Deep-ocean origin of the freshwater eels

Of more than 800 species of eels of the order Anguilliformes, only freshwater eels (genus Anguilla with 16 species plus three subspecies) spend most of their lives in freshwater during their catadromous life cycle. Nevertheless, because their spawning areas are located offshore in the open ocean, they migrate back to their specific breeding places in the ocean, often located thousands of kilometres away. The evolutionary origin of such enigmatic behaviour, however, remains elusive because of the uncertain phylogenetic position of freshwater eels within the principally marine anguilliforms. Here, we show strong evidence for a deep oceanic origin of the freshwater eels, based on the phylogenetic analysis of whole mitochondrial genome sequences from 56 species representing all of the 19 anguilliform families. The freshwater eels occupy an apical position within the anguilliforms, forming a highly supported monophyletic group with various oceanic midwater eel species. Moreover, reconstruction of the growth habitats on the resulting tree unequivocally indicates an origination of the freshwater eels from the midwater of the deep ocean. This shows significant concordance with the recent collection of mature adults of the Japanese eel in the upper midwater of the Pacific, suggesting that they have retained their evolutionary origin as a behavioural trait in their spawning areas.     

Phylogenetic relationships of elopomorph fishes inferred from mitochondrial ribosomal DNA sequences

The superorder Elopomorpha, a grouping which includes all teleost fishes that possess a specialized leptocephalous larva [true eels (Anguilliformes), gulpers and bobtail snipe eels (Saccopharyngiformes), bonefishes, spiny eels, and halosaurs (Albuliformes, including Notacanthiformes), ladyfishes and tarpons (Elopiformes, including Megalopiformes)] comprises >800 species for which phylogenetic relationships are poorly understood. In the present study, we analyzed mitochondrial DNA sequences in segments of the 12S and 16S rRNA genes in 33 elopomorph taxa encompassing all of the previously proposed orders, and 9 of the 15 currently recognized families of the Anguilliformes, as well as outgroup representatives from the superorders Osteoglossomorpha (nine species) and Clupeomorpha (three species), to develop phylogenetic hypotheses based on distance and parsimony methods. Both methods failed to support the monophyly of the Elopomorpha, casting doubt on the validity of the leptocephalus as an elopomorph synapomorphy. The orders Elopiformes, Albuliformes, and Anguilliformes, however, were resolved as monophyletic assemblages. Parsimony analysis supported the separation of the Anguilliformes into two groups (primitive and advanced) based on the presence of divided versus fused frontal bones. In addition, the molecular data indicated a close affinity of the anguilliform Thalassenchelys coheni (incertae sedis), known only from the leptocephalus, with the family Serrivomeridae. The implications of these data as regards the evolution of the elopomorph assemblage are discussed.     

Some nematodes from eels (Anguilliformes: Anguillidae) in Japan,with descriptions of two new species

Systematic Parasitology - Recent occasional examinations of two species of eels (Anguilliformes: Anguillidae) in Japan, the Japanese eel Anguilla japonica Temminck & Schlegel from central...     

Molecular phylogeny of elopomorph fishes inferred from mitochondrial 12S ribosomal RNA sequences

Wang, C. H., Kuo, C. H., Mok, H. K. & Lee, S. C. (2003). Molecular phylogeny of elopomorph fishes inferred from mitochondrial 12S ribosomal RNA sequences. — Zoologica Scripta , 32 , 231–241.
Fishes of the superorder Elopomorpha include tenpounders ( Elops ), tarpon ( Megalops ), bonefishes ( Albula ), spiny eels ( Notacanthus ), apodes, and gulper eels; despite highly diversified morphological features, all undergo a leptocephalus larval stage and are thus treated (although with some dissenting views) as monophyletic. Following analysis of 12S rRNA sequences we present results that confirm a monophyletic Elopomorpha clearly separated from Clupeomorpha. Elops and Megalops share a common ancestor and are clustered in a subclade at the bottom of Elopomorpha. Albula and Notacanthus share a common ancestor forming the sister group to Anguilliformes. Saccopharyngiformes is not a sister group of Anguilliformes, as the single species sequenced here is nested deeply within the latter. Neither the suborder Congroidei nor the superfamily Congroidea within Anguilliformes are monophyletic.     

