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Bone and tooth microstructure in extinct and extant mammals and implications for growth and life history evolution, with an emphasis on cervids as a case study


Kolb, Christian. Bone and tooth microstructure in extinct and extant mammals and implications for growth and life history evolution, with an emphasis on cervids as a case study. 2016, University of Zurich, Faculty of Science.

Abstract

Since pioneering works in the middle of the 19th century, our knowledge of the histology of hard tissues of mammals has much increased. It has been demonstrated that bone and tooth histological traits correlate with biological variables and provide reliable estimates of growth and life history patterns in mammals. The variation of the key trait body size within clades of this group is common, especially if we consider extinct species. The developmental
and life history changes behind this evolutionary pattern are a rich subject of investigation.
This dissertation aims at investigating bone and tooth microstructure as markers of such changes.
In chapters 1.7 and 2, the knowledge and methods on synapsid (modern mammals as well as extinct ancestors and close relatives) bone microstructure and palaeohistology were systematically reviewed. Potential future research fields and techniques were discussed. Synapsid bone shows a large variety of bone tissues: Woven-fibred bone (disorganised), parallel-fibred bone, lamellar bone (arranged in thin layers), and fibrolamellar bone (mixture of woven-fibred and parallel-fibred/lamellar bone). New bone histological data on two extant marsupial species and of several extinct mainland and island placental mammals are presented. The bone cortex of extant marsupials consists of mainly parallel-fibred bone with a varying orientation of vascular canals. Hippopotamus minor, an extinct dwarf island
hippopotamid from the Late Pleistocene (~126 –12 kya) of Cyprus, shows fibrolamellar bone with a reticular (anastomosing) to plexiform (circumferential with radial connections) arrangement of vascular canals. Mikrotia magna, an extinct island rodent from the Late Miocene (~12–5 Mya) of Gargano, shows parallel-fibred primary bone with reticular vascularisation whereas another extinct island rodent, the dormouse Leithia sp. from the Pleistocene (~2.6-0.012 Mya) of Sicily, displays lamellar primary bone and a high amount of remodelling. The bone cortex of one continental and three island species of the extinct lagomorph Prolagus is characterised mainly by parallel-fibred primary bone with varying orientation of vascular canals. Paraceratherium sp. from the Late Oligocene (~28-23 Mya) of Turkey, the extinct giant rhinocerotoid, is represented by dense Haversian bone. Sinomegaceros yabei, the extinct Japanese giant deer from the Late Pleistocene, is characterised by high growth rates. Bone histological and skeletochronological (based on growth mark analysis) traits of sampled island mammals in comparison to mainland relatives suggest the presence of various modes of life history modifications on islands to depend on
factors of island evolution such as island size, distance from mainland, time of evolution, climate, and phylogeny.
Deer (Cervidae) represent an ideal case study for exploring body size and life history evolution, as they are characterised by a rich fossil record, a generally well-known phylogeny, and exceptional examples of body size evolution. In chapter 3, the hard tissue histology of eight deer species, including the illustrative genus Candiacervus with two dwarfed morphotypes from the Pleistocene of Crete, and the extinct giant deer Megaloceros giganteus, both closely related to the recent fallow deer, Dama dama, was examined. Long bones of all deer species sampled mainly possess primary plexiform fibrolamellar bone indicating a comparable mode of growth. Dwarf Candiacervus are characterised by low absolute growth rates, Megaloceros giganteus by high rates, and Dama dama by intermediate to low ones. The small, basal deer from the Early Miocene (~23-16 Mya), Procervulus praelucidus, shows the lowest growth rates recorded. Growth rates as derived by Sander & Tückmantel (2003) plotted against the anteroposterior bone diameter as a proxy for body mass indicate three groups: A group showing low growth rates, including dwarf Candiacervus and Procervulus, an intermediate group with Capreolus capreolus (roe deer) and Muntiacus muntjak (Indian muntjac), and one with high growth rates including Megaloceros giganteus, Alces alces (elk), Cervus elaphus (red deer), and Dama dama. Dwarf Candiacervus and Procervulus praelucidus indicate late attainment of skeletal maturity. Two senile Megaloceros specimens revealed, after tooth cementum analysis, ages of 16 and 19 years whereas two old dwarf Candiacervus specimens gave ages of 12 and 18 years. In an allometric (in relation to body
size) context, dwarf Candiacervus therefore had an extended lifespan compared to deer of similar body size. After comparison with other clades of mammals, it is concluded that various modes of skeletal tissue modification in evolution are linked with changes in size and life history that have occurred in parallel. In chapter 4, the histological dataset on cervids presented in chapter 3 was expanded. The long bone histology of the extinct “basal” deer Dicrocerus elegans and Euprox sp. from the Miocene (~23-5 Mya) was examined. Those species together with growth rates of the extinct Japanese giant deer, Sinomegaceros yabei, were included in the dataset of chapter 3
and ancestral growth rates among cervids and their correlation with body size were estimated. Dicrocerus shows a relatively high growth rate for its body size and attainment of skeletal maturity after five years. The growth rate condition found in Procervulus and Euprox is different and documents diversity in life history evolution of Miocene cervids. Scaling of skeletal elements in relation to size is a fundamental question of biology. By broad sampling of a wide range of body sizes, previous examinations have discovered general principles. However, for understanding scaling patterns of bones, it is essential to consider effects of confounding factors related to different lifestyles. In chapter 5, cervids, comprising various body sizes in contrast to a relatively uniform lifestyle, were comprehensively sampled and the mid-diaphyseal structure of their long bones was studied. Compactness parameters do not scale allometrically in cervid long bones. However, femoral cross-sectional shape scales positively allometric. This points towards greater directional bending rigidity in large-sized taxa. Relative cortical thickness (P) is more constrained in large-sized taxa. Therefore, it is concluded that tubular bones of large-sized terrestrial animals are more intensively selected for an energy-saving mid-diaphyseal structure since the P parameter is known to be centred around a mass-saving biomechanical optimum.
Keywords: Mammals, Palaeohistology, Body size, Life history, Island evolution, Bone tissue, Cementum analysis, Cervids, Marsupialia, Rodentia, Prolagus, Hippopotamus, Deinogalerix, Paraceratherium

