Michael I. Coates

A new time-scale for ray-finned fish evolution

The Actinopterygii (ray-finned fishes) is the largest and most diverse vertebrate group, but little is agreed about the timing of its early evolution. Estimates using mitochondrial genomic data suggest that the major actinopterygian clades are much older than divergence dates implied by fossils. Here, the timing of the evolutionary origins of these clades is reinvestigated using morphological, and nuclear and mitochondrial genetic data. Results indicate that existing fossil-based estimates of the age of the crown-group Neopterygii, including the teleosts, Lepisosteus (gar) and Amia (bowfin), are at least 40 Myr too young. We present new palaeontological evidence that the neopterygian crown radiation is a Palaeozoic event, and demonstrate that conflicts between molecular and morphological data for the age of the Neopterygii result, in part, from missing fossil data. Although our molecular data also provide an older age estimate for the teleost crown, this range extension remains unsupported by the fossil evidence. Nuclear data from all relevant clades are used to demonstrate that the actinopterygian whole-genome duplication event is teleost-specific. While the date estimate of this event overlaps the probable range of the teleost stem group, a correlation between the genome duplication and the large-scale pattern of actinopterygian phylogeny remains elusive.

Early tetrapod relationships revisited

In an attempt to investigate differences between the most widely discussed hypotheses of early tetrapod relationships, we assembled a new data matrix including 90 taxa coded for 319 cranial and postcranial characters. We have incorporated, where possible, original observations of numerous taxa spread throughout the major tetrapod clades. A stem‐based (total‐group) definition of Tetrapoda is preferred over apomorphy‐ and node‐based (crown‐group) definitions. This definition is operational, since it is based on a formal character analysis. A PAUP* search using a recently implemented version of the parsimony ratchet method yields 64 shortest trees. Differences between these trees concern: (1) the internal relationships of aistopods, the three selected species of which form a trichotomy; (2) the internal relationships of embolomeres, with Archeria crassidisca and Pholiderpeton scutigerum collapsed in a trichotomy with a clade formed by Anthracosaurus russelli and Pholiderpeton attheyi; (3) the internal relationships of derived dissorophoids, with four amphibamid species forming an unresolved node with a clade consisting of micromelerpetontids and branchiosaurids and a clade consisting of albanerpetontids plus basal crown‐group lissamphibians; (4) the position of albenerpetontids and Eocaecilia micropoda, which form an unresolved node with a trichotomy subtending Karaurus sharovi, Valdotriton gracilis and Triadobatrachus massinoti;(5) the branching pattern of derived diplocaulid nectrideans, with Batrachiderpeton reticulatum and Diceratosaurus brevirostris collapsed in a trichotomy with a clade formed by Diplocaulus magnicornis and Diploceraspis burkei. The results of the original parsimony run ‐ as well as those retrieved from several other treatments of the data set (e.g. exclusion of postcranial and lower jaw data;character reweighting; reverse weighting) ‐ indicate a deep split of early tetrapods between lissamphibian‐ and amniote‐related taxa. Colosteids, Crassigyrinus, Whatcheeria and baphetids are progressively more crownward stemtetrapods. Caerorhachis, embolomeres, gephyrostegids, Solenodonsaurus and seymouriamorphs are progressively more crownward stem‐amniotes. Eucritta is basal to temnospondyls, with crown‐lissamphibians nested within dissorophoids. Westlothiana is basal to Lepospondyli, but evidence for the monophyletic status of the latter is weak. Westlothiana and Lepospondyli form the sister group to diadectomorphs and crown‐group amniotes. Tuditanomorph and microbrachomorph microsaurs are successively more closely related to a clade including proximodistally: (1) lysorophids; (2) Acherontiscus as sister taxon to adelospondyls; (3) scincosaurids plus diplocaulids; (4) urocordylids plus aïstopods. A data set employing cranial characters only places microsaurs on the amniote stem, but forces remaining lepospondyls to appear as sister group to colosteids on the tetrapod stem in several trees. This arrangement is not significantly worse than the tree topology obtained from the analysis of the complete data set. The pattern of sister group relationships in the crownward part of the temnospondyl‐lissamphibian tree re‐emphasizes the important role of dissorophoids in the lissamphibian origin debate. However, no specific dissorophoid can be identiffed as the immediate sister taxon to crown‐group lissamphibians. The branching sequence of various stem‐group amniotes reveals a coherent set of internested character‐state changes related to the acquisition of progressively more terrestrial habits in several Permo‐Carboniferous forms.

