El conocimiento de las poblaciones del pasado a través de los restos óseos: análisis paleohistológico sobre huesos largos arqueológicos

Proyecto fin de carrera en Biología Evolutiva y Biodiversida

Dental histology of late Miocene hipparionins compared with extant Equus, and its implications for Equidae life history

Hipparionins were a dominant element of the late Miocene faunas of Europe; however, their biology and ecology remain incompletely understood. In this paper, we explore the pace of life history of different-sized hipparionin horses, using dental histology, and compare it with extant equids. In doing so we consider (i) the size diversity of hipparionins, (ii) their generally smaller size compared to extant equids, and (iii) the allometric coupling between size and life history. In particular, we reconstruct the dental growth in lower first/second molars and in later-formed lower third molars for three hipparionin taxa: two dwarf species (Hipparion periafricanum and H. gromovae), and a larger species (H. concudense). We also analyze dental growth in an extant zebra (Equus quagga) for comparative purposes. Our results reveal that, within each species, there are differences in enamel growth parameters between the first/second molars and third molars. These results illustrate the differences in the developmental timing of these teeth and the existence of a relationship between dental growth parameters with somatic growth. We also find that hipparionin teeth grow at slower rates and tend to erupt later in time than in extant Equus. Dwarf hipparionins, moreover, exhibit lower enamel extension rates than the larger species, but similar formation and eruption times. Considering the link between dental development and life history, these results suggest a slower pace of growth of selected hipparionins compared to extant equids, and a further slower life history than expected for their size in the two dwarf forms

Insular giant leporid matured later than predicted by scaling

The island syndrome describes morphological, behavioral, and life history traits that evolve in parallel in endemic insular organisms. A basic axiom of the island syndrome is that insular endemics slow down their pace of life. Although this is already confirmed for insular dwarfs, a slow life history in giants may not be adaptive, but merely a consequence of increasing body size.We tested this question in the fossil insular giant leporid Nuralagus rex. Using bone histology, we constructed both a continental extant taxon model derived from experimentally fluorochrome-labeled Lepus europaeus to calibrate life history events, and a growth model for the insular taxon. N. rex grew extremely slowly and delayed maturity well beyond predictions from continental phylogenetically corrected scaling models. Our results support the life history axiom of the island syndrome as generality for insular mammals, regardless of whether they have evolved into dwarfs or giants

Palaeohistology reveals a slow pace of life for the dwarfed Sicilian elephant

Altres ajuts: CERCA Programme/Generalitat de CatalunyaThe 1-m-tall dwarf elephant Palaeoloxodon falconeri from the Pleistocene of Sicily (Italy) is an extreme example of insular dwarfism and epitomizes the Island Rule. Based on scaling of life-history (LH) traits with body mass, P. falconeri is widely considered to be 'r-selected' by truncation of the growth period, associated with an early onset of reproduction and an abbreviated lifespan. These conjectures are, however, at odds with predictions from LH models for adaptive shifts in body size on islands. To settle the LH strategy of P. falconeri, we used bone, molar, and tusk histology to infer growth rates, age at first reproduction, and longevity. Our results from all approaches are congruent and provide evidence that the insular dwarf elephant grew at very slow rates over an extended period; attained maturity at the age of 15 years; and had a minimum lifespan of 68 years. This surpasses not only the values predicted from body mass but even those of both its giant sister taxon (P. antiquus) and its large mainland cousin (L. africana). The suite of LH traits of P. falconeri is consistent with the LH data hitherto inferred for other dwarfed insular mammals. P. falconeri, thus, not only epitomizes the Island Rule but it can also be viewed as a paradigm of evolutionary change towards a slow LH that accompanies the process of dwarfing in insular mammals

Life history inferences in extant and extinct Equus from the histological analysis of bone and enamel tissues

