Empirical Morphospace Research Articles

Morphological disparity trends in Devonian trilobites from North Africa

AbstractThe Devonian was a time of drastic environmental change that shaped the morphology of trilobites. This study aims to investigate their morphological evolution and to show the influence of some abiotic and biotic factors (bathymetry, feeding habits and visual abilities) on their shape. A dataset was compiled to investigate the shape of three structures (cephalon as a whole, central part of the cephalon, and pygidium) of Devonian trilobites from North Africa, using a geometric morphometric approach. Based on empirical morphospaces, the morphological changes were quantified through the Devonian stages. The results reveal important variations in the morphological disparity of the glabella shape, the facial suture location, the pygidial length and the presence of spines. In the Lochkovian, morphological disparity was low, subsequently increased in the Pragian with numerous innovations, and reached a maximum in the Emsian. If the morphospace occupancy remained until the Eifelian, a severe loss of disparity occurred in the Givetian, a time known for important environmental changes. Disparity then remained low in the Late Devonian. The shapes inherited from the Silurian persisted throughout the Devonian whereas Pragian novelties were most affected by losses. These persistent shapes were more versatile for environmental adaptation, helping those trilobites to survive the environmental events. Similarly, the trilobite orders that survived Devonian events had a wide morphological spectrum and were better adapted to withstand environmental change.

Going round the twist—an empirical analysis of shell coiling in helicospiral gastropods

AbstractThe logarithmic helicospiral has been the most widely accepted model of regularly coiled molluscan form since it was proposed by Moseley and popularized by Thompson and Raup. It is based on an explicit assumption that shells are isometric and grow exponentially, and an implicit assumption that the external form of the shell follows the internal shape, which implies that the parameters of the spiral could be reconstructed from the external whorl profile. In this contribution, we show that these assumptions fail on all 25 gastropod species we examine. Using a dataset of 176 fossil and modern gastropod shells, we construct an empirical morphospace of coiling using the parameters of whorl expansion rate, translation rate, and rate of increasing distance from coiling axis, plus rate of aperture shape change, from their best-fit models. We present a case study of change in shell form through geologic time in the austral family Struthiolariidae to demonstrate the utility of our approach for evolutionary paleobiology. We fit various functions to the shell-coiling parameters to demonstrate that the best morphological model is not the same for each parameter. We present a set of R routines that will calculate helicospiral parameters from sagittal sections through coiled shells and allow workers to compare models and choose appropriate sets of parameters for their own datasets. Shell-form parameters in the Struthiolariidae highlight a hitherto neglected hypothesis of relationship between Antarctic Perissodonta and the enigmatic Australian genus Tylospira that fits the biogeographic and stratigraphic distribution of both genera.

Morphospace analysis leads to an evo-devo model of digit patterning.

Biological forms occupy a constrained portion of theoretical morphospaces. Developmental models accounting for empirical morphospaces are necessary to achieve a better understanding of this phenomenon. We analyzed the phalangeal formulas (PFs) in lizards and relatives' hands by comparing them with a set of simulated PFs that compose a theoretical morphospace. We detected that: (1) the empirical morphospace is severely limited in size, (2) the PFs comply with two properties of phalangeal count per digit, namely the ordering rule (DI ≤ DII ≤ DIII ≤ DIV ≥ DV), and the contiguity relationship (neighbor digits differ on average in one phalanx), (3) the totality of the PFs can be categorized into four categories of hands aligned along a feasibility gradient. We also reconstructed the evolution of PFs and found a stepwise trajectory from the plesiomorphic PF towards reduced conditions. Finally, we propose a developmental model as the generative mechanism behind the PFs. It is consistent with the bulk of evidence managed and involves an ordered digit primordia initialization timed with periodic signals of joint formation coming from digit tips. Our approach is also useful to address the study of other meristic sequences in nature such as dental, floral, and branchial formulas.

Why should we investigate the morphological disparity of plant clades?

Disparity refers to the morphological variation in a sample of taxa, and is distinct from diversity or taxonomic richness. Diversity and disparity are fundamentally decoupled; many groups attain high levels of disparity early in their evolution, while diversity is still comparatively low. Diversity may subsequently increase even in the face of static or declining disparity by increasingly fine sub-division of morphological 'design' space (morphospace). Many animal clades reached high levels of disparity early in their evolution, but there have been few comparable studies of plant clades, despite their profound ecological and evolutionary importance. This study offers a prospective and some preliminary macroevolutionary analyses. Classical morphometric methods are most suitable when there is reasonable conservation of form, but lose traction where morphological differences become greater (e.g. in comparisons across higher taxa). Discrete character matrices offer one means to compare a greater diversity of forms. This study explores morphospaces derived from eight discrete data sets for major plant clades, and discusses their macroevolutionary implications. Most of the plant clades in this study show initial, high levels of disparity that approach or attain the maximum levels reached subsequently. These plant clades are characterized by an initial phase of evolution during which most regions of their empirical morphospaces are colonized. Angiosperms, palms, pines and ferns show remarkably little variation in disparity through time. Conifers furnish the most marked exception, appearing at relatively low disparity in the latest Carboniferous, before expanding incrementally with the radiation of successive, tightly clustered constituent sub-clades. Many cladistic data sets can be repurposed for investigating the morphological disparity of plant clades through time, and offer insights that are complementary to more focused morphometric studies. The unique structural and ecological features of plants make them ideally suited to investigating intrinsic and extrinsic constraints on disparity.

