Extremely slow rate of evolution in the HOX cluster revealed by comparison between Tanzanian and Indonesian coelacanths

Coelacanths are known as "living fossils" because their morphology has changed very little from that in the fossil record. To elucidate why coelacanths have evolved so slowly is thus of primary importance in evolutionary biology. In the present study, we determined the entire sequence of the HOX cluster of the Tanzanian coelacanth (Latimeria chalumnae) and compared it with that of the Indonesian coelacanth (L. menadoensis), which was available in the literature. The most intriguing result was the extremely small genetic divergence between the two coelacanths. The synonymous divergence of the HOX coding region between the two coelacanths was estimated to be 0.07%, which is ~11-fold smaller than that of human-chimp. When we applied the estimated divergence time of the two coelacanths of 6 million years ago (MYA) and 30 MYA, which were proposed in independent mitochondrial DNA analyses, the synonymous substitution rate of the coelacanth HOX cluster was estimated to be ~11-fold and 56-fold smaller than that of human-chimp, respectively. Thus, the present study implies that the reduction of the nucleotide substitution rate in coelacanth HOX genes may account for the conservation of coelacanth morphology during evolution.     

The ecology and conservation of the coelacanth Latimeria chalumnae

Synopsis Studies on the ecology of the living coelacanth, Latimeria chalumnae, are reviewed and assessed. Early predictions on the life history of the coelacanth have proved to be accurate but recent findings have improved our understanding of its habitat and feeding preferences, diel activity patterns and social behaviour. A history of coelacanth conservation reveals that there has been a sustained concern for the survival of this species which has eventually culminated in several effective conservation actions in recent years. The coelacanth is threatened by a number of socio-economic and biological factors, but international action directed at managing the fishery in the Comoros should ensure that the species survives. Recent observations on living coelacanths in their natural environment have greatly improved our knowledge of the behaviour and relative abundance of adults. Important priorities for future research include studies on the distribution and abundance of juveniles and breeding adults, both off the Comoros and elsewhere. The coelacanth is a highly specialised, precocial fish which occupies a unique place in biology. Co-ordinated international efforts should continue to be made to understand and conserve this remarkable fish.     

A newly recognized fossil coelacanth highlights the early morphological diversification of the clade

Previously considered an actinopterygian or an osteichthyan incertae sedis, the Devonian (Givetian-Frasnian) Holopterygius nudus is reinterpreted as a coelacanth. This genus is among the oldest coelacanths known from articulated remains, but its eel-like morphology marks a considerable departure from the conventional coelacanth body plan. A cladistic analysis places Holopterygius as the sister taxon of the Carboniferous (Serpukhovian) genus Allenypterus. Despite the specialized morphology of these genera, they occupy a surprisingly basal position in coelacanth phylogeny; only Diplocercides and Miguashaia are further removed from the crown. A morphometric analysis reveals that coelacanths were anatomically disparate early in their history. Conflicts between this result and those of previous studies challenge the adequacy of systematic character sets for describing historical patterns of morphological variety. Coelacanths have long had an iconic place in the study of vertebrate evolution for their apparent anatomical conservatism over geological time, but Holopterygius provides clear evidence for rapid morphological evolution early in the history of this clade.     

The demography of the coelacanth Latimeria chalumnae

Synopsis The very sparse data that are available on the abundance, population structure and biology of the coelacanth Latimeria chalumnae off Grand Comoro are summarised, and some simple numerical analyses are carried out to explore certain aspects of the population dynamics, particularly the age-profile of the population. The object has not been to provide estimates of key demographic parameters, such as mortality rates, but to propose various scenarios that are useful for comparison with real data as they become available. The analysis also makes it possible to reach some preliminary conclusions that are relevant to the management of the coelacanth population. For instance, it appears that the catch rate of coelacanths by artisanal fishermen may have a negligible effect on coelacanth survivorship, and it is more likely that population size and structure are determined by natural mortality rates and birth rates. It is suggested that predation is the main cause of natural mortality and that the main predators of coelacanths are likely to be large sharks. Interference with the traditional patterns of the Comoran artisanal fishery may threaten the coelacanth. Several important gaps in our knowledge of coelacanth demography are identified.     

