Sequencing three crocodilian genomes to illuminate the evolution of archosaurs and amniotes

The International Crocodilian Genomes Working Group (ICGWG) will sequence and assemble the American alligator (Alligator mississippiensis), saltwater crocodile (Crocodylus porosus) and Indian gharial (Gavialis gangeticus) genomes. The status of these projects and our planned analyses are described.     

Vertebrate limb development and possible clues to diversity in limb form

Chick embryos are good models for vertebrate development. The principles that underlie chick wing development have been discovered and there is increasing knowledge about the molecules involved. The importance of identifying molecules is that this provides a direct link to understanding the genetic basis of diversity in form. Chick wing development will be compared with limb development in other vertebrates. Possible mechanisms that could lead to variations in form, including limb reductions and limblessness, differences between fore- and hindlimbs, limb proportions, and interdigital webbing can be suggested.     

Developmental morphology of limb reduction in Hemiergis (Squamata: Scincidae): chondrogenesis,osteogenesis, and heterochrony

Digit loss is a common theme in tetrapod evolution that may involve changes in several developmental processes. The skink genus Hemiergis provides an ideal model to study these processes in closely related taxa: within three Western Australian Hemiergis species, digit quantity ranges between two and five. For three consecutive reproductive seasons, gravid females of Hemiergis were collected in the field and their embryos prepared for histological analysis of limb skeletal development (chondrogenesis and osteogenesis). Comparative studies of skeletal developmental morphology demonstrate that limbs with fewer than five digits do not result from a simple truncation of a putative ancestral (five-digit) developmental program. The developmental and adult morphologies in two-, three-, and four-digit Hemiergis are neither predicted nor explained by a simple model of heterochrony involving either chondrogenesis or osteogenesis. In postnatal Hemiergis, digit number and relative limb length do not correlate in a simple linear fashion. Instead, limb size and digit reduction may correlate with substrate conditions and burrowing behavior.     

Limb morphogenesis in the branchiopod crustacean, Thamnocephalus platyurus, and the evolution of proximal limb lobes within Anostraca

Crustacean limbs exhibit highly diverse morphologies. One major route of diversification is in the number and position of branches arising from the proximal part of the limb. Here I describe development of larvae of the branchiopod crustacean, Thamnocephalus platyurus and describe in detail the development of the thoracic limbs. The thoracic limbs bear proximal branches both medially and laterally. The most proximal branches on either side (gnathobase and pre-epipod) show a similar developmental history: they develop via fusion of two rudiments into a single adult branch. However, phylogenetic analysis suggests that the developmental fusions have distinct evolutionary histories. In one case (gnathobase), the developmental rudiments reflect the ancestral adult morphology of two distinct branches. In the other (pre-epipod), the rudiments are an apparent novelty within the Anostraca and develop into two adult structures in only a single derived family.     

Ancestral patterns in bird limb development: A new look at Hampé's experiment

The “Archaeopteryx limb” of experimentally treated bird embryos has become a standard quotation in the growing literature on developmental factors in evolution. It has not only been claimed that an early manipulation of the chick limb produces a series of atavistic skeletal features, but the experiment is also frequently interpreted within a genome-centered concept of atavism. The present study provides a morphological, quantitative, and comparative analysis of the skeletal and muscular reactions to the classic barrier insertion experiment of Hampé. The main result of this operation, traditionally seen as a “full length fibula”, is shown to be a relative effect due to tibia shortening, while all the other ancestral skeletal features, which are usually pointed out as being provoked by the elongated fibula, do not appear. The experimentally generated fibula/tibia length ratio and distance, however, mimic the pattern in developing reptilian limbs and are seen to induce secondary effects in the muscular system that are reminiscent of archosaur reptiles. Similar muscle patterns are found as interspecific variations in several bird species. The revised view of the skeletal changes and the additional data on muscular effects allow for a renewed interpretation of the experiment, shifting the emphasis from atavisms to the role of heterochrony, developmental integration, and epigenetic constraint in the evolutionary modification of organismic structures.     

