Michel Laurin

The Evolution of Body Size, Cope's Rule and the Origin of Amniotes

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 Copes rule of phyletic size increase applies to early reptiliomorphs but that it does not apply to early stegocephalians globally.

Fossils, Molecules, Divergence Times, and the Origin of Lissamphibians

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.

CHAPTER 2 – A NEW PERSPECTIVE ON TETRAPOD PHYLOGENY

This chapter provides an in-depth explanation of the origin of amniotes. It follows articles from various authors, especially those that compare hypotheses on the origin of lissamphibians where Temnospondyls and Lepospondyls were considered. Several investigations have been made on the closest relatives of amniotes like the Anthracosaurs, Aiadectomorpha, and the Seymouriamorphs that can provide insights to the origin and determines which early terrestrial Choanates are relatives of amniotes, Lissamphibians, and the crown group Tetrepoda. Some conclusions indicate that Lissanphibubians are part of Temnospongyli and have other relatives like Microsauria, Colosteidae, Nectridea, and Ichthyostegidae. Diadectormorpha is considered to be the sister of Amniota and that Seymouriamorpha, Anthracosauroidaeae, Crassigyrinus, and Loxommatoidea were related to this clade and thus all known terrestrial Paleozoic Choanates except Ichthyostegids were part of lissamphibians and amniotes. Various method matrices have been used to come up with the different results and conclusive discussions of the comparisons of previous phylogenies, decay index and robustness of the clades, the origin of Lissamphibians, the status of Anthracosaurs, status of the crown group of terrestrial Choanates, and the evolution of selected characters.

Phylogenetic Signal in Bone Microstructure of Sauropsids

In spite of the fact that the potential usefulness of bone histology in systematics has been discussed for over one and a half centuries, the presence of a phylogenetic signal in the variation of histological characters has rarely been assessed. A quantitative assessment of phylogenetic signal in bone histological characters could provide a justification for performing optimizations of these traits onto independently generated phylogenetic trees (as has been done in recent years). Here we present an investigation on the quantification of the phylogenetic signal in the following bone histological, microanatomical, and morphological traits in a sample of femora of 35 species of sauropsids: vascular density, vascular orientation, index of Haversian remodeling, cortical thickness, and cross-sectional area (bone size). For this purpose, we use two methods, regressions on distance matrices tested for significance using permutations (a Mantel test) and random tree length distribution. Within sauropsids, these bone microstructural traits have an optimal systematic value in archosaurs. In this taxon, a Mantel test shows that the phylogeny explains 81.8% of the variation of bone size and 86.2% of the variation of cortical thickness. In contrast, a Mantel test suggests that the phylogenetic signal in histological traits is weak: although the phylogeny explains 18.7% of the variation of vascular density in archosaurs, the phylogenetic signal is not significant either for vascular orientation or for the index of Haversian remodeling. However, Mantel tests seem to underestimate the proportion of variance of the dependent character explained by the phylogeny, as suggested by a PVR (phylogenetic eigenvector) analysis. We also deal with some complementary questions. First, we evaluate the functional dependence of bone vascular density on bone size by using phylogenetically independent contrasts. Second, we perform a variation partitioning analysis and show that the phylogenetic signal in bone vascular density is not a by-product of phylogentic signal in bone size. Finally, we analyze the evolution of cortical thickness in diapsids by using an optimization by squared change parsimony and discuss the functional significance of this character in terms of decreased buoyancy in crocodiles and mass saving in birds. These results are placed in the framework of the constructional morphology model, according to which the variation of a character in a clade has a historical (phylogenetic) component, a functional (adaptive) component, and a structural (architectural) component.

The evolution of long bone microstructure and lifestyle in lissamphibians

Abstract The compactness profile of femoral cross-sections and body size of 105 specimens of 46 species of lissamphibians was studied to assess the effect of lifestyle (aquatic, amphibious, or terrestrial). Several tests that incorporate phylogenetic information (permutational multiple linear regression incorporating phylogenetic distances, logistic regression using phylogenetic weighting, concentrated-changes tests) show that the return to a fully aquatic lifestyle is associated with an increase in the compactness of the femur and an increase in body size. However, amphibious taxa cannot be distinguished from terrestrial ones solely on the basis of size or compactness. Body size and compactness profile parameters of the femur exhibit a phylogenetic signal (i.e., closely related taxa tend to be more similar to each other than to distantly related taxa). Mathematical equations obtained from our data by using logistic regression with phylogenetic weighting are used to infer the lifestyle of four early stegocephalians. The results are generally congruent with prevailing paleontological interpretations, which suggests that this method could be applied to infer the lifestyle of early taxa whose lifestyle is poorly understood.

The importance of global parsimony and historical bias in understanding tetrapod evolution. Part I. Systematics, middle ear evolution and jaw suspension

Abstract A phylogenetic analysis based on a data matrix of 43 taxa and 155 osteological characters has produced a new hypothesis of tetrapod phylogeny that is drastically different from the established consensus. Among Paleozoic taxa, only diadectomorphs appear to be related to amniotes. In contrast to previous hypotheses, lissamphibians appear to have been derived from lepospondyls. Seymouriamorphs, gephyrostegids, embolomeres, temnospondyls, and loxommatids are stem-tetrapods. The new phylogeny suggests that the absence of a tympanic middle ear in salamanders and gymnophiones is a primitive character.

