Lonely at the Top: isolated mountain tops served as ice age refugia

Nebria is a genus of flightless beetle found in montane alpine habitats, sometimes at altitudes over 3,000m. Nebria have special adaptations, such as anti-freeze enzymes, which allow them to thrive on snowy mountain tops where other insects could not. In fact, Nebria feed upon arthropod fallout, insects which are blown to high altitudes and become immobilized on the cold snow. These same cold-tolerant adaptations may prevent them from surviving at lower altitudes (Lohse et al. 2011). As a result, their mountain top homes act like isolated “sky islands.’ Dispersing between sky islands is challenging when you can’t fly.

Glaciers covered large portions of the Northern hemisphere during the last ice age, from about 2.5 million years ago to 10,000 years ago. Most alpine habitat was lost between plunging snow lines and encroaching glaciers. Alpine species, like Nebria, had to relocate to survive. There are two competing hypotheses for where they may have found refuge. The first suggests that montane species survived on isolated peaks, called nunataks, which protruded above the surrounding ice, and were too steep for snow accumulation. The second proposes that species migrated to ice-free areas at the periphery of the mountains, called massifs de refuge, and then recolonized mountain peaks after the ice receded.

We can test these hypotheses by examining the historical gene flow between populations. Phylogeneticists use DNA to recreate organisms’ evolutionary histories. Large portions of the genome are non-coding regions, and mutations occurring within them have no effect on the organism’s fitness, so they can accumulate freely over time, without being weeded out by natural selection. It is possible to infer how populations are related by comparing the differences in these regions. A phylogenetic tree is a graphical representation of these relationships. Mutations occur at a stable rate for a given gene, making it possible to estimate divergence dates for branches on the tree. Genes that mutate quickly inform us about recent divergences while slower genes allow us to look father into the past.

Nebria are ideal candidates for studying glacial refugia. Beetles surviving on a nunatak  would be extremely isolated, preventing gene flow between neighboring populations. They would therefore be more closely related to each other than to their neighbors. On a phylogenetic tree, all of the individuals within a population would form a clade, which would split from the tree before the beginning of the last ice age (Figure 1). Under the massif de refuge hypothesis, populations could freely intermix. Gene flow would continue throughout the ice age, and populations would either fail to form clades, or the clades would branch off after the ice had retreated (Figure 1).

Figure 1: A hypothetical phylogeny illustrating the two hypotheses. Under the nunatak hypothesis, the populations diverge before the last ice age (left). Under the massif de refuge hypothesis, the populations diverge after the iceage (right). Image by Adam Haberski.

The Evidence

To test these hypotheses, Taiwanese scientists (Weng et al. 2016) collected over 100 specimens of Nebria, and the closely related genus Leistus, from seven mountain peaks in Taiwan (Figure 2). Although there were no glaciers in Taiwan, these mountains were buried in deep snow during the last ice age.  The scientists sequenced four genes with varying mutation rates and inferred a phylogeny. What they discovered was that Taiwanese Nebria used both the nunatak and massif de refuge strategies. Most species showed a history of long isolation between populations, consistent with the nunatak hypothesis. Populations diverged between 3.67 and 0.65 million years ago, before the last glacial maximum. One species, Nebria uenoiana, showed a different pattern. Populations of N. uenoiana did not diverge until 0.17 million years ago, when it experienced a rapid radiation at the end of the ice age, consistent with the massif de refuge hypothesis.

Figure 2: Map showing the 7 sampling locations. Mountains higher than 2,000m are shaded gray. Reprinted from Weng et al. 2016.

What makes N. uenoiana different from the others? It has wings. Wing loss has often been correlated with altitude. High altitude habitats are tree-less, and thus lack the complex vertical components which make flight advantageous in forests (Kavanaugh 1985). Wing loss may therefore be favored by selection because it represents a significant energy savings. N. uenoiana was the only species in this study to retain its wings, and the extra mobility they provided allowed N. uenoiana to disperse long distances to find an ice-free area.

What does this mean for species today?

Ground beetles thrived in the cooler climate of the Pleistocene, and retreated to mountain tops during the warmer Holocene (Kavanaugh 1979). In essence, Nebria today are already using the nunatak hypothesis to escape the heat. As the climate continues to warm, shrubs are advancing up slope displacing alpine habitat (Klanderud and Totland 2005, Cannone et al. 2007), and the perennial snowfields Nebria depend on for food are disappearing. Alpine species cope with warming temperatures by moving to higher altitudes (Kavanaugh 1985). However, they will not be able to survive once the mountain top becomes too warm. Species adapted to a wider range of elevations, or with better dispersal capabilities, like N. uenoiana, may be able to disperse to cooler habitat on taller mountains or at higher latitudes. Long-term sampling is needed to determine how modern Nebria are coping with a rapidly warming climate.

Further Reading

This Science Daily article chronicles the efforts of one entomologist to collect Nebria in a warming climate. David Kavanaugh first collected Nebria in the Sierra Nevada range in 1968. He revisited these sites 30 years later to collect specimens for DNA sampling and found the habitat profoundly changed. Beetles which were once common at 6,500 feet had migrated to 13,000 to find suitable habitat.



  • Cannone, N., Sgorbati, S., & Guglielmin, M. (2007). Unexpected impacts of climate change on alpine vegetation.  Frontiers in Ecology and the Environment,  5(7), 360-364. DOI:  10.1890/1540-9295(2007)5[360:UIOCCO]2.0.CO;2
  • Kavanaugh, D. H. (1979). Investigations on present climatic refugia in North America through studies on the distributions of carabid beetles: concepts, methodology and prospectus. In Carabid Beetles (pp. 369-381). Springer Netherlands. DOI:  10.1007/978-94-009-9628-1_19
  • Kavanaugh, D. H. (1985). On wing atrophy in carabid beetles (Coleoptera: Carabidae), with special reference to Nearctic Nebria. Series Entomologica (Dordrecht), 33, 408-31. (PDF LINK)
  • Klanderud, K., & Totland, Ø. (2005). Simulated climate change altered dominance hierarchies and diversity of an alpine biodiversity hotspot.  Ecology,  86(8), 2047-2054. DOI:  10.1890/04-1563
  • Lohse, K., Nicholls, J. A., & Stone, G. N. (2011). Inferring the colonization of a mountain range–refugia vs. nunatak survival in high alpine ground beetles.  Molecular Ecology,  20(2), 394-408. DOI:  10.1111/j.1365-294X.2010.04929.x
  • Weng, Y. M., Yang, M. M., & Yeh, W. B. (2016). A comparative phylogeographic study reveals discordant evolutionary histories of alpine ground beetles (Coleoptera, Carabidae).  Ecology and evolution. DOI:  10.1002/ece3.2006