Evolutionary Genetics of Hypoxia and Cold Tolerance in Mammals

Zhu, Kangli; Ge, Deyan; Wen, Zhixin; Xia, Lin; Yang, Qisen

doi:10.1007/s00239-018-9870-8

Cited by 21 publications

(20 citation statements)

References 106 publications

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“…Whereas high-elevation landscapes impose a series of physiological and biochemical evolutionary constraints generating parallel responses across distantly related lineages (e.g. Luo et al, 2013;Ramirez et al, 2007;Zhu, Ge, et al, 2018), our results point to the opposite pattern at the morphological level. High-elevation pikas exhibit the greatest phenotypic diversity in the genus, suggesting a greater degree of specialization to distinct microhabitats.…”

Section: Discussionmentioning

confidence: 50%

“…As a well-known driver of phenotypic diversity and habitat shifts (Brown & Wilson, 1956), competition has shaped the evolution of insular (Grant & Grant, 2006) and continental (Davies et al, 2007;Drury et al, 2018) lineages, especially in relation to resource-use traits. Thus, contrary to the physiological adaptive convergence exhibited by high-elevation pikas to cope with hypoxic landscapes (Zhu, Ge, et al, 2018), it seems that the cranium has undergone adaptive divergence to cope with the biotic stress of food limitation. This hypothesis also explains the low performance of our phylogenetic ANOVA models in predicting skull forms across elevation zones-rather than a common (convergent) cranial morphology, pikas show a large phenotypic pool at high elevations, reflecting adaptations to distinct alpine microhabitats.…”

Section: Discussionmentioning

confidence: 87%

“…For example, in extremely hot and dry environments, desert mammals exhibit physiological mechanisms that optimize water conservation (Donald & Pannabecker, 2015), nocturnal habits and a fossorial lifestyle to avoid heat stress (Schmidt-Nielsen & Schmidt-Nielsen, 1952;Walsberg, 2000), and cranial adaptations that enhance hearing and facilitate predator avoidance (Alhajeri & Steppan, 2018). Subterranean species tend to have morphological adaptations for digging (reduced limbs and pinnae, robust feet and claws), well-developed sensory systems for exploring dark places (auditory, olfactory and mechanical receptors) and physiological specializations for overcoming chronic hypoxia and hypercapnia (Fang et al, 2014;Lacey et al, 2000;Nevo, 1979;Ramirez, Folkow, & Blix, 2007;Zhu, Ge, Wen, Xia, & Yang, 2018). Understanding the complexity of evolutionary and ecological strategies that allow species to thrive under extreme conditions requires assessments at multiple levels of organization.…”

Section: Introductionmentioning

confidence: 99%

“…Numerous studies have investigated genetic pathways and physiological changes among high-elevation organisms, revealing a large array of strategies for improving oxygen affinity across distantly related lineages (e.g. Ge, Cai, et al, 2013;Lim, Witt, Graham, & Davalos, 2019;Luo, Yang, & Gao, 2013;Ramirez et al, 2007;Shao et al, 2015;Zhu, Ge, et al, 2018;Zhu, Guan, et al, 2018). In contrast, few studies have assessed adaptive responses in traits associated with resource use (i.e.…”

Section: Introductionmentioning

confidence: 99%

“…Genetic and physiological adaptations to life at high altitudes have been intensively described in pikas, indicating both cold and hypoxia tolerance (e.g. Li et al, 2001;Luo et al, 2008;Rankin, Galbreath, & Teeter, 2017;Yang et al, 2008;Zhu, Ge, et al, 2018). Nonetheless, the 34 living species occur in a represents a landmark in the evolutionary history of pikas.…”

Section: Introductionmentioning

confidence: 99%

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

Feijó

Wen

et al. 2020

Functional Ecology

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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.

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Section: Discussionmentioning

confidence: 50%

Section: Discussionmentioning

confidence: 87%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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

Feijó

Wen

et al. 2020

Functional Ecology

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Linking gene expression and phenotypic changes in the developmental and evolutionary origins of osteosclerosis in the ribs of bowhead whales (Balaena mysticetus)

et al. 2020

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Bowhead whales are among the longest-lived mammals with an extreme lifespan of about 211 years. During the first 25 years of their lives, rib bones increase in mineral density and the medulla transitions from compact to trabecular bone. Molecular drivers associated with these phenotypic changes in bone remain unknown. This study assessed expression levels of osteogenic genes from samples of rib bones of bowheads. Samples were harvested from prenatal to 86-year-old whales, representing the first third of the bowhead lifespan. Fetal to 2-year-old bowheads showed expression levels consistent with the rapid deposition of the bone extracellular matrix. Sexually mature animals showed expression levels associated with low rates of osteogenesis and increased osteoclastogenesis. After the first 25 years of life, declines in osteogenesis corresponded with increased expression of EZH2, an epigenetic regulator of osteogenesis. These findings suggest EZH2 may be at least one epigenetic modifier that contributes to the age-related changes in the rib bone phenotype along with the transition from compact to trabecular bone. Ancient cetaceans and their fossil relatives also display these phenotypes, suggesting EZH2 may have shaped the skeleton of whales in evolutionary history.

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Molecular insights into anatomy and physiology

Cooper

Gorbunova

2021

The Bowhead Whale

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Evolutionary Genetics of Hypoxia and Cold Tolerance in Mammals

Cited by 21 publications

References 106 publications

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

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

Linking gene expression and phenotypic changes in the developmental and evolutionary origins of osteosclerosis in the ribs of bowhead whales (Balaena mysticetus)

Molecular insights into anatomy and physiology

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