Publications by authors named "Michel Laurin"

31 Publications

A microanatomical and histological study of the scales of the Devonian sarcopterygian Miguashaia bureaui and the evolution of the squamation in coelacanths.

J Anat 2021 Mar 21. Epub 2021 Mar 21.

Département Origines & Évolution, UMR 7207 (MNHN-Sorbonne Université-CNRS), CR2P, Centre de Recherche en Paléontologie-Paris, Muséum national d'Histoire naturelle, Paris, France.

Coelacanths have traditionally been described as morphologically conservative throughout their long evolutionary history, which spans more than 400 million years. After an initial burst during the Devonian, a morphological stasis was long thought to have prevailed since the Carboniferous, as shown by the extant Latimeria. New fossil discoveries have challenged this view, with punctual and sometimes unusual departures from the general coelacanth Bauplan. The dermal skeleton is considered to represent one, if not the main, example of morphological stasis in coelacanth evolution and as a consequence, has remained poorly surveyed. The lack of palaeohistological data on the dermoskeleton has resulted in a poor understanding of the early establishment and evolution of the coelacanth squamation. Here we describe the scales of Miguashaia bureaui from the Upper Devonian of Miguasha, Québec (Canada), revealing histological data for a Palaeozoic coelacanth in great detail and adding to our knowledge on the dermal skeleton of sarcopterygians. Miguashaia displays rounded scales ornamented by tubercules and narrow ridges made of dentine and capped with enamel. At least two generations of superimposed odontodes occur, which is reminiscent of the primitive condition of stem osteichthyans like Andreolepis or Lophosteus, and onychodonts like Selenodus. The middle vascular layer is well developed and shows traces of osteonal remodelling. The basal plate consists of a fully mineralised lamellar bone with a repetitive rotation pattern every five layers indicating a twisted plywood-like arrangement of the collagen plies. Comparisons with the extant Latimeria and other extinct taxa show that these features are consistently conserved across coelacanth evolution with only minute changes in certain taxa. The morphological and histological features displayed in the scales of Miguashaia enable us to draw a comprehensive picture of the onset of the coelacanth squamation and to propose and discuss evolutionary scenarios for the coelacanth dermoskeleton.
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http://dx.doi.org/10.1111/joa.13428DOI Listing
March 2021

Raising names from the dead: A time-calibrated phylogeny of frog shells (Bursidae, Tonnoidea, Gastropoda) using mitogenomic data.

Mol Phylogenet Evol 2021 03 11;156:107040. Epub 2020 Dec 11.

Institut de Systématique, Évolution, Biodiversité ISYEB - Muséum national d'Histoire naturelle, CNRS, Sorbonne Université, EPHE, Université des Antilles, 57 rue Cuvier, CP26, F-75005 Paris, France.

With 59 Recent species, Bursidae, known as «frog shells», are a small but widely distributed group of tropical and subtropical gastropods that are most diverse in the Indo-West Pacific. The present study is aimed at reconstructing phylogenetic relationships of bursid gastropods based on extensive and representative taxon sampling. Five genetic markers (cytochrome c oxidase subunit I (cox1), 16 s and 12 s rRNA mitochondrial genes, 28 s rRNA and Histone H3 nuclear gene) were sequenced for over 30 species in every known genus but Crossata. Furthermore, we sequenced the complete mt-genome of 9 species (10 specimens) (Aspa marginata, Marsupina bufo, Korrigania quirihorai, Korrigania fijiensis, Tutufa rubeta, Bursa lamarckii, Lampasopsis rhodostoma (twice), Bufonaria perelegans and Bursa aff. tuberosissima). Our analysis recovered Bursidae as a monophyletic group, whereas the genus Bursa was found to be polyphyletic. The genera Talisman and Dulcerana are resurrected and the genera Alanbeuella gen. nov. and Korrigania gen. nov. are described. Dating analysis using 21 extinct taxa for node and simplified tip calibrations was performed, showing a diversification of the group in two phases. Diversification may be linked to tectonic events leading to biodiversity relocation from the western Tethys toward the Indo-Pacific.
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http://dx.doi.org/10.1016/j.ympev.2020.107040DOI Listing
March 2021

Exact Distribution of Divergence Times from Fossil Ages and Tree Topologies.

Syst Biol 2020 11;69(6):1068-1087

CR2P ("Centre de Recherches de Paléontologie - Paris; UMR 7207), CNRS/MNHN/Sorbonne Université, Muséum National d'Histoire Naturelle, Paris, France.

Being given a phylogenetic tree of both extant and extinct taxa in which the fossil ages are the only temporal information (namely, in which divergence times are considered unknown), we provide a method to compute the exact probability distribution of any divergence time of the tree with regard to any speciation (cladogenesis), extinction, and fossilization rates under the Fossilized Birth-Death model. We use this new method to obtain a probability distribution for the age of Amniota (the synapsid/sauropsid or bird/mammal divergence), one of the most-frequently used dating constraints. Our results suggest an older age (between about 322 and 340 Ma) than has been assumed by most studies that have used this constraint (which typically assumed a best estimate around 310-315 Ma) and provide, for the first time, a method to compute the shape of the probability density for this divergence time. [Divergence times; fossil ages; fossilized birth-death model; probability distribution.].
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http://dx.doi.org/10.1093/sysbio/syaa021DOI Listing
November 2020

The relationship between genome size and metabolic rate in extant vertebrates.

Philos Trans R Soc Lond B Biol Sci 2020 03 13;375(1793):20190146. Epub 2020 Jan 13.

Department of Earth Sciences, Montana State University, Bozeman, MT 59717, USA.

