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Evolution and Development of the Strepsirrhine Primate Skull Renaud Lebrun

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Evolution and Development of the Strepsirrhine Primate Skull Renaud Lebrun Evolution and Development of the Strepsirrhine Primate Skull Renaud Lebrun To cite this version: Renaud Lebrun. Evolution and Development of the Strepsirrhine Primate Skull. Paleontology. Uni- versité de Montpellier 2; Universität Zürich - Switzerland, 2008. English. tel-01874272 HAL Id: tel-01874272 https://hal.archives-ouvertes.fr/tel-01874272 Submitted on 14 Sep 2018 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. EVOLUTION AND DE V E LOPM E NT OF TH E STR E P S IRRHIN E PRIMAT E SKULL Dissertation zur Erlangung der naturwissenschaftlichen Doktorwürde (Dr. sc. nat.) vorgelegt der Mathematisch-naturwissenschaftlichen Fakultät der Universität Zürich Doppeldoktorat Universität Zürich - l’Université Montpellier II Von Renaud Lebrun aus Frankreich Promotionskomitee Dr. Franck Guy Prof. Dr. Jean-Jacques Jaeger (Leitung der Dissertation) Dr. Marcia Ponce de León Prof. Dr. Christoph Zollikofer (Leitung der Dissertation) Zürich, 2008 T H E S E pour obtenir le grade de DOCTEUR DE L’UNIVERSITE MONTPELLIER II Discipline : Paléontologie Ecole Doctorale : S.I.B.A.G.H.E - Thèse de doctorat double entre l’UNIVERSITE MONTPELLIER II et l’UNIVERSITE de ZÜRICH présentée et soutenue publiquement par Renaud Lebrun Le 04 avril 2008 Titre : EVOLUTION AND DEVELOPMENT OF THE STREPSIRRHINE PRIMATE SKULL Rapporteurs Prof. Dr. William Hylander,. Rapporteur Dr. Christopher Beard,. .Rapporteur Jury Prof. Dr. Monique Vianey-Liaud, . Présidente du Jury Dr. Franck Guy, . .Examinateur Prof. Dr. Jean-Jacques Jaeger,. Directeur de Thèse Prof. Dr. William Hylander,. Membre invité Dr. Marcia Ponce de León,. .Examinateur Prof. Dr. Marcelo Sánchez, . Examinateur Prof. Dr. Christoph Zollikofer,. Directeur de Thèse A mes parents. Abstract Since Haeckel (1866), the evolutionary modification of ontogeny has been recognized as an important source of morphological innovation. Due to recent advances in developmental ge- netics and phenotypic analysis, evolutionary developmental (evo-devo) studies have regained considerable interest and led to fundamental changes in our understanding of how ontogeny and phylogeny are related. This thesis investigates the relationship between ontogeny and phylogeny in strepsirrhine primates. The suborder Strepsirrhini, which comprises galagos, lorises and Malagasy lemurs, is thought to have retained most of the ancestral primate condition (as opposed to the suborder Haplorrhini, which comprises tarsiers and anthropoids). Nevertheless, strepsirrhines are highly diverse in their morphology. Here, the focus is on cranial diversity, which is analyzed from a developmental perspective with a new set of geometric morphometric tools. First, patterns of cranio-mandibular variability in extant adult primates are analyzed. Taking into account the phylogenetic constraints applying to the skull morphology permits a quantifi- cation of how dietary specialization and activity patterns influence cranio-mandibular morphol- ogy in both primates suborders. Also, the skull morphology in strepsirrhines and haplorrhines is clearly distinct, and it is shown here that differences between and within infraorders can be traced back to differences in developmental modes. According to a hypothesis proposed by Beard (1988), “strepsirrhinism” represents the prim- itive condition of the primate skull. This thesis shows that the cranial morphology of the Omo- myidae – a basal haplorrhine taxon comprising the genera Rooneyia, Necrolemur and Micro- choerus – is closer to that of extant strepsirrhines than to that of haplorrhines, while the cranial morphology of Tarsius is closer to that of other extant haplorrhines, i.e., the anthropoids. Thus, it is probable that the shift towards a modern haplorrhine morphology occurred in one omomyid lineage, to the exclusion of the three genera mentioned above. New arguments are proposed to support the hypothesis that the cranio-mandibular mor- phologies of the cheirogaleids and galagids are the least derived from the ancestral condition of toothcombed strepsirrhines. This thesis presents a comparative geometric morphometric analysis of cranio-mandibular development in ten strepsirrhine and two haplorrhine species. Haplorrhines and strepsirrhines differ widely in ontogenetic trajectory direction, length and position. Within the strepsirrhines, divergence between taxon-specific ontogenetic trajectories and allometric grade shifts are more pronounced in lemurs than in