Extreme High-Elevation Mammal Surveys Reveal Unexpectedly High Upper Range Limits of Andean Mice.

AbstractIn the world's highest mountain ranges, uncertainty about the upper elevational range limits of alpine animals represents a critical knowledge gap regarding the environmental limits of life and presents a problem for detecting range shifts in response to climate change. Here we report results of mountaineering mammal surveys in the Central Andes, which led to the discovery of multiple species of mice living at extreme elevations that far surpass previously assumed range limits for mammals. We livetrapped small mammals from ecologically diverse sites spanning >6,700 m of vertical relief, from the desert coast of northern Chile to the summits of the highest volcanoes in the Andes. We used molecular sequence data and whole-genome sequence data to confirm the identities of species that represent new elevational records and to test hypotheses regarding species limits. These discoveries contribute to a new appreciation of the environmental limits of vertebrate life.

Discovery of the world's highest-dwelling mammal.

Environmental limits of animal life are invariably revised when the animals themselves are investigated in their natural habitats. Here we report results of a scientific mountaineering expedition to survey the high-altitude rodent fauna of Volcán Llullaillaco in the Puna de Atacama of northern Chile, an effort motivated by video documentation of mice (genus Phyllotis) at a record altitude of 6,205 m. Among numerous trapping records at altitudes of >5,000 m, we captured a specimen of the yellow-rumped leaf-eared mouse (Phyllotis xanthopygus rupestris) on the very summit of Llullaillaco at 6,739 m. This summit specimen represents an altitudinal world record for mammals, far surpassing all specimen-based records from the Himalayas and other mountain ranges. This discovery suggests that we may have generally underestimated the altitudinal range limits and physiological tolerances of small mammals simply because the world's high summits remain relatively unexplored by biologists.

The skull variation of the olive field mouse Abrothrix olivacea (Cricetidae: Abrotrichini) is localized and correlated to the ecogeographic features of its geographic distribution.

The relationship between phenotypic variation and landscape heterogeneity has been extensively studied to understand how the environment influences patterns of morphological variation and differentiation of populations. Several studies had partially addressed intraspecific variation in the sigmodontine rodent Abrothrix olivacea, focusing on the characterization of physiological aspects and cranial variation. However, these had been conducted based on geographically restricted populational samples, and in most cases, the aspects characterized were not explicitly contextualized with the environmental configurations in which the populations occurred. Here, the cranial variation of A. olivacea was characterized by recording twenty cranial measurements in 235 individuals from 64 localities in Argentina and Chile, which widely cover the geographic and environmental distribution of this species. The morphological variation was analyzed and ecogeographically contextualized using multivariate statistical analyses, which also included climatic and ecological variation at the localities where the individuals were sampled. Results indicate that the cranial variation of this species is mostly clustered in localized patterns associated to the types of environments, and that the levels of cranial differentiation are higher among the populations from arid and treeless zones. Additionally, the ecogeographical association of cranial size variation indicate that this species does not follow Bergmann's rule and that island populations exhibit larger cranial sizes compared to their continental counterparts distributed at the same latitudes. These results suggest that cranial differentiation among the populations of this species is not homogeneous throughout its geographic distribution, and that the patterns of morphological differentiation are also not completely consistent with the patterns of genetic structuring that have been described recently. Finally, the analyses performed to ponder morphological differentiation among populations suggest that the contribution of genetic drift in the formation of these patterns can be ruled out among Patagonian populations, and that the selective effect imposed by the environment could better explain them.

Elevational range extension of the Puna Mouse, Punomys (Cricetidae), with the first record of the genus from Chile.

We report an elevational record for the Andean sigmodontine Puna Mouse Punomys, which is also the first record of the genus in Chile. The record is based on a mummified specimen that we discovered at an elevation of 5,461 m (17,917 feet) in the caldera of Volcán Acamarachi, Región de Antofagasta, Chile. Results of a morphological assessment suggest that the specimen can be provisionally referred to the species P. lemminus. This new record also extends the known geographic distribution of the genus by 700 km to the south and brings the known Chilean mammal richness to a total of 170 living species and 88 genera. This finding highlights the need for increased survey efforts in more remote, high-elevation regions and demonstrates that there is still much to be learned about the mammal fauna of the Andean Altiplano.

Se reporta un registro altitudinal para el roedor sigmodontino Punomys, el cual corresponde a su vez al primer hallazgo del género para Chile. Este se basa en un espécimen momificado encontrado a una elevación de 5,461 m en la caldera del Volcán Acamarachi, Región de Antofagasta, Chile. Los caracteres morfológicos sugieren que el espécimen puede ser referido provisionalmente a la especie P. lemminus. Este nuevo registro amplía la distribución geográfica conocida del género en 700 km al sur, y eleva la riqueza de mamíferos vivientes chilenos a un nuevo total de 170 especies y 88 géneros. Este hallazgo resalta la necesidad de aumentar los esfuerzos de prospección en las regiones más remotas y de mayor altitud y demuestra que aún queda mucho por aprender sobre el ensamble de los mamíferos del Altiplano andino.

