Long-living Mammals Research Articles

Inferring longevity from advanced rib remodelling in insular dwarf deer

AbstractDwarfed insular mammals are of significant interest to evolutionary biology because of their morphological and physiological adaptations triggered by variables inherent to geographical isolation. One life history trait that is expected to be modified in relation to body size reduction is extended longevity facilitated by ecological parameters such as predator and competitor release and fluctuating resource availability. However, systematic examination of longevity in extreme cases of dwarfism is difficult as such cases are largely represented by fossils of extinct species. We studied seven rib fragments of the extraordinary endemic Pleistocene dwarf deer Candiacervus (size 2) to test whether its bone matrix shows evidence for extensive bone remodelling typically seen in large and long-living mammals. We found that all ribs had well-remodelled Haversian bone, implying several generations of resorption and re-deposition processes. Osteon density was high relative to small bone cross-section size, with examples of porosity similar to that seen in elderly animals. We report the first combined micro-morphological and micro-morphometric record of Candiacervus rib histology, agreeing with previous literature discussing the evolutionary biology of dwarf ruminants. Further experimental validation of osteon density in extant deer will confirm whether dwarfed Candiacervus indeed lived longer than expected for its body mass.

Brain Plasticity in Mammals: An Example for the Role of Comparative Medicine in the Neurosciences.

Comparative medicine deals with similarities and differences between veterinary and human medicine. All mammals share most basic cellular and molecular mechanisms, thus justifying murine animal models in a translational perspective; yet “mice are not men,” thus some biases can emerge when complex biological processes are concerned. Brain plasticity is a cutting-edge, expanding topic in the field of Neurosciences with important translational implications, yet, with remarkable differences among mammals, as emerging from comparative studies. In particular, adult neurogenesis (the genesis of new neurons from brain stem cell niches) is a life-long process in laboratory rodents but a vestigial, mostly postnatal remnant in humans and dolphins. Another form of “whole cell” plasticity consisting of a population of “immature” neurons which are generated prenatally but continue to express markers of immaturity during adulthood has gained interest more recently, as a reservoir of young neurons in the adult brain. The distribution of the immature neurons also seems quite heterogeneous among different animal species, being confined within the paleocortex in rodents while extending into neocortex in other mammals. A recent study carried out in sheep, definitely showed that gyrencephalic, large-sized brains do host higher amounts of immature neurons, also involving subcortical, white, and gray matter regions. Hence, “whole cell” plasticity such as adult neurogenesis and immature neurons are biological processes which, as a whole, cannot be studied exclusively in laboratory rodents, but require investigation in comparative medicine, involving large-sized, long-living mammals, in order to gain insights for translational purposes.

Clusters of DCX+ cells "trapped" in the subcortical white matter of early postnatal Cetartiodactyla (Tursiops truncatus, Stenella coeruloalba and Ovis aries).

The cytoskeletal protein doublecortin (DCX) is a marker for neuronal cells retaining high potential for structural plasticity, originating from both embryonic and adult neurogenic processes. Some of these cells have been described in the subcortical white matter of neonatal and postnatal mammals. In mice and humans it has been shown they are young neurons migrating through the white matter after birth, reaching the cortex in a sort of protracted neurogenesis. Here we show that DCX+ cells in the white matter of neonatal and young Cetartiodactyla (dolphin and sheep) form large clusters which are not newly generated (in sheep, and likely neither in dolphins) and do not reach the cortical layers, rather appearing "trapped" in the white matter tissue. No direct contact or continuity can be observed between the subventricular zone region and the DCX+ clusters, thus indicating their independence from any neurogenic source (in dolphins further confirmed by the recent demonstration that periventricular neurogenesis is inactive since birth). Cetartiodactyla include two orders of large-brained, relatively long-living mammals (cetaceans and artiodactyls) which were recognized as two separate monophyletic clades until recently, yet, despite the evident morphological distinctions, they are monophyletic in origin. The brain of Cetartiodactyla is characterized by an advanced stage of development at birth, a feature that might explain the occurrence of "static" cell clusters confined within their white matter. These results further confirm the existence of high heterogeneity in the occurrence, distribution and types of structural plasticity among mammals, supporting the emerging view that multiple populations of DCX+, non-newly generated cells can be abundant in large-brained, long-living species.

