Primate study may yield new CJD clues...as researchers fume over blocked research.
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Physiology: hibernation in a tropical primate.
The Madagascan fat-tailed dwarf lemur, Cheirogaleus medius, hibernates in tree holes for seven months of the year, even though winter temperatures rise to over 30 degrees C. Here we show that this tropical primate relies on a flexible thermal response that depends on the properties of its tree hole: if the hole is poorly insulated, body temperature fluctuates widely, passively following the ambient temperature; if well insulated, body temperature stays fairly constant and the animal undergoes regular spells of arousal. Our findings indicate that arousals are determined by maximum body temperatures and that hypometabolism in hibernating animals is not necessarily coupled to a low body temperature.
Animals↗
The existence of the vomeronasal organ in postnatal chimpanzees and evidence for its homology with that of humans.
It is currently thought that New World monkeys, prosimians, and humans are the only primates to possess vomeronasal organs (VNOs) as adults. Recent studies of the human VNO suggest that previous investigations on Old World primates may have missed the VNO. We examined nasal septa from the chimpanzee (Pan troglodytes) grossly and histologically for comparison with nasal septa from humans, Old World monkeys (Macaca fascicularis, M. nemistrina) and prosimian primates (Microcebus murinus, Otolemur garnettii). Grossly, chimpanzees had depressions on the nasal septum similar to fossae reported anterior to the VNO openings in humans. Histologically, chimpanzees and humans had bilateral epithelial tubes which were above the superior margin of the paraseptal cartilages (vomeronasal cartilage homologue). The epithelial tubes had a homogeneous ciliated epithelium. These structures were thus positionally and structurally identical to the human VNO and unlike the well-developed prosimian VNOs which were surrounded by vomeronasal cartilage. Macaques had no structures which resembled the VNO of either the prosimians or humans. The results demonstrate that the VNO is present postnatally in the chimpanzee and is almost identical to the human VNO in its anatomical position and histological structure. This in turn suggests that the reported absence of the VNO in at least some adult Old World primates is artifactual, and that further study may provide evidence for its existence in other species.
Adult↗
Observations on the vomeronasal organ of prenatal Tarsius bancanus borneanus with implications for ancestral morphology.
Adult primates have at least five known phenotypes of vomeronasal organ (VNO), ranging from the typical morphology seen in most other mammals to complete absence. With such morphological disparity, the phylogenetic value and any inferences on ancestral VNO morphology of the primate VNO are left uncertain. The present study investigated the VNO of embryonic and fetal Tarsius bancanus borneanus (n = 4) in comparison with prenatal specimens from four other species of primates in an effort to clarify adult morphological variations. In all except one of the fetal primates, the VNO communicated to the nasopalatine duct. One exception occurred in the largest fetal Tarsius (25 mm crown-rump length), in which the VNO communicated with the nasal cavity alone. The vomeronasal neuroepithelium was well differentiated from a thinner, non-sensory epithelium in all Tarsius and New World monkeys studied, as well as late embryonic and fetal Microcebus myoxinus. In anterior sections, this neuroepithelium was found in a more superior location in Tarsius and New World monkeys compared with Microcebus myoxinus. In all primates, masses of cell bodies were found superior to the VNO, intermingled with nerve fibres. These morphologically resembled luteinizing hormone-releasing hormone neurons described in other mammals, including humans, suggesting that a primitive association of these neurons with the VNO may exist in all primate taxa. The present study revealed that prenatal similarities exist in Tarsius and New World primates in VNO epithelial morphology. However, these are transient stages of morphology. If tarsiers and anthropoids do represent a clade (Haplorhini), then the atypical morphology seen in adult tarsiers and New World monkeys probably represents the adult VNO morphology of a haplorhine common ancestor.
Anatomy, Comparative↗
Brain and buffy coat transmission of bovine spongiform encephalopathy to the primate Microcebus murinus.