Mitogenomic evidence for the monophyly of elopomorph fishes (Teleostei) and the evolutionary origin of the leptocephalus larva

The monophyly of Elopomorpha (eels and their relatives) has long been one of the most problematic issues in systematic ichthyology. Since established the Elopomorpha based on the existence of the leaf-like larval form, termed a leptocephalus, no one has corroborated their monophyly using character matrices derived from both morphological and molecular data during the last 30 years. We investigated their monophyly and interrelationships at the ordinal level using complete mitochondrial genomic (mitogenomic) data from 33 purposefully chosen species (data for nine species being newly determined during the study) that fully represent the major teleostean and elopomorph lineages. Partitioned Bayesian analyses were conducted with the two data sets that comprised concatenated nucleotide sequences from 12 protein-coding genes (with and without third codon positions), 22 transfer RNA genes, and two ribosomal RNA genes. The resultant trees were well resolved and largely congruent, with most internal branches being supported by high statistical values. Mitogenomic data strongly supported the monophyly of Elopomorpha, indicating the validity of the leptocephalus as an elopomorph synapomorphy. The order Elopiformes occupied the most basal position in the elopomorph phylogeny, with the Albuliformes and a clade comprising the Anguilliformes and the Saccopharyngiformes forming a sister group. The most parsimonious reconstruction of the three previously recognized, distinct larval types of elopomorphs onto the molecular phylogeny revealed that one of the types (fork-tailed type) had originated as the common ancestor of the Elopomorpha, the other two (filament-tailed and round-tailed types) having diversified separately in two more derived major clades.     

Highly differentiated and conserved sex chromosome in fish species (Aulopus japonicus: Teleostei, Aulopidae)

While highly differentiated and long-conserved sex chromosomes such as XY and ZW chromosomes are observed, respectively, in mammalian and avian species, no counterparts to such chromosomes were observed in fish until we reported in the previous study that well-conserved and highly differentiated ZW sex chromosomes existed in the family of Synodontidae. Then, the problem was if the evolutionary history of the fish ZW chromosomes was long enough to be comparable to the mammalian and avian counterparts. To tackle the problem, we had to extend our finding of the fish sex chromosomes further than a family alone. For this purpose, we chose Aulopus japonicus that belonged to one of the related families to Synodontidae.Our cytogenetic and fluorescence in situ hybridization (FISH) analyses have clearly demonstrated that A. japonicus also has ZW chromosomes. We have also found that 5S rDNA clusters are located on the Z and W chromosomes in this species. Using nontranscribed intergenic sequences in the 5S rDNA clusters as PCR primers, we successfully amplified a 6-kb-long female-specific sequence on the W chromosome. The 6-kb-long sequence contained one transposable element and two tRNA sequences. The function of the sequence remains to be studied. Our Southern blot analysis confirmed that the 6-kb sequence was located only on the W chromosome.Therefore, it is now said that highly differentiated ZW chromosomes have been conserved over two fish families. As these families were reported to have been diverged 30-60 million years ago, the fish ZW chromosomes have an evolutionary history corresponding to the history of the families. This is perhaps the first case that fish sex chromosomes are shown to have such a long evolutionary lineage.     

Elongation of the body in eels

The shape of the body affects how organisms move, where they live, and how they feed. One body plan that has long engaged the interest of both evolutionary biologists and functional morphologists is axial elongation. There is a growing interest in the correlates and evolution of elongation within different terrestrial and aquatic vertebrate clades. At first glance, Anguilliformes may appear to exhibit a single cylindrical form but there is considerable diversity underlying this seemingly simplified body plan. Here, we explore evolution of the axial skeleton in 54 anguilliform taxa and some close relatives. We describe the diversity of axial elongation as well as investigate how characters such as head length, branchial-arch length, and shape of the pectoral fins correlate with vertebral number to possibly facilitate changes in absolute diameter of the body. Overall, we find that precaudal vertebral numbers and caudal vertebral numbers are evolving independently across elopomorph fishes. We also find that precaudal and caudal vertebral aspect ratios are evolving together across elopomorph fishes. When focusing within Anguilliformes we find striking diversity in the mechanisms of elongation of the body, including almost every trend for axial elongation known within actinopterygian fishes. The three major clades of eels we examined have slightly different mechanisms of elongation. We also find a suite of morphological characters associated with elongation in anguilliform fishes that appears to coincide with a more fossorial lifestyle such as high elongation ratios, a more posteriorly extended-branchial region, and a reduction in the size of the pectoral fins. Lastly, we point out that a diverse range of derived behaviors such as head- and tail-first burrowing, rotational feeding, and knotting around prey are only found in long cylindrical vertebrates.     