Genome size has long been hypothesized to affect the metabolic rate in various groups of animals. The mechanism behind this proposed association is the nucleotypic effect, in which large nucleus and cell sizes influence cellular metabolism through surface area-to-volume ratios. Here, we provide a review of the recent literature on the relationship between genome size and metabolic rate. We also conduct an analysis using phylogenetic comparative methods and a large sample of extant vertebrates. We find no evidence that the effect of genome size improves upon models in explaining metabolic rate variation. Not surprisingly, our results show a strong positive relationship between metabolic rate and body mass, as well as a substantial difference in metabolic rate between endothermic and ectothermic vertebrates, controlling for body mass. The presence of endothermy can also explain elevated rate shifts in metabolic rate whereas genome size cannot. We further find no evidence for a punctuated model of evolution for metabolic rate. Our results do not rule out the possibility that genome size affects cellular physiology in some tissues, but they are consistent with previous research suggesting little support for a direct functional connection between genome size and basal metabolic rate in extant vertebrates. This article is part of the theme issue 'Vertebrate palaeophysiology'.
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http://dx.doi.org/10.1098/rstb.2019.0146DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7017434PMC
March 2020

On trends and patterns in macroevolution: Williston's law and the branchiostegal series of extant and extinct osteichthyans.

BMC Evol Biol 2019 06 10;19(1):117. Epub 2019 Jun 10.

CR2P, UMR 7207 (CNRS/MNHN/Sorbonne Université), Muséum National d'Histoire Naturelle, Bâtiment de Géologie, Case postale 48, 43 rue Buffon, F-75231, cedex 05, Paris, France.

Background: The branchiostegal series consists of an alignment of bony elements in the posterior portion of the skull of osteichthyan vertebrates. We trace the evolution of the number of elements in a comprehensive survey that includes 440 extant and 66 extinct species. Using a newly updated actinopterygian tree in combination with phylogenetic comparative analyses, we test whether osteichthyan branchiostegals follow an evolutionary trend under 'Williston's law', which postulates that osteichthyan lineages experienced a reduction of bony elements over time.

Results: We detected no overall macroevolutionary trend in branchiostegal numbers, providing no support for 'Williston's law'. This result is robust to the subsampling of palaeontological data, but the estimation of the model parameters is much more ambiguous.

Conclusions: We find substantial evidence for a macroevolutionary dynamic favouring an 'early burst' of trait evolution over alternative models. Our study highlights the challenges of accurately reconstructing macroevolutionary dynamics even with large amounts of data about extant and extinct taxa.
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http://dx.doi.org/10.1186/s12862-019-1436-xDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6558815PMC
June 2019

Phylogeny of Paleozoic limbed vertebrates reassessed through revision and expansion of the largest published relevant data matrix.

PeerJ 2019 4;6:e5565. Epub 2019 Jan 4.

Centre de Recherches sur la Paléobiologie et les Paléoenvironnements (CR2P), Centre national de la Recherche scientifique (CNRS)/Muséum national d'Histoire naturelle (MNHN)/Sorbonne Université, Paris, France.

The largest published phylogenetic analysis of early limbed vertebrates (Ruta M, Coates MI. 2007. 5:69-122) recovered, for example, Seymouriamorpha, Diadectomorpha and (in some trees) Caudata as paraphyletic and found the "temnospondyl hypothesis" on the origin of Lissamphibia (TH) to be more parsimonious than the "lepospondyl hypothesis" (LH)-though only, as we show, by one step. We report 4,200 misscored cells, over half of them due to typographic and similar accidental errors. Further, some characters were duplicated; some had only one described state; for one, most taxa were scored after presumed relatives. Even potentially continuous characters were unordered, the effects of ontogeny were not sufficiently taken into account, and data published after 2001 were mostly excluded. After these issues are improved-we document and justify all changes to the matrix-but no characters are added, we find (Analysis R1) much longer trees with, for example, monophyletic Caudata, Diadectomorpha and (in some trees) Seymouriamorpha; either crownward or rootward of ; and Anthracosauria either crownward or rootward of Temnospondyli. The LH is nine steps shorter than the TH (R2; constrained) and 12 steps shorter than the "polyphyly hypothesis" (PH-R3; constrained). (Lysorophia) is not found next to Lissamphibia; instead, a large clade that includes the adelogyrinids, urocordylid "nectrideans" and aïstopods occupies that position. As expected from the taxon/character ratio, most bootstrap values are low. Adding 56 terminal taxa to the original 102 increases the resolution (and decreases most bootstrap values). The added taxa range in completeness from complete articulated skeletons to an incomplete lower jaw. Even though the lissamphibian-like temnospondyls , and and the extremely peramorphic salamander are added, the difference between LH (R4; unconstrained) and TH (R5) rises to 10 steps, that between LH and PH (R6) to 15; the TH also requires several more regains of lost bones than the LH. , in which we tentatively identify a postbranchial lamina, emerges rather far from amniote origins in a gephyrostegid-chroniosuchian grade. Bayesian inference (Analysis EB, settings as in R4) mostly agrees with R4. High posterior probabilities are found for Lissamphibia (1.00) and the LH (0.92); however, many branches remain weakly supported, and most are short, as expected from the small character sample. We discuss phylogeny, approaches to coding, methods of phylogenetics (Bayesian inference vs. equally weighted vs. reweighted parsimony), some character complexes (e.g. preaxial/postaxial polarity in limb development), and prospects for further improvement of this matrix. Even in its revised state, the matrix cannot provide a robust assessment of the phylogeny of early limbed vertebrates. Sufficient improvement will be laborious-but not difficult.
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http://dx.doi.org/10.7717/peerj.5565DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6322490PMC
January 2019

Exceptional soft tissues preservation in a mummified frog-eating Eocene salamander.

PeerJ 2017 3;5:e3861. Epub 2017 Oct 3.

Département Histoire de la Terre, UMR 7207, Centre de Recherches sur la Paléobiodiversité et les Paléoenvironnements, CNRS/MNHN/UPMC (Sorbonne Universités), Museum national d'Histoire naturelle, Paris, France.