Braincase evolution in suchian archosaurs (Reptilia: Diapsida): evidence from the rauisuchian Batrachotomus kupferzellensis

The osteology of an almost complete braincase of the rauisuchian archosaur Batrachotomus kupferzellensis Gower from the Middle Triassic of Germany is described. There is a possibly discrete epiotic ossification, the metotic fissure is undivided by bone (i.e. there is a metotic foramen), the medial wall of the otic capsule is mostly ossified, the cerebral branch of the internal carotid artery entered the lateral surface of the parabasisphenoid, the ventral ramus of the opisthotic is more prominent laterally than a strong subvertical ridge on the exoccipital and basioccipital that lies posterior to the external foramen for the hypoglossal nerve, and the perilymphatic foramen faces away from the otic capsule in a posterior direction. Braincase morphology in the rauisuchians Saurosuchus galilei , Postosuchus kirkpatricki, and Tikisuchus romeri is reviewed. A matrix of 27 braincase characters for 12 archosaurian taxa is analysed. The most parsimonious hypothesis is consistent with the currently orthodox view of archosaurian phylogeny, except in that aetosaurians are more closely related to crocodylomorphs than is any rauisuchian. This phylogeny is used in a brief interpretation of the evolution of derived braincase features present in extant crocodilians. © 2002 The Linnean Society of London, Zoological Journal of the Linnean Society , 2002, 136 , 49–76.     

Palaeontology and Evolutionary Developmental Biology: A Science of the Nineteenth and Twenty–first Centuries

A wind of change has swept through palaeontology in the past few decades. Contrast Sir Peter Medawar’s dismissive: ‘palaeontology is a particularly undemanding branch of science’ (as recalled by John Maynard Smith in Sabbagh 1999, p. 158) with ‘Palaeontology: grasping the opportunities in the science of the twenty–first century’, the title of a contribution to a special issue of Geobios by the Cambridge palaeontologist, Simon Conway Morris (1998a). The winds of change have come partly from palaeontologists seeking to broaden the impact of their studies and partly from biologists (neontologists) realizing the contributions that palaeontology can make to their disciplines. Consequently, impressions of past life preserved in stone are coming alive. Fossils are being described and analyzed using new tools and languages as the static fossil record becomes a record of transitions in patterns that can be explained and related to biological, ecological, climatic and tectonic changes. The latest addition is evolutionary developmental biology, or ‘evo–devo’, whose language provides a new basis upon which to interpret anatomical change, both materially and mechanistically. In this review I examine the major contributions made by palaeontology, how palaeontology has been linked to evolution and to embryology in the past, and how links with evo–devo have enlivened and will continue to enliven both palaeontology and evo–devo. Closer links between the two fields should illuminate important unresolved issues related to the origin of the metazoans (e.g. Why is there a conflict between molecular clocks and the fossil record in timing the metazoan radiation; were Precambrian metazoan ancestors similar to extant larvae or to miniature adults?) and to diversification of the metazoans (e.g. How do developmental constraints bias the direction of evolution; how do microevolutionary developmental processes relate to macroevolutionary changes?).     

Modularity and heterochrony in the evolution of the ceratopsian dinosaur frill

The fossil record provides compelling examples of heterochrony at macroevolutionary scales such as the peramorphic giant antlers of the Irish elk. Heterochrony has also been invoked in the evolution of the distinctive cranial frill of ceratopsian dinosaurs such as Triceratops. Although ceratopsian frills vary in size, shape, and ornamentation, quantitative analyses that would allow for testing hypotheses of heterochrony are lacking. Here, we use geometric morphometrics to examine frill shape variation across ceratopsian diversity and within four species preserving growth series. We then test whether the frill constitutes an evolvable module both across and within species, and compare growth trajectories of taxa with ontogenetic growth series to identify heterochronic processes. Evolution of the ceratopsian frill consisted primarily of progressive expansion of its caudal and caudolateral margins, with morphospace occupation following taxonomic groups. Although taphonomic distortion represents a complicating factor, our data support modularity both across and within species. Peramorphosis played an important role in frill evolution, with acceleration operating early in neoceratopsian evolution followed by progenesis in later diverging cornosaurian ceratopsians. Peramorphic evolution of the ceratopsian frill may have been facilitated by the decoupling of this structure from the jaw musculature, an inference that predicts an expansion of morphospace occupation and higher evolutionary rates among ceratopsids as indeed borne out by our data. However, denser sampling of the meager record of early‐diverging taxa is required to test this further.     

