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. 2022 Sep 18;43(5):813-826.
doi: 10.24272/j.issn.2095-8137.2022.072.

Genomics and morphometrics reveal the adaptive evolution of pikas

Rui-Xiang Tang  1   2 , Jiao Wang  1 , Yi-Fei Li  3 , Cheng-Ran Zhou  1   4 , Guan-Liang Meng  5 , Feng-Jun Li  1 , Yue Lan  1 , Megan Price  1 , Lars Podsiadlowski  5 , Yan Yu  1 , Xu-Ming Wang  2 , Yin-Xun Liu  1   2 , Bi-Song Yue  1 , Shan-Lin Liu  6 , Zhen-Xin Fan  1   7 , Shao-Ying Liu  8
Affiliations

Genomics and morphometrics reveal the adaptive evolution of pikas

Rui-Xiang Tang et al. Zool Res. .

Abstract
in English, Chinese

Pikas (Lagomorpha: Ochotonidae) are small mouse-like lagomorphs. To investigate their adaptation to different ecological environments during their dispersal from the Qinghai-Xizang (Tibet) Plateau (QTP), we collected 226 pikas and measured 20 morphological characteristics and recorded habitat information. We also sequenced the genome of 81 specimens, representing 27 putative pika species. The genome-wide tree based on 4 090 coding genes identified five subgenera, i.e., Alienauroa, Conothoa, Lagotona, Ochotona, and Pika, consistent with morphometric data. Morphologically, Alienauroa and Ochotona had similar traits, including smaller size and earlier divergence time compared to other pikas. Consistently, the habitats of Alienauroa and Ochotona differed from those of the remaining subgenera. Phylogenetic signal analysis detected 83 genes significantly related to morphological characteristics, including several visual and hearing-related genes. Analysis of shared amino acid substitutions and positively selected genes (PSGs) in Alienauroa and Ochotona identified two genes, i.e., mitochondrial function-related TSFM (p.Q155E) and low-light visual sensitivity-related PROM1 (p.H419Y). Functional experiments demonstrated that TSFM-155E significantly enhanced mitochondrial function compared to TSFM-155Q in other pikas, and PROM1-419Y decreased the modeling of dynamic intracellular chloride efflux upon calcium uptake. Alienauroa and Ochotona individuals mostly inhabit different environments (e.g., subtropical forests) than other pikas, suggesting that a shift from the larger ancestral type and changes in sensory acuity and energy enhancement may have been required in their new environments. This study increases our understanding of the evolutionary history of pikas.

鼠兔（兔形目:鼠兔科）是一种小型的哺乳动物。为了研究鼠兔从青藏高原迁徙过程中对不同生态环境的适应性进化，我们采集了226只鼠兔并测量了每个个体的20项形态特征数据，还记录了它们的生境信息。我们进一步对代表了27个推定的不同鼠兔物种的81个标本进行了基因组测序。基于4090个编码基因的全基因组系统发育树和形态学数据，我们均鉴定出5个鼠兔亚属，即 Alienauroa, Conothoa, Lagotona, Ochotona和 Pika。与其他鼠兔相比， Alienauroa和 Ochotona具有更相似的形态特征，比如均具有更小的体型。另外， Alienauroa和 Ochotona亚属的生境与其他三个亚属有明显差异。系统发育信号分析发现83个与形态特征显著相关的基因，包括多个与视觉和听觉相关的基因。通过对 Alienauroa和 Ochotona亚属的共有氨基酸替换和正选择基因(PSGs)分析，我们鉴定到与线粒体功能相关基因 TSFM (p.Q155E)和与弱光视觉敏感性相关基因 PROM1 (p.H419Y)的突变位点。细胞功能实验表明，与其他三个亚属鼠兔的TSFM-155Q相比， Alienauroa和 Ochotona亚属的TSFM-155E显著增强了线粒体功能。而与PROM1-419H相比， Alienauroa和 Ochotona亚属的PROM1-419Y降低了细胞内氯离子外排对钙吸收的动态模拟。 Alienauroa和 Ochotona亚属的个体大多居住在与其他三个亚属不同的环境中（例如，亚热带森林），这表明新的环境可能还会促进它们从体型较大的祖先形态演化为更小的体型，并促进感觉敏锐度和能量生产利用效率的增强。该研究通过综合基因组学和形态学数据的分析，并结合细胞功能实验，增加了我们对鼠兔进化历史的认识。.

Keywords: Adaptive evolution; Genomics; Morphometrics; Pikas; Sensory and energy functions.

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Figures

Figure 1
Figure 1
Geographical distribution, morphological characteristics, and species tree with divergence times of pikas
Figure 2
Figure 2
Morphological characteristics of pikas
Figure 3
Figure 3
Phylogenetic signal analysis and shared amino acid substitutions
Figure 4
Figure 4
Functional validation of identified variants on TSFM and PROM1
See this image and copyright information in PMC

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