El estudio de life histories proporciona información sobre la biología y ecología de las especies, incluyendo las condiciones ecológicas de su ecosistema, su biodiversidad, su demografía y su vulnerabilidad. La life history de vertebrados actuales y extintos puede ser reconstruida a partir de la microestructura ósea y dental. Sin embargo, el estudio de mamíferos clave en paleontología y ecología, como los équidos, es aún escaso. La presente tesis doctoral tiene como objetivo analizar la histología ósea y dental de Equus actuales y extintos para inferir sus características biológicas y de life history más importantes. La muestra actual se compone de huesos y dientes de asno salvaje asiático, cebra común y cebra de Grevy. Su estudio ha proporcionado un marco sólido para el análisis de Equus fósiles, limitado en esta tesis a especies del Pleistoceno Medio y Superior. Los resultados obtenidos de histología ósea en équidos actuales muestran que el tipo de tejido varía a lo largo de la ontogenia, registrando el crecimiento del individuo. Los cambios de tejido óseo también se han relacionado con ciertas características de life history. Así, el cambio de hueso fibrolamellar a lamellar (external fundamental system) en fémures de équidos se ha visto asociado a la madurez reproductiva. Eventos clave del ciclo vital, como el nacimiento, quedan igualmente registrados en el tejido óseo de los équidos. Por primera vez en mamíferos, esta tesis doctoral describe una marca de crecimiento no cíclica en huesos apendiculares, cuya deposición está relacionada con una reducción/parada del crecimiento en los potros durante el nacimiento (línea neonatal). Este descubrimiento es de gran importancia para la reconstrucción histológica de life histories en mamíferos actuales y extintos. El estudio esqueletocronológico en Equus actuales ha revelado, además, que el fémur es el mejor hueso para obtener datos de life history y que las curvas de crecimiento reflejan la madurez esquelética. Por otro lado, el contaje de marcas diarias en el esmalte de équidos actuales ha proporcionado nuevas tasas de secreción que invalidan estudios incorrectos previos. El estudio del esmalte dental realizado en primeros molares inferiores de Equus indica, además, que el desarrollo de este diente consta de tres fases. Cada una de ellas presenta un patrón y una tasa de crecimiento específica, y está relacionada con modificaciones ontogenéticas y estructurales del diente. Asimismo, el análisis histológico muestra que el esmalte se extiende más allá del cérvix, dificultando la toma de medidas de la altura de la corona a partir de la apariencia externa del diente. Los resultados obtenidos indican, también, que el desgaste del primer molar es mucho más pronunciado en etapas tempranas de la ontogenia, y que la corona de este diente tarda en formarse el doble de tiempo en el asno asiático que en las cebras africanas debido, probablemente, a diferencias en hábitat y longevidad entre especies. Además, se ha analizado la histología ósea de las especies del Pleistoceno Medio E. steinheimensis y E. mosbachensis y el esmalte dental de las del Pleistoceno Superior E. ferus y E. hydruntinus, en un primer intento por reconstruir la life history de Equus fósiles. Esto, a su vez, ha permitido analizar los cambios evolutivos de tamaño corporal descritos en Equus durante el Pleistoceno europeo bajo una perspectiva de life history. Los resultados preliminares obtenidos en esta tesis indican que los équidos más grandes del Pleistoceno Medio crecían a tasas más elevadas que las especies del Pleistoceno Superior y actuales, más pequeñas. Este resultado se corresponde con reconstrucciones paleoambientales y con modelos teóricos de life history que proponen la disponibilidad de recursos como una de las presiones de selección más importantes en la determinación del tamaño corporal.The study of life histories provides