Genomic insights into the mystery of mouse mummies on the summits of Atacama volcanoes.

Our understanding of the limits of animal life is continually revised by scientific exploration of extreme environments. Here we report the discovery of mummified cadavers of leaf-eared mice, Phyllotis vaccarum, from the summits of three different Andean volcanoes at elevations 6,029-6,233 m above sea level in the Puna de Atacama in Chile and Argentina. Such extreme elevations were previously assumed to be completely uninhabitable by mammals. In combination with a live-captured specimen of the same species from the nearby summit of Volcán Llullaillaco (6,739 m)1, the summit mummies represent the highest altitude physical records of mammals in the world. We also report a chromosome-level genome assembly for P. vaccarum that, in combination with a whole-genome re-sequencing analysis and radiocarbon dating analysis, provides insights into the provenance and antiquity of the summit mice. Radiocarbon data indicate that the most ancient of the mummies are, at most, a few centuries old. Genomic polymorphism data revealed a high degree of continuity between the summit mice and conspecifics from lower elevations in the surrounding Altiplano. Genomic data also revealed equal numbers of males and females among the summit mice and evidence of close kinship between some individuals from the same summits. These findings bolster evidence for resident populations of Phyllotis at elevations >6,000 m and challenge assumptions about the environmental limits of vertebrate life and the physiological tolerances of small mammals.

Extreme high-elevation mammal surveys reveal unexpectedly high upper range limits of Andean mice.

In the world's highest mountain ranges, uncertainty about the upper elevational range limits of alpine animals represents a critical knowledge gap regarding the environmental limits of life and presents a problem for detecting range shifts in response to climate change. Here we report results of mountaineering mammal surveys in the Central Andes, which led to the discovery of multiple species of mice living at extreme elevations that far surpass previously assumed range limits for mammals. We live-trapped small mammals from ecologically diverse sites spanning >6700 m of vertical relief, from the desert coast of northern Chile to the summits of the highest volcanoes in the Andes. We used molecular sequence data and whole-genome sequence data to confirm the identities of species that represent new elevational records and to test hypotheses regarding species limits. These discoveries contribute to a new appreciation of the environmental limits of vertebrate life.

Climate influences the genetic structure and niche differentiation among populations of the olive field mouse Abrothrix olivacea (Cricetidae: Abrotrichini).

Even when environmental variation over time and space is commonly considered as an important driver of population divergence, few evaluations of intraspecific genetic variation explicitly assess whether observed structure has been caused by or is correlated with landscape heterogeneity. Several phylogeographic studies have characterized the mitochondrial diversity of Abrothrix olivacea, but none has incorporated landscape genetics analyses and ecological niche modeling, leaving a gap in the understanding of the species evolutionary history. Here, these aspects were addressed based on 186 single nucleotide polymorphisms, extracted from sequences of 801 bp of Cytb gene, gathered from 416 individuals collected at 103 localities in Argentina and Chile. Employing multivariate statistical analyses (gPCA, Mantel and Partial Mantel Tests, Procrustes Analysis, and RDA), associations between genetic differences and geographic and climatic distances were evaluated. Presence data was employed to estimate the potential geographic distribution of this species during historical and contemporary climatic scenarios, and to address differences among the climatic niches of their main mitochondrial lineages. The significant influence of landscape features in structuring mitochondrial variability was evidenced at different spatial scales, as well as the role of past climatic dynamics in driving geographic range shifts, mostly associated to Quaternary glaciations. Overall, these results suggest that throughout geographic range gene flow is unevenly influenced by climatic dissimilarity and the geographic distancing, and that studied lineages do not exhibit distributional signals of climatic niche conservatism. Additionally, genetic differentiation occurred by more complex evolutionary processes than mere disruption of gene flow or drift.

Evidence of a population of leaf-eared mice Phyllotis vaccarum above 6,000 m in the Andes and a survey of high-elevation mammals.

Biologists have long pondered the extreme limits of life on Earth, including the maximum elevation at which species can live and reproduce. Here we review evidence of a self-sustaining population of mice at an elevation that exceeds that of all previously reported for mammals. Five expeditions over 10 years to Volcán Llullaillaco on the Argentina/Chile border observed and collected mice at elevations ranging from 5,070 m at the mountain's base to the summit at 6,739 m (22,110 feet). Previously unreported evidence includes observations and photographs of live animals and mummified remains, environmental DNA, and a soil microbial community reflecting animal activity that are evaluated in combination with previously reported video recordings and capture of live mice. All of the evidence identifies the mouse as the leaf-eared mouse Phyllotis vaccarum, and it robustly places the population within a haplotype group containing individuals from the Chilean Atacama Desert and nearby regions of Argentina. A critical review of the literature affirms that this population is not only an elevational record for mammals but for all terrestrial vertebrates to date, and we further find that many extreme elevations previously reported for mammals are based on scant or dubious evidence.