Effects of an adaptive zone shift on morphological and ecological diversification in terapontid fishes

A fundamental goal of evolutionary ecology is understanding the processes responsible for contemporary patterns of morphological diversity and species richness. Transitions across the marine–freshwater interface are regarded as key triggers for adaptive radiation of many clades. Using the Australian terapontid fish family as a model system we employed phylogenetic analyses to compare the rates of ecological (dietary) and morphological evolution between marine and freshwater species of the family. Results suggested significantly higher rates of phenotypic evolution in key dietary and morphological characters in freshwater species compared to marine counterparts. Moreover, there was significant correlation between several of these dietary and morphological characters, suggesting an underlying ecomorphological aspect to these greater rates of phenotypic evolution in freshwater clades. Australia’s biogeographic history, which has precluded colonisation by many of the major ostariophysan fish families that make up much global freshwater fish diversity, appears to have provided the requisite ‘ecological opportunity’ to facilitate the radiation of invading marine-derived fish clades.     

Continuous and arrested morphological diversification in sister clades of characiform fishes: a phylomorphospace approach

Understanding how and why certain clades diversify greatly in morphology whereas others do not remains a major theme in evolutionary biology. Projecting families of phylogenies into multivariate morphospaces can distinguish two scenarios potentially leading to unequal morphological diversification: unequal magnitude of change per phylogenetic branch, and unequal efficiency in morphological innovation. This approach is demonstrated using a case study of skulls in sister clades within the South American fish superfamily Anostomoidea. Unequal morphological diversification in this system resulted not from the morphologically diverse clade changing more on each phylogenetic branch, but from that clade distributing an equal amount of change more widely through morphospace and innovating continually. Although substantial morphological evolution occurred throughout the less diverse clade's history, most of that clade's expansion in morphospace occurred in the most basal branches, and more derived portions of that radiation oscillated within previously explored limits. Because simulations revealed that there is a maximum 2.7% probability of generating two clades that differ so greatly in the density of lineages within morphospace under a null Brownian model, the observed difference in pattern likely reflects a difference in the underlying evolutionary process. Clade-specific factors that may have promoted or arrested morphological diversification are discussed.     

Mitochondrial and nuclear genes suggest that stony corals are monophyletic but most families of stony corals are not (Order Scleractinia, Class Anthozoa, Phylum Cnidaria)

Modern hard corals (Class Hexacorallia; Order Scleractinia) are widely studied because of their fundamental role in reef building and their superb fossil record extending back to the Triassic. Nevertheless, interpretations of their evolutionary relationships have been in flux for over a decade. Recent analyses undermine the legitimacy of traditional suborders, families and genera, and suggest that a non-skeletal sister clade (Order Corallimorpharia) might be imbedded within the stony corals. However, these studies either sampled a relatively limited array of taxa or assembled trees from heterogeneous data sets. Here we provide a more comprehensive analysis of Scleractinia (127 species, 75 genera, 17 families) and various outgroups, based on two mitochondrial genes (cytochrome oxidase I, cytochrome b), with analyses of nuclear genes (ss-tubulin, ribosomal DNA) of a subset of taxa to test unexpected relationships. Eleven of 16 families were found to be polyphyletic. Strikingly, over one third of all families as conventionally defined contain representatives from the highly divergent "robust" and "complex" clades. However, the recent suggestion that corallimorpharians are true corals that have lost their skeletons was not upheld. Relationships were supported not only by mitochondrial and nuclear genes, but also often by morphological characters which had been ignored or never noted previously. The concordance of molecular characters and more carefully examined morphological characters suggests a future of greater taxonomic stability, as well as the potential to trace the evolutionary history of this ecologically important group using fossils.     

