacanth.
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The term was coined by Charles

Darwin, and is operationally used to
indicate that a species is a surviving
representative of an ancient lineage that
still retains some key features shared
with archaic fossils. Typically such a
lineage will have survived one or more
mass extinctions. Examples of living
fossils often cited include the sharks,
ginkgo trees, metasequoia, lampshell
brachiopods, horseshoe crabs, and
as defined here surely the coelacanth.
However, a common misconception is
that the phrase implies that evolution
has not acted on the organism over
these long timescales, something
that is clearly shown not to be true
for coelacanths based on gross
differences in the skeletal morphology
of fossilized specimens, especially
of forms prior to the Mesozoic.
While it is difficult to measure the
rate of morphological evolution of
extinct coelacanths, analyses of the
coelacanth’s protein coding genes have
shown, enigmatically, that its relative
rate of molecular evolution is slower
than that of other fishes and tetrapods. Figure 1. Phylogenetic tree showing major vertebrate lineages.
The implications of this relative rate The tree is based on recent phylogenomic analyses, where branch lengths indicate evolu-
difference remain speculative with tionary distances. (1) The Sarcopterygii (sensu stricto) includes the coelacanth, lungfish and
respect to the morphological evolution Tetrapoda. The coelacanth and lungfish occupy key positions, bridging the gap between the
of the coelacanth. ray-finned fish and the tetrapods. Their more substantial internal skeleton, especially with
respect to elements of the fins, was an important preadaptation utilized by early tetrapods.
(2) Lungfish + Tetrapoda. The development of a specialized lung and associated respiratory
What does the future hold for the physiologies allowed lungfish, and presumably early tetrapods, to extract oxygen from the
coelacanth? Many companion genome air in habitats that periodically dried up. (3) Tetrapoda. Tetrapods completed the transition to
papers that report surveys of various a terrestrial mode of life by developing well supported limbs and stronger skeletons, modi-
aspects of coelacanth biology have fying their sensory systems and becoming more efficient at conserving water. Drawings by
been published or are soon to be Catherine Hamilton.
published. The coelacanth genome
will continue to play a key role in
evolutionary developmental biology the past few years from the eastern Forey, P. (1998). History of the Coelacanth Fishes.
Springer Publishing.
studies with respect to the origin of the coast of Africa, enabling more in-depth Lampert, K.P., Fricke, H., Hissmann, K., Schauer,
tetrapods and their unique adaptations. anatomical investigations. And fossil J., Blassmann, K., Ngatunga, B.P., and Schartl,
coelacanths are continually being M. (2012). Population divergence in East
Furthermore, sequence data from African coelacanths. Curr. Biol. 22, 439–440.
additional coelacanth specimens discovered, including a recent form Liang, D., Shen, X.X., and Zhang, P. (2013) One
are starting to provide important from the Triassic that differs greatly thousand two hundred ninety nuclear genes
from a genome-wide survey support lungfishes
insights into the genetic diversity in from the modern day Latimeria by virtue as the sister group of tetrapods. Mol. Biol.
modern populations, insights that will of its fork-tailed morphology. We have Evol. 30, 1803–1807.
lots to learn about this iconic species. Meyer, A., and Dolven, S.I. (1992). Molecules,
be needed for future conservation fossils, and the origin of tetrapods. J. Mol.
efforts given its endangered status. Evol. 35, 102–113.
Accurate estimates of coelacanth Nikaido, M., Noguchi, H., Nishihara, H., Toyoda,
A., Suzuki, Y., Kajitani, R., Suzuki, H., Okuno,
population sizes are still lacking, but Where can I find out more? M., Aibara, M., Ngatunga, B.P., et al. (2013).
Amemiya, C.T., Alföldi, J., Lee, A.P., Fan, S.,
evidence suggests they have extremely Philippe, H., Maccallum, I., Braasch, I.,
Coelacanth genomes reveal signatures for
evolutionary transition from water to land.
restricted ranges. Accidental captures Manousaki, T., Schneider, I., Rohner, N.,
Genome Res. 23, 1740–1748.
by oilfish fishermen seem to be et al. (2013). The African coelacanth genome
Schneider, I., and Shubin, N.H. (2013). The origin
provides insights into tetrapod evolution.
placing these endangered fish under of the tetrapod limb: from expeditions to
Nature 496, 311–316.
enhancers. Trends. Genet. 29, 419–426.
increasing pressure. The Coelacanth Amemiya, C.T., Powers, T.P., Prohaska, S.J.,
Smith, J.L.B. (1939). A living fish of mesozoic
Grimwood, J., Schmutz, J., Dickson, M.,
Conservation Council and the South Miyake, T., Schoenborn, M.A., Myers, R.M.,
type. Nature 143, 455–456.
African Coelacanth Conservation and Ruddle, F.H., et al. (2010). Complete HOX
cluster characterization of the coelacanth 1Benaroya Research Institute at Virginia
Genome Resource Programme were
provides further evidence for slow evolution Mason, 1201 Ninth Avenue Seattle, WA 98101,
specifically launched to help research of its genome. Proc. Natl. Acad. Sci. USA 107, USA. 2Department of Biology University of
and tackle these urgent issues. Many 3622–3627.
Washington 106 Kincaid Seattle, WA 98195,
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intact specimens of coelacanths have coelacanths are not ‘living fossils’. BioEssays USA.
been captured and preserved within 35, 332–338. *E-mail: camemiya@benaroyaresearch.org