Divergent adaptations in resource-use traits explain how pikas thrive on the roof of the world

Life in extreme environments is possible through multilevel adaptations to
physical and biotic stresses. At high elevations, species face numerous
challenges, besides low oxygen levels, but previous studies have focused
on genetic and physiological adaptations to chronic hypoxia while
overlooking other key strategies for thriving in alpine landscapes. Here,
we investigate resource-use trait adaptations to extreme elevations using
pikas as a model, lagomorphs distributed up to 6200 metres and reaching
maximum diversity on the Qinghai-Tibet plateau, the highest plateau on
Earth. Specifically, we assess cranial evolution in pikas using geometric
morphometric and phylogenetic comparative techniques to determine whether
adaptations among high-elevation biota shown at the molecular and
physiological levels also occur in resource-use traits. We further explore
the roles of two contrasting lifestyles (burrowing and rocky-dwelling) in
cranial evolution. We found that alpine species exhibit striking
phenotypic specialization to distinct microhabitats. Contrary to
physiological and genetic adaptive convergence, we show that the cranium
has undergone adaptive divergence likely reflecting past resource
competition in highlands and long-term association with alpine landscapes.
Our analyses also reveal that the evolution of burrowing lifestyle allows
high-elevation pikas to explore novel niches and boosts their phenotypic
diversification. In addition to cold and hypoxia tolerance, high cranial
specialization, the appearance of burrowing habits, and strong niche
separation explain how pikas overcome alpine stresses and flourish on the
highest plateau on Earth. By contrast, when moving to spatially complex
and heterogeneous vegetation zonation, pikas exhibit generalist skull
forms able to exploit diverse habitats. These findings mirror previously
reported intraspecific patterns in mammals, suggesting a general
morphological response in resource-exploiting traits to cope with distinct
selection pressures across elevation zones. Phenotypic diversity is
further constrained by rocky habitats, resulting in convergent skulls. Our
study highlights that adaptations to extreme environments occur at
multiple levels of organization, but can lead to distinct evolutionary
paths depending on which selective forces they respond to. The evolution
of burrowing behaviour represents a landmark in the evolutionary history
of pikas. We further show that rocky habitats impose strong ecological
pressures, leading to convergent responses in resource-use traits, which
is rarely documented in mammals.