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

Abstract

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.

Keywords: Andes; Phyllotis; Puna de Atacama; distribution limits; high altitude; species limits.

Figure 1:

Collection localities. A, Sixty collection localities in northern Chile and bordering regions of Argentina and Bolivia, with elevations ranging from sea level to 6,739 m (see table S1 for details). B, Locations of 21 surveyed volcanoes along the spine of the Andean cordillera (see table S2 for details).

Figure 2:

Maximum likelihood tree (ln = −8,956.735) estimated for cytb gene sequences of Phyllotis. Numbers at nodes correspond to ultrafast bootstrap support values (only values for species and relationships among species are shown). For specimens collected as part of the present study, terminal labels refer to specimen catalog numbers, GenBank accession numbers, and localities (table S1). For sequences downloaded from GenBank, terminal labels refer to accession numbers. Phyllotis specimens that we collected from especially high elevations are labeled “5–6 km” and “>6 km.” The clade shown in orange comprises Phyllotis specimens with limatus-like cytb haplotypes that we collected well outside the known range of P. limatus in northern Chile (see text for details).

Figure 3:

Genomic tests of alternative hypotheses regarding the latitudinal and elevational range limits of Phyllotis limatus. A, Southern range limit of P. limatus and northern range limit of P. vaccarum, according to traditional criteria based on morphological variation and mitochondrial DNA (mtDNA) variation (Steppan et al. 2007; Steppan and Ramirez 2015). B, Hypothesis for revised range limits of P. limatus based on the collection of mice with limatus-like cytb haplotypes in northern Chile (forming the southern limatus clade shown in fig. 2) that occur well outside the traditionally assumed range of the species (but that occur well within the known range of P. vaccarum). Symbols denote collection localities where we recovered mice with cytb haplotypes that fall into three well-supported clades, one representative of P. vaccarum, one representative of P. limatus as traditionally recognized (northern limatus-type), and one that appears to represent a southern subclade of P. limatus (southern limatus-type). If mice with the southern limatus-type mtDNA are in fact referable to P. limatus, the newly collected specimens would represent a considerable southward extension of the species’ known latitudinal range and a >1,250-m upward extension of the species’ known elevational range (Steppan and Ramirez 2015). The inset tree depicts inferred relationships among the three abovementioned cytb clades, according to the phylogeny estimate shown in figure 2. C, Estimated phylogeny based on whole mitochondrial genomes recovers the same topology as the cytb tree for vaccarum and the two limatus subclades (fig. 2). D, In contrast to the relationships based on mtDNA, principal components analysis of whole-genome polymorphism data demonstrates that mice with southern imatusl-type mtDNA group with vaccarum to the exclusion of mice with northern limatus-type mtDNA. The genomic data indicate that mice with the southern limatus-type mtDNA haplotypes are in fact referable to P. vaccarum, whereas those with the northern limatus-type mtDNA haplotypes are referable to P. limatus.