BACKGROUND: More than 100 cases of variant CJD resulting from infections with bovine spongiform encephalopathy (BSE) have accumulated in the United Kingdom since 1995. Concern about the possibility of secondary transmissions via blood and blood components donated by infected individuals has prompted a variety of international donor deferral policies that will continue until laboratory and epidemiologic evidence provides a consensus about potential risk. STUDY DESIGN AND METHODS: BSE was passaged through macaque monkeys and then adapted to the prosimian microcebe (Microcebus murinus). Brain homogenate and buffy coat from an affected microcebe were separately inoculated intracerebrally into three healthy microcebes (two animals received brain and one received buffy coat). RESULTS: All three inoculated microcebes became ill after incubation periods of 16 to 18 months. Clinical, histopathologic, and immunocytologic features were similar in each of the recipients. CONCLUSION: Buffy coat from a symptomatic microcebe infected 17 months earlier with BSE contained the infectious agent. This observation represents the first documented transmission of BSE from the blood of an experimentally infected primate, which in view of rodent buffy coat infectivity precedents and the known host range of BSE is neither unexpected nor cause for alarm.
Animals↗
Survival without recovery after mass extinctions.
Because many survivors of mass extinctions do not participate in postrecovery diversifications, and therefore fall into a pattern that can be termed "Dead Clade Walking" (DCW), the effects of mass extinctions extend beyond the losses observed during the event itself. Analyses at two taxonomic levels provide a first-order test of the prevalence of DCWs by using simple and very conservative operational criteria. For four of the Big Five mass extinctions of the Phanerozoic, the marine genera that survived the extinction suffered approximately 10-20% attrition in the immediately following geologic stage that was significantly greater than the losses sustained in preextinction stages. The stages immediately following the three Paleozoic mass extinctions also account for 17% of all order-level losses in marine invertebrates over that interval, which is, again, significantly greater than that seen for the other stratigraphic stages (no orders are lost immediately after the end-Triassic or end-Cretaceous mass extinctions). DCWs are not evenly distributed among four regional molluscan time-series following the end-Cretaceous extinction, demonstrating the importance of spatial patterns in recovery dynamics. Although biotic interactions have been invoked to explain the differential postextinction success of clades, such hypotheses must be tested against alternatives that include stochastic processes in low-diversity lineages-which is evidently not a general explanation for the ordinal DCW patterns, because postextinction fates are not related to the size of extinction bottlenecks in Paleozoic orders-and ongoing physical environmental changes.
Animals↗
Ancient single origin for Malagasy primates.
We report new evidence that bears decisively on a long-standing controversy in primate systematics. DNA sequence data for the complete cytochrome b gene, combined with an expanded morphological data set, confirm the results of a previous study and again indicate that all extant Malagasy lemurs originated from a single common ancestor. These results, as well as those from other genetic studies, call for a revision of primate classifications in which the dwarf and mouse lemurs are placed within the Afro-Asian lorisiforms. The phylogenetic results, in agreement with paleocontinental data, indicate an African origin for the common ancestor of lemurs and lorises (the Strepsirrhini). The molecular data further suggest the surprising conclusion that lemurs began evolving independently by the early Eocene at the latest. This indicates that the Malagasy primate lineage is more ancient than generally thought and places the split between the two strepsirrhine lineages well before the appearance of known Eocene fossil primates. We conclude that primate origins were marked by rapid speciation and diversification sometime before the late Paleocene.
Animals↗
Age-related effects on the biological clock and its behavioral output in a primate.
In humans, activity rhythms become fragmented and attenuated in the elderly. This suggests an alteration of the circadian system per se that could in turn affect the expression of biological rhythms. In primates, very few studies have analyzed the effect of aging on the circadian system. The mouse lemur provides a unique model of aging in non-human primates. To assess the effect of aging on the circadian system of this primate, we recorded the circadian and daily rhythms of locomotor activity of mouse lemurs of various ages. We also examined age-related changes in the daily rhythm of immunoreactivities for vasoactive intestinal polypeptide (VIP) and arginine-vasopressin (AVP) in suprachiasmatic nucleus neurons (SCN), two major peptides of the biological clock. Compared to adult animals, aged mouse lemurs showed a significant increase in daytime activity and an advanced activity onset. Moreover, when maintained in constant dim red light, aged animals exhibited a shortening of the free-running period compared to adult animals. In adults, AVP immunoreactivity (ir) peaked during the second part of the day, and VIP ir peaked during the night. In aged mouse lemurs, the peaks of AVP ir and VIP ir were significantly shifted with no change in amplitude. AVP ir was most intense at the beginning of the night; whereas, VIP ir peaked at the beginning of the daytime. A weakened oscillator could account for the rhythmic disorders often observed in the elderly. Changes in the daily rhythms of AVP ir and VIP ir may affect the ability of the SCN to transmit rhythmic information to other neural target sites, and thereby modify the expression of some biological rhythms.
