TY - JOUR

T1 - Emergence of a Chimeric Globin Pseudogene and Increased Hemoglobin Oxygen Affinity Underlie the Evolution of Aquatic Specializations in Sirenia

AU - Signore, Anthony V.

AU - Paijmans, Johanna L. A.

AU - Hofreiter, Michael

AU - Fago, Angela

AU - Weber, Roy E.

AU - Springer, Mark S.

AU - Campbell, Kevin L.

PY - 2019/6/1

Y1 - 2019/6/1

N2 - As limits on O2 availability during submergence impose severe constraints on aerobic respiration, the oxygen bindingglobin proteins of marine mammals are expected to have evolved under strong evolutionary pressures during their landto-sea transition. Here, we address this question for the order Sirenia by retrieving, annotating, and performing detailedselection analyses on the globin repertoire of the extinct Steller’s sea cow (Hydrodamalis gigas), dugong (Dugong dugon),and Florida manatee (Trichechus manatus latirostris) in relation to their closest living terrestrial relatives (elephants andhyraxes). These analyses indicate most loci experienced elevated nucleotide substitution rates during their transition to afully aquatic lifestyle. While most of these genes evolved under neutrality or strong purifying selection, the rate ofnonsynonymous/synonymous replacements increased in two genes (Hbz-T1 and Hba-T1) that encode the a-type chainsof hemoglobin (Hb) during each stage of life. Notably, the relaxed evolution of Hba-T1 is temporally coupled with theemergence of a chimeric pseudogene (Hba-T2/Hbq-ps) that contributed to the tandemly linked Hba-T1 of stem sireniansvia interparalog gene conversion. Functional tests on recombinant Hb proteins from extant and ancestral sireniansfurther revealed that the molecular remodeling of Hba-T1 coincided with increased Hb–O2 affinity in early sirenians.Available evidence suggests that this trait evolved to maximize O2 extraction from finite lung stores and suppress tissueO2 offloading, thereby facilitating the low metabolic intensities of extant sirenians. In contrast, the derived reduction inHb–O2 affinity in (sub)Arctic Steller’s sea cows is consistent with fueling increased thermogenesis by these once colossalmarine herbivore

AB - As limits on O2 availability during submergence impose severe constraints on aerobic respiration, the oxygen bindingglobin proteins of marine mammals are expected to have evolved under strong evolutionary pressures during their landto-sea transition. Here, we address this question for the order Sirenia by retrieving, annotating, and performing detailedselection analyses on the globin repertoire of the extinct Steller’s sea cow (Hydrodamalis gigas), dugong (Dugong dugon),and Florida manatee (Trichechus manatus latirostris) in relation to their closest living terrestrial relatives (elephants andhyraxes). These analyses indicate most loci experienced elevated nucleotide substitution rates during their transition to afully aquatic lifestyle. While most of these genes evolved under neutrality or strong purifying selection, the rate ofnonsynonymous/synonymous replacements increased in two genes (Hbz-T1 and Hba-T1) that encode the a-type chainsof hemoglobin (Hb) during each stage of life. Notably, the relaxed evolution of Hba-T1 is temporally coupled with theemergence of a chimeric pseudogene (Hba-T2/Hbq-ps) that contributed to the tandemly linked Hba-T1 of stem sireniansvia interparalog gene conversion. Functional tests on recombinant Hb proteins from extant and ancestral sireniansfurther revealed that the molecular remodeling of Hba-T1 coincided with increased Hb–O2 affinity in early sirenians.Available evidence suggests that this trait evolved to maximize O2 extraction from finite lung stores and suppress tissueO2 offloading, thereby facilitating the low metabolic intensities of extant sirenians. In contrast, the derived reduction inHb–O2 affinity in (sub)Arctic Steller’s sea cows is consistent with fueling increased thermogenesis by these once colossalmarine herbivore

U2 - 10.1093/molbev/msz044

DO - 10.1093/molbev/msz044

M3 - Article

VL - 36

SP - 1134

EP - 1147

JO - Molecular Biology and Evolution

JF - Molecular Biology and Evolution

SN - 0737-4038

IS - 6

ER -