Fossils are almost always represented by hard tissues but we present here the exceptional case of a three-dimensionally preserved specimen that was 'mummified' (likely between 40 and 34 million years ago) in a terrestrial karstic environment. This fossil is the incomplete body of a salamander, , whose skeleton and external morphology are well preserved, as revealed by phase-contrast synchrotron X-ray microtomography. In addition, internal structures composed of soft tissues preserved in three dimensions are now identified: a lung, the spinal cord, a lumbosacral plexus, the digestive tract, muscles and urogenital organs that may be cloacal glands. These are among the oldest known cases of three-dimensional preservation of these organs in vertebrates and shed light on the ecology of this salamander. Indeed, the digestive tract contains remains of a frog, which represents the only known case of an extinct salamander that fed on a frog, an extremely rare type of predation in extant salamanders. These new data improve our scarce knowledge on soft tissue anatomy of early urodeles and should prove useful for future biologists and palaeontologists working on urodele evolutionary biology. We also suggest that the presence of bat guano and carcasses represented a close source of phosphorus, favouring preservation of soft tissues. Bone microanatomy indicates that was likely amphibious or terrestrial, and was probably not neotenic.
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http://dx.doi.org/10.7717/peerj.3861DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5629955PMC
October 2017

Likelihood of Tree Topologies with Fossils and Diversification Rate Estimation.

Syst Biol 2017 Nov;66(6):964-987

Département Histoire de la Terre CR2P, Sorbonne Universités, CNRS/MNHN/UPMC, Muséum National d'Histoire Naturelle, 75005 Paris, France.

Since the diversification process cannot be directly observed at the human scale, it has to be studied from the information available, namely the extant taxa and the fossil record. In this sense, phylogenetic trees including both extant taxa and fossils are the most complete representations of the diversification process that one can get. Such phylogenetic trees can be reconstructed from molecular and morphological data, to some extent. Among the temporal information of such phylogenetic trees, fossil ages are by far the most precisely known (divergence times are inferences calibrated mostly with fossils). We propose here a method to compute the likelihood of a phylogenetic tree with fossils in which the only considered time information is the fossil ages, and apply it to the estimation of the diversification rates from such data. Since it is required in our computation, we provide a method for determining the probability of a tree topology under the standard diversification model. Testing our approach on simulated data shows that the maximum likelihood rate estimates from the phylogenetic tree topology and the fossil dates are almost as accurate as those obtained by taking into account all the data, including the divergence times. Moreover, they are substantially more accurate than the estimates obtained only from the exact divergence times (without taking into account the fossil record). We also provide an empirical example composed of 50 Permo-Carboniferous eupelycosaur (early synapsid) taxa ranging in age from about 315 Ma (Late Carboniferous) to 270 Ma (shortly after the end of the Early Permian). Our analyses suggest a speciation (cladogenesis, or birth) rate of about 0.1 per lineage and per myr, a marginally lower extinction rate, and a considerable hidden paleobiodiversity of early synapsids. [Extinction rate; fossil ages; maximum likelihood estimation; speciation rate.].
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http://dx.doi.org/10.1093/sysbio/syx045DOI Listing
November 2017

Evolution of organogenesis and the origin of altriciality in mammals.

Evol Dev 2016 07;18(4):229-44

Paläontologisches Institut und Museum der Universität Zürich, Karl Schmid Strasse 4, 8006 Zürich, Switzerland.

Mammals feature not only great phenotypic disparity, but also diverse growth and life history patterns, especially in maturity level at birth, ranging from altriciality to precocity. Gestation length, morphology at birth, and other markers of life history are fundamental to our understanding of mammalian evolution. Based on the first synthesis of embryological data and the study of new ontogenetic series, we reconstructed estimates of the ancestral chronology of organogenesis and life-history modes in placental mammals. We found that the ancestor of marsupial and placental mammals was placental-like at birth but had a long, marsupial-like infancy. We hypothesize that mammalian viviparity might have evolved in association with the extension of growth after birth, enabled through lactation, and that mammalian altriciality is inherited from the earliest amniotes. The precocial lifestyle of extant sauropsids and that of many placental mammals were acquired secondarily. We base our conclusions on the best estimates and provide a comprehensive discussion on the methods used and the limitations of our dataset. We provide the most comprehensive embryological dataset ever published, "rescue" old literature sources, and apply available methods and illustrate thus an approach on how to investigate comparatively organogenesis in macroevolution.
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http://dx.doi.org/10.1111/ede.12194DOI Listing
July 2016

Comparative data on the differentiation and growth of bone ornamentation in gnathostomes (Chordata: Vertebrata).

J Morphol 2016 May 10;277(5):634-70. Epub 2016 Mar 10.

CR2P (UMR 7207), CNRS/MNHN/UPMC, Département Histoire de la Terre, Muséum National d'histoire Naturelle, Bâtiment de Géologie CC 48, 57 Rue Cuvier F-75231, Paris, Cedex 05, France.

Bone ornamentation, in the form of rounded pits framed by a network of ridges, is a frequent feature among a great diversity of gnathostome taxa. However, the basic osteogenic processes controlling the differentiation and development of these reliefs remain controversial. The present study is a broad comparative survey of this question with the classical methods used in hard tissue histology and paleohistology. Distinct processes, unevenly distributed among taxa, are involved in the creation and growth of pits and ridges. The simplest one is mere differential growth between pit bottom (slow growth) and ridge top (faster growth). The involvement of several complex remodeling processes, with the local succession of resorption and reconstruction cycles, is frequent and occurs in all major gnathostome clades. Some broad, inclusive clades (e.g., Temnospondyli) display consistency in the mechanisms controlling ornamentation, whereas other clades (e.g., Actinopterygii) are characterized by the diversity of the mechanisms involved. If osteogenic mechanisms are taken into account, bone ornamentation should be considered as a character extremely prone to homoplasy. Maximum likelihood (ML) optimizations reveal that the plesiomorphic mechanism creating ornamentation is differential apposition rate over pits (slow growth) and ridges (faster growth). In some taxas e.g., temnospondyls vs lissamphibians or pseudosuchians, bone ornamentation is likely to be a homoplastic feature due to a convergence process driven by similar selective pressures. ML models of character evolution suggest that the presence of resorption in the development of ornamentation may be selectively advantageous, although support for this conclusion is only moderate.
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http://dx.doi.org/10.1002/jmor.20525DOI Listing
May 2016

Testing for Depéret's Rule (Body Size Increase) in Mammals using Combined Extinct and Extant Data.