Aging↗
Comparison of likelihood and Bayesian methods for estimating divergence times using multiple gene Loci and calibration points, with application to a radiation of cute-looking mouse lemur species.
Divergence time and substitution rate are seriously confounded in phylogenetic analysis, making it difficult to estimate divergence times when the molecular clock (rate constancy among lineages) is violated. This problem can be alleviated to some extent by analyzing multiple gene loci simultaneously and by using multiple calibration points. While different genes may have different patterns of evolutionary rate change, they share the same divergence times. Indeed, the fact that each gene may violate the molecular clock differently leads to the advantage of simultaneous analysis of multiple loci. Multiple calibration points provide the means for characterizing the local evolutionary rates on the phylogeny. In this paper, we extend previous likelihood models of local molecular clock for estimating species divergence times to accommodate multiple calibration points and multiple genes. Heterogeneity among different genes in evolutionary rate and in substitution process is accounted for by the models. We apply the likelihood models to analyze two mitochondrial protein-coding genes, cytochrome oxidase II and cytochrome b, to estimate divergence times of Malagasy mouse lemurs and related outgroups. The likelihood method is compared with the Bayes method of Thorne et al. (1998, Mol. Biol. Evol. 15:1647-1657), which uses a probabilistic model to describe the change in evolutionary rate over time and uses the Markov chain Monte Carlo procedure to derive the posterior distribution of rates and times. Our likelihood implementation has the drawbacks of failing to accommodate uncertainties in fossil calibrations and of requiring the researcher to classify branches on the tree into different rate groups. Both problems are avoided in the Bayes method. Despite the differences in the two methods, however, data partitions and model assumptions had the greatest impact on date estimation. The three codon positions have very different substitution rates and evolutionary dynamics, and assumptions in the substitution model affect date estimation in both likelihood and Bayes analyses. The results demonstrate that the separate analysis is unreliable, with dates variable among codon positions and between methods, and that the combined analysis is much more reliable. When the three codon positions were analyzed simultaneously under the most realistic models using all available calibration information, the two methods produced similar results. The divergence of the mouse lemurs is dated to be around 7-10 million years ago, indicating a surprisingly early species radiation for such a morphologically uniform group of primates.
Animals↗
Relationship between urinary estrogen levels before conception and sex ratio at birth in a primate, the gray mouse lemur.
BACKGROUND: In primates, including humans, bias of sex ratio at birth has been reported to depend on maternal condition at conception. In a Malagasy primate, the gray mouse lemur, male-biased sex ratio at birth occurred in captive parous females. The male bias was previously demonstrated to be pre-conceptual and independent of the female's nutritional state. It was hypothesized to be related to changes in hormonal state at ovulation. METHODS AND RESULTS: The relationship between urinary estradiol (E2) levels during the follicular phase until estrus and litter production (number and sex of newborns) was assessed in 91 females mated under controlled conditions. Changes in E2 levels prior to ovulation followed the typical primate pattern characterized by a gradual rise during the 10 days preceding the sharp increase at estrus. A clear decline in E2 levels occurred with ageing. Direction of the sex ratio bias was unrelated to E2 levels at ovulation time but was significantly dependent on E2 levels during the follicular phase. Reduced E2 levels prior to estrus led to male-biased litters. CONCLUSION: This study suggests that hormonal stimulation during the follicular phase plays a role in shifting sex ratio at conception through changes in the local environment of the ova. This hypothesis deserves testing by assessing estrogen levels throughout the follicular phase in other primate species including humans.
Age Factors↗
Relationship between urinary estrogen levels before conception and sex ratio at birth in a primate, the gray mouse lemur.
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Animals↗
Removal of the olfactory bulbs modifies the gonadal responses to photoperiod in the lesser mouse lemur (Microcebus murinus).
