Hibernation slows epigenetic ageing in yellow-bellied marmots.

Species that hibernate generally live longer than would be expected based solely on their body size. Hibernation is characterized by long periods of metabolic suppression (torpor) interspersed by short periods of increased metabolism (arousal). The torpor-arousal cycles occur multiple times during hibernation, and it has been suggested that processes controlling the transition between torpor and arousal states cause ageing suppression. Metabolic rate is also a known correlate of longevity; we thus proposed the 'hibernation-ageing hypothesis' whereby ageing is suspended during hibernation. We tested this hypothesis in a well-studied population of yellow-bellied marmots (Marmota flaviventer), which spend 7-8 months per year hibernating. We used two approaches to estimate epigenetic age: the epigenetic clock and the epigenetic pacemaker. Variation in epigenetic age of 149 samples collected throughout the life of 73 females was modelled using generalized additive mixed models (GAMM), where season (cyclic cubic spline) and chronological age (cubic spline) were fixed effects. As expected, the GAMM using epigenetic ages calculated from the epigenetic pacemaker was better able to detect nonlinear patterns in epigenetic ageing over time. We observed a logarithmic curve of epigenetic age with time, where the epigenetic age increased at a higher rate until females reached sexual maturity (two years old). With respect to circannual patterns, the epigenetic age increased during the active season and essentially stalled during the hibernation period. Taken together, our results are consistent with the hibernation-ageing hypothesis and may explain the enhanced longevity in hibernators.

Epigenetic models developed for plains zebras predict age in domestic horses and endangered equids.

Effective conservation and management of threatened wildlife populations require an accurate assessment of age structure to estimate demographic trends and population viability. Epigenetic aging models are promising developments because they estimate individual age with high accuracy, accurately predict age in related species, and do not require invasive sampling or intensive long-term studies. Using blood and biopsy samples from known age plains zebras (Equus quagga), we model epigenetic aging using two approaches: the epigenetic clock (EC) and the epigenetic pacemaker (EPM). The plains zebra EC has the potential for broad application within the genus Equus given that five of the seven extant wild species of the genus are threatened. We test the EC's ability to predict age in sister taxa, including two endangered species and the more distantly related domestic horse, demonstrating high accuracy in all cases. By comparing chronological and estimated age in plains zebras, we investigate age acceleration as a proxy of health status. An interaction between chronological age and inbreeding is associated with age acceleration estimated by the EPM, suggesting a cumulative effect of inbreeding on biological aging throughout life.

Correlates of maternal glucocorticoid levels in a socially flexible rodent.

While it is generally accepted that social isolation has detrimental effects on social species, little is known about the importance of social interactions in less social species-particularly for wild reproductive females. We studied socially-flexible yellow-bellied marmots (Marmota flaviventer) and asked whether features of the social environment are associated with maternal fecal glucocorticoid metabolite (FGM) concentrations. Since changes in maternal baseline glucocorticoids may have positive or negative consequences for offspring fitness, we were also interested in estimating their relationship with measures of reproductive success. We fitted generalized linear mixed effects models to a dataset including maternal FGM measurements, social network metrics, maternal/alloparental care, and pup FGM and survival. Agonistic interactions were positively associated with maternal FGM levels, while mothers that engaged in relatively more affiliative interactions had reduced FGM levels when living in environments with low predator pressure. Pups associated with mothers exhibiting high FGM levels had low annual survival rates, received less maternal/alloparental care and had higher FGM levels. Interestingly, offspring from mothers with high FGM levels were more likely to survive the summer when born in small litters. In sum, social interactions likely influence and are influenced by glucocorticoid levels of facultatively social females. Potential benefits of social bonds may be context-specific, and agonistic interactions may be tightly correlated with fitness. Female marmots exhibiting high FGM levels had overall low reproductive success, which is predicted by the cort-fitness hypothesis. However, under adverse conditions, offspring summer survival can be maximized if pups are born in small litters.

Spatial and temporal patterns of diversification on the Amazon: A test of the riverine hypothesis for all diurnal primates of Rio Negro and Rio Branco in Brazil.