Silver coelacanths from Spain are not proofs of a Pre-scientific Discovery

In 1964 and 1965, two silver fish pendants depicting coelacanths and thought to be religious votive from Spanish churches were purchased on the art market in Spain, dated between the 17th and late 19th century, long before the discovery for science of the living coelacanth in 1938. It was speculated that they originated either from the Mediterranean, subtropical Atlantic, or subtropical Pacific (de Sylva 1966, Bruton 1985, Anonymous 1993, Greenwell 1994, Raynold & Mangiacopra 1995). Some authors believe that the silver fish pendants represent a new species of coelacanthiforms (Raynold & Mangiacopra 1995), others claimed the pendants to be only a wishful fantasy of scientists and not coelacanths at all (Thomson 1991). However, new studies revealed that the silver fish artefacts are indeed coelacanths but were in fact produced more recently with the Comorian coelacanth, Latimeria chalumnae, as a model.     

Bibliography of the living coelacanth Latimeria chalumnae,with comments on publication trends

Synopsis A list of published references on the coelacanth Latimeria chalumnae is provided. All known publications in the scientific literature are included as well as popular articles and press reports that are considered to provide new information or interpretations. Marked trends are noticeable in the literature as different disciplines have been applied to research on the coelacanth over the past five decades. The bibliography lists a total of 823 publications including 490 papers in journals, 37 books, 3 theses, 45 chapters in books, 166 popular articles, 22 reports and 60 newspaper articles. Studies on taxonomy and morphology initially dominated the literature followed by reports on research in the fields of physiology, behaviour, breeding biology, ecology and conservation as frozen and eventually live specimens became available for study. The literature on the living coelacanth is predominantly in English, French, Japanese and German but references in 12 other languages were also traced. The dominant authors in the first decades of coelacanth research were the French scientists J. Millot and J. Anthony and the South African describer of the first and second coelacanths, J.L.B. Smith. In subsequent years French, British, American, South African, Japanese, Canadian and German authors, among others, have made significant contributions.     

Predicting suitable environments and potential occurrences for coelacanths (Latimeria spp.)

Extant coelacanths (Latimeria chalumnae) were first discovered in the western Indian Ocean in 1938; in 1998, a second species of coelacanth, Latimeria menadoensis, was discovered off the north coast of Sulawesi, Indonesia, expanding the known distribution of the genus across the Indian Ocean Basin. This study uses ecological niche modeling techniques to estimate dimensions of realized niches of coelacanths and generate hypotheses for additional sites where they might be found. Coelacanth occurrence information was integrated with environmental and oceanographic data using the Genetic Algorithm for Rule-set Production (GARP) and a maximum entropy algorithm (Maxent). Resulting models were visualized as maps of relative suitability of sites for coelacanths throughout the Indian Ocean, as well as scatterplots of ecological variables. Our findings suggest that the range of coelacanths could extend beyond their presently known distribution and suggests alternative mechanisms for currently observed distributions. Further investigation into these hypotheses could aid in forming a more complete picture of the distributions and populations of members of genus Latimeria, which in turn could aid in developing conservation strategies, particularly in the case of L. menadoensis.     

Early Growth Stages in Coelacanth Fishes

ALL known specimens of the Recent coelacanth fish, Latimeria, are large specimens (mostly more than 100 cm total length) and only one female with eggs has been recorded^1,2. Consequently, the ontogeny and the early growth stages of the Recent coelacanth are unknown. In the fossil record, one specimen of Holophagus (= Undina) from the Upper Jurassic of Solnhofen, southern Germany, has been recorded with two young coelacanths inside³. Watson has argued from this finding that the coelacanths are viviparous but it seems more reasonable to interpret this fossil specimen as a cannibal that had just swallowed two young of its own kind. This interpretation is favoured by the position of the two specimens and by the discovery of other fossil coelacanths containing large specimens of other kinds of fishes in their stomachs⁴.     