Syst Biol 2016 Jan 27;65(1):98-108. Epub 2015 Oct 27.

UMR 7207, CNRS/MNHN/UPMC, Centre de Recherche sur la Paléodiversité et les Paléoenvironments (CR2P), Muséum national d'Histoire naturelle, Département Histoire de la Terre, 57 rue Cuvier, F-75231 Paris Cedex 05, France;

Whether or not evolutionary lineages in general show a tendency to increase in body size has often been discussed. This tendency has been dubbed "Cope's rule" but because Cope never hypothesized it, we suggest renaming it after Depéret, who formulated it clearly in 1907. Depéret's rule has traditionally been studied using fossil data, but more recently a number of studies have used present-day species. While several paleontological studies of Cenozoic placental mammals have found support for increasing body size, most studies of extant placentals have failed to detect such a trend. Here, we present a method to combine information from present-day species with fossil data in a Bayesian phylogenetic framework. We apply the method to body mass estimates of a large number of extant and extinct mammal species, and find strong support for Depéret's rule. The tendency for size increase appears to be driven not by evolution toward larger size in established species, but by processes related to the emergence of new species. Our analysis shows that complementary data from extant and extinct species can greatly improve inference of macroevolutionary processes.
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http://dx.doi.org/10.1093/sysbio/syv075DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4678255PMC
January 2016

Assessment of modularity in the urodele skull: an exploratory analysis using ossification sequence data.

Authors:
Michel Laurin

J Exp Zool B Mol Dev Evol 2014 Dec 9;322(8):567-85. Epub 2014 May 9.

Sorbonne Universités, CR2P, CNRS/MNHN/UPMC, Muséum National d'Histoire Naturelle, Paris, France.

The potential presence of developmental modules is studied in the urodele skull using several classical statistical methods that have not previously been used in this context. Principal component analysis (PCA) of ossification sequence data on 21 bones in 21 extant urodele species suggests the presence of up to four developmental modules, but examination of statistically significant correlations using phylogenetic independent contrasts (PIC) and correcting for multiple tests using the false discovery rate suggests the presence of only two modules of uneven size and of two bones that may not be part of these modules. Thus, PCA does not appear to be a reliable method to investigate modularity; direct investigation of statistically significant correlations using PIC or other phylogeny-informed methods is recommended. A binomial test of the distribution of significant correlations between characters shows significant heterogeneity, which suggests that modularity is indeed present in the data. A cluster analysis gives inconsistent results that apparently do not reflect developmental modules. The data include a phylogenetic signal, as shown by a permutation-based test with squared change parsimony, but this is detectable only when the whole matrix is analyzed, and a plot of the tree onto developmental space through Evolutionary PCA shows that homoplasy is pervasive. Evolutionary rates between characters vary about 90-fold. Canonical variates analyses suggest that obligatorily neotenic urodeles may be discriminated from other urodeles on the basis of cranial ossification sequence data.
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http://dx.doi.org/10.1002/jez.b.22575DOI Listing
December 2014

Gradual adaptation of bone structure to aquatic lifestyle in extinct sloths from Peru.

Proc Biol Sci 2014 May 12;281(1782):20140192. Epub 2014 Mar 12.

Département Histoire de la Terre, Muséum national d'Histoire naturelle, Sorbonne Universités - CR2P (CNRS, MNHN, UPMC-Paris06), , 57 rue Cuvier, CP38, 75005 Paris, France.

Non-pathological densification (osteosclerosis) and swelling (pachyostosis) of bones are the main modifications affecting the skeleton of land vertebrates (tetrapods) that returned to water. However, a precise temporal calibration of the acquisition of such adaptations is still wanting. Here, we assess the timing of such acquisition using the aquatic sloth Thalassocnus, from the Neogene of the Pisco Formation, Peru. This genus is represented by five species occurring in successive vertebrate-bearing horizons of distinct ages. It yields the most detailed data about the gradual acquisition of aquatic adaptations among tetrapods, in displaying increasing osteosclerosis and pachyostosis through time. Such modifications, reflecting a shift in the habitat from terrestrial to aquatic, occurred over a short geological time span (ca 4 Myr). Otherwise, the bones of terrestrial pilosans (sloths and anteaters) are much more compact than the mean mammalian condition, which suggests that the osteosclerosis of Thalassocnus may represent an exaptation.
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http://dx.doi.org/10.1098/rspb.2014.0192DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3973278PMC
May 2014

A re-interpretation of the Eocene anuran Thaumastosaurus based on microCT examination of a 'mummified' specimen.

PLoS One 2013 25;8(9):e74874. Epub 2013 Sep 25.

Muséum national d'Histoire naturelle, Unité mixte de recherche 7207, Centre national de la recherche scientifique/Muséum national d'histoire naturelle/Université Pierre et Marie Curie, Paris, France.

What originally appeared to be only an external cast of an anuran 'mummy' from the Quercy Phosphorites (southwestern France) was described as Rana plicata during the 19th century. Its geographical provenance is only vaguely known; therefore its precise age within the Paleogene was uncertain. The taxon was erected on the basis of the external morphology of the specimen, which includes few diagnostic characters. As a further complication, the name Rana plicata was recently shown to be unavailable at the time of the description, and the name Rana cadurcorum was proposed as a replacement. In order to see whether internal features were fossilized, the fossil was CT scanned. This showed that a large part of the skeleton is preserved. Unexpectedly, the scans revealed that the skull of the mummy is almost identical to that of Thaumastosaurus gezei, another anuran from the late middle or late Eocene of the Quercy Phosphorites. The few observed differences are attributable to intraspecific and ontogenetic variation, and R. cadurcorum is a junior subjective synonym of T. gezei. The mummy is therefore probably from the same time interval as T. gezei. The latter was previously known only by its skull, but the mummy provides important information on the postcranial skeleton. Earlier assessments, based only on the skull, placed Thaumastosaurus close to South American hyloid anurans, but a new phylogenetic analysis including postcranial characters reveals ranoid affinities. This study exemplifies the usefulness of modern imaging technologies that allow non-destructive study of previously inaccessible internal anatomical features.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0074874PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3783478PMC
August 2014

Movement in a gravitational field: The question of limb interarticular coordination in terrestrial vertebrates.