First Radiological Study of a Complete Dental Ontogeny Sequence of an Extinct Equid: Implications for Equidae Life History and Taphonomy

The sequence of cheek teeth mineralization, eruption, and replacement of an extinct horse species is here documented with radiological techniques for the first time thanks to the exceptional preservation of Hipparion sp. mandibles from Cerro de los Batallones (Madrid Basin, Spain). The sequence of dental ontogeny in mammals provides valuable insights about life history traits, such as the pace of growth, and about the mode of formation of fossiliferous assemblages. We have determined that the order of permanent cheek teeth mineralization and eruption of hipparionine horses is m1, m2, (p2, p3), p4, m3. Cheek teeth mineralization timing of hipparionine horses coincides with the one observed in modern equids. In turn, there are differences in the eruption timing of the p4 and m3 between horses belonging to the Anchitheriinae and Hipparionini compared to equids of the Equus genus that might be related to the shorter durability of the deciduous tooth dp4 in anchitheriine and hipparionine horses and, more broadly, to an increased durability of equid teeth through their evolutionary history. Based on the dental eruption sequence, hipparionine horses are slow-growing, long-living mammals. The Hipparion sp. assemblage from Batallones-10 conforms to an attritional model, as individuals more vulnerable to natural mortality predominate.

Do large brains of long-living mammals prefer non-newly generated, immature neurons?

Do large brains of long-living mammals prefer non-newly generated, immature neurons?

Non-Newly Generated, "Immature" Neurons in the Sheep Brain Are Not Restricted to Cerebral Cortex.

A newly proposed form of brain structural plasticity consists of non-newly generated, "immature" neurons of the adult cerebral cortex. Similar to newly generated neurons, these cells express the cytoskeletal protein Doublecortin (DCX), yet they are generated prenatally and then remain in a state of immaturity for long periods. In rodents, the immature neurons are restricted to the paleocortex, whereas in other mammals, they are also found in neocortex. Here, we analyzed the DCX-expressing cells in the whole sheep brain of both sexes to search for an indicator of structural plasticity at a cellular level in a relatively large-brained, long-living mammal. Brains from adult and newborn sheep (injected with BrdU and analyzed at different survival times) were processed for DCX, cell proliferation markers (Ki-67, BrdU), pallial/subpallial developmental origin (Tbr1, Sp8), and neuronal/glial antigens for phenotype characterization. We found immature-like neurons in the whole sheep cortex and in large populations of DCX-expressing cells within the external capsule and the surrounding gray matter (claustrum and amygdala). BrdU and Ki-67 detection at neonatal and adult ages showed that all of these DCX+ cells were generated during embryogenesis, not after birth. These results show that the adult sheep, unlike rodents, is largely endowed with non-newly generated neurons retaining immature features, suggesting that such plasticity might be particularly important in large-brained, long-living mammals.SIGNIFICANCE STATEMENT Brain plasticity is important in adaptation and brain repair. Structural changes span from synaptic plasticity to adult neurogenesis, the latter being highly reduced in large-brained, long-living mammals (e.g., humans). The cerebral cortex contains "immature" neurons, which are generated prenatally and then remain in an undifferentiated state for long periods, being detectable with markers of immaturity. We studied the distribution and developmental origin of these cells in the whole brain of sheep, relatively large-brained, long-living mammals. In addition to the expected cortical location, we also found populations of non-newly generated neurons in several subcortical regions (external capsule, claustrum, and amygdala). These results suggests that non-neurogenic, parenchymal structural plasticity might be more important in large mammals with respect to adult neurogenesis.

Dental Eruption Series and Replacement Pattern in Miocene Prosantorhinus (Rhinocerotidae) as Revealed by Macroscopy and X-ray: Implications for Ontogeny and Mortality Profile

Fossil evidence of complete sequences of dental ontogeny in extinct mammals is rare but contains valuable information on the animal’s physiology, life history, and individual age. Here, we analyzed an exceptionally high number of juvenile dentaries at different developmental stages including highly fragile tooth germs of the extinct rhinoceros Prosantorhinus germanicus from the Miocene fossil lagerstatte Sandelzhausen in Germany. We used dental wear stages, eruption stages, and tooth germ development in order to reconstruct the tooth replacement pattern for P. germanicus. The results allow for the distinction of 11 dental eruption stages and document a tooth eruption sequence of (d2, d3), (d1, d4), m1, m2, p2, p3, p4, m3; a pattern identical to that reported for the extant African rhinoceros, Diceros bicornis. Moreover, our findings indicate that P. germanicus falls into the life history category of slow-growing, long-living mammals. The dental eruption stages of the fossil rhinoceros were correlated with data of living rhinoceroses in order to gain insight into the age-at-death distribution of P. germanicus at Sandelzhausen. The juvenile mortality profile of P. germanicus shows a trend of selective mortality at an inferred age range of about 3 months to 3 years. As this age range represents a life phase of increased natural risk of mortality, our findings indicate a gradual accumulation of corpses (attritional fossil assemblage). This result supports the interpretation of a taphocenosis found at the Sandelzhausen fossil site.

The Putative Son's Attractiveness Alters the Perceived Attractiveness of the Putative Father.

