Genomic and radiocarbon insights into the mystery of mouse mummies on the summits of >6000 m Andean volcanoes

Abstract

Our understanding of the limits of animal life is continually revised by scientific exploration of extreme environments. Here we report the discovery of numerous mummified cadavers of leaf-eared mice, Phyllotis vaccarum, from the summits of three different Andean volcanoes at elevations 6029-6233 m (19,780 - 20,449 ft) above sea level in the Puna de Atacama (Chile-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 (6739 m [=22,110 ft]), the 13 summit mummies represent the highest physical records of mammals in the world. We report a chromosome-level genome assembly for P. vaccarum in combination with a whole-genome re-sequencing analysis and radiocarbon dating analysis that provide insights into the provenance and antiquity of the summit mice. We test alternative hypotheses to explain the existence of mouse graveyards on the summits of Atacama volcanoes. Radiocarbon data indicate that the most ancient of the mummies were 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 summit groups. These findings bolster evidence for self-sustaining populations of Phyllotis at elevations >6000 m and challenge assumptions about the environmental limits of vertebrate life and the physiological tolerances of small mammals.

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

“…Our finding highlights the value of conducting surveys in inaccessible, poorly explored regions of South America, and suggests that the Andean Altiplano is a region where increased survey work can yield important biodiversity information and surprising new discoveries for native small mammals (Storz et al 2020(Storz et al , 2023Rengifo et al 2022). With our new record of Punomys, the number of living mammal species and genera in Chile now stands at 170 and 88, respectively (D'Elía et al 2020;Rodríguez-San Pedro et al 2022Quiroga-Carmona et al 2023).…”

“…In combination with our discovery of the Punomys mummy at 5,461 m, the discovery of mummies of leaf-eared mice (P. vaccarum) on the summits of multiple >6,000 m Atacama volcanoes (Storz et al 2023) and live-capture and photographic records of Phyllotis at elevations 6,205-6,739 m (Storz et al 2020;Steppan et al 2022) demonstrate that Andean rodents exist at elevations that far surpass previously assumed limits. In comparison to highland rodent taxa like Phyllotis, which tend to have fairly broad elevational ranges, the notable feature of Punomys is that it appears to be restricted to puna habitats >4,400 m (Pearson 1951).…”

“…Given that we discovered the mummy at an elevation of 5,461 m, the Chilean specimen also represents an elevational record for the genus Punomys, as previous specimens in Peru and Bolivia were collected between 4,450 and 4,770 m asl (Pacheco and Patton 1995;Salazar-Bravo et al 2011). With this new specimen-based elevational record, Punomys is second only to P. vaccarum as the mammal taxon with the highest known elevational range limit (Storz et al 2020(Storz et al , 2023. In addition to the new elevational record for Punomys, our Chilean specimen also represents a ~700 km southward extension of the known latitudinal range of the genus.…”

“…In recent years, high-elevation surveys in the Central Andes have revealed that we still have much yet to learn about the elevational range limits of small mammals. For example, mountaineering mammal surveys of multiple volcanoes in the Chilean Puna de Atacama have documented evidence of Andean leaf-eared mice, Phyllotis vaccarum (previously referred to as P. xanthopygus rupestris), living at elevations well above 6,000 m (Storz et al 2020(Storz et al , 2023Steppan et al 2022), and mammal surveys in the Andean Altiplano of northwestern Argentina have documented surprisingly diverse rodent assemblages at elevations >4,000 m (Pearson 1951(Pearson , 1982Pearson and Ralph 1978;Urquizo et al 2022). Thus, as part of a continuing effort to further redress Linnean and Wallacean shortfalls for Andean small mammals, here we report the first Chilean record of the genus Punomys, a record that also significantly extends the elevational and latitudinal range of the taxon.…”