The sexual activity of the lesser mouse lemur, unlike that of most living primates, is clearly dependent on photoperiod. Males responded to long daylengths (> 12 h light/day) by rapid testicular development and an increase in testosterone levels reaching 65.8 +/- 1.5 ng/ml (n = 12) after 3 wk of inductive photoperiod. Levels were maintained unchanged until 14 wk of exposure to long photoperiod, when spontaneous gonadal regression was observed. Under short daylengths, intact males exhibited regressed gonadal function with low plasma concentrations of testosterone: 5.4 +/- 1 ng/ml. To investigate the effect of olfactory bulb deprivation on gonadal responses to photoperiod, 12 males were bulbectomized (BX) during exposure to either long (n = 8, BX1) or short (n = 4, BX2) daylengths. In both groups of BX males, responses to long or short daylengths were maintained. However, the timing and the amplitude of gonadal responses to photoperiod were modified; BX males underwent a significant delay in testis development and also had reduced testosterone levels (53.3 +/- 2.3 ng/ml and 37.3 +/- 0.9 ng/ml for BX1 and BX2 groups, respectively). Moreover, BX males did not exhibit spontaneous gonadal regression after 14 wk of exposure to long daylengths, indicating that the photorefractory state did not appear, at least under our experimental conditions. In this primate, olfactory bulbs exert an important effect on the neuroendocrinological control of reproductive responsiveness to photoperiod.
Animals↗
Age effects on pheromone induced Fos expression in olfactory bulbs of a primate.
In the gray mouse lemur, a prosimian primate, aging is associated with a reduction of olfactory behaviors and sexual stimulation. To assess the effect of aging on the central response to pheromone stimulation in this primate, we measured the c-fos expression in the main and accessory olfactory bulbs of adult and aged male mouse lemurs, following exposure to the volatile phase of urine from proestrous females. In adults, pheromone exposure increased the number of Fos-positive neurons in the main olfactory bulb without changes in the accessory olfactory bulb. Fos expression was not increased by the odorant stimulation in aged mouse lemurs. Our results may explain the age-related decrease in behaviors associated with olfactory stimulation in this primate.
Aging↗
The hidden matrilineal structure of a solitary lemur: implications for primate social evolution.
Kin selection affects many aspects of social behaviour, especially in gregarious animals in which relatives are permanently associated. In most group-living primates with complex social behaviour, females are philopatric and organized into matrilines. Models of primate social evolution assume that females in solitary primates are also organized into matrilines. We examined the genetic structure and the mating system of a population of Coquerel's dwarf lemur (Mirza coquereli), a solitary primate from Madagascar, to test this assumption. Our genetic and behavioural analyses revealed that this population of solitary individuals is indeed structured into matrilines, even though this pattern was not predicted by behavioural data. Specifically, females sharing a mitochondrial DNA haplotype were significantly clustered in space and the average genetic and geographical distances among them were negatively correlated. Not all females were philopatric, but there is no evidence for the successful settlement of dispersing females. Although not all adult males dispersed from their natal range, they were not significantly clustered in space and all of them roamed widely in search of oestrous females. As a result, paternity was widely spread among males and mixed paternities existed, indicating that scramble competition polygyny is the mating system of this species. Our data therefore revealed facultative dispersal in both sexes with a strong bias towards female philopatry in this primitive primate. We further conclude that complex kinship structures also exist in non-gregarious species, where their consequences for social behaviour are not obvious.
Animals↗
The role of survival for the evolution of female philopatry in a solitary forager, the grey mouse lemur (Microcebus murinus).
It is widely accepted that natal philopatry is a prerequisite for the evolution of sociality. The life-history hypothesis maintains that longevity of adults results in extended territory tenure and thus limits breeding vacancies for offspring, which makes natal philopatry more likely. Here, we tested the importance of longevity for natal philopatry in females of a basal primate, the grey mouse lemur (Microcebus murinus). This species is regarded as being solitary due to its foraging habits but while males disperse, female offspring in this species forgo dispersal and form long-term sleeping groups with their mothers. We tested whether high adult survival could be a cause for natal philopatry of female offspring. In addition, we assessed costs and benefits associated with space sharing between mothers and daughters and whether mothers actively increase survival of daughters by beqeauthal of territories, information transfer about resources or thermoregulation. Contrary to our predictions, adult females had low-survival rates. Space sharing appeared to improve survival of both, mothers and daughters. This could be a result of information transfer about sleeping sites and thermoregulatory benefits. Our results cast doubt on the idea that longevity predisposes species for social traits and provide support for benefits of philopatry.
Animals↗
Microsatellite analyses reveal fine-scale genetic structure in grey mouse lemurs (Microcebus murinus).