An inventory of all known specimens of the coelacanth Latimeria chalumnae,with comments on trends in the catches

Synopsis A list is presented of all known specimens of the coelacanth Latimeria chalumnae based on a survey of the literature and of museum, aquarium and university holdings. Details are given of the date, place, time and depth of capture, the name and age of the fisherman, the length, weight and sex of the fish, the first literature record, the method of preservation and the present location of specimens, if known. A new number is assigned to each specimen. At least 172 coelacanths are known to have been caught since 1938. The first coelacanth was caught off South Africa but all properly documented, subsequent specimens have been caught off the islands of Grand Comoro and Anjouan in the Comoros. An appeal is made to the Comoran authorities for each specimen that is caught to be made available for scientific study. Museum authorities are also encouraged to allow their specimens to be X-rayed or dissected so that vital information can be obtained on fecundity, foetal nutrition and dietary preferences. It is essential for the coelacanth conservation effort that this inventory is maintained by the Coelacanth Conservation Council.     

Population divergence in East African coelacanths

The coelacanth, Latimeria chalumnae, occurs at the Eastern coast of Africa from South Africa up to Kenya. It is often referred to as a living fossil mainly because of its nearly unchanged morphology since the Middle Devonian. As it is a close relative to the last common ancestor of fish and tetrapods, molecular studies mostly focussed on their phylogenetic relationships. We now present a population genetic study based on 71 adults from the whole known range of the species. Despite an overall low genetic diversity, there is evidence for divergence of local populations. We assume that originally the coelacanths at the East African Coast derived from the Comoros population, but have since then diversified into additional independent populations: one in South Africa and another in Tanzania. Unexpectedly, we find a split of the Comoran coelacanths into two sympatric subpopulations. Despite its undeniably slow evolutionary rate, the coelacanth still diversifies and is therefore able to adapt to new environmental conditions.     

Habitat and population size of the coelacanth Latimeria chalumnae at Grand Comoro

Synopsis In 1987 and 1989 coelacanths were observed for the first time in their natural habitat with the help of submersibles. Coelacanths were found between 150–253 m depth, their preferential depth seems to be around 200 m; the water temperature ranged between 16.5–22.8° C. During the day coelacanths aggregate in small non-aggressive groups in sheltered lava-caves. Caves might be a limiting factor for distribution. At night they leave the caves for hunting by drifting singly along the steep lava slopes. They migrate between different caves located within a large home range covering more than 8 km coastline. Coelacanths are site-attached, some for a period of at least 2 years. Our own observations and earlier catch records show that only the west coast of Grand Comoro is a suitable coelacanth habitat with more structural complexity and prey fish abundance than other coastlines of the island. From our survey we estimated a total coelacanth population off Grand Comoro to be 150–210 individuals; a saturated population would be 370–510 individuals. This small relict population seems to be stable. International protection of coelacanths against commercial interests is needed     

Why coelacanths are not ‘living fossils’

A series of recent studies on extant coelacanths has emphasised the slow rate of molecular and morphological evolution in these species. These studies were based on the assumption that a coelacanth is a ‘living fossil’ that has shown little morphological change since the Devonian, and they proposed a causal link between low molecular evolutionary rate and morphological stasis. Here, we have examined the available molecular and morphological data and show that: (i) low intra‐specific molecular diversity does not imply low mutation rate, (ii) studies not showing low substitution rates in coelacanth are often neglected, (iii) the morphological stability of coelacanths is not supported by paleontological evidence. We recall that intra‐species levels of molecular diversity, inter‐species genome divergence rates and morphological divergence rates are under different constraints and they are not necessarily correlated. Finally, we emphasise that concepts such as ‘living fossil’, ‘basal lineage’, or ‘primitive extant species’ do not make sense from a tree‐thinking perspective. Editor's suggested further reading in BioEssays Tree thinking for all biology: the problem with reading phylogenies as ladders of progress Abstract     

Relationship among coelacanths,lungfishes, and tetrapods: A phylogenetic analysis based on mitochondrial cytochrome oxidase I gene sequences

To clarify the relationship among coelacanths, lungfishes, and tetrapods, the amino acid sequences deduced from the nucleotide sequences of mitochondrial cytochrome oxidase subunit I (COI) genes were compared. The phylogenetic tree of these animals, including the coelacanth Latimeria chalumnae and the lungfish Lepidosiren paradoxa, was inferred by several methods. These analyses consistently indicate a coelacanth/lungfish clade, to which little attention has been paid by previous authors with the exception of some morphologists. Overall evidence of other mitochondrial genes reported previously and the results of this study equally support the coelacanth/lungfish and lungfish/tetrapod clades, ruling out the coelacanth/tetrapod clade.Correspondence to: K. Watanabe 0592     