Eur Phys J E Soft Matter 2013 May 17;36(5):49. Epub 2013 May 17.

CRIS EA 647 (P3M), Université de Lyon, Villeurbanne, France.

In this paper, we demonstrated that interarticular coordination of terrestrial tetrapods emerges from an environment highly constrained by friction and the gravitational field. We briefly review recent works on the jumping behavior in squamates, lemurs and amphibians. We then explore previously published work as well as some unpublished experimental data on human jumping. Finally, we end by inferring locomotion in some of the first limbed vertebrates using a simulation procedure. All these data show that despite changes in shape, structure, and motor controls of taxa, the same spatio-temporal sequence of joint displacements always occurs when the movement is executed in a terrestrial environment. Comparison with aquatic locomotion argues for the hypothesis that this pattern emerged in early terrestrial tetrapods as a response to the gravitational constraint and the terrestrial frictional environment.
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http://dx.doi.org/10.1140/epje/i2013-13049-4DOI Listing
May 2013

Inner architecture of vertebral centra in terrestrial and aquatic mammals: a two-dimensional comparative study.

J Morphol 2013 May 8;274(5):570-84. Epub 2013 Feb 8.

Department of Microstructure Physics and Alloy Design, Max Planck Institute for Iron Research, Duesseldorf, Germany.

Inner vertebral architecture is poorly known, except in human and laboratory animals. In order to document this topic at a broad comparative level, a 2D-histomorphometric study of vertebral centra was conducted in a sample of 98 therian mammal species, spanning most of the size range and representing the main locomotor adaptations known in therian taxa. Eleven variables relative to the development and geometry of trabecular networks were extracted from CT scan mid-sagittal sections. Phylogeny-informed statistical tests were used to reveal the respective influences of phylogeny, size, and locomotion adaptations on mammalian vertebral structure. The use of random taxon reshuffling and squared change parsimony reveals that 9 of the 11 characteristics (the two exceptions are total sectional area and structural polarization) contain a phylogenetic signal. Linear discriminant analyses suggest that the sampled taxa can be arranged into three categories with respect to locomotion mode: a) terrestrial + flying + digging + amphibious forms, b) coastal oscillatory aquatic taxa, and c) pelagic oscillatory aquatic forms represented by oceanic cetaceans. Pairwise comparison tests and linear regressions show that, when specific size increases, the length of trabecular network (Tt.Tb.Le), as well as trabecular proliferation in total sections (Pr.Tb.Tt), increase with positive allometry. This process occurs in all locomotion categories but is particularly pronounced in pelagic oscillators. Conversely, mean trabecular width has a lesser increase with size in pelagic oscillators. Trabecular orientation is not influenced by size. All tests were corrected for multiple testing. By using six structural variables or indices, locomotion mode can be predicted with a 97.4% success rate for terrestrial forms, 66.7% for coastal oscillatory, and 81.3% for pelagic oscillatory. The possible functional meaning of these results and their potential use for paleobiological inference of locomotion in extinct taxa are discussed.
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http://dx.doi.org/10.1002/jmor.20122DOI Listing
May 2013

The reconstructed evolutionary process with the fossil record.

J Theor Biol 2012 Dec 13;315:26-37. Epub 2012 Sep 13.

Institut de Mathématiques de Luminy, FRE 3529, CNRS, Aix-Marseille Université, Case 907, Campus de Luminy, 13288 MARSEILLE Cedex 9, France.

Using the fossil record yields more detailed reconstructions of the evolutionary process than what is obtained from contemporary lineages only. In this work, we present a stochastic process modeling not only speciation and extinction, but also fossil finds. Next, we derive an explicit formula for the likelihood of a reconstructed phylogeny with fossils, which can be used to estimate the speciation and extinction rates. Finally, we provide a comparative simulation-based evaluation of the accuracy of estimations of these rates from complete phylogenies (including extinct lineages), from reconstructions with contemporary lineages only and from reconstructions with contemporary lineages and the fossil record. Results show that taking the fossil record into account yields more accurate estimates of speciation and extinction rates than considering only contemporary lineages.
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http://dx.doi.org/10.1016/j.jtbi.2012.08.046DOI Listing
December 2012

Evolution of genes involved in gamete interaction: evidence for positive selection, duplications and losses in vertebrates.

PLoS One 2012 5;7(9):e44548. Epub 2012 Sep 5.

UMR85 Physiologie de la Reproduction et des Comportements, INRA, Nouzilly, France.

Genes encoding proteins involved in sperm-egg interaction and fertilization exhibit a particularly fast evolution and may participate in prezygotic species isolation [1], [2]. Some of them (ZP3, ADAM1, ADAM2, ACR and CD9) have individually been shown to evolve under positive selection [3], [4], suggesting a role of positive Darwinian selection on sperm-egg interaction. However, the genes involved in this biological function have not been systematically and exhaustively studied with an evolutionary perspective, in particular across vertebrates with internal and external fertilization. Here we show that 33 genes among the 69 that have been experimentally shown to be involved in fertilization in at least one taxon in vertebrates are under positive selection. Moreover, we identified 17 pseudogenes and 39 genes that have at least one duplicate in one species. For 15 genes, we found neither positive selection, nor gene copies or pseudogenes. Genes of teleosts, especially genes involved in sperm-oolemma fusion, appear to be more frequently under positive selection than genes of birds and eutherians. In contrast, pseudogenization, gene loss and gene gain are more frequent in eutherians. Thus, each of the 19 studied vertebrate species exhibits a unique signature characterized by gene gain and loss, as well as position of amino acids under positive selection. Reflecting these clade-specific signatures, teleosts and eutherian mammals are recovered as clades in a parsimony analysis. Interestingly the same analysis places Xenopus apart from teleosts, with which it shares the primitive external fertilization, and locates it along with amniotes (which share internal fertilization), suggesting that external or internal environmental conditions of germ cell interaction may not be the unique factors that drive the evolution of fertilization genes. Our work should improve our understanding of the fertilization process and on the establishment of reproductive barriers, for example by offering new leads for experiments on genes identified as positively selected.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0044548PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3434135PMC
February 2013

Recent progress in paleontological methods for dating the Tree of Life.

