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

Abstract

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 6,200 m 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.

Lagomorpha as a Model Morphological System

“…Considerable homoplasy in the morphology of leporid species was identified by Corbet (1983) after examining 21 morphological characteristics for 22 leporid species. More recent morphometric studies of lagomorphs have also found a high degree of homoplasy, low phylogenetic signal, and adaptive divergence in skull shape (Ge et al, 2015;Kraatz and Sherratt, 2016;Feijó et al, 2020). These studies highlight the difficulties in reconstructing a robust phylogeny for lagomorphs, particularly at the intergeneric level, by using morphological data.…”

Multilocus phylogeny reveals habitat driven cryptic diversity in Ochotona rufescens (Ochotonidae)

“…The O. rufescens lineages in Western and Central Asia formed geographically structured groups, but this pattern of molecular divergence was not paralleled by corresponding morphometric divergence and not entirely compatible with previously recognized taxonomic boundaries. Morphometric analyses, including the type specimens of O. r. rufescens , O. r. regina , O. r. vizier , O. r. shukurovi and O. r. vulturna , demonstrated no variation in morphometric characters among Afghan pikas (Mohammadi et al, 2018), which can be a result of adaptive pressure related to behaviour, lack of divergent selection, high degree of homoplasy, and adaptive divergence in skull shape (Bickford et al, 2007; Dahal et al, 2017; Egea et al, 2016; Feijó et al, 2020; Kraatz & Sherratt, 2016) or strong stabilizing evolution (Mohammadi et al, 2018; Yu et al, 2000). The lack of morphometric diversity in Afghan pikas in external and cranial measurements make taxonomic decisions based on these alone difficult.…”

The role of herbivores in the grassland carbon budget for Three‐Rivers Headwaters region, Qinghai–Tibetan Plateau, China

“…Plateau pika, therefore, are considered to play a key role in food chains (Z. Guo et al, 2012; Lai & Smith, 2003; Smith & Foggin, 1999; Y. Zhang et al, 2016), although regarded as a harmful species (Chen et al, 2017; N. Fan et al, 1999; Pang & Guo, 2017; W. Wei et al, 2020), and have an adaptive strategy with a higher mortality and higher regeneration in its population (Nie et al, 2022). On the other hand, alpine creatures have to struggle with environmental and biological stresses through multilevel adaptations in the extreme environmental conditions of lower air temperature and lower atmospheric oxygen concentration (Dahal et al, 2020; Feijó et al, 2020). All of these would result in rodents having higher retained carbon spent on reproduction.…”

“…Wei et al, 2020), and have an adaptive strategy with a higher mortality and higher regeneration in its population (Nie et al, 2022). On the other hand, alpine creatures have to struggle with environmental and biological stresses through multilevel adaptations in the extreme environmental conditions of lower air temperature and lower atmospheric oxygen concentration (Dahal et al, 2020;Feijó et al, 2020). All of these would result in rodents having higher retained carbon spent on reproduction.…”