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Disparity and Geometry of the Skull in Archosauria (Reptilia: Diapsida)

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Disparity and Geometry of the Skull in Archosauria (Reptilia: Diapsida) Blackwell Science, LtdOxford, UKBIJBiological Journal of the Linnean Society0024-4066The Linnean Society of London, 2003? 2003 80? 6788 Original Article ARCHOSAURIAN SKULL DISPARITY J. MARUGÁN-LOBÓN and Á. D. BUSCALIONI Biological Journal of the Linnean Society, 2003, 80, 67–88. With 9 figures Disparity and geometry of the skull in Archosauria (Reptilia: Diapsida) JESÚS MARUGÁN-LOBÓN* and ÁNGELA D. BUSCALIONI Departamento. Biología, Unidad de Palaeontología, Facultad Ciencias, Universidad Autónoma de Madrid, 28049 Cantoblanco (Madrid), Spain Received 27 June 2002; accepted for publication 5 February 2003 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 mor- phospace 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 numer- ical 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 pro- portions. 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, imply- ing 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 approx- imately 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 mor- phology in macroevolution. © 2003 The Linnean Society of London, Biological Journal of the Linnean Society, 2003, 80, 67–88. ADDITIONAL KEYWORDS: macroevolution – morphospace – theoretical morphology. INTRODUCTION 1800 mm displayed by the huge Giganotosaurus caro- linii (Calvo & Coria, 1998). The spectrum of cranial At present, close to 10 000 extant species (9951 birds shapes is also highly varied, from the widespread plat- and 27 crocodiles) represent the archosaur lineage irostral condition in modern crocodiles, through the which, along with the vast number of extinct species oreinirostral of certain extinct crocodiles and dino- studied and described, has probably been one of the saurs, to the well-known beaked modern birds. most diverse groups of vertebrates on the planet. A relationship between habitats and cranial diver- Occupying almost the entirety of existing habitats sity has often been suggested, and the evolution of the during the Mesozoic (fresh and salty aquatic, aerial rostral shape has usually been considered dependant and terrestrial mediums), archosaur morphology can only on adaptation, either trophic, ethological or both be characterized, among other features, by extreme (Proctor & Lynch, 1993 for modern birds, and an over- skull diversity in shape and size (Witmer, 1995). This view in Brochu, 2001 for modern crocodiles). In accor- diversity matches the high disparity in overall size dance with this functional paradigm, the facial system these organisms can and could reach, where, for has been analysed thoroughly, although strictly in instance, skull sizes range from the 30 mm of hum- terms of the properties of its discrete conforming ele- mingbirds (Trochilidae) up to the approximately ments (Lewontin, 2000); thus functional constraints have been historically well explored in the archosau- *Corresponding author. E-mail: [email protected] rian cranial anatomy (Busbey, 1995 on modern croco- © 2003 The Linnean Society of London, Biological Journal of the Linnean Society, 2003, 80, 67–88 67 68 J. MARUGÁN-LOBÓN and Á. D. BUSCALIONI diles). Furthermore, this approach has led to the facial existence of morphological limitations due to struc- skeleton being viewed as an independent structure tural constraints between the rostrum, braincase and within the skull (Zusi, 1993), whereas the rostrum has orbital proportions. only occasionally been evaluated in close relation to Theoretical morphology and its operative tool, the other parts of the skull complex. morphospace, is the instrument we have used to inves- Our objective is to explore skull disparity and its tigate the natural limits of the skull geometry in the possible geometric basis, including analysing the ros- clade Archosauria. Within this theoretical back- trum within the skull of the archosaurian lineage. We ground, the creation of a hybrid morphospace, mixing have considered two-dimensional classic morphomet- information from both theoretical and empirical rics, in lateral view. According to our method, the