Morphospace occupation in thalattosuchian crocodylomorphs: skull shape variation, species delineation and temporal patterns

Abstract: Skull shape variation in thalattosuchians is examined using geometric morphometric techniques in order to delineate species, especially with respect to the classification of Callovian species, and to explore patterns of disparity during their evolutionary history. The pattern of morphological diversity in thalattosuchian skulls was found to be very similar to modern crocodilians: the main sources of variation are the length and the width of the snout, but these broad changes are correlated with size of supratemporal fenestra and frontal bone, length of the nasal bone, size of the orbit and premaxilla and position of the narial opening. Patterns of shape variation, in combination with discrete‐state morphology and stratigraphic and geographic range data were used to distinguish nine species of teleosaurid and 14 species of metriorhynchid, with the four currently recognized Callovian species being split into eight. Metriorhynchids were found to be more disparate from the average shape of morphospace than teleosaurids. However, short‐snouted metriorhynchids and long‐snouted teleosaurids showed the greatest amount of disparity with respect to snout morphotypes, indicating that each group tended to explore opposite areas of morphospace. Phylogeny was found to have a moderate influence on the pattern of morphospace occupation in metriorhynchids, but little effect in teleosaurids suggesting that other factors or constraints control the pattern of skull shape variation in thalattosuchians. A comparison of thalattosuchians with dyrosaur/pholidosaurids shows that thalattosuchians have a unique skull morphology, implying that there are multiple ways to construct a ‘long snout’. Moreover, the skull geometry of the problematic species Pelagosaurus typus was found to converge on the teleosaurid area of morphospace. Finally, the temporal distribution of thalattosuchian species and morphotypes demonstrate a clear and highly correlated relationship with sea level curves and mass extinction events through the Jurassic and the Early Cretaceous.     

Journeys through discrete‐character morphospace: synthesizing phylogeny,tempo, and disparity

Palaeontologists have long employed discrete categorical data to capture morphological variation in fossil species, using the resulting character–taxon matrices to measure evolutionary tempo, infer phylogenies and capture morphological disparity. However, to date these have been seen as separate approaches despite a common goal of understanding morphological evolution over deep time. Here I argue that there are clear advantages to considering these three lines of enquiry in a single space: the phylomorphospace. Conceptually these high‐dimensional spaces capture how a phylogenetic tree explores morphospace and allow us to consider important process questions around evolutionary rates, constraints, convergence and directional trends. Currently the literature contains fundamentally different approaches used to generate such spaces, with no direct comparison between them, despite the differing evolutionary histories they imply. Here I directly compare five different phylomorphospace approaches, three with direct literature equivalents and two that are novel. I use a single empirical case study of coelurosaurian theropod dinosaurs (152 taxa, 853 characters) to show that under many analyses the literature‐derived approaches tend to reflect introduced phylogenetic (rather than the intended morphological) signal. The two novel approaches, which produce limited ancestral state estimates prior to ordination, are able to minimize this phylogenetic signal and thus exhibit more realistic amounts of phylogenetic signal, rate heterogeneity, and convergent evolution.     

早期生命形态演化研究中的定量方法

定量古生物学是现代古生物学的一个分支,提倡用定量的手段来研究地质历史时期生命的演化过程。我国从事定量古生物研究的群体较小,特别是对前寒武纪早期生命演化的定量研究还没有系统地展开。这篇文章将主要介绍如何利用定量手段来研究前寒武纪化石的形态演化。对于前寒武纪化石,由于大部分化石分类属性的不确定性,通常使用几何性状对化石的最基本形态结构进行分析,并用存在/缺失(1/0)这种离散变量对每个性状进行量化。非参数多维标量分析方法[Non-parametric multidimensional scaling analysis(MDS)]可以将高维度的离散数据投影到二维或者三维的形态空间上,进而探讨生物群在形态空间中所占有的范围;由离散变量计算得出的生物群的表形分异度(morphological disparity)可以用MDS方差或者平均差异参数[Mean dissimilarity coeffi-cient(MDC)]来计算。形态空间的范围(morphospace range)和表形分异度是相互联系的,如果形态空间范围是固定的,那么表形分异度实际上代表了生物群在形态空间中的分布密度。在解释数据之前,需要对可能存在的样本效应进行测试。常用的方法包括稀释法(rarefaction)、随机取样法(randomization)和自举法(bootstrapping)等。为了帮助读者进一步了解这些方法的使用,文中列举了三个实例:伊迪卡拉生物的形态演化,元古代宏观藻类的形态演化和元古代及寒武纪疑源类的演化。     