Phylogenetic effects on functional traits and life history strategies of Australian freshwater fish

Understanding the biogeographic and phylogenetic basis to interspecific differences in species’ functional traits is a central goal of evolutionary biology and community ecology. We quantify the extent of phylogenetic influence on functional traits and life‐history strategies of Australian freshwater fish to highlight intercontinental differences as a result of Australia's unique biogeographic and evolutionary history. We assembled data on life history, morphological and ecological traits from published sources for 194 Australian freshwater species. Interspecific variation among species could be described by a specialist–generalist gradient of variation in life‐history strategies associated with spawning frequency, fecundity and spawning migration. In general, Australian fish showed an affinity for life‐history strategies that maximise fitness in hydrologically unpredictable environments. We also observed differences in trait lability between and within life history, morphological and ecological traits where in general morphological and ecological traits were more labile. Our results showed that life‐history strategies are relatively evolutionarily labile and species have potentially evolved or colonised in freshwaters frequently and independently allowing them to maximise population performance in a range of environments. In addition, reproductive guild membership showed strong phylogenetic constraint indicating that evolutionary history is an important component influencing the range and distribution of reproductive strategies in extant species assemblages. For Australian freshwater fish, biogeographic and phylogenetic history contribute to broad taxonomic differences in species functional traits, while finer scale ecological processes contribute to interspecific differences in smaller taxonomic units. These results suggest that the lability or phylogenetic relatedness of different functional traits affects their suitability for testing hypothesis surrounding community level responses to environmental change.     

Contrasting patterns of density‐dependent selection at different life stages can create more than one fast–slow axis of life‐history variation

There has been much recent research interest in the existence of a major axis of life‐history variation along a fast–slow continuum within almost all major taxonomic groups. Eco‐evolutionary models of density‐dependent selection provide a general explanation for such observations of interspecific variation in the "pace of life." One issue, however, is that some large‐bodied long‐lived “slow” species (e.g., trees and large fish) often show an explosive “fast” type of reproduction with many small offspring, and species with “fast” adult life stages can have comparatively “slow” offspring life stages (e.g., mayflies). We attempt to explain such life‐history evolution using the same eco‐evolutionary modeling approach but with two life stages, separating adult reproductive strategies from offspring survival strategies. When the population dynamics in the two life stages are closely linked and affect each other, density‐dependent selection occurs in parallel on both reproduction and survival, producing the usual one‐dimensional fast–slow continuum (e.g., houseflies to blue whales). However, strong density dependence at either the adult reproduction or offspring survival life stage creates quasi‐independent population dynamics, allowing fast‐type reproduction alongside slow‐type survival (e.g., trees and large fish), or the perhaps rarer slow‐type reproduction alongside fast‐type survival (e.g., mayflies—short‐lived adults producing few long‐lived offspring). Therefore, most types of species life histories in nature can potentially be explained via the eco‐evolutionary consequences of density‐dependent selection given the possible separation of demographic effects at different life stages.     

Evolution of dimorphisms of the proteasome subunit beta type 8 gene (PSMB8) in basal ray-finned fish

The proteasome subunit beta type 8 (PSMB8) gene encodes a catalytic subunit of immunoproteasome that plays a central role in the processing of antigenic peptides presented by major histocompatibility complex class I molecules. The A- and F-type alleles defined by the 31st amino acid residue determining cleaving specificity have been identified from ray-finned fish, amphibia, and reptiles. These two types show extremely long-term trans-species polymorphism in Polypteriformes, Cypriniformes, and Salmoniformes, suggesting the presence of very ancient lineages termed A and F. To elucidate the evolution of the PSMB8 dimorphism in basal ray-finned fish, we analyzed Pantodon buchholzi (Osteoglossiformes), seven species of Anguilliformes, and Hypomesus nipponensis (Osmeriformes). Both A and F lineage sequences were identified from P. buchholzi and H. nipponensis, confirming that these two lineages have been conserved by basal ray-finned fish. However, both the A- and F-type alleles found in Anguilliformes species belonged to the F lineage irrespective of their types. This apparently suggests that the A lineage was lost in the common ancestor of Anguilliformes, and recovery of the A type within the F lineage occurred in Anguilliformes. The apparent loss of the F lineage and recovery of the F type within the A lineage have already been reported from tetrapods and higher teleosts. However, this is the first report on the reverse situation and reveals the dynamic evolution of the PSMB8 dimorphism.     