The Devonian tetrapod Acanthostega gunnari Jarvik: postcranial anatomy, basal tetrapod interrelationships and patterns of skeletal evolution

The postcranial skeleton of Acanthostega gunnari from the Famennian of East Greenland displays a unique, transitional, mixture of features conventionally associated with fishand tetrapod-like morphologies. The rhachitomous vertebral column has a primitive, barely differentiated atlas-axis complex, encloses an unconstricted notochordal canal, and the weakly ossified neural arches have poorly developed zygapophyses. More derived axial skeletal features include caudal vertebral proliferation and, transiently, neural radials supporting unbranched and unsegmented lepidotrichia. Sacral and post-sacral ribs reiterate uncinate cervical and anterior thoracic rib morphologies: a simple distal flange supplies a broad surface for iliac attachment. The octodactylous forelimb and hindlimb each articulate with an unsutured, foraminate endoskeletal girdle. A broad-bladed femoral shaft with extreme anterior torsion and associated flattened epipodials indicates a paddle-like hindlimb function. Phylogenetic analysis places Acanthostega as the sister-group of Ichthyostega plus all more advanced tetrapods. Tulerpeton appears to be a basal stemamniote plesion, tying the amphibian-amniote split to the uppermost Devonian. Caerorhachis may represent a more derived stem-amniote plesion. Postcranial evolutionary trends spanning the taxa traditionally associated with the fish-tetrapod transition are discussed in detail. Comparison between axial skeletons of primitive tetrapods suggests that plesiomorphic fish-like morphologies were re-patterned in a cranio-caudal direction with the emergence of tetrapod vertebral regionalisation. The evolution of digited limbs lags behind the initial enlargement of endoskeletal girdles, whereas digit evolution precedes the elaboration of complex carpal and tarsal articulations. Pentadactylous limbs appear to have stabilised independently in amniote and amphibian lineages; the colosteid Greererpeton has a pentadactylous manus, indicating that basal amphibian forelimbs may not be restricted to patterns of four digits or less.

A lamprey from the Devonian period of South Africa

Lampreys are the most scientifically accessible of the remaining jawless vertebrates, but their evolutionary history is obscure. In contrast to the rich fossil record of armoured jawless fishes, all of which date from the Devonian period and earlier, only two Palaeozoic lampreys have been recorded, both from the Carboniferous period. In addition to these, the recent report of an exquisitely preserved Lower Cretaceous example demonstrates that anatomically modern lampreys were present by the late Mesozoic era. Here we report a marine/estuarine fossil lamprey from the Famennian (Late Devonian) of South Africa, the identity of which is established easily because many of the key specializations of modern forms are already in place. These specializations include the first evidence of a large oral disc, the first direct evidence of circumoral teeth and a well preserved branchial basket. This small agnathan, Priscomyzon riniensis gen. et sp. nov., is not only more conventionally lamprey-like than other Palaeozoic examples, but is also some 35 million years older. This finding is evidence that agnathans close to modern lampreys had evolved before the end of the Devonian period. In this light, lampreys as a whole appear all the more remarkable: ancient specialists that have persisted as such and survived a subsequent 360 million years.

Dates, nodes and character conflict: addressing the Lissamphibian origin problem

Synopsis Extant amphibians consist of Salientia (frogs), Caudata (salamanders), and Gymnophiona (caecilians). The mutual relationships of these groups are controversial, with either Batrachia (Salientia + Caudata) or Procera (Gymnophiona + Caudata) as emerging clades in recent molecular and morphological analyses. The monophyly of amphibians as a whole is supported by independent data, but their origins and affinities with early tetrapods are debated. A new cladistic analysis of early tetrapods retrieves Temnospondyli (the most species‐rich group of early tetrapods) as the closest relatives of crown group amphibians. One temnospondyl group, the Dissorophoidea, forms a series of consecutive outgroups to crown amphibians. In particular, the Lower Permian amphibamid Doleserpeton is the most derived plesion on the amphibian stem. The Albanerpetontidae, a group of salamander‐like tetrapods ranging from the Jurassic to the Pliocene, are placed as stem Gymnophiona. The shortest trees support the Batrachia hypothesis. However, the Procera hypothesis is not a significantly worse fit for the whole character set. Exhaustive treatment of characters and taxa is the most appropriate way to disentangle contrasting phylogenetic signals in large matrices. Tests of different crown topologies show that placement of amphibians within lepospondyls (e.g. as sister taxon to Lysorophia) is not a significantly worse fit for the whole character set than a close temnospondyl‐lissamphibian relationship. However, the latter phylogenetic hypothesis best captures the most coherent assembly of derived lissamphibian apomorphies.

Acanthodes and shark-like conditions in the last common ancestor of modern gnathostomes

Acanthodians, an exclusively Palaeozoic group of fish, are central to a renewed debate on the origin of modern gnathostomes: jawed vertebrates comprising Chondrichthyes (sharks, rays and ratfish) and Osteichthyes (bony fishes and tetrapods). Acanthodian internal anatomy is primarily understood from Acanthodes bronni because it remains the only example preserved in substantial detail, central to which is an ostensibly osteichthyan braincase. For this reason, Acanthodes has become an indispensible component in early gnathostome phylogenies. Here we present a new description of the Acanthodes braincase, yielding new details of external and internal morphology, notably the regions surrounding and within the ear capsule and neurocranial roof. These data contribute to a new reconstruction that, unexpectedly, resembles early chondrichthyan crania. Principal coordinates analysis of a character–taxon matrix including these new data confirms this impression: Acanthodes is quantifiably closer to chondrichthyans than to osteichthyans. However, phylogenetic analysis places Acanthodes on the osteichthyan stem, as part of a well-resolved tree that also recovers acanthodians as stem chondrichthyans and stem gnathostomes. As such, perceived chondrichthyan features of the Acanthodes cranium represent shared primitive conditions for crown group gnathostomes. Moreover, this increasingly detailed picture of early gnathostome evolution highlights ongoing and profound anatomical reorganization of vertebrate crania after the origin of jaws but before the divergence of living clades.