Do different disparity proxies converge on a common signal? Insights from the cranial morphometrics and evolutionary history of Pterosauria (Diapsida: Archosauria)

Disparity, or morphological diversity, is often quantified by evolutionary biologists investigating the macroevolutionary history of clades over geological timescales. Disparity is typically quantified using proxies for morphology, such as measurements, discrete anatomical characters, or geometric morphometrics. If different proxies produce differing results, then the accurate quantification of disparity in deep time may be problematic. However, despite this, few studies have attempted to examine disparity of a single clade using multiple morphological proxies. Here, as a case study for this question, we examine the disparity of the volant Mesozoic fossil reptile clade Pterosauria, an intensively studied group that achieved substantial morphological, ecological and taxonomic diversity during their 145+ million-year evolutionary history. We characterize broadscale patterns of cranial morphological disparity for pterosaurs for the first time using landmark-based geometric morphometrics and make comparisons to calculations of pterosaur disparity based on alternative metrics. Landmark-based disparity calculations suggest that monofenestratan pterosaurs were more diverse cranially than basal non-monofenestratan pterosaurs (at least when the aberrant anurognathids are excluded), and that peak cranial disparity may have occurred in the Early Cretaceous, relatively late in pterosaur evolution. Significantly, our cranial disparity results are broadly congruent with those based on whole skeleton discrete character and limb proportion data sets, indicating that these divergent approaches document a consistent pattern of pterosaur morphological evolution. Therefore, pterosaurs provide an exemplar case demonstrating that different proxies for morphological form can converge on the same disparity signal, which is encouraging because often only one such proxy is available for extinct clades represented by fossils. Furthermore, mapping phylogeny into cranial morphospace demonstrates that pterosaur cranial morphology is significantly correlated with, and potentially constrained by, phylogenetic relationships.     

Allometric space and allometric disparity: a developmental perspective in the macroevolutionary analysis of morphological disparity

Here, we advance novel uses of allometric spaces--multidimensional spaces specifically defined by allometric coefficients--with the goal of investigating the focal role of development in shaping the evolution of morphological disparity. From their examination, operational measures of allometric disparity can be derived, complementing standard signals of morphological disparity through an intuitive and process-oriented refinement of established analytical protocols used in disparity studies. Allometric spaces thereby become a promising context to reveal different patterns of evolutionary developmental changes and to assess their relative prevalence and importance. Such spaces offer a novel domain of investigation of phenotypic variation and should help in detecting large-scale trends, thus placing various macroevolutionary phenomena in an explicitly developmental context. Ammonoidea (Cephalopoda) at the Lower-Middle Jurassic transition were chosen as a case study to illustrate this methodological approach. We constructed two phenotypic spaces: a static, adult one (adult morphospace) and a dynamic, developmental one (allometric space). Comparative disparity analyses show a strikingly stable occupation in both spaces, despite extensive change in taxonomic composition. In contrast, disparity analyses of subclades reveal clearly distinct morphological and allometric disparity dynamics. Allometric approaches allow developmental insights into morphological diversification otherwise intractable from the analysis of adult morphospace alone.     