Molecular phylogeny and evolution of the freshwater eel, genus Anguilla

A molecular phylogenetic analysis was conducted on all of the known catadromous eel species of the genus Anguilla to assess their relationships and evolutionary history. The analyses of a total of 1427 bp of the mitochondrial 16S ribosomal RNA and 1140 bp of the complete cytochrome b gene sequences suggested that the genus Anguilla was monophyletic in origin, with A. borneensis as the most basal species. Four clades/species groups that correspond to their geographical ranges were indicated, Indo-Atlantic (three species), Oceania (two species), tropical Pacific (two species), and Indo-Pacific (five species), with ambiguous positions for A. japonica and A. reinhardti. This grouping conflicts with that of a previous morphological study, since the broad undivided maxillary and short-fin type, which were thought to be phylogenetically important, were paraphyletic in the molecular analysis. However, the molecular phylogeny and the present geographic distribution of species suggested historical dispersion of the genus Anguilla according to the Tethys corridor hypothesis, which proposed that anguillid eels originated near present-day Indonesia and dispersed westward along paleo-circumglobal equatorial currents. The westward-moving strain entered the paleo-Atlantic through the Tethys Sea and was ancestral to present-day European and American species.     

Phylogeny of the snailfishes (Teleostei: Liparidae) based on molecular and morphological data

Liparidae (snailfishes) is one of the most diverse and abundant fish families in polar and deep-sea habitats. However, the evolution of this family is poorly known because of the rarity of many species and difficulties in scoring morphological characters. We perform phylogenetic analyses of Liparidae using sequences from two mtDNA genes, 16S (585 bp) and cytochrome b (426 bp), and 84 morphological characters from 24 species of Liparidae and 4 species of Cyclopteridae (outgroup). The present study confirms earlier hypotheses that the shallow-water genera, such as Liparis and Crystallichthys, occupy basal positions and that deep-water genera, such as Careproctus, Elassodiscus, Rhinoliparis, Paraliparis, Rhodichthys and Psednos, are increasingly derived. The later two genera form a terminal clade which does not include Paraliparis. The topology shows that the family has undergone a reductive type of evolution, with a gradual loss of characters (e.g. sucking disc/pelvic fins, pseudobranchial filaments, skin spinules). Nectoliparis, which had previously been placed either as the basal most genus or among the most derived genera, are found to occupy the most basal position among the taxa analyzed. This result indicates that the sucking disc has been lost at least twice during the evolution of the Liparidae. The basal position of Nectoliparis is supported by its plesiomorphic otolith morphology, whereas an advanced overgrown otolith ostium, unique among teleosts, is found to be apomorphic for a clade containing the derived genera: Paraliparis, Psednos, Rhinoliparis and Rhodichthys. We also identify the presence of probable nuclear inserts of mitochondrial DNA (Numts) in three species of Careproctus and in Elassodiscus caudatus.     

The joint evolution of the Myxozoa and their alternate hosts: A cnidarian recipe for success and vast biodiversity

The relationships between parasites and their hosts are intimate, dynamic and complex; the evolution of one is inevitably linked to the other. Despite multiple origins of parasitism in the Cnidaria, only parasites belonging to the Myxozoa are characterized by a complex life cycle, alternating between fish and invertebrate hosts, as well as by high species diversity. This inspired us to examine the history of adaptive radiations in myxozoans and their hosts by determining the degree of congruence between their phylogenies and by timing the emergence of myxozoan lineages in relation to their hosts. Recent genomic analyses suggested a common origin of Polypodium hydriforme, a cnidarian parasite of acipenseriform fishes, and the Myxozoa, and proposed fish as original hosts for both sister lineages. We demonstrate that the Myxozoa emerged long before fish populated Earth and that phylogenetic congruence with their invertebrate hosts is evident down to the most basal branches of the tree, indicating bryozoans and annelids as original hosts and challenging previous evolutionary hypotheses. We provide evidence that, following invertebrate invasion, fish hosts were acquired multiple times, leading to parallel cospeciation patterns in all major phylogenetic lineages. We identify the acquisition of vertebrate hosts that facilitate alternative transmission and dispersion strategies as reason for the distinct success of the Myxozoa, and identify massive host specification‐linked parasite diversification events. The results of this study transform our understanding of the origins and evolution of parasitism in the most basal metazoan parasites known.     