Authors:
Michel Laurin

Front Genet 2012 13;3:130. Epub 2012 Jul 13.

UMR 7207, CNRS/MNHN/UPMC, Earth History Department, Muséum National d'Histoire Naturelle, Paris, France.

Dating the Tree of Life (TOL) has become a major goal of biological research. Beyond the intrinsic interest of reconstructing the history of taxonomic diversification, time-calibrated trees (timetrees for short, as used throughout below) are required in many types of comparative analyses, where branch lengths are used to assess the conservation importance of lineages, correlation between characters, or to assess phylogenetic niche conservatism, among other uses. Improvements in dating the TOL would thus benefit large segments of the biological community, ranging from conservation biology and ecology through functional biology and paleontology. Recently, progress has been made on several fronts: in compiling databases and supertrees incorporating paleontological data, in computing confidence intervals on the true stratigraphic range of taxa, and in using birth-and-death processes to assess the probability distribution of the time of origin of specified taxa. Combined paleontological and molecular dating has also progressed through the insertion of extinct taxa into data matrices, which allows incorporation of their phylogenetic uncertainty into the dating analysis.
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http://dx.doi.org/10.3389/fgene.2012.00130DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3395881PMC
October 2012

Developmental characters in phylogenetic inference and their absolute timing information.

Syst Biol 2011 Oct 28;60(5):630-44. Epub 2011 Mar 28.

UMR CNRS 7207 "Centre de Recherches sur la Paléobiodiversité et les Paléoenvironnements," Muséum National d'Histoire Naturelle, Département Histoire de la Terre, Bâtiment de Géologie, Case Postale 48, 43 Rue Buffon, F-75231 Paris Cedex 05, France.

Despite the recent surge of interest in studying the evolution of development, surprisingly little work has been done to investigate the phylogenetic signal in developmental characters. Yet, both the potential usefulness of developmental characters in phylogenetic reconstruction and the validity of inferences on the evolution of developmental characters depend on the presence of such a phylogenetic signal and on the ability of our coding scheme to capture it. In a recent study, we showed, using simulations, that a new method (called the continuous analysis) using standardized time or ontogenetic sequence data and squared-change parsimony outperformed event pairing and event cracking in analyzing developmental data on a reference phylogeny. Using the same simulated data, we demonstrate that all these coding methods (event pairing and standardized time or ontogenetic sequence data) can be used to produce phylogenetically informative data. Despite some dependence between characters (the position of an event in an ontogenetic sequence is not independent of the position of other events in the same sequence), parsimony analysis of such characters converges on the correct phylogeny as the amount of data increases. In this context, the new coding method (developed for the continuous analysis) outperforms event pairing; it recovers a lower proportion of incorrect clades. This study thus validates the use of ontogenetic data in phylogenetic inference and presents a simple coding scheme that can extract a reliable phylogenetic signal from these data.
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http://dx.doi.org/10.1093/sysbio/syr024DOI Listing
October 2011

The cecal appendix: one more immune component with a function disturbed by post-industrial culture.

Anat Rec (Hoboken) 2011 Apr 2;294(4):567-79. Epub 2011 Mar 2.

UMR 7207, CNRS/MNHN/UPMC, Centre de Recherches sur la Paléobiodiversité et les Paléoenvironnements, Muséum National d'Histoire Naturelle, Paris, France.

This review assesses the current state of knowledge regarding the cecal appendix, its apparent function, and its evolution. The association of the cecal appendix with substantial amounts of immune tissue has long been taken as an indicator that the appendix may have some immune function. Recently, an improved understanding of the interactions between the normal gut flora and the immune system has led to the identification of the appendix as an apparent safe-house for normal gut bacteria. Further, a variety of observations related to the evolution and morphology of the appendix, including the identification of the structure as a "recurrent trait" in some clades, the presence of appendix-like structures in monotremes and some non-mammalian species, and consistent features of the cecal appendix such as its narrow diameter, provide direct support for an important function of the appendix. This bacterial safe-house, which is likely important in the event of diarrheal illness, is presumably of minimal importance to humans living with abundant nutritional resources, modern medicine and modern hygiene practices that include clean drinking water. Consistent with this idea, epidemiologic studies demonstrate that diarrheal illness is indeed a major source of selection pressure in developing countries but not in developed countries, whereas appendicitis shows the opposite trend, being associated with modern hygiene and medicine. The cecal appendix may thus be viewed as a part of the immune system that, like those immune compartments that cause allergy, is vital to life in a "natural" environment, but which is poorly suited to post-industrialized societies.
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http://dx.doi.org/10.1002/ar.21357DOI Listing
April 2011

Assessment of the relative merits of a few methods to detect evolutionary trends.

Authors:
Michel Laurin

Syst Biol 2010 Dec 11;59(6):689-704. Epub 2010 Oct 11.

UMR 7207, CNRS/MNHN/UPMC, Centre de Recherches sur la Paléobiodiversité et les Paléoenvironnements, Département Histoire de la Terre, Muséum National d'Histoire Naturelle, Bâtiment de Géologie, Paris, France.