Coelacanth Conservation Council

Winston Churchill once called a backbencher, who remained silent for nearly twenty years in the British House of Lords and then got up to make a great speech, that coelacanth of a man. Since then the coelacanth has become a metanym for someone or something that rises up from the past with a great message to tell. True to form, the Coelacanth Conservation Council (CCC) newsletter has performed the same phoenix-like transformation; after being moribund for five years, while the editor was employed at a busy commercial aquarium in Cape Town, the newsletter has responded with alacrity to the discovery of coelacanths in Indonesia and will resume its services to coelacanthophiles worldwide.Since the last newsletter was published in December 1993, the world has changed dramatically, especially with respect to information technology. Information on the coelacanth (and every other imaginable topic) is now readily available on the internet; the fun of establishing the first coelacanth internet site (http://www.dinofish.com) is described by Jerry Hamlin in this newsletter. We nevertheless thought that the CCC newsletter provides a unique, hardcopy service by updating the official coelacanth inventory and bibliography and by publishing interesting accounts of recent developments in coelacanth research and conservation. So we are resuming regular publication, thanks to raja laut. In the future, the sequence of coelacanth specimens in the inventory of specimens will not be strictly chronological as information is often received on specimens long after they were caught; we nevertheless consider it worth recording all the specimens that come to our attention, in the order that they are reported to us.     

The Second Recorded Living Coelacanth from North Sulawesi

A detailed account of the second coelacanth specimen known to have been captured in Indonesian waters is provided. The account is written in the official format of the Coelacanth Conservation Council's (CCC) inventory of known specimens of the living coelacanth Latimeria chalumnae, and the specimen is herein numbered CCC no. 175. Morphological measurements and fin ray counts are recorded. A comparison of these measurements and meristic data with those recorded for Comoran specimens of Latimeria chalumnae shows that the present specimen has a similar allometry to L. chalumnae. Ongoing genetic analyses should reveal the depth of divergence between the two known populations of living coelacanths and help determine if this specimen is conspecific with its Comoran counterparts.     

A fiftieth anniversary reflection on the living coelacanth,Latimeria chalumnae: some new interpretations of its natural history and conservation status

Synopsis It all started about 400 million years ago, when representatives of a group of fish-like fleshy-finned creatures appeared in the fossil record (or was it through a childhood dream shared by all of us that we would one day study the coelacanth?). Many of the coelacanth's characters placed them close to the ancestry of terrestrial vertebrates. About 70 million years ago they disappeared from the fossil record. The discovery in 1938 of the first living coelacanth, in 1952 of the second and until now over 200 specimens parallels in excitement an encounter with a live dinosaur on a weekend walk, and in significance even more than that. For this year's 50th anniversary of the famous discovery of the first living coelacanth, we retraced the routes and visited the main actors of this zoological drama. New insights into coelacanth natural history were facilitated by novel interpretation of earlier data and our expeditions to the Comoro Islands, retracing the route of the second specimen, measuring unrecorded specimens, interviewing fishermen and describing their fishing crafts, and taking part in recent events on land and water near the only known habitat of the living coelacanth. Entry into this habitat and observations from the research submersible GEO opened up a new era in coelacanth research. Past studies of preserved specimens, which were caught as an incidental bycatch, were supplemented for the first time by studies of free-living coelacanths in their natural habitat. The first film footage taken from the submersible revealed the entirely unfishlike movements of this creature. Its mode of locomotion is a combination of flying and gliding, interspersed with head stands and belly-up drifts which appear to defy gravity. The narrow range of habitat in which the coelacanth has been encountered has led us to realize how vulnerable this ancient relict is. The members of our expeditions therefore cooperated in establishing an international organisation to coordinate efforts to conserve the coelacanth. Editorial     

Oldest coelacanth, from the Early Devonian of Australia

Coelacanths are well-known sarcopterygian (lobe-finned) fishes, which together with lungfishes are the closest extant relatives of land vertebrates (tetrapods). Coelacanths have both living representatives and a rich fossil record, but lack fossils older than the late Middle Devonian (385-390 Myr ago), conflicting with current phylogenies implying coelacanths diverged from other sarcopterygians in the earliest Devonian (410-415 Myr ago). Here, we report the discovery of a new coelacanth from the Early Devonian of Australia (407-409 Myr ago), which fills in the approximately 20 Myr 'ghost range' between previous coelacanth records and the predicted origin of the group. This taxon is based on a single lower jaw bone, the dentary, which is deep and short in form and possesses a dentary sensory pore, otherwise seen in Carboniferous and younger taxa.     

