A Genomic Fossil Reveals Key Steps in Hemoglobin Loss by the Antarctic Icefishes

Antarctic icefishes are the only vertebrates that do not have hemoglobin and erythrocytes in their