valuable insights into many aspects of a species’ biology and ecology, including the ecological conditions of its ecosystem, its biodiversity, its demography and its vulnerability to extinction. Life histories of extant and extinct vertebrates can be reconstructed from bone and dental microstructure. However, histological research in key mammalian groups for paleontology and ecology, such as equids, is still little explored. The present PhD thesis aims to analyze bone and dental histology in extant and extinct Equus to obtain information about their most important life history and biological traits. The extant sample of the present dissertation comprises bones and teeth of Asiatic wild ass, plains zebra and Grevy’s zebra. Their detailed histological study has provided a solid framework for the subsequent analysis of fossil Equus species, which has been limited here to Middle and Late Pleistocene taxa. Results obtained from bone histology in living equids show that bone tissue types vary through ontogeny, recording individual growth. This dissertation also indicates that changes in bone tissue types are related to certain life history characteristics. Thus, for instance, results of this thesis reveal that the transition from fibrolamellar to lamellar bone (i.e. external fundamental system) in equid femora is associated with the onset of reproductive maturity. Key life history events, such as the moment of birth, are also registered in the bone tissue of equids. For the first time in mammals, the present dissertation describes a non-cyclical bone growth mark in the limb bones of equids whose timing of deposition agrees with a period of growth arrest/decline during birth in foals (neonatal line). This discovery is of high importance for the histological reconstruction of life histories in extant and extinct mammals. Bone skeletochronology in extant Equus further reveals that the femur is the best bone to obtain life history data in equids, and that bone growth curves yield information about skeletal maturity. On the other hand, the counting of incremental markings of daily periodicity in equid enamel yields new estimates of daily secretion rates for these mammals that invalidate previous inaccurate studies. The detailed study of dental enamel in first lower molars of extant Equus also shows that the development of this tooth involves three different stages. Each of them presents a specific rate and pattern of growth, and is related to ontogenetic and structural modifications of the tooth. The histological analysis performed here further indicates that enamel extends beyond the molar’s cervix in equids, hampering measurements of the crown height from the external appearance of the tooth. Results of this thesis also reveals that the time of first lower molar crown formation in the Asiatic wild ass doubles that of the African zebras, probably due to differences in habitat and longevity among these species. Dental histology further yields information about rates of wear in equids, indicating much higher wear rates for the first lower molar early in ontogeny than commonly thought. In a first attempt to reconstruct the life history of extinct Equus, bone histology was analyzed in the Middle Pleistocene species E. steinheimensis and E. mosbachensis and dental enamel was studied in the Late Pleistocene taxa E. ferus and E. hydruntinus. The preliminary findings obtained from these investigations allowed the first analysis of the body size trend towards dwarfing in European Pleistocene Equus under a life history perspective. First results indicate that larger Middle Pleistocene equids grew at higher rates than smaller Late Pleistocene and extant species. This finding agrees with published paleoenvironmental reconstructions and conforms to life history models that propose resource availability as one of the main selection pressures influencing adult body size