The complete mitochondrial DNA sequence of the shark Mustelus manazo: evaluating rooting contradictions to living bony vertebrates

A remarkable example of a misleading mitochondrial protein tree is presented, involving ray-finned fishes, coelacanths, lungfishes, and tetrapods, with sea lampreys as an outgroup. In previous molecular phylogenetic studies on the origin of tetrapods, ray-finned fishes have been assumed as an outgroup to the tetrapod/lungfish/coelacanth clade, an assumption supported by morphological evidence. Standard methods of molecular phylogenetics applied to the protein-encoding genes of mitochondria, however, give a bizarre tree in which lamprey groups with lungfish and, therefore, ray-finned fishes are not the outgroup to a tetrapod/lungfish/coelacanth clade. All of the dozens of published phylogenetic methods, including every possible modification to maximum likelihood known to us (such as inclusion of site heterogeneity and exclusion of potentially misleading hydrophobic amino acids), fail to place the ray-finned fishes in a biologically acceptable position. A likely cause of this failure may be the use of an inappropriate outgroup. Accordingly, we have determined the complete mitochondrial DNA sequence from the shark, Mustelus manazo, which we have used as an alternative and more proximal outgroup than the lamprey. Using sharks as the outgroup, lungfish appear to be the closest living relative of tetrapods, although the possibility of a lungfish/coelacanth clade being the sister group of tetrapods cannot be excluded.      

The histological structure of the calcified lung of the fossil coelacanth Axelrodichthys araripensis (Actinistia: Mawsoniidae)

Abstract: The palaeohistological study of the calcified internal organ of Axelrodichthys araripensis Maisey, 1986, a coelacanthiform from the Lower Cretaceous of Brazil (Crato (Aptian) and Santana (Albian) formations of the Araripe Basin), shows that the walls of this organ consist of osseous blades of variable thickness separated from each other by the matrix. This indicates that, in the living individuals, the walls were reinforced by ossified plates, probably separated by conjunctive tissue. This calcified sheath present in Axelrodichthys, as well as in other fossil coelacanths, lies in ventral position relative to the gut and its single anterior opening is located under the opercle, suggesting a direct connection with the pharynx or the oesophagus. The calcified organ of Axelrodichthys, like that of other fossil coelacanths, is here regarded as an ‘ossified lung’ and compared with the ‘fatty lung’ of the extant coelacanth Latimeria. The reinforcement of the pulmonary walls by the overlying osseous blades could be interpreted as a means of adapting volumetric changes in the manner of bellows, a necessary function for ventilation in pulmonary respiration. Other functional hypotheses such as hydrostatic and/or acoustic functions are also discussed.     

First discovery of a primitive coelacanth fin fills a major gap in the evolution of lobed fins and limbs

The fossil record provides unique clues about the primitive pattern of lobed fins, the precursors of digit-bearing limbs. Such information is vital for understanding the evolutionary transition from fish fins to tetrapod limbs, and it guides the choice of model systems for investigating the developmental changes underpinning this event. However, the evolutionary preconditions for tetrapod limbs remain unclear. This uncertainty arises from an outstanding gap in our knowledge of early lobed fins: there are no fossil data that record primitive pectoral fin conditions in coelacanths, one of the three major groups of sarcopterygian (lobe-finned) fishes. A new fossil from the Middle-Late Devonian of Wyoming preserves the first and only example of a primitive coelacanth pectoral fin endoskeleton. The strongly asymmetrical skeleton of this fin corroborates the hypothesis that this is the primitive sarcopterygian pattern, and that this pattern persisted in the closest fish-like relatives of land vertebrates. The new material reveals the specializations of paired fins in the modern coelacanth, as well as in living lungfishes. Consequently, the context in which these might be used to investigate evolutionary and developmental relationships between vertebrate fins and limbs is changed. Our data suggest that primitive actinopterygians, rather than living sarcopterygian fishes and their derived appendages, are the most informative comparators for developmental studies seeking to understand the origin of tetrapod limbs.