BONE PROFILER: A TOOL TO QUANTIFY, MODEL, AND STATISTICALLY COMPARE BONE-SECTION COMPACTNESS PROFILES

Bone cross sections show many characteristics that have been used to infer various properties of the individual or taxon from which they were prepared. Life history traits (Castanet et al., 1993), locomotor patterns (Casinos, 1996), habitat (Laurin et al., 2000), metabolism (Ricqlès, 1983), and growth rate (Rimblot-Baly et al., 1995) are some examples. However, bone microstructure is very complex, and few objective, quantitative methods (other than very simple ones, such as the cortico-diaphyseal index, or the global compactness) are available to describe bone sections in a way that enables statistical inference or comparison. Several cross-sectional properties, such as the cross-sectional area, centroid coordinates relative to reference axes, second moments of area about x and y axes, principal second moments of area and their orientation, section modulus, and polar moment of area have been obtained using SLICE (Nagurka and Hayes, 1980) by Ruff and Hayes (1983) and others, while Cubo and Casinos (1998) produced their own software for similar purposes. These parameters are especially useful for studying the stiffness, strength, or resistance of bones for animals of known weight and living in similar habitats. They do not describe how the bone tissue is organized. To model bone tissue distribution in sections, we need to reduce its complexity to a limited number of variables that can be further compared using statistical tests. Among the various characteristics of bone sections that could be analyzed, we decided to work mainly on compactness (amount of bone present on a given surface) because this characteristic has previously been suspected to provide much information about the life style of taxa (Laurin et al., 2000). Furthermore, compactness can be measured relatively easily from a bone section (because it only requires knowledge about the presence or absence of bone on a given area). In contrast, bone mineral density requires the use of quantitative micro-radiography that is technically more demanding. An additional advantage of working with compactness is that it can be measured both on extant animals and on fossils. Bone mineral density can usually not be evaluated on fossil bones because of the variable amount of permineralization and other diagenetic phenomena that affect fossil tissues.

Cranial morphology and affinities of Microbrachis, and a reappraisal of the phylogeny and lifestyle of the first amphibians

Abstract An anatomical study of Microbrachis reveals inaccuracies in previous studies, especially in the palate and cranial proportions. The vomer and the pterygoid reach the midline anteriorly, and the postorbital does not appear to reach the tabular. The skull is higher in our cranial reconstruction than previously thought. A phylogenetic analysis of early stegocephalians places Microbrachis at a fairly basal position in the clade that includes “microsaurs,” lysorophians, and lissamphibians. This analysis corroborates previous suggestions that lissamphibians are part of a clade that includes the taxa classically referred to as “lepospondyls,” and that seymouriamorphs and temnospondyls are not part of Tetrapoda. Statistical tests on another recent amphibian phylogeny reveal that its different placement of the origin of lissamphibians is not statistically more parsimonious than the placement that we suggest. Our analysis also suggests that the first evolutionary radiation of amphibians took place in an aquatic environment because most of the first groups of amphibians to have differentiated, namely adelogyrinids, nectrideans, and Microbrachis, appear to have been aquatic or amphibious taxa. However, the lifestyle of many early amphibians is difficult to assess.

Microanatomy of the radius and lifestyle in amniotes (Vertebrata, Tetrapoda)

Radial cross‐sections of 49 species of extant and two species of extinct amniotes of known lifestyle have been studied in order to assess the relationship between lifestyle (aquatic, amphibious or terrestrial) and bone microanatomy. Most compactness profile and body size parameters exhibit a phylogenetic signal; therefore, classical statistical tests should not be used. Permutational multiple linear regressions show an ecological signal in most compactness profile parameters and in the cross‐section maximal diameter. A linear discriminant analysis is performed with these parameters to distinguish the various lifestyles. The discriminant function based on taxa of known lifestyle is used to infer the lifestyle of three extinct amniotes: the early nothosaur Pachypleurosaurus (amphibious), the therapsid Lystrosaurus (amphibious) and the synapsid Ophiacodon (aquatic). These predictions are congruent with classical palaeoecological interpretations. This model may be very useful when attempting to infer the ancestral lifestyle of amniotes and other early limbed vertebrates.

Evolution of bone microanatomy of the tetrapod tibia and its use in palaeobiological inference.

Bone microanatomy appears to track changes in various physiological or ecological properties of the individual or the taxon. Analyses of sections of the tibia of 99 taxa show a highly significant (P ≤ 0.005) relationship between long‐bone microanatomy and habitat. Randomization tests reveal a highly significant (P ≤ 0.005) phylogenetic signal on several compactness profile parameters and lifestyle. Discriminant analyses yield an inference model which has a success rate of 63% when lifestyle is coded into three states (aquatic, amphibious and terrestrial) or 83% for a binary model (aquatic vs. amphibious to terrestrial). Lifestyle is inferred to have been terrestrial for the stem‐tetrapod Discosauriscus (Early Permian), the basal synapsid Dimetrodon (Early Permian), the dicynodont therapsid Dicynodon (Late Permian), an unindentified gorgonopsian (Late Permian); the parareptile Pareiasaurus (Middle or Late Permian) is modelled as being aquatic, but was more likely amphibious.