Abstract

Since pioneering works in the middle of the 19th century, our knowledge of the histology of hard tissues of mammals has much increased. It has been demonstrated that bone and tooth histological traits correlate with biological variables and provide reliable estimates of growth and life history patterns in mammals. The variation of the key trait body size within clades of this group is common, especially if we consider extinct species. The developmental
and life history changes behind this evolutionary pattern are a rich subject of investigation.
This dissertation aims at investigating bone and tooth microstructure as markers of such changes.
In chapters 1.7 and 2, the knowledge and methods on synapsid (modern mammals as well as extinct ancestors and close relatives) bone microstructure and palaeohistology were systematically reviewed. Potential future research fields and techniques were discussed. Synapsid bone shows a large variety of bone tissues: Woven-fibred bone (disorganised), parallel-fibred bone, lamellar bone (arranged in thin layers), and fibrolamellar bone (mixture of woven-fibred and parallel-fibred/lamellar bone). New bone histological data on two extant marsupial species and of several extinct mainland and island placental mammals are presented. The bone cortex of extant marsupials consists of mainly parallel-fibred bone with a varying orientation of vascular canals. Hippopotamus minor, an extinct dwarf island
hippopotamid from the Late Pleistocene (~126 –12 kya) of Cyprus, shows fibrolamellar bone with a reticular (anastomosing) to plexiform (circumferential with radial connections) arrangement of vascular canals. Mikrotia magna, an extinct island rodent from the Late Miocene (~12–5 Mya) of Gargano, shows parallel-fibred primary bone with reticular vascularisation whereas another extinct island rodent, the dormouse Leithia sp. from the Pleistocene (~2.6-0.012 Mya) of Sicily, displays lamellar primary bone and a high amount of remodelling. The bone cortex of one continental and three island species of the extinct lagomorph Prolagus is characterised mainly by parallel-fibred primary bone with varying orientation of vascular canals. Paraceratherium sp. from the Late Oligocene (~28-23 Mya) of Turkey, the extinct giant rhinocerotoid, is represented by dense Haversian bone. Sinomegaceros yabei, the extinct Japanese giant deer from the Late Pleistocene, is characterised by high growth rates. Bone histological and skeletochronological (based on growth mark analysis) traits of sampled island mammals in comparison to mainland relatives suggest the presence of various modes of life history modifications on islands to depend on
factors of island evolution such as island size, distance from mainland, time of evolution, climate, and phylogeny.
Deer (Cervidae) represent an ideal case study for exploring body size and life history evolution, as they are characterised by a rich fossil record, a generally well-known phylogeny, and exceptional examples of body size evolution. In chapter 3, the hard tissue histology of eight deer species, including the illustrative genus Candiacervus with two dwarfed morphotypes from the Pleistocene of Crete, and the extinct giant deer Megaloceros giganteus, both closely related to the recent fallow deer, Dama dama, was examined. Long bones of all deer species sampled mainly possess primary plexiform fibrolamellar bone indicating a comparable mode of growth. Dwarf Candiacervus are characterised by low absolute growth rates, Megaloceros giganteus by high rates, and Dama dama by intermediate to low ones. The small, basal deer from the Early Miocene (~23-16 Mya), Procervulus