Combining ontogenetic and evolutionary scales of morphological disparity: a study of early Jurassic ammonites

Two major research themes in Evolutionary Developmental Biology and in Paleobiology, respectively, have each become central for the analysis and interpretation of morphological changes in evolution: the study of ontogeny/phylogeny connections, mainly within the widespread and controversial framework of heterochrony; and the study of morphological disparity, the morphological signal of biodiversity, describing secular changes in morphospace occupation during the history of any given clade. Although enriching in their respective fields, these two themes have remained rather isolated to date, despite the potential value of integrating them as some recent studies begin to suggest. Here, we explore the recent notion of developmental morphospace-morphospace carrying ontogenetic information-as a potential tool for bridging the gap between disparity dynamics and developmental dynamics. We elaborate this approach with a case study of Early Jurassic ammonite family Hildoceratidae (Mollusca, Cephalopoda). Morphometric analyses of the shell shape of 20 species spanning the morphological spectrum of the family are used to quantify and contrast juvenile and adult disparity levels. Adult disparity is significantly greater than juvenile disparity at the family level; yet, some subclades also display different patterns. In addition, comparisons of ontogenetic trajectories underline the prevalence of heterochrony-based evolutionary modifications within subfamilies (via ontogenetic scaling); they also point to the probable existence of pervasive developmental constraints structuring inhomogeneous morphospace occupation.     

Bathymetric patterns of morphological disparity in deep-sea gastropods from the western North Atlantic basin

Understanding patterns of species richness requires knowledge of the individual roles species play in community structure. Here, I use gastropod shells as a source of information about both their ecological and their evolutionary functions in generating bathymetric gradients of diversity. Specifically, morphological disparity of shell architecture in deep-sea gastropods is evaluated over a depth gradient in the western North Atlantic by constructing an empirical morphospace based on an eigenshape analysis. Morphological disparity is quantified by calculating the centroid, total range, and dispersion of the morphospace at each station along the depth gradient. The results indicate that local faunas are drawn from a regional pool with the same variance but that average dissimilarity in forms reflects the number of species in the sample. The range of the morphospace at local scales is also less than at regional scales, resulting from the variability of the morphospace centroid over depth. Although the position of the morphospace changes with depth, morphological disparity remains unaffected. Despite the lack of bathymetric patterns in variance, patterns in nearest neighbor distance persist. The findings suggest the importance of interacting ecological and evolutionary processes at varying spatiotemporal scales for both morphological disparity and species richness.     

The complex effects of mass extinctions on morphological disparity

Studies of biodiversity through deep time have been a staple for biologists and paleontologists for over 60 years. Investigations of species richness (diversity) revealed that at least five mass extinctions punctuated the last half billion years, each seeing the rapid demise of a large proportion of contemporary taxa. In contrast to diversity, the response of morphological diversity (disparity) to mass extinctions is unclear. Generally, diversity and disparity are decoupled, such that diversity may decline as morphological disparity increases, and vice versa. Here, we develop simulations to model disparity changes across mass extinctions using continuous traits and birth-death trees. We find no simple null for disparity change following a mass extinction but do observe general patterns. The range of trait values decreases following either random or trait-selective mass extinctions, whereas variance and the density of morphospace occupation only decline following trait-selective events. General trends may differentiate random and trait-selective mass extinctions, but methods struggle to identify trait selectivity. Long-term effects of mass extinction trait selectivity change support for phylogenetic comparative methods away from the simulated Brownian motion toward Ornstein-Uhlenbeck and Early Burst models. We find that morphological change over mass extinction is best studied by quantifying multiple aspects of morphospace occupation.     

Comparable disparity in the appendicular skeleton across the fish–tetrapod transition,and the morphological gap between fish and tetrapod postcrania

Appendicular skeletal traits are used to quantify changes in morphological disparity and morphospace occupation across the fish–tetrapod transition and to explore the informativeness of different data partitions in phylogeny reconstruction. Anterior appendicular data yield trees that differ little from those built from the full character set, whilst posterior appendicular data result in considerable loss of phylogenetic resolution and tree branch rearrangements. Overall, there is a significant incongruence in the signals associated with pectoral and pelvic data. The appendicular skeletons of fish and tetrapods attain similar levels of morphological disparity (at least when data are rarefied at the maximum sample size for fish in our study) and occupy similarly sized regions of morphospace. However, fish appear more dispersed in morphospace than tetrapods do. All taxa show a heterogeneous distribution in morphospace, and there is a clear separation between fish and tetrapods despite the presence of several evolutionarily intermediate taxa.     