Not all roads can be taken: development induces anisotropic accessibility in morphospace.

Morphospaces are quantitative representations of phenotype space that are widely used in studies of morphological evolution. Do current conceptualizations of morphospaces, however, appropriately reflect the evolutionary dynamics of organisms depicted in these spaces? Most empirical morphospace studies implicitly consider variability of biological forms as isotropic, but such a view appears inadequate when the properties of development mediating phenotypic changes are considered. Here, a trilobite case study is used to visualize the constraints imposed by development on the accessibility structure of morphospace. Variability in the resultant morphospace is strongly anisotropic and reveals discordances between the apparent range of possible phenotypes and their actual accessibility. Homoplasy, directionality, and asymmetry of evolutionary transitions appear as natural consequences of anisotropic variability and point out the limitation of morphological distance for evolutionary inference. Measures of distance in morphospace should be used with considerable caution and must be complemented with developmentally meaningful measures of evolutionary accessibility.

The disparity of priapulid, archaeopriapulid and palaeoscolecid worms in the light of new data

Priapulids and their extinct relatives, the archaeopriapulids and palaeoscolecids, are vermiform, carnivorous ecdysozoans with an armoured, extensible proboscis. These worms were an important component of marine communities during the Palaeozoic, but were especially abundant and diverse in the Cambrian. Today, they comprise just seven genera in four families. Priapulids were among the first groups used to test hypotheses concerning the morphological disparity of Cambrian fossils relative to the extant fauna. A previous study sampled at the generic level, concluding that Cambrian genera embodied marginally less morphological diversity than their extant counterparts. Here, we sample predominantly at the species level and include numerous fossils and some extant forms described in the last fifteen years. Empirical morphospaces for priapulids, archaeopriapulids and palaeoscolecids are relatively insensitive to changes in the taxon or character sample: their overall form has altered little, despite the markedly improved sampling. Cambrian and post-Cambrian genera occupy adjacent rather than broadly overlapping regions of these spaces, and Cambrian species still show lower morphological disparity than their post-Cambrian counterparts. Crucially, the significance of this difference has increased with improved taxon sampling over research time. In contrast with empirical morphospaces, the phylogeny of priapulids, archaeopriapulids and palaeoscolecids derived from morphological characters is extremely sensitive to details of taxon sampling and the manner in which characters are weighted. However, the extant Priapulidae and Halicryptidae invariably resolve as sister families, with this entire clade subsequently being sister group to the Maccabeidae. In our most inclusive trees, the extant Tubiluchidae are separated from these other living taxa by a number of small, intervening fossil clades.

Constraint and adaptation in the evolution of carnivoran skull shape

The evolutionary history of the Order Carnivora is marked by episodes of iterative evolution. Although this pattern is widely reported in different carnivoran families, the mechanisms driving the evolution of carnivoran skull morphology remain largely unexplored. In this study we use coordinate-point extended eigenshape analysis (CP-EES) to summarize aspects of skull shape in large fissiped carnivores. Results of these comparisons enable the evaluation of the role of different factors constraining the evolution of carnivoran skull design. Empirical morphospaces derived from mandible anatomy show that all hypercarnivores (i.e., those species with a diet that consists almost entirely of vertebrate flesh) share a set of traits involved in a functional compromise between bite force and gape angle, which is reflected in a strong pattern of morphological convergence. Although the paths followed by different taxa to reach this “hypercarnivore shape-space” differ because of phylogenetic constraints, the morphological signature of hypercarnivory in the mandible is remarkably narrow and well constrained. In contrast, CP-EES of cranial morphology does not reveal a similar pattern of shape convergence among hypercarnivores. This suggests a lesser degree of morphological plasticity in the cranium compared to the mandible, which probably results from a compromise between different functional demands in the cranium (e.g., feeding, vision, olfactory sense, and brain processing) whereas the mandible is only involved in food acquisition and processing. Combined analysis of theoretical and empirical morphospaces for these skull data also show the lower anatomical disparity of felids and hyaenids compared to canids and ursids. This indicates that increasing specialization within the hypercarnivorous niche may constrain subsequent morphological and ecological flexibility. During the Cenozoic, similar skull traits appeared in different carnivoran lineages, generated by similar selection pressures (e.g., toward hypercarnivory) and shared developmental pathways. These pathways were likely the proximate source of constraints on the degree of variation associated with carnivoran skull evolution and on its direction.

The flourishing diversity of models in theoretical morphology: from current practices to future macroevolutionary and bioenvironmental challenges

For decades, theoretical morphological studies of different groups of organisms have been successfully pursued in biological, paleontological, and computational contexts, often with distinct modeling approaches and research questions. A regular influx of new perspectives and varied expertise has contributed to the emergence of a veritable multidisciplinary outlook for theoretical morphology. The broadening of this discipline is reflected in a substantial increase in the number of models, leading to a bewildering diversity that has yet to be scrutinized. In this work, we tackle this issue in a synthetic fashion, with a quantitative meta-analysis that allows an objective comparison of theoretical morphological models treated as entities. By analogy with empirical morphospace analyses of actual organisms, we performed a multivariate ordination of a representative sample of models, producing a metaspace of models in which patterns of similarity and difference are visualized. A phenetic tree was used to characterize the relationships between models. Four major groups have been identified, and their disparity analyzed. We suggest this typology as a useful starting point to identify a core set of fundamental principles and protocols for better interpretation of the plethora of current models and for more efficient construction of models in the future. This in turn can help in diversifying the scope of macroevolutionary, developmental, and bioenvironmental questions in theoretical morphology.

Does shape matter? Morphological diversity and differential survivorship among Triassic ammonoid genera

Variation in longevity of taxa in the fossil record has been recognized, but few studies have tested for correlation between position in morphospace and differential survivorship. A sample of 322 Triassic ammonoid species, each one representing a genus, was studied to test whether longer-lived genera were significantly further from the centre of morphospace than shorter-lived genera. Two empirical morphospaces were constructed from morphological data, and the deviation of each genus from the “average form” (centroid) was calculated. Spearman Rank Correlation and Kruskal-Wallis tests were used to test for any significant relationships between distance from the centre of morphospace and longevity. Some longer-lived taxa tended to plot further from the centre of morphospace, but the amounts of variance in longevity accounted for were small and largely statistically non-significant. Ammonoid clade-level morphological stasis appears to be the product of repeated reoccupation of the centre of morphospaces after taxonomic turnover events.

1.3 Billion years of acritarch history: An empirical morphospace approach

Acritarchs are a group of organic-walled vesicular microfossils interpreted as protists, and are among the first eukaryotes preserved in the fossil record. Taxonomic inconsistencies amongst acritarch workers have made it difficult to address the evolutionary history of this group through more traditional methods (i.e., biodiversity through species counts). We have constructed an empirical morphospace to examine the first 1.3 billion years of acritarch evolution. We show that protist morphologic evolution is broadly correlated with major environmental and biologic revolutions in Earth history such as late Neoproterozoic global glaciations, the first appearance of the Ediacaran metazoans and the Cambrian explosion. Our results also show that protist morphologic expansion precedes their taxonomic diversification; this pattern, similar to that seen in Phanerozoic animal clades, suggests that early morphospace saturation and convergence are common occurrences in eukaryote macroevolution. In addition, our data do not support a monotonic increase in maximum diameter of acritarch vesicles through the Proterozoic; instead, maximum vesicle diameter appears to fluctuate in the Proterozoic before decreasing significantly in the early Cambrian.

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.

Disparity and geometry of the skull in Archosauria (Reptilia: Diapsida)

A metric comparison of 155 fossil and extant species in lateral view based on the proportions of three homologous units (braincase, orbit and rostrum) reveals the existence of an archosaurian skull geometry. An empirical morphospace depicting skull proportions shows that the most variable unit is the rostrum. Three skull types based on rostral proportion are proposed: meso-, longi- and brevirostral. These types depend, on one hand, on a direct numerical relationship between the braincase and the orbit, with a mean ratio of 1:1; never surpassing a 2:1 or 1:2 ratio limit. On the other hand, skull types show a significant negative correlation between braincase and rostrum proportions. Close relationships have been obtained between orbit and the rostrum, although with lower significance and a geometric meaning specific to each group. Skull types depend mainly on the proportional relationship between the rostrum and the braincase. Mesorostral types account for more natural occurrences within morphospace, implying a plesiomorphic condition in Archosauria. Skulls with highest longirostral values (flying forms) display a more restrictive braincase–orbit ratio relationship. Brevirostrals are limited to the smallest skull lengths, up to approximately 180 mm. 85% of brevirostral modern birds have altricial post-hatchling development. General allometric pattern is very similar for all sampled archosaurs, although giant taxa (i.e. non-avian theropods) display a different type of skull proportional growth, closer to isometry. Results reveal the existence of a constructional skull geometry, highlighting the importance of the deviance of the structural design from adaptive explanations on craniofacial morphology in macroevolution.

The spirit of D'arcy Thompson dwells in empirical morphospace.

Applications of the concept of a morphological space to the study of biological form during the past three decades are reviewed. Common features of the various types of morphological spaces constructed by morphometricians during this period are identified and used to construct a space of morphological spaces. This semiquantitative analysis reveals that the use of empirical morphospace by contemporary researchers is similar to Thompson's classic method of coordinate grid transformations, in the description of biological form.