Limb bone histology records birth in mammals.

The annual cyclicality of cortical bone growth marks (BGMs) allows reconstruction of some important life history traits, such as longevity, growth rate or age at maturity. Little attention has been paid, however, to non-cyclical BGMs, though some record key life history events such as hatching (egg-laying vertebrates), metamorphosis (amphibians), or weaning (suggested for Microcebus and the hedgehog). Here, we investigate the relationship between non-cyclical BGMs and a stressful biological event in mammals: the moment of birth. In the present study, we histologically examine ontogenetic series of femora, tibiae and metapodia in several extant representatives of the genus Equus (E. hemionus, E. quagga and E. grevyi). Our analysis reveals the presence of a non-cyclical growth mark that is deposited around the moment of birth, analogous to the neonatal line described for teeth. We therefore refer to it as neonatal line. The presence of this feature within the bone cross-section agrees with a period of growth arrest in newborn foals regulated by the endocrine system. The neonatal line is accompanied by modifications in bone tissue type and vascularization, and has been identified in all bones studied and at different ontogenetic ages. Our discovery of a non-cyclical BGM related to the moment of birth in mammals is an important step towards the histological reconstruction of life histories in extant and fossil equids

Limb bone histology records birth in mammals

Altres ajuts: CERCA Programme/Generalitat de CatalunyaThe annual cyclicality of cortical bone growth marks (BGMs) allows reconstruction of some important life history traits, such as longevity, growth rate or age at maturity. Little attention has been paid, however, to non-cyclical BGMs, though some record key life history events such as hatching (egg-laying vertebrates), metamorphosis (amphibians), or weaning (suggested for Microcebus and the hedgehog). Here, we investigate the relationship between non-cyclical BGMs and a stressful biological event in mammals: the moment of birth. In the present study, we histologically examine ontogenetic series of femora, tibiae and metapodia in several extant representatives of the genus Equus (E. hemionus, E. quagga and E. grevyi). Our analysis reveals the presence of a non-cyclical growth mark that is deposited around the moment of birth, analogous to the neonatal line described for teeth. We therefore refer to it as neonatal line. The presence of this feature within the bone cross-section agrees with a period of growth arrest in newborn foals regulated by the endocrine system. The neonatal line is accompanied by modifications in bone tissue type and vascularization, and has been identified in all bones studied and at different ontogenetic ages. Our discovery of a non-cyclical BGM related to the moment of birth in mammals is an important step towards the histological reconstruction of life histories in extant and fossil equids

The life history of European Middle Pleistocene equids : first insights from bone histology

Evolutionary trends in body size are a central issue of study in Palaeontology. However, and despite body size being one of the most important life history traits of an animal, iconic size-decrease trends such as the one experienced by Equus during the European Pleistocene have never been analysed under a life history framework. Here, we studied the metapodial bone histology of two large Middle Pleistocene species (Equus mosbachensis and Equus steinheimensis) to reconstruct key life history traits that correlate with body size (e.g. size at birth, growth rate), and compare them with that of smaller extant Equus (Equus grevyi, Equus quagga, Equus zebra and Equus hemionus). Our results show that neonatal size of these Middle Pleistocene equids fits predictions from body mass scaling. We estimate a similar age of epiphyseal fusion for the metapodia of E. mosbachensis and E. steinheimensis and that of extant equids. Our findings also reveal that extinct equids grew at higher rates than extant Equus. This result conforms to the predictions of life history theory on environments with different levels of resource availability and provides a new framework of study for body size shifts on European Pleistocene equids

Perimeter of <i>E</i>. <i>hemionus</i>’ perinatal bones and perimeter of the neonatal line (NL) identified in other ontogenetic stages of the same species.

<p>Perimeter of <i>E</i>. <i>hemionus</i>’ perinatal bones and perimeter of the neonatal line (NL) identified in other ontogenetic stages of the same species.</p

Limb bone histology records birth in mammals

<div><p>Abstract</p><p>The annual cyclicality of cortical bone growth marks (BGMs) allows reconstruction of some important life history traits, such as longevity, growth rate or age at maturity. Little attention has been paid, however, to non-cyclical BGMs, though some record key life history events such as hatching (egg-laying vertebrates), metamorphosis (amphibians), or weaning (suggested for <i>Microcebus</i> and the hedgehog). Here, we investigate the relationship between non-cyclical BGMs and a stressful biological event in mammals: the moment of birth. In the present study, we histologically examine ontogenetic series of femora, tibiae and metapodia in several extant representatives of the genus <i>Equus</i> (<i>E</i>. <i>hemionus</i>, <i>E</i>. <i>quagga</i> and <i>E</i>. <i>grevyi</i>). Our analysis reveals the presence of a non-cyclical growth mark that is deposited around the moment of birth, analogous to the neonatal line described for teeth. We therefore refer to it as neonatal line. The presence of this feature within the bone cross-section agrees with a period of growth arrest in newborn foals regulated by the endocrine system. The neonatal line is accompanied by modifications in bone tissue type and vascularization, and has been identified in all bones studied and at different ontogenetic ages. Our discovery of a non-cyclical BGM related to the moment of birth in mammals is an important step towards the histological reconstruction of life histories in extant and fossil equids.</p></div