Formation and reduction of provisional ventral foregut diverticulum in the embryos of Anguilliformes as the recapitulation of lungs

We described the development and subsequent reduction of ventral foregut diverticulum in the early ontogenesis of Anguilliformes in plankton samples collected in the coastal waters of central Vietnam. The diverticulum is a provisional structure derived from the ventral-lateral area of the caudal esophagus. It develops as a protrusion from the esophagus wall and consists of one cell layer. An increase in the volume of the diverticulum results from the proliferation of these cells and transformation of their shape. It was found that the development of the ventral diverticulum in eels is similar to the early stages of lungs formation in other vertebrates. The formation of ventral diverticulum of the esophagus was recorded in all studied embryos. The time and the extent of its development differs between species and can serve as an additional morphological character in the taxonomic identification of eels at early stages of their ontogeny.     

The Primitive Thylakoid-Less Cyanobacterium Gloeobacter Is a Common Rock-Dwelling Organism

Cyanobacteria are an ancient group of photosynthetic prokaryotes, which are significant in biogeochemical cycles. The most primitive among living cyanobacteria, Gloeobacter violaceus, shows a unique ancestral cell organization with a complete absence of inner membranes (thylakoids) and an uncommon structure of the photosynthetic apparatus. Numerous phylogenetic papers proved its basal position among all of the organisms and organelles capable of plant-like photosynthesis (i.e., cyanobacteria, chloroplasts of algae and plants). Hence, G. violaceus has become one of the key species in evolutionary study of photosynthetic life. It also numbers among the most widely used organisms in experimental photosynthesis research. Except for a few related culture isolates, there has been little data on the actual biology of Gloeobacter, being relegated to an “evolutionary curiosity” with an enigmatic identity. Here we show that members of the genus Gloeobacter probably are common rock-dwelling cyanobacteria. On the basis of morphological, ultrastructural, pigment, and phylogenetic comparisons of available Gloeobacter strains, as well as on the basis of three new independent isolates and historical type specimen, we have produced strong evidence as to the close relationship of Gloeobacter to a long known rock-dwelling cyanobacterial morphospecies Aphanothece caldariorum. Our results bring new clues to solving the 40 year old puzzle of the true biological identity of Gloeobacter violaceus, a model organism with a high value in several biological disciplines. A probable broader distribution of Gloeobacter in common wet-rock habitats worldwide is suggested by our data, and its ecological meaning is discussed taking into consideration the background of cyanobacterial evolution. We provide observations of previously unknown genetic variability and phenotypic plasticity, which we expect to be utilized by experimental and evolutionary researchers worldwide.     

High connectivity among habitats precludes the relationship between dispersal and range size in tropical reef fishes

The hypothesis that pelagic larval duration (PLD) influences range size in marine species with a benthic adult stage and a pelagic larval period is intuitively attractive; yet, studies conducted to date have failed to support it. A possibility for the lack of a relationship between PLD and range size may stem from the failure of past studies to account for the effect of species evolutionary ages, which may add to the dispersal capabilities of species. However, if dispersal over ecological (i.e. PLD) and across evolutionary (i.e. species evolutionary age) time scales continues to show no effect on range size then an outstanding question is why? Here we collected data on PLD, evolutionary ages and range sizes of seven tropical fish families (five families were reef‐associated and two have dwell demersal habitats) to explore the independent and interactive effects of PLD and evolutionary age on range size. Separate analyses on each family showed that even after controlling for evolutionary age, PLD has an insignificant or a very small effect on range size. To shed light on why dispersal has such a limited effect on range size, we developed a global ocean circulation model to quantify the connectivity among tropical reefs relative to the potential dispersal conferred by PLD. We found that although there are several areas of great isolation in the tropical oceans, most reef habitats are within the reach of most species given their PLDs. These results suggest that the lack of habitat isolation can potentially render the constraining effect of dispersal on range size insignificant and explain why dispersal does not relate to range size in reef fishes.