Information on genetic structure can be used to complement direct inferences on social systems and behaviour. We studied the genetic structure of the solitary grey mouse lemur (Microcebus murinus), a small, nocturnal primate endemic to western Madagascar, with the aim of getting further insight on its breeding structure. Tissue samples from 167 grey mouse lemurs in an area covering 12.3 km2 in Kirindy Forest were obtained from trapping. The capture data indicated a noncontinuous distribution of individuals in the study area. Using 10 microsatellite markers, significant genetic differentiation in the study area was demonstrated and dispersal was found to be significantly male biased. Furthermore, we observed an overall excess of homozygotes in the total population (F(IT) = 0.131), which we interpret as caused by fine-scale structure with breeding occurring in small units. Evidence for a clumped distribution of identical homozygotes was found, supporting the notion that dispersal distance for breeding was shorter than that for foraging, i.e. the breeding neighbourhood size is smaller than the foraging neighbourhood size. In conclusion, we found a more complex population structure than what has been previously reported in studies performed on smaller spatial scales. The noncontinuous distribution of individuals and the effects of social variables on the genetic structure have implications for the interpretation of social organization and the planning of conservation activities that may apply to other solitary and endangered mammals as well.
Animals↗
Arginine-vasopressin and vasointestinal polypeptide rhythms in the suprachiasmatic nucleus of the mouse lemur reveal aging-related alterations of circadian pacemaker neurons in a non-human primate.
The suprachiasmatic nucleus (SCN) of the hypothalamus, the mammalian circadian pacemaker, is entrained by external cues and especially by photic information. Light is transmitted primarily via the retinohypothalamic tract, which terminates in the ventral part (or core) of the SCN, where vasoactive intestinal polypeptide (VIP)-containing neurons are located. VIP cells are mainly intrinsic and project to the dorsal part (or shell) of the SCN, where neurons containing arginine-vasopressin (AVP) reside. As aging leads to marked changes in the expression of circadian rhythms, we examined in primates whether age-related decay in biological rhythmicity is associated with changes in the oscillation of peptide expression in SCN neurons. We used double immunohistochemistry and quantitative analysis in the SCN of mouse lemurs, which provide a unique model of aging in non-human primates. In adult animals, VIP-positive and AVP-positive SCN neurons exhibited daily rhythms of their number and immunostaining intensity: AVP immunoreactivity peaked during the second part of the day, and VIP peaked during the night. In aged mouse lemurs, the peaks of AVP and VIP immunopositivity were significantly shifted, so that AVP was most intense at the beginning of the night, whereas VIP peaked at the beginning of daytime. The results show that the circadian rhythm of neuropeptides in the SCN is modified by aging in primates, with a differential regulation of the two main peptidergic cell populations. These changes may affect the ability of the SCN to transmit rhythmic information to other neural target sites, and thereby to modify the expression of some biological rhythms.
Aging↗
Microcebus murinus: a useful primate model for human cerebral aging and Alzheimer's disease?
Age-associated dementia, in particular Alzheimer's disease (AD), will be a major concern of the 21st century. Research into normal brain aging and AD will therefore become increasingly important. As for other areas of medicine, the availability of good animal models will be a limiting factor for progress. Given the complexity of the human brain, the identification of appropriate primate models will be essential to further knowledge of the disease. In this review, we describe the features of brain aging and age-associated neurodegeneration in a small lemurian primate, the Microcebus murinus, also referred to as the mouse lemur. The mouse lemur has a relatively short life expectancy, and animals over 5 years of age are considered to be elderly. Among elderly mouse lemurs, the majority show normal brain aging, whereas approximately 20% develop neurodegeneration. This Microcebus age-associated neurodegeneration is characterized by a massive brain atrophy, abundant amyloid plaques, a cytoskeletal Tau pathology and a loss of cholinergic neurons. While elderly mouse lemurs with normal brain aging maintain memory function and social interaction, animals with age-associated neurodegeneration lose their cognitive and social capacities and demonstrate certain similarities with age-associated human AD. We conclude that M. murinus is an interesting primate model for the study of normal brain aging and the biochemical dysfunctions occurring in age-associated neurodegeneration. Mouse lemurs might also become an increasingly important model for the development of novel treatments in this domain.
Aging↗