Plant transposable elements: Their role in evolution

Transposable elements (TE) are natural constituents of plant genomes. However, their presence only becomes apparent if they become dislodged from their resident positions in the genome and transpore into another gene, thereby inducing a mutation. Such TE-induced mutations are somatically unstable because they revert to wild type and hence reconstitute the expression of the mutated gene. The frequent somatic excision of the TE results in a variegated phenotype. Since this instability is inherited in a Mendelian manner the variegated phenotype is nuclear determined. By this criterion TE have been shown to occur in more than 30 species belonging to different families and genera. Many questions arise when dealing with TE: their structure and functions, and the biological significance of the activity of elements in the differentiation of a normal plant or in the evolution of plant genes.     

Integration and dissociation of limb elements in flying vertebrates: a comparison of pterosaurs, birds and bats

Flapping flight has evolved independently in three vertebrate clades: pterosaurs, birds and bats. Each clade has a unique flight mechanism involving different elements of the forelimb. Here, patterns of limb integration are examined using partial correlation analysis within species and matrix correlation analysis across species to test whether the evolution of flapping flight has involved developmental dissociation of the serial homologues in the fore- and hind limb in each clade. Our sample included seven species of birds, six species of bats, and three species of pterosaurs for which sufficient sample sizes were available. Our results showed that, in contrast to results previously reported for quadrupedal mammals, none of the three clades demonstrated significant integration between serial homologues in the fore- and hind limb. Unexpectedly, there were few consistent patterns of within-forelimb correlations across each clade, suggesting that wing integration is not strongly constrained by functional relationships. However, there was significant integration within the hind limbs of pterosaurs and birds, but not bats, possibly reflecting the differing functions of hind limbs (e.g. upright support vs. suspension) in these clades.     

Patterns of morphospace occupation and mechanical performance in extant crocodilian skulls: A combined geometric morphometric and finite element modeling approach

Extant and fossil crocodilians have long been divided into taxonomic and/or ecological groups based on broad patterns of skull shape, particularly the relative length and width of the snout. However, these patterns have not been quantitatively analyzed in detail, and their biomechanical and functional implications are similarly understudied. Here, we use geometric morphometrics and finite element analysis to explore the patterns of variation in crocodilian skull morphology and the functional implications of those patterns. Our results indicate that skull shape variation in extant crocodiles is much more complex than previously recognized. Differences in snout length and width are the main components of shape variation, but these differences are correlated with changes in other regions of the skull. Additionally, there is considerable disparity within general classes such as longirostrine and brevirostrine forms. For example, Gavialis and Tomistoma occupy different parts of morphospace implying a significant difference in skull shape, despite the fact that both are traditionally considered longirostrine. Skull length and width also strongly influence the mechanical performance of the skull; long and narrow morphotypes (e.g., Tomistoma) experience the highest amount of stress during biting, whereas short and broad morphotypes (e.g., Caiman latirostris) experience the least amount of stress. Biomechanical stress and the hydrodynamic properties of the skull show a strong relationship with the distribution of crocodilians in skull morphospace, whereas phylogeny and biogeography show weak or no correlation. Therefore, ecological specializations related to feeding and foraging likely have the greatest influence on crocodilian skull shape. J. Morphol., 2008. © 2008 Wiley‐Liss, Inc.     