Some of the most basic questions about the history of life concern evolutionary trends. These include determining whether or not metazoans have become more complex over time, whether or not body size tends to increase over time (the Cope-Depéret rule), or whether or not brain size has increased over time in various taxa, such as mammals and birds. Despite the proliferation of studies on such topics, assessment of the reliability of results in this field is hampered by the variability of techniques used and the lack of statistical validation of these methods. To solve this problem, simulations are performed using a variety of evolutionary models (gradual Brownian motion, speciational Brownian motion, and Ornstein-Uhlenbeck), with or without a drift of variable amplitude, with variable variance of tips, and with bounds placed close or far from the starting values and final means of simulated characters. These are used to assess the relative merits (power, Type I error rate, bias, and mean absolute value of error on slope estimate) of several statistical methods that have recently been used to assess the presence of evolutionary trends in comparative data. Results show widely divergent performance of the methods. The simple, nonphylogenetic regression (SR) and variance partitioning using phylogenetic eigenvector regression (PVR) with a broken stick selection procedure have greatly inflated Type I error rate (0.123-0.180 at a 0.05 threshold), which invalidates their use in this context. However, they have the greatest power. Most variants of Felsenstein's independent contrasts (FIC; five of which are presented) have adequate Type I error rate, although two have a slightly inflated Type I error rate with at least one of the two reference trees (0.064-0.090 error rate at a 0.05 threshold). The power of all contrast-based methods is always much lower than that of SR and PVR, except under Brownian motion with a strong trend and distant bounds. Mean absolute value of error on slope of all FIC methods is slightly higher than that of phylogenetic generalized least squares (PGLS), SR, and PVR. PGLS performs well, with low Type I error rate, low error on regression coefficient, and power comparable with some FIC methods. Four variants of skewness analysis are examined, and a new method to assess significance of results is presented. However, all have consistently low power, except in rare combinations of trees, trend strength, and distance between final means and bounds. Globally, the results clearly show that FIC-based methods and PGLS are globally better than nonphylogenetic methods and variance partitioning with PVR. FIC methods and PGLS are sensitive to the model of evolution (and, hence, to branch length errors). Our results suggest that regressing raw character contrasts against raw geological age contrasts yields a good combination of power and Type I error rate. New software to facilitate batch analysis is presented.
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http://dx.doi.org/10.1093/sysbio/syq059DOI Listing
December 2010

Use of paleontological and molecular data in supertrees for comparative studies: the example of lissamphibian femoral microanatomy.

J Anat 2009 Aug 5;215(2):110-23. Epub 2009 Jun 5.

UMR 7179, Equipe squelette des vertebrés, Université Paris 6, Paris, France.

A new method to assemble time-calibrated supertrees is able to incorporate paleontological and molecular dates. This method, along with new branch length transformations, is implemented in the Stratigraphic Tools for Mesquite. It was used here to analyse a dataset on bone microanatomy, body size and habitat of 46 species of lissamphibians through a variety of methods (Felsenstein independent contrasts, variance partition with phylogenetic eigenvector regression, discriminant analyses and simple regressions). Our analyses showed that the new methods can produce adequate standardization for several characters on a tree whose branch lengths can represent evolutionary time. The analyses confirmed previous conclusions about the presence of an ecological signal in bone microanatomical data.
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http://dx.doi.org/10.1111/j.1469-7580.2009.01104.xDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC2740958PMC
August 2009

Evolution of ossification sequences in salamanders and urodele origins assessed through event-pairing and new methods.

Evol Dev 2009 Mar-Apr;11(2):170-90

UMR CNRS, Université Paris 6, Paris, France.

Ossification sequences of the skull in extant Urodela and in Permo-Carboniferous Branchiosauridae have already been used to study the origin of lissamphibians. But most of these studies did not consider some recent methods developed to analyze the developmental sequences within a phylogenetic framework. Here, we analyze the ossification sequences of 24 cranial bones of 23 extant species of salamanders using the event-pairing method. This reveals new developmental synapomorphies for several extant salamander taxa and ancestral sequences for Urodela under four alternative reference phylogenies. An analysis with the 12 bones for which ossification sequence data are available in urodeles and in the branchiosaurid Apateon is also performed in order to compare the ancestral condition of the crown-group of Urodela to the sequence of Apateon. This reveals far more incompatibilities than previously suggested. The similarities observed between some extant salamanders and branchiosaurids may result from extensive homoplasy, as the extreme variation observed in extant Urodela suggests, or be plesiomorphic, as the conservation of some ossification patterns observed in other remotely related vertebrates like actinopterygians suggests. We propose a new, simpler method based on squared-change optimization to estimate the relative timing of ossification of various bones of hypothetical ancestors, and use independent-contrasts analysis to estimate the confidence intervals around these times. Our results show that the uncertainty of the ancestral ossification sequence of Urodela is much greater than event-pairing suggests. The developmental data do not allow to conclude that branchiosaurids are closely related to salamanders and their limited taxonomic distribution in Paleozoic taxa precludes testing hypotheses about lissamphibian origins. This is true regardless of the analytical method used (event-pairing or our new method based on squared-change parsimony). Simulations show that the new analytical method is generally more powerful to detect evolutionary shifts in developmental timing, and has lower Type I error rate than event-pairing. It also makes fewer errors in ancestral character value or state assignment than event-pairing.
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http://dx.doi.org/10.1111/j.1525-142X.2009.00318.xDOI Listing
August 2009

Constraints and selection: insights from microsporogenesis in Asparagales.

Evol Dev 2007 Sep-Oct;9(5):460-71

Laboratoire Ecologie, Systématique et Evolution, Batiment 360, Université Paris-Sud, 91405 Orsay Cédex, France.

Developmental constraints have been proposed to interfere with natural selection in limiting the available set of potential adaptations. Whereas this concept has long been debated on theoretical grounds, it has been investigated empirically only in a few studies. In this article, we evaluate the importance of developmental constraints during microsporogenesis (male meiosis in plants), with an emphasis on phylogenetic patterns in Asparagales. Different developmental constraints were tested by character reshuffling or by simulated distributions. Among the different characteristics of microsporogenesis, only cell wall formation appeared as constrained. We show that constraints may also result from biases in the correlated occurrence of developmental steps (e.g., lack of successive cytokinesis when wall formation is centripetal). We document such biases and their potential outcomes, notably the establishment of intermediate stages, which allow development to bypass such constraints. These insights are discussed with regard to potential selection on pollen morphology.
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http://dx.doi.org/10.1111/j.1525-142X.2007.00183.xDOI Listing
December 2007

Fossils, molecules, divergence times, and the origin of lissamphibians.