Diversity trends and their ontogenetic basis: an exploration of allometric disparity in rodents

It has been hypothesized that most morphological evolution occurs by allometric differentiation. Because rodents encapsulate a phenomenal amount of taxonomic diversity and, among several clades, contrasting levels of morphological diversity, they represent an excellent subject to address the question: how variable are allometric patterns during evolution? We investigated the influence of phylogenetic relations and ecological factors on the results of the first quantification of allometric disparity among rodents by exploring allometric space, a multivariate morphospace here derived from, and encapsulating all, the ontogenetic trajectories of 34 rodent species from two parallel phylogenetic radiations. Disparity was quantified using angles between ontogenetic trajectories for different species and clades. We found an overlapping occupation of allometric space by muroid and hystricognath species, revealing both clades possess similar abilities to evolve in different directions of phenotypic space, and anatomical diversity does not act to constrain the labile nature of allometric patterning. Morphological features to enable efficient processing of food serve to group rodents in allometric space, reflecting the importance of convergent morphology, rather than shared evolutionary history, in the generation of allometric patterns. Our results indicate that the conserved level of morphological integration found among primates cannot simply be extended to all mammals.     

The first 50Myr of dinosaur evolution: macroevolutionary pattern and morphological disparity

The evolutionary radiation of dinosaurs in the Late Triassic and Early Jurassic was a pivotal event in the Earth's history but is poorly understood, as previous studies have focused on vague driving mechanisms and have not untangled different macroevolutionary components (origination, diversity, abundance and disparity). We calculate the morphological disparity (morphospace occupation) of dinosaurs throughout the Late Triassic and Early Jurassic and present new measures of taxonomic diversity. Crurotarsan archosaurs, the primary dinosaur 'competitors', were significantly more disparate than dinosaurs throughout the Triassic, but underwent a devastating extinction at the Triassic-Jurassic boundary. However, dinosaur disparity showed only a slight non-significant increase after this event, arguing against the hypothesis of ecological release-driven morphospace expansion in the Early Jurassic. Instead, the main jump in dinosaur disparity occurred between the Carnian and Norian stages of the Triassic. Conversely, dinosaur diversity shows a steady increase over this time, and measures of diversification and faunal abundance indicate that the Early Jurassic was a key episode in dinosaur evolution. Thus, different aspects of the dinosaur radiation (diversity, disparity and abundance) were decoupled, and the overall macroevolutionary pattern of the first 50Myr of dinosaur evolution is more complex than often considered.     

Disparity and Evolutionary Rate Do Not Explain Diversity Patterns in Muroid Rodents (Rodentia: Muroidea)

A positive correlation between diversity and disparity/evolutionary rate is predicted by multiple evolutionary theories. However, recent empirical studies in various taxa do not always find such an association. Similarly, we find no correlation between these two levels of variation, based on cranial morphometric data and molecular phylogenetic data from 317 muroid rodent species and dipodoid outgroups, analyzed using three-dimensional geometric morphometrics. This disassociation was found using both phylogenetic and non-phylogenetic approaches, indicating that an increase in clade richness is not necessarily followed by an increase in morphological divergence and vice versa. Furthermore, the distribution of muroid families in morphospace is highly overlapping suggesting greater variation within than between clades. Taken together with the observation that families with the most distinctive cranial morphologies (nesomyids, dipodids, and spalacids) are the least diverse, indicates that evolution of new cranial morphologies may not play an important role in the diversification of muroid rodents.     