Fossil horses from "Eohippus" (Hyracotherium) to Equus, 2: rates of dental evolution revisited

Rates of dental evolution are calculated for four upper first molar (M¹) characters of 26 ancestral-descendant species pairs of Cenozoic horses from North America. On average, crown height evolved significantly more rapidly (= 0.104 darwins, d) than did occlusal dimensions (length and width; = 0.045 d and 0.047 d, respectively). As might be expected, low-crowned Eocene and Oligocene horses ( Hyracotherium through Mesohippus ) exhibit relatively slow rates of dental evolution. During the major early Miocene adaptive shift from browsers to grazers ( Parahippus to Merychippus ), only crown height evolved rapidly. Advanced Miocene-Pliocene three-toed hipparions and one-toed equines are generally normal, or horotelic, in their rates of dental evolution. The most rapid rates are exhibited in Miocene browsing anchitheres and the dwarf genus Pseudhipparion. Horses do not show the very high rates of dental evolution reported elsewhere for Paleogene mammals. The traditional notion of horses being a prime example of rapid morphological evolution as seen from the fossil record is not corroborated by the data presented here.     

Additional postcranial elements of Teilhardina belgica: The oldest European primate

Teilhardina belgica is one of the earliest fossil primates ever recovered and the oldest fossil primate from Europe. As such, this taxon has often been hypothesized as a basal tarsiiform on the basis of its primitive dental formula with four premolars and a simplified molar cusp pattern. Until recently [see Rose et al.: Am J Phys Anthropol 146 (2011) 281–305; Gebo et al.: J Hum Evol 63 (2012) 205–218], little was known concerning its postcranial anatomy with the exception of its well‐known tarsals. In this article, we describe additional postcranial elements for T. belgica and compare these with other tarsiiforms and with primitive adapiforms. The forelimb of T. belgica indicates an arboreal primate with prominent forearm musculature, good elbow rotational mobility, and a horizontal, rather than a vertical body posture. The lateral hand positions imply grasps adaptive for relatively large diameter supports given its small body size. The hand is long with very long fingers, especially the middle phalanges. The hindlimb indicates foot inversion capabilities, frequent leaping, arboreal quadrupedalism, climbing, and grasping. The long and well‐muscled hallux can be coupled with long lateral phalanges to reconstruct a foot with long grasping digits. Our phyletic analysis indicates that we can identify several postcranial characteristics shared in common for stem primates as well as note several derived postcranial characters for Tarsiiformes. Am J Phys Anthropol 156:388–406, 2015. © 2014 Wiley Periodicals, Inc.     

Transposable elements: powerful facilitators of evolution

Transposable elements (TEs) are powerful facilitators of genome evolution, and hence of phenotypic diversity as they can cause genetic changes of great magnitude and variety. TEs are ubiquitous and extremely ancient, and although harmful to some individuals, they can be very beneficial to lineages. TEs can build, sculpt, and reformat genomes by both active and passive means. Lineages with active TEs or with abundant homogeneous inactive populations of TEs that can act passively by causing ectopic recombination are potentially fecund, adaptable, and taxonate readily. Conversely, taxa deficient in TEs or possessing heterogeneous populations of inactive TEs may be well adapted in their niche, but tend to prolonged stasis and may risk extinction by lacking the capacity to adapt to change, or diversify. Because of recurring intermittent waves of TE infestation, available data indicate a compatibility with punctuated equilibrium, in keeping with widely accepted interpretations of evidence from the fossil record. We propose a general and holistic synthesis on how the presence of TEs within genomes makes them flexible and dynamic, so that genomes themselves are powerful facilitators of their own evolution     