Syst Biol 2007 Jun;56(3):369-88

Comparative Osteohistology, UMR CNRS 7179, Université Paris 6, Paris, France.

A review of the paleontological literature shows that the early dates of appearance of Lissamphibia recently inferred from molecular data do not favor an origin of extant amphibians from temnospondyls, contrary to recent claims. A supertree is assembled using new Mesquite modules that allow extinct taxa to be incorporated into a time-calibrated phylogeny with a user-defined geological time scale. The supertree incorporates 223 extinct species of lissamphibians and has a highly significant stratigraphic fit. Some divergences can even be dated with sufficient precision to serve as calibration points in molecular divergence date analyses. Fourteen combinations of minimal branch length settings and 10 random resolutions for each polytomy give much more recent minimal origination times of lissamphibian taxa than recent studies based on a phylogenetic analyses of molecular sequences. Attempts to replicate recent molecular date estimates show that these estimates depend strongly on the choice of calibration points, on the dating method, and on the chosen model of evolution; for instance, the estimate for the date of the origin of Lissamphibia can lie between 351 and 266 Mya. This range of values is generally compatible with our time-calibrated supertree and indicates that there is no unbridgeable gap between dates obtained using the fossil record and those using molecular evidence, contrary to previous suggestions.
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http://dx.doi.org/10.1080/10635150701397635DOI Listing
June 2007

Confirmation of Romer's Gap as a low oxygen interval constraining the timing of initial arthropod and vertebrate terrestrialization.

Proc Natl Acad Sci U S A 2006 Nov 25;103(45):16818-22. Epub 2006 Oct 25.

Department of Biology, University of Washington, Seattle, WA 98195, USA.

The first terrestrialization of species that evolved from previously aquatic taxa was a seminal event in evolutionary history. For vertebrates, one of the most important terrestrialized groups, this event was interrupted by a time interval known as Romer's Gap, for which, until recently, few fossils were known. Here, we argue that geochronologic range data of terrestrial arthropods show a pattern similar to that of vertebrates. Thus, Romer's Gap is real, occupied an interval from 360 million years before present (MYBP) to 345 MYBP, and occurred when environmental conditions were unfavorable for air-breathing, terrestrial animals. These model results suggest that atmospheric oxygen levels were the major driver of successful terrestrialization, and a low-oxygen interval accounts for Romer's Gap. Results also show that terrestrialization among members of arthropod and vertebrate clades occurred in two distinct phases. The first phase was a 65-million-year (My) interval from 425 to 360 MYBP, representing an earlier, prolonged event of complete arthropod terrestrialization of smaller-sized forms (425-385 MYBP) and a subsequent, modest, and briefer event of incipient terrestrialization of larger-sized, aquatic vertebrates (385-360 MYBP). The second phase began at 345 MYBP, characterized by numerous new terrestrial species emerging in both major clades. The first and second terrestrialization phases bracket Romer's Gap, which represents a depauperate spectrum of major arthropod and vertebrate taxa before a major Late Paleozoic colonization of terrestrial habitats.
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http://dx.doi.org/10.1073/pnas.0607824103DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC1636538PMC
November 2006

The evolution of body size, Cope's rule and the origin of amniotes.

Authors:
Michel Laurin

Syst Biol 2004 Aug;53(4):594-622

Equipe Formations squelettiques FRE CNRS 2696, Case 7077, Université Paris 7, Paris, France.

The evolution of body size in tetrapods is assessed using a database that includes 107 early stegocephalian species ranging in time from the Frasnian (Upper Devonian) to the Tatarian (Upper Permian). All analyses use methods that incorporate phylogenetic information (topology and branch lengths). In all tests, the impact of alternative topologies and branch lengths are assessed. Previous reports that raised doubts about the accuracy of squared-change parsimony assessment of ancestral character value appear to have used datasets in which there was no phylogenetic signal. Hence, squared-change parsimony may be more reliable than suggested in recent studies, at least when a phylogenetic signal is present in the datasets of interest. Analysis using random taxon reshuffling on three reference phylogenies shows that cranial and presacral length include a strong phylogenetic signal. Character optimization of body size in stegocephalians using squared-change parsimony on a time-calibrated phylogeny incorporating branch length information is used to test a previously published scenario on the origin of amniotes and of the amniotic egg that implies that the ancestors of amniotes were small (no more than 10 cm in snout-vent length), and that their size increased subsequent to the appearance of the amniotic egg. The optimization suggests that first amniotes were somewhat larger than previously hypothesized; the estimated snout-vent length is about 24 cm, and the lower end of the 95% confidence interval of the phylogeny that yields the smallest inferred size suggests that no ancestor of amniotes measured less than 12 cm in snout-vent length. Character optimization, permutational multiple linear regressions, and independent contrast analyses show that Cope's rule of phyletic size increase applies to early reptiliomorphs but that it does not apply to early stegocephalians globally.
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http://dx.doi.org/10.1080/10635150490445706DOI Listing
August 2004

Meaning of the name tetrapoda in the scientific literature: an exchange.

Syst Biol 2004 Feb;53(1):68-80

Equipe Formations Squelettiques, UMR CNRS 8570, Case 7077, Université Paris 7, 75005 Paris, France.

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http://dx.doi.org/10.1080/10635150490264716DOI Listing
February 2004

Tetrapod phylogeny, amphibian origins, and the definition of the name tetrapoda.

Authors:
Michel Laurin

Syst Biol 2002 Apr;51(2):364-9

Equipe "Formations squelettiques" UMR CNRS 8570, Case 7077, Université Paris 7, 75005 Paris, France.

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http://dx.doi.org/10.1080/10635150252899815DOI Listing
April 2002