Investigating Morphospace Occupation in Multi-Scale Ecological and Evolutionary Data Using Regression Tree: Case Studies and Perspectives

A key challenge in ecology and evolutionary biology is to explain the origin, structure and temporal patterns of phenotypic diversity. With regard to the potentially complex determinism of phenotypic differences, the issue should be comprehended in a general view, across multiple scales and an increasing number of phenomic studies investigate shape variation through large taxonomic, biogeographic or temporal scales. In this context, there is an ever-increasing need to develop new tools for a coherent understanding of morphospace occupation by disentangling and quantifying the main determinants of phenotypic changes. The present study briefly introduce the possibility to use multivariate regression tree technique to cope with morphological data, as embedded in a geometric morphometric framework. It emphasizes that hierarchical partitioning methods produce a hierarchy between causal variables that may help analyzing complexity in multi-scale ecological and evolutionary data. I therefore suggest that morphological studies would benefit from the combined use of the classical statistical models with rapidly emerging and diversifying methods of machine-learning. Doing so allows one to primary explore in an extensive exploratory manner the hierarchy of nested organisational levels underlying morphological variation, and then conduct hypothesis-driven analysis by focusing on a relevant scale or by investigating the appropriate model that reflects hypothesized nested influence of explanatory variables. The outlined approach may help investigating morphospace occupation in an explicitly hierarchical quantitative context.     

From success to persistence: Identifying an evolutionary regime shift in the diverse Paleozoic aquatic arthropod group Eurypterida,driven by the Devonian biotic crisis

Mass extinctions have altered the trajectory of evolution a number of times over the Phanerozoic. During these periods of biotic upheaval a different selective regime appears to operate, although it is still unclear whether consistent survivorship rules apply across different extinction events. We compare variations in diversity and disparity across the evolutionary history of a major Paleozoic arthropod group, the Eurypterida. Using these data, we explore the group's transition from a successful, dynamic clade to a stagnant persistent lineage, pinpointing the Devonian as the period during which this evolutionary regime shift occurred. The late Devonian biotic crisis is potentially unique among the “Big Five” mass extinctions in exhibiting a drop in speciation rates rather than an increase in extinction. Our study reveals eurypterids show depressed speciation rates throughout the Devonian but no abnormal peaks in extinction. Loss of morphospace occupation is random across all Paleozoic extinction events; however, differential origination during the Devonian results in a migration and subsequent stagnation of occupied morphospace. This shift appears linked to an ecological transition from euryhaline taxa to freshwater species with low morphological diversity alongside a decrease in endemism. These results demonstrate the importance of the Devonian biotic crisis in reshaping Paleozoic ecosystems.     

Horseshoe crab phylogeny and independent colonizations of fresh water: ecological invasion as a driver for morphological innovation

Xiphosurids are an archaic group of aquatic chelicerate arthropods, generally known by the colloquial misnomer of ‘horseshoe crabs’. Known from marine environments as far back as the early Ordovician, horseshoe crabs are generally considered ‘living fossils’ – descendants of a bradytelic lineage exhibiting little morphological or ecological variation throughout geological time. However, xiphosurids are known from freshwater sediments in the Palaeozoic and Mesozoic; furthermore, the contention that xiphosurids show little morphological variation has never been tested empirically. Attempts to test this are hampered by the lack of a modern phylogenetic framework with which to explore different evolutionary scenarios. Here, I present a phylogenetic analysis of Xiphosurida and explore patterns of morphospace and environmental occupation of the group throughout the Phanerozoic. Xiphosurids are shown to have invaded non‐marine environments independently at least five times throughout their evolutionary history, twice resulting in the radiation of major clades – bellinurines and austrolimulids – that occupied novel regions of morphospace. These clades show a convergent ecological pattern of differentiation, speciation and subsequent extinction. Horseshoe crabs are shown to have a more dynamic and complex evolutionary history than previously supposed, with the extant species representing only a fraction of the group's past ecological and morphological diversity.     