praelucidus, shows the lowest growth rates recorded. Growth rates as derived by Sander & Tückmantel (2003) plotted against the anteroposterior bone diameter as a proxy for body mass indicate three groups: A group showing low growth rates, including dwarf Candiacervus and Procervulus, an intermediate group with Capreolus capreolus (roe deer) and Muntiacus muntjak (Indian muntjac), and one with high growth rates including Megaloceros giganteus, Alces alces (elk), Cervus elaphus (red deer), and Dama dama. Dwarf Candiacervus and Procervulus praelucidus indicate late attainment of skeletal maturity. Two senile Megaloceros specimens revealed, after tooth cementum analysis, ages of 16 and 19 years whereas two old dwarf Candiacervus specimens gave ages of 12 and 18 years. In an allometric (in relation to body
size) context, dwarf Candiacervus therefore had an extended lifespan compared to deer of similar body size. After comparison with other clades of mammals, it is concluded that various modes of skeletal tissue modification in evolution are linked with changes in size and life history that have occurred in parallel. In chapter 4, the histological dataset on cervids presented in chapter 3 was expanded. The long bone histology of the extinct “basal” deer Dicrocerus elegans and Euprox sp. from the Miocene (~23-5 Mya) was examined. Those species together with growth rates of the extinct Japanese giant deer, Sinomegaceros yabei, were included in the dataset of chapter 3
and ancestral growth rates among cervids and their correlation with body size were estimated. Dicrocerus shows a relatively high growth rate for its body size and attainment of skeletal maturity after five years. The growth rate condition found in Procervulus and Euprox is different and documents diversity in life history evolution of Miocene cervids. Scaling of skeletal elements in relation to size is a fundamental question of biology. By broad sampling of a wide range of body sizes, previous examinations have discovered general principles. However, for understanding scaling patterns of bones, it is essential to consider effects of confounding factors related to different lifestyles. In chapter 5, cervids, comprising various body sizes in contrast to a relatively uniform lifestyle, were comprehensively sampled and the mid-diaphyseal structure of their long bones was studied. Compactness parameters do not scale allometrically in cervid long bones. However, femoral cross-sectional shape scales positively allometric. This points towards greater directional bending rigidity in large-sized taxa. Relative cortical thickness (P) is more constrained in large-sized taxa. Therefore, it is concluded that tubular bones of large-sized terrestrial animals are more intensively selected for an energy-saving mid-diaphyseal structure since the P parameter is known to be centred around a mass-saving biomechanical optimum.
Keywords: Mammals, Palaeohistology, Body size, Life history, Island evolution, Bone tissue, Cementum analysis, Cervids, Marsupialia, Rodentia, Prolagus, Hippopotamus, Deinogalerix, Paraceratherium

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Additional indexing

Item Type:Dissertation
Referees:Sánchez-Villagra Marcelo R, Scheyer T M, Ozgul Arpat, Costeur Loïc
Communities & Collections:07 Faculty of Science > Paleontological Institute and Museum
Dewey Decimal Classification:560 Fossils & prehistoric life
Language:English
Date:2016
Deposited On:09 Jan 2017 15:03
Last Modified:09 Jan 2017 15:03
Number of Pages:205
Related URLs:http://www.recherche-portal.ch/ZAD:default_scope:ebi01_prod010723450 (Library Catalogue)

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