Durante mucho tiempo los biólogos han reflexionado sobre los límites extremos de altura a la que las especies pueden vivir y reproducirse. Aquí presentamos nueva evidencia sobre la existencia de una población de ratones establecida a una elevación que supera todos los reports previos para mamíferos. Durante 10 años fueron realizadas 5 expediciones al Volcán Llullaillaco, ubicado en la frontera entre Argentina y Chile; observando y colectando ratones en elevaciones que van desde los 5,070 m hasta la cima de 6,739 m (22,110 feet). La nueva evidencia incluye fotografías de restos momificados, ADN ambiental y la actividad microbiana del suelo que confirman la presencia del animal, la cual fue analizada junto a videos reportados anteriormente y la captura de ejemplares vivos. Toda esta información indica que dicha población corresponde al ratón orejudo amarillento Phyllotis vaccarum y lo posicionan dentro de un grupo de haplotipos compuesto por individuos del Desierto de Atacama y regiones cercanas en Argentina. La revisión crítica de la literatura demostró que esta población no solo es un récord de elevación para los mamíferos, sino para todos los vertebrados terrestres; igualmente, que los reportes de elevaciones extremas reportados para mamíferos se derivan de evidencias escasas y dudosas.

Andean non-volant small mammals: A dataset of community assemblages of non-volant small mammals from the high Andes.

Information from diversity inventories was used to study patterns of biodiversity and species distribution, to identify potential priority areas for conservation, and to guide future sampling efforts. In this context, we compiled information on non-volant small mammal communities from the high Andes (>2000 m). Here, we present an open source dataset containing information on diversity (species composition, number of individuals captured), inventory design (type of traps, sampling efforts), and environment (habitat) for both unpublished and published information. This study covers 630 mammalian communities, geographically distributed throughout the Andes in Venezuela, Colombia, Ecuador, Peru, Bolivia, Argentina, and Chile. We compiled a total of 26,412 individual records belonging to 240 species; the order with greatest number of records was Rodentia (n = 25,319, 96.06%), followed by Didelphimorphia (n = 373, 1.42%), Eulipotyphla (n = 358, 1.36%) and Paucituberculata, (n = 307, 1.16%). Andean non-volant small mammal communities harbor a range from 1 to 17 species, with 93.06% of sites being composed of one to five species, 27.78% of sites with species richness varying from 6 to 10 species, and 4.17% sites composed of more than 10 species. Multiple sampling methods were used to survey non-volant small mammals; the most representative methods were snap-traps and Sherman traps, or a combination of both, in more than 81% of the studies. This data paper represents the first large dataset of faunal species inventories for the Andes. There are no copyright restrictions associated with the use of this dataset. Please cite this data paper when its data are used total or partially in research or teaching.

Genetic variation of the Chilean endemic long-haired mouse Abrothrix longipilis (Rodentia, Supramyomorpha, Cricetidae) in a geographical and environmental context.

Quaternary climate and associated vegetational changes affected the fauna of the Chilean Mediterranean ecosystem. Here we studied the genetic variation of the long-haired mouse, Abrothrix longipilis, a sigmodontine rodent endemic to this area. Within an environmentally explicit context, we examined the geographic distribution of the genetic diversity and demographic history of the species based on sequences of the mitochondrial Cytochrome-b gene of 50 individuals from 13 localities and a large panel of single nucleotide polymorphisms of 17 individuals from 6 localities. The gene genealogy of A. longipilis revealed three intraspecific lineages that are allopatric and latitudinally segregated (northern, central, and southern lineages) with an estimated crown age for the whole species clade of 552.3 kyr B.P. A principal component analysis based on 336,596 SNP loci is in line with the information given by the the mitochondrial gene genealogy. Along its complete distributional range, A. longipilis showed patterns of isolation by distance and also isolation by environment. The general pattern of historical demography showed stability for most intraspecific lineages of A. longipilis. Northern and central lineages showed signals of historical demographic stability, while the southern lineage showed contrasting signals. In agreement with this, the niche models performed showed that in the northern range of A. longipilis, areas of high suitability for this species increased towards the present time; areas of central range would have remained relatively stable, while southern areas would have experienced more change through time. In summary, our study shows three distinct allopatric lineages of A. longipilis, each showing slightly different demographic history.