lorises. This pattern of evolutionary modification of ontogenetic trajectories is interpreted in the context of the rapid adaptive radiation of lemurs. The last section uses insights obtained from the evolutionary developmental analysis of extant taxa for a comparative analysis of fossil strepsirrhine taxa. The morphologies of extant and extinct strepsirrhines are compared. In particular, the morphology of the skull is well known from two adapiform subfamilies, Adapinae and Notharctinae. Among the adapines, a size increase has oc- curred in the Leptadapis lineage via a shift in allometric grade, which suggests phyletic gigantism in this genus. Adapiforms exhibit longer ontogenetic trajectories than extant strepsirrhines. A trend toward a shortening of ontogenetic trajectories has occurred in the evolutionary history of strep- sirrhines. This can be related to a context of general increase in encephalization within this lineage. Table of contents Abstract ........................................................... 1 Introduction ....................................................... 1 Chapter 1. Materials and Methods .................................... 9 1. Materials ............................................................... .11 1.1 Taxonomic framework. 11 1.2 Sample. 11 1.3 CT data acquisition. 12 1.4 Reconstruction . 12 2. Methods used throughout this manuscript ...................................13 2.1 Landmark protocols and landmark acquisition. 16 2.2 Procrustes superimposition. 17 2.3 Principal Component Analysis (PCA). 18 2.4 Canonical Variate Analysis (CVA) and classification procedures.. 18 2.5 Allometry . 19 2.6 Visualization of the results.. 22 3. MorphoTools: a geometric morphometric application framework ...............24 3.1 General architecture of MorphoTools.. 25 3.2 The sample scheme. 26 3.3 Visualization and outputs. 30 Chapter 2. What determines the morphological variation of the primate skull? ............................................................ 33 1. Introduction .............................................................35 2. Materials and methods ................................................... .38 2.1 Sample composition. 38 2.2 Dietary and activity patterns categories used for the study of adaptation . 38 2.3 Methods. 39 3. Results ................................................................ .44 3.1 Patterns of shape variability . 44 3.2 The effects of adaptation on the skull morphology . 46 3.3 Phylogenetic constraints in primate skulls . 53 4. Discussion ...............................................................54 4.1 Morphology and adaptation.. 54 4.2 Phylogenetic constraints explain the morphological differences between haplorrhines and strepsirrhines . 56 Chapter 3. “Strepsirrhinism”: is it a primitive or derived condition in pri- mates? ........................................................... 61 1. Introduction .............................................................63 2. Materials and Methods ....................................................64 2.1 Materials. 64 i 2.2 Methods. 64 3. Results ..................................................................65 3.1 PCA and classification procedure. 65 3.2 Phenetic analysis . 67 4. Discussion ...............................................................67 4.1 Rooneyia and the validity of A Protoanthropoidea taxon . 67 4.2 The ancestral condition of the primate skull architecture. 68 Chapter 4. Patterns of morphological variability in the strepsirrhine skull. 73 1. Introduction .............................................................75 2. Materials and Methods ....................................................76 2.1 Sample composition. 76 2.2 Methods. 76 3. Results ................................................................ .80 3.1 General patterns of shape variability . 80 3.2 Family-specific allometric patterns . 84 3.3 Morphology is distinctive at the family level . 87 3.4 Estimation of the ancestral morphology of toothcombed strepsirrhines.. 90 4. Discussion ...............................................................90 4.1 Allometry . 90 4.2 The ancestral morphology of toothcombed strepsirrhines. 92 1. Introduction .............................................................97 2. Materials and methods ................................................... .99 2.1 Sample composition. 99 2.2 Landmark protocol. 99 2.3 Common time scales. 99 2.4 The allometric component of ontogenetic shape change. 100 2.5 Patterns of shape change during ontogeny . 100 2.6 Interspecific differences in ontogenetic trajectory direction, length and position . 101 2.7
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