Evolution and development of the strepsirrhine primate skull
Lebrun, Renaud. Evolution and development of the strepsirrhine primate skull. 2008, University of Zurich / Univ. Montpellier, Faculty of Science.
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 genetics 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 quantification of how dietary specialization and activity patterns influence cranio-mandibular morphology 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 primitive condition of the primate skull. This thesis shows that the cranial morphology of the Omomyidae – a basal haplorrhine taxon comprising the genera Rooneyia, Necrolemur and Microchoerus – 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 morphologies 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 occurred 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 strepsirrhines. This can be related to a context of general increase in encephalization within this lineage. Abstract 2: Due to recent advances in developmental genetics and phenotypic analysis, evolutionary developmental (evo-devo) studies 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. Here, the focus is on cranial diversity, which is analyzed from a developmental perspective, and with a new set of geometric morphometric tools. A comparative geometric morphometric analysis of cranio-mandibular development is conducted in ten strepsirrhines 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. The insights obtained from the evolutionary developmental analysis of extant taxa are used for a comparative analysis of Eocene fossil strepsirrhine taxa belonging to the infraorder Adapiformes. Among the adapine adapiforms, an increase in size via allometric grade shift has occurred in the Leptadapis lineage, 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 strepsirrhines. This trend can be related to the expression of developmental constraints in a context of selection for increase in encephalization.
Zusammenfassung 2 Aufgrund jüngerer Fortschritte in der Entwicklungsgenetik sowie der phänotypischen Analyse ist das Interesse an der evolutionären Entwicklungsbiologie enorm gestiegen, und hat zu grundlegenden Veränderungen im Verständnis der Beziehung von Ontogenese und Phylogenese geführt. Diese Arbeit untersucht die Beziehung zwischen Ontogenese und Phylogenese am Beispiel der Feuchtnasenaffen (Strepsirrhini). Die kraniale Diversität dieser Primaten wird mit einer Palette neuer morphometrischer Werkzeuge analysiert. Resultate aus der evolutionären Entwicklungsbiologie existierender Taxa werden für eine vergleichende Analyse von fossilen Taxa der aus dem Eozän stammenden Unterordnung Adapiformes benutzt. Die evolutionäre Geschichte der Strepsirhini weist auf eine Tendenz in Richtung verkürzter ontogenetischer Trajektorien hin. Dies kann in einem Zusammenhang allgemeiner Enzephalisation in dieser Abstammungslinie gesehen werden.
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 genetics 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 quantification of how dietary specialization and activity patterns influence cranio-mandibular morphology 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 primitive condition of the primate skull. This thesis shows that the cranial morphology of the Omomyidae – a basal haplorrhine taxon comprising the genera Rooneyia, Necrolemur and Microchoerus – 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 morphologies 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 occurred 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 strepsirrhines. This can be related to a context of general increase in encephalization within this lineage. Abstract 2: Due to recent advances in developmental genetics and phenotypic analysis, evolutionary developmental (evo-devo) studies 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. Here, the focus is on cranial diversity, which is analyzed from a developmental perspective, and with a new set of geometric morphometric tools. A comparative geometric morphometric analysis of cranio-mandibular development is conducted in ten strepsirrhines 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. The insights obtained from the evolutionary developmental analysis of extant taxa are used for a comparative analysis of Eocene fossil strepsirrhine taxa belonging to the infraorder Adapiformes. Among the adapine adapiforms, an increase in size via allometric grade shift has occurred in the Leptadapis lineage, 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 strepsirrhines. This trend can be related to the expression of developmental constraints in a context of selection for increase in encephalization.
Zusammenfassung 2 Aufgrund jüngerer Fortschritte in der Entwicklungsgenetik sowie der phänotypischen Analyse ist das Interesse an der evolutionären Entwicklungsbiologie enorm gestiegen, und hat zu grundlegenden Veränderungen im Verständnis der Beziehung von Ontogenese und Phylogenese geführt. Diese Arbeit untersucht die Beziehung zwischen Ontogenese und Phylogenese am Beispiel der Feuchtnasenaffen (Strepsirrhini). Die kraniale Diversität dieser Primaten wird mit einer Palette neuer morphometrischer Werkzeuge analysiert. Resultate aus der evolutionären Entwicklungsbiologie existierender Taxa werden für eine vergleichende Analyse von fossilen Taxa der aus dem Eozän stammenden Unterordnung Adapiformes benutzt. Die evolutionäre Geschichte der Strepsirhini weist auf eine Tendenz in Richtung verkürzter ontogenetischer Trajektorien hin. Dies kann in einem Zusammenhang allgemeiner Enzephalisation in dieser Abstammungslinie gesehen werden.
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