Testing the directionality of evolution: the case of chydorid crustaceans

Although trends are of central interest to evolutionary biology, it is only recently that methodological advances have allowed rigorous statistical tests of putative trends in the evolution of discrete traits. Oligomerization is one such proposed trend that may have profoundly influenced evolutionary pathways in many types of animals, especially arthropods. It is a general hypothesis that repeated structures (such as appendage segments and spines) tend to evolve primarily through loss. Although largely untested, this principle of loss is commonly invoked in morphological studies of crustaceans for drawing conclusions about the systematic placements of taxa and about their phylogeny. We present a statistical evaluation of this hypothesis using a molecular phylogeny and character matrix for a family of crustaceans, the Chydoridae, analysed using maximum likelihood methods. We find that a unidirectional (loss-only) model of character evolution is a very poor fit to the data, but that there is evidence of a trend towards loss, with loss rates of structures being perhaps twice the rates of gain. Thus, our results caution against assuming loss a priori, in the absence of appropriate tests for the characters under consideration. However, oligomerization, considered as a tendency but not a rule, may indeed have had ramifications for the types of functional and ecological shifts that have been more common during evolutionary diversification.     

Heterochronic developmental shift caused by thyroid hormone in larval sand dollars and its implications for phenotypic plasticity and the evolution of nonfeeding development

Recent work on a diverse array of echinoderm species has demonstrated, as is true in amphibians, that thyroid hormone (TH) accelerates development to metamorphosis. Interestingly, the feeding larvae of several species of sea urchins seem to obtain TH through their diet of planktonic algae (exogenous source), whereas nonfeeding larvae of the sand dollar Peronella japonica produce TH themselves (endogenous source). Here we examine the effects of TH (thyroxine) and a TH synthesis inhibitor (thiourea) on the development of Dendraster excentricus, a sand dollar with a feeding larva. We report reduced larval skeleton lengths and more rapid development of the juvenile rudiment in the exogenous TH treatments when compared to controls. Also, larvae treated with exogenous TH reached metamorphic competence faster at a significantly reduced juvenile size, representing the greatest reduction in juvenile size ever reported for an echinoid species with feeding larvae. These effects of TH on D. excentricus larval development are strikingly similar to the phenotypically plastic response of D. excentricus larvae reared under high food conditions. We hypothesize that exogenous (algae-derived) TH is the plasticity cue in echinoid larvae, and that the larvae use ingested TH levels as an indicator for larval nutrition, ultimately signaling the attainment of metamorphic competence. Furthermore, our experiments with the TH synthesis inhibitor thiourea indicate that D. excentricus larvae can produce some TH endogenously. Endogenous TH production might, therefore, be a shared feature among sand dollars, facilitating the evolution of nonfeeding larval development in that group. Mounting evidence on the effects of thyroid hormones in echinoderm development suggests life-history models need to incorporate metamorphic hormone effects and the evolution of metamorphic hormone production.     

Terrestriality constrains salamander limb diversification: Implications for the evolution of pentadactyly

Patterns of phenotypic evolution can abruptly shift as species move between adaptive zones. Extant salamanders display three distinct life cycle strategies that range from aquatic to terrestrial (biphasic), to fully aquatic (paedomorphic) and to fully terrestrial (direct development). Life cycle variation is associated with changes in body form such as loss of digits, limb reduction or body elongation. However, the relationships among these traits and life cycle strategy remain unresolved. Here, we use a Bayesian modelling approach to test whether life cycle transitions by salamanders have influenced rates, optima and integration of primary locomotory structures (limbs and trunk). We show that paedomorphic salamanders have elevated rates of limb evolution with optima shifted towards smaller size and fewer digits compared to all other salamanders. Rate of hindlimb digit evolution is shown to decrease in a gradient as life cycles become more terrestrial. Paedomorphs have a higher correlation between hindlimb digit loss and increases in vertebral number, as well as reduced correlations between limb lengths. Our results support the idea that terrestrial plantigrade locomotion constrains limb evolution and, when lifted, leads to higher rates of trait diversification and shifts in optima and integration. The basic tetrapod body form of most salamanders and the independent losses of terrestrial life stages provide an important framework for understanding the evolutionary and developmental mechanisms behind major shifts in ecological zones as seen among early tetrapods during their transition from water to land.