The role of Amazonian rivers as drivers of speciation through vicariance remains controversial. Here we explore the riverine hypothesis by comparing spatial and temporal concordances in pattern of diversification for all diurnal primates of Rio Negro and its largest tributary, Rio Branco. We built a comprehensive comparative phylogenetic timetree to identify sister lineages of primates based on mitochondrial cytochrome b DNA sequences from 94 samples, including 19 of the 20 species of diurnal primates from our study region and 17 related taxa from elsewhere. Of the ten primate genera found in this region, three had populations on opposite banks of Rio Negro that formed reciprocally monophyletic clades, with roughly similar divergence times (Cebus: 1.85 Ma, HPD 95% 1.19-2.62; Callicebus: 0.83 Ma HPD 95% 0.36-1.32, Cacajao: 1.09 Ma, 95% HPD 0.58-1.77). This also coincided with time of divergence of several allopatric species of Amazonian birds separated by this river as reported by other authors. Our data offer support for the riverine hypothesis and for a Plio-Pleistocene time of origin for Amazonian drainage system. We showed that Rio Branco was an important geographical barrier, limiting the distribution of six primate genera: Cacajao, Callicebus, Cebus to the west and Pithecia, Saguinus, Sapajus to the east. The role of this river as a vicariant agent however, was less clear. For example, Chiropotes sagulata on the left bank of the Rio Branco formed a clade with C. chiropotes from the Amazonas Department of Venezuela, north of Rio Branco headwaters, with C. israelita on the right bank of the Rio Branco as the sister taxon to C. chiropotes+C. sagulata. Although we showed that the formation of the Rio Negro was important in driving diversification in some of our studied taxa, future studies including more extensive sampling of markers across the genome would help determine what processes contributed to the evolutionary history of the remaining primate genera.

Biogeography of squirrel monkeys (genus Saimiri): South-central Amazon origin and rapid pan-Amazonian diversification of a lowland primate.

The squirrel monkey, Saimiri, is a pan-Amazonian Pleistocene radiation. We use statistical phylogeographic methods to create a mitochondrial DNA-based timetree for 118 squirrel monkey samples across 68 localities spanning all Amazonian centers of endemism, with the aim of better understanding (1) the effects of rivers as barriers to dispersal and distribution; (2) the area of origin for modern Saimiri; (3) whether ancestral Saimiri was a lowland lake-affiliated or an upland forest taxa; and (4) the effects of Pleistocene climate fluctuation on speciation. We also use our topology to help resolve current controversies in Saimiri taxonomy and species relationships. The Rondônia and Inambari centers in the southern Amazon were recovered as the most likely areas of origin for Saimiri. The Amazon River proved a strong barrier to dispersal, and squirrel monkey expansion and diversification was rapid, with all speciation events estimated to occur between 1.4 and 0.6Ma, predating the last three glacial maxima and eliminating climate extremes as the main driver of squirrel monkey speciation. Saimiri expansion was concentrated first in central and western Amazonia, which according to the "Young Amazon" hypothesis was just becoming available as floodplain habitat with the draining of the Amazon Lake. Squirrel monkeys also expanded and diversified east, both north and south of the Amazon, coincident with the formation of new rivers. This evolutionary history is most consistent with a Young Amazon Flooded Forest Taxa model, suggesting Saimiri has always maintained a lowland wetlands niche and was able to greatly expand its range with the transition from a lacustrine to a riverine system in Amazonia. Saimiri vanzolinii was recovered as the sister group to one clade of Saimiri ustus, discordant with the traditional Gothic vs. Roman morphological division of squirrel monkeys. We also found paraphyly within each of the currently recognized species: S. sciureus, S. ustus, and S. macrodon. We discuss evidence for taxonomic revision within the genus Saimiri, and the need for future work using nuclear markers.

Kinship and social behavior of lowland tapirs (Tapirus terrestris) in a central Amazon landscape.

We tested the hypothesis that tapirs tolerate individuals from adjacent and overlapping home ranges if they are related. We obtained genetic data from fecal samples collected in the Balbina reservoir landscape, central Amazon. Samples were genotyped at 14 microsatellite loci, of which five produced high quality informative genotypes. Based on an analysis of 32 individuals, we inferred a single panmictic population with high levels of heterozygosity. Kinship analysis identified 10 pairs of full siblings or parent-offspring, 10 pairs of half siblings and 25 unrelated pairs. In 10 cases, the related individuals were situated on opposite margins of the reservoir, suggesting that tapirs are capable of crossing the main river, even after damming. The polygamous model was the most likely mating system for Tapirus terrestris. Moran's I index of allele sharing between pairs of individuals geographically close (<3 km) was similar to that observed between individual pairs at larger distances (>3 km). Confirming this result, the related individuals were not geographically closer than unrelated ones (W = 188.5; p = 0.339). Thus, we found no evidence of a preference for being close to relatives and observed a tendency for dispersal. The small importance of relatedness in determining spatial distribution of individuals is unusual in mammals, but not unheard of. Finally, non-invasive sampling allowed efficient access to the genetic data, despite the warm and humid climate of the Amazon, which accelerates DNA degradation.