Evolution of Cranial Shape in Caecilians (Amphibia: Gymnophiona)

Insights into morphological diversification can be obtained from the ways the species of a clade occupy morphospace. Projecting a phylogeny into morphospace provides estimates of evolutionary trajectories as lineages diversified information that can be used to infer the dynamics of evolutionary processes that produced patterns of morphospace occupation. We present here a large-scale investigation into evolution of morphological variation in the skull of caecilian amphibians, a major clade of vertebrates. Because caecilians are limbless, predominantly fossorial animals, diversification of their skull has occurred within a framework imposed by the functional demands of head-first burrowing. We examined cranial shape in 141 species, over half of known species, using X-ray computed tomography and geometric morphometrics. Mapping an existing phylogeny into the cranial morphospace to estimate the history of morphological change (phylomorphospace), we find a striking pattern: most species occupy distinct clusters in cranial morphospace that closely correspond to the main caecilian clades, and each cluster is separated by unoccupied morphospace. The empty spaces in shape space are unlikely to be caused entirely by extinction or incomplete sampling. The main caecilian clades have different amounts of morphological disparity, but neither clade age nor number of species account for this variation. Cranial shape variation is clearly linked to phyletic divergence, but there is also homoplasy, which is attributed to extrinsic factors associated with head-first digging: features of caecilian crania that have been previously argued to correlate with differential microhabitat use and burrowing ability, such as subterminal and terminal mouths, degree of temporal fenestration (stegokrotaphy/zygokrotaphy), and eyes covered by bone, have evolved and many combinations occur in modern species. We find evidence of morphological convergence in cranial shape, among species that have eyes covered by bone, resulting in a narrow bullet-shaped head. These results reveal a complex history, including early expansion of morphospace and both divergent and convergent evolution resulting in the diversity we observe today.     

GEOMETRIC MORPHOMETRICS OF THE SKULL ROOF OF STEREOSPONDYLS (AMPHIBIA: TEMNOSPONDYLI)

Abstract:  Geometric morphometric analysis using relative warps is applied to the skull roof of 62 species of stereospondyls and their closest outgroups (i.e. basal archegosauriforms) from among temnospondyl amphibians. Twenty-one landmarks and five taxonomic groups are used for comparisons. Their skull evolution is quantified in a morphospace defined by two relative warps axes. The majority of groups show poor concordance between morphological and phylogenetic distances. The only exception is represented by Yates and Warren's study of stereospondyl relationships, in which concordance is high. Only basal archegosauriforms and rhinesuchids show significant overlap in morphospace, although this might be due to low sample sizes. Regression of estimated mean disparity against taxon sample size shows that species within both the trematosauroid and the rhytidostean groups are more widely dispersed in morphospace than species belonging to any of the remaining stereospondyl groups. Stereospondyl skull evolution was characterized by divergence between major clades and convergence within those clades. Changes in patterns of morphospace occupation through time agree with the hypothesis of an 'explosive' radiation in the early Early Triassic, after the extinction of basal archegosauriforms at the end of the Permian.     

Contrasting patterns of disparity suggest differing constraints on the evolution of trilobite cephalic structures during the Cambrian ‘explosion’

Trilobites are an abundant group of Palaeozoic marine euarthropods that appear abruptly in the fossil record c. 521 million years ago. Quantifying the development of morphological variation (or ‘disparity’) through time in fossil groups like trilobites is critical in understanding evolutionary radiations such as the Cambrian ‘explosion’. Here, I use geometric morphometrics to quantify ‘cumulative disparity’ in functionally-important structures within the trilobite cephalon across their initial radiation during Cambrian Series 2. Overall cephalic disparity increased rapidly and attained a maximum within several million years. This pattern is dominated by the cephalic outline (in particular the genal spines), reflecting rapid, convergent expansion to the extremes of morphospace in a few early families. In contrast, removing the outline and focusing on structures such as the glabella and eye ridges (associated with feeding and vision, respectively) showed a more gradual increase in disparity, closer in line with taxonomic diversity and supporting the hypothesis of a relatively accurate trilobite fossil record. These contrasting patterns suggest that disparity in different structures was constrained in different ways, with extrinsic (ecological) factors probably having the major impact on overall disparity. It also implies that patterns of disparity in isolated substructures cannot necessarily be taken individually as representative of overall morphologies.