End-Devonian extinction and a bottleneck in the early evolution of modern jawed vertebrates

The Devonian marks a critical stage in the early evolution of vertebrates: It opens with an unprecedented diversity of fishes and closes with the earliest evidence of limbed tetrapods. However, the latter part of the Devonian has also been characterized as a period of global biotic crisis marked by two large extinction pulses: a “Big Five” mass extinction event at the Frasnian-Famennian stage boundary (374 Ma) and the less well-documented Hangenberg event some 15 million years later at the Devonian-Carboniferous boundary (359 Ma). Here, we report the results of a wide-ranging analysis of the impact of these events on early vertebrate evolution, which was obtained from a database of vertebrate occurrences sampling over 1,250 taxa from 66 localities spanning Givetian to Serpukhovian stages (391 to 318 Ma). We show that major vertebrate clades suffered acute and systematic effects centered on the Hangenberg extinction involving long-term losses of over 50% of diversity and the restructuring of vertebrate ecosystems worldwide. Marine and nonmarine faunas were equally affected, precluding the existence of environmental refugia. The subsequent recovery of previously diverse groups (including placoderms, sarcopterygian fish, and acanthodians) was minimal. Tetrapods, actinopterygians, and chondrichthyans, all scarce within the Devonian, undergo large diversification events in the aftermath of the extinction, dominating all subsequent faunas. The Hangenberg event represents a previously unrecognized bottleneck in the evolutionary history of vertebrates as a whole and a historical contingency that shaped the roots of modern biodiversity.

Fins, limbs, and tails: outgrowths and axial patterning in vertebrate evolution

Current phylogenies show that paired fins and limbs are unique to jawed vertebrates and their immediate ancestry. Such fins evolved first as a single pair extending from an anterior location, and later stabilized as two pairs at pectoral and pelvic levels. Fin number, identity, and position are therefore key issues in vertebrate developmental evolution. Localization of the AP levels at which developmental signals initiate outgrowth from the body wall may be determined by Hox gene expression patterns along the lateral plate mesoderm. This regionalization appears to be regulated independently of that in the paraxial mesoderm and axial skeleton. When combined with current hypotheses of Hox gene phylogenetic and functional diversity, these data suggest a new model of fin/limb developmental evolution. This coordinates body wall regions of outgrowth with primitive boundaries established in the gut, as well as the fundamental nonequivalence of pectoral and pelvic structures. BioEssays 20:371–381, 1998.

Evolutionary patterns in early tetrapods. I. Rapid initial diversification followed by decrease in rates of character change

Although numerous studies have examined morphological diversification during major radiations of marine taxa, much less attention has been paid to terrestrial radiations. Here, we examine rates of character change over phylogeny and over time for Palaeozoic limbed tetrapods. Palaeozoic tetrapods show significant decreases in rates of character change whether the rate is measured per sampled cladistic branch or per million years along phylogeny. Given changes per branch, rates decrease significantly from the Devonian through the Pennsylvanian, but not from the Pennsylvanian through the Permian. Given changes per million years, rates decrease significantly over each boundary, although the decrease is least significant over the Pennsylvanian–Permian boundary. Decreasing rates per million years through the Permian might be an artefact of the method being able to ascribe longer durations to Permian branches than to Carboniferous ones; however, it is difficult to ascribe the general pattern of decreasing rates of change over time to sampling biases or methodological biases. Thus, the results implicate biological explanations for this pattern.

Fins to limbs: what the fossils say1

SUMMARY A broad phylogenetic review of fins, limbs, and girdles throughout the stem and base of the crown group is needed to get a comprehensive idea of transformations unique to the assembly of the tetrapod limb ground plan. In the lower part of the tetrapod stem, character state changes at the pectoral level dominate; comparable pelvic level data are limited. In more crownward taxa, pelvic level changes dominate and repeatedly precede similar changes at pectoral level. Concerted change at both levels appears to be the exception rather than the rule. These patterns of change are explored by using alternative treatments of data in phylogenetic analyses. Results highlight a large data gap in the stem group preceding the first appearance of limbs with digits. It is also noted that the record of morphological diversity among stem tetrapods is somewhat worse than that of basal crown group tetrapods. The pre‐limbed evolution of stem tetrapod paired fins is marked by a gradual reduction in axial segment numbers (mesomeres); pectoral fins of the sister group to limbed tetrapods include only three. This reduction in segment number is accompanied by increased regional specialization, and these changes are discussed with reference to the phylogenetic distribution of characteristics of the stylopod, zeugopod, and autopod.