A body of literature has investigated female mate choice in the pre-mating context (pre-mating sexual selection). Humans, however, are long-living mammals forming pair-bonds which sequentially produce offspring. Post-mating evaluations of a partner's attractiveness may thus significantly influence the reproductive success of men and women. I tested herein the theory that the attractiveness of putative sons provides extra information about the genetic quality of fathers, thereby influencing fathers' attractiveness across three studies. As predicted, facially attractive boys were more frequently attributed to attractive putative fathers and vice versa (Study 1). Furthermore, priming with an attractive putative son increased the attractiveness of the putative father with the reverse being true for unattractive putative sons. When putative fathers were presented as stepfathers, the effect of the boy's attractiveness on the stepfather's attractiveness was lower and less consistent (Study 2). This suggests that the presence of an attractive boy has the strongest effect on the perceived attractiveness of putative fathers rather than on non-fathers. The generalized effect of priming with beautiful non-human objects also exists, but its effect is much weaker compared with the effects of putative biological sons (Study 3). Overall, this study highlighted the importance of post-mating sexual selection in humans and suggests that the heritable attractive traits of men are also evaluated by females after mating and/or may be used by females in mate poaching.

Comparison of Metal Concentrations in Bones of Long-Living Mammals

The aim of this study was to compare zinc, copper, lead, cadmium, and mercury concentrations in the bones of long-living mammals—humans (Homo sapiens) and Canidae (dogs Canis familiaris and foxes Vulpes vulpes) from northwestern Poland and to determine the usefulness of Canidae as bioindicators of environmental exposure to metals in humans. Zinc concentrations in cartilage with adjacent compact bone and in spongy bone were highest in foxes (∼120 mg/kg dry weight (dw)) and lowest in dogs (80 mg/kg dw). Copper concentrations in cartilage with adjacent compact bone were greatest in foxes (1.17 mg/kg dw) and smallest in humans (∼0.8 mg/kg dw), while in spongy bone they were greatest in dogs (0.76 mg/kg dw) and lowest in foxes (0.45 mg/kg dw). Lead concentrations in both analyzed materials were highest in dogs (>3 mg/kg dw) and lowest in humans (>0.6 mg/kg dw). Cadmium concentration, also in both the analyzed materials, were highest in foxes (>0.15 mg/kg dw) and lowest in humans (>0.04 mg/kg dw). Mercury concentration in bones was low and did not exceed 0.004 mg/kg dw in all the examined species. The concentrations of essential metals in the bones of the examined long-living mammals were similar. The different concentrations of toxic metals were due to environmental factors. As bone tissues are used in the assessment of the long-term effects of environmental exposure to heavy metals on the human body, ecotoxicological studies on the bones of domesticated and wild long-living mammals, including Canidae, may constitute a significant supplement to this research.

The possible role of membrane lipids in the exceptionally long life of the short-beaked echidna,Tachyglossus aculeatus.

The short-beaked echidna (Tachyglossus aculeatus) is an exceptionally long-living mammal having a maximal lifespan of -50 years. This is about four times that predicted from its body mass and, consequently, its longevity quotient is ∼4.This longevity quotient is similar to two other exceptionally long-living mammalian species; the naked mole-rat (Heterocephalus glaber) and Homo sapiens. In recent times, the types of fats that make up cellular membrane have been implicated in the determination of a species' maximum lifespan. This modification of the oxidative stress theory of aging, which has been called the membrane pacemaker theory of aging, derives from the fact that polyunsaturated fats are very susceptible to lipid peroxidation whereas monounsaturated fats are resistant to peroxidation. As a test of the theory we measured the fatty acid composition of membrane lipids isolated from tissues of echidnas.We found that, as In the other long-living mammals, echidna membranes are more monounsaturated and less polyunsaturated than would be predicted from their body size and that the peroxidation Index of their membrane lipids is what their maximum longevity would predict.

The exceptional longevity of an egg-laying mammal, the short-beaked echidna ( Tachyglossus aculeatus) is associated with peroxidation-resistant membrane composition

The echidna Tachyglossus aculeatus is a monotreme mammal from Australia that is exceptionally long-living. Its documented maximum lifespan of 50 years is 3.7 times that predicted from its body mass. Other exceptionally long-living mammals (naked mole-rats and humans) are known to have peroxidation-resistant membrane composition, raising the question about echidnas. Phospholipids were extracted from skeletal muscle, liver and liver mitochondria of echidnas and fatty acid composition measured. As with other exceptionally long-living mammals, membrane lipids of echidna tissues were found to have a lower content of polyunsaturates and a higher content of monounsaturates than predicted for their body size. The peroxidation index (=peroxidation susceptibility) calculated from this membrane composition was lower-than-expected for their body size, indicating that the cellular membranes of echidnas would be peroxidation-resistant. Additionally when the calculated peroxidation index was plotted against maximum lifespan, the echidna values conformed to the relationship for mammals in general. These findings support the membrane pacemaker theory of aging and emphasise the potential importance of membrane fatty acid composition in aging and in the determination of maximum longevity.