approaches, has developed into a fruitful exploratory skull, taken as bone tissue, incorporates three ana- tool (see Rasskin-Gutman, 1995; McGhee, 1999; tomical units: facial skeleton (rostrum), cranial box Chapman & Rasskin-Gutman, 2001; Rasskin-Gutman (braincase), and orbits. Our starting hypothesis sug- & Buscalioni, 2001) which has yielded prospective gests the occurrence of a geometric pattern in the macroevolutionary hypotheses and predictions. Mor- archosaurian skull, forecasting that, despite skull dis- phospace analysis sets the context in which to pose parity (in terms of overall size, rostral proportion, and questions about how the distribution of organic shapes even braincase lateral extent), a set of relationships occurs in nature by means of an evaluation of the will underlie phylogenetic and functional factors in extent of occupied space, and how a particular geom- the archosaurian skull design. Thus, this study etry is conformed against all possible combinatory intends to gain insights on macroevolutionary pat- occurrences (Fig. 1). Our evolutionary analysis of the terns for the archosaurian skull, highlighting the skull patterns was undertaken horizontally (Wagner, 100%100% IMPOSSIBLEIMPOSSIBLE fofor OrbitOrbit 90 10 80 20 70 30 60 40 % Orbit % Rostrum 50 50 40 60 30 70 20 80 10 90 100%100% IMPOSSIBLEIMPOSSIBLE 90 80 70 60 50 40 30 20 10 100%100% IMPOSSIBLIMPOSSIBLE fofor BraincaseBraincase fofor RostrumRostrum % Braincase Figure 1. Theoretical morphospace of skull proportions. The triangular diagram shows all the possible combinations theoretically achievable. On each axis are percentages for rostrum (R), the orbit (O) and the braincase (B). Note that the skull theoretical designs are all of the same height and only vary on their horizontal length. Impossible theoretical and natural occurrences are represented by the apices of the triangle (meaning 100% of appearance of one unit alone) and by the midpoints of the sides of the triangle (50% each for two units). All possible combinations gather within the range delimited by the area of the triangle where they can be infinite, and strictly between the three elements. © 2003 The Linnean Society of London, Biological Journal of the Linnean Society, 2003, 80, 67–88 ARCHOSAURIAN SKULL DISPARITY 69 2001) throughout the clade Archosauria (i.e. Eupark- THE SAMPLE AND THE METRICS eria, Scleromochlus + Pterosauria, Ornithischia, Sau- The Appendix shows the list of the archosaurian spe- ropodomorpha, non-avian and avian theropods). Our cies sampled. The whole sample consists of 155 objective was to develop a model of skull variation in specimens belonging to five monophyletic groups archosaurs by means of a simple metric statement. (Euparkeria, Scleromochlus Pterosauria, Ornithis- Data was explored statistically to test for allometry + chia, Sauropodomorpha, Theropoda – including Aves). between pairs of anatomical skull units (rostrum, Several authors have successively verified the mono- orbit and braincase) in order to reveal the possible fac- phyly of these groups; a taxonomically congruent den- tors underlying their macroevolutionary patterns. drogram including all groups is depicted in Figure 2. Throughout the study we use the terms ‘theropods’ THE GEOMETRY OF THE SKULL and ‘birds’ paraphyletically only for the sake of sim- plicity when comparing groups, although by ‘thero- Geometric statements on the amniote skull can be pods’ we mean strictly all extinct avian and non-avian advanced intuitively. For example, Gould (1993) sum- theropods, while ‘birds’ is used to express all extant marizes the history and works by Petrus Camper avian theropods. The sample includes both extinct and (1722–1789), an anatomist whose research revealed a extant species; the former were measured on casts relationship between the cranial vault and the ante- from real specimens available at the Universidad rior face in humans. In order to quantify this relation- Autónoma de Madrid or were taken from literature. ship, Camper defined the ‘Facial Angle’, whose values The results obtained were also used to check the reli- depict a negative covariation between both cranial ability of skull reconstructions. Extant birds were
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