Evolution of Hemoglobin Genes in a Subterranean Rodent Species (Lasiopodomys mandarinus).

Hong Sun,Kaihong Ye,Zhenlong Wang,Dan Pan,Shiming Gu,Denghui Liu

doi:10.3390/biology9050106

Abstract

The Mandarin vole (Lasiopodomys mandarinus), a typical subterranean rodent, has undergone hematological adaptations to tolerate the hypoxic/hypercapnic underground environment. Hemoglobin (Hb) genes encode respiratory proteins functioning principally in oxygen binding and transport to various tissues and organs. To investigate the evolution of α- and β-hemoglobin (Hb) in subterranean rodent species, we sequenced Hb genes of the Mandarin vole and the related aboveground Brandt’s vole (L. brandtii). Sequencing showed that in both voles, α-globin was encoded by a cluster of five functional genes in the following linkage order: HBZ, HBA-T1, HBQ-T1, HBA-T2, and HBQ-T2; among these, HBQ-T2 is a pseudogene in both voles. The β-globin gene cluster in both voles also included five functional genes in the following linkage order: HBE, HBE/HBG, HBG, HBB-T1, and HBB-T2. Phylogenetic analysis revealed that the Mandarin vole underwent convergent evolution with its related aboveground species (Brandt’s vole) but not with other subterranean rodent species. Selection pressure analyses revealed that α- and β-globin genes are under strong purifying selection (ω < 1), and branch-site analyses identified positive selection sites on HBAT-T1 and HBB-T1 in different subterranean rodent species. This suggests that the adaptive evolution of these genes enhanced the ability of Hb to store and transport oxygen in subterranean rodent species. Our findings highlight the critical roles of Hb genes in the evolution of hypoxia tolerance in subterranean rodent species.

Highlights

Subterranean rodent species spend their whole lives in complete darkness at relatively stable temperatures in hypoxic and hypercapnic underground burrow systems [1,2]
The ability of subterranean rodent species to survive under conditions of high CO2 and low O2 levels without severe deleterious physiological effects or behavioral changes [4,5,6] suggests that it will be interesting to investigate the specific adaptations of mammals that live in naturally rodent species
In the Mandarin vole, HBQ-T2 is a pseudogene, and in terms of chromosomal structure beginning with HBZ and terminating with HBQ-T2

Summary

Introduction

Subterranean rodent species spend their whole lives in complete darkness at relatively stable temperatures in hypoxic and hypercapnic underground burrow systems [1,2]. The ability of subterranean rodent species to survive under conditions of high CO2 and low O2 levels without severe deleterious physiological effects or behavioral changes [4,5,6] suggests that it will be interesting to investigate the specific adaptations of mammals that live in naturally rodent species. The important adaptation of subterranean rodent species to hypoxic environments are the increased blood vessel density, increased erythrocytosis, and improved hemoglobin (Hb) capacity of O2 delivery and storage [6,8,10]. Hb is responsible for the transport of O2 from the lungs to O2 -demanding tissues, suggesting that this protein plays an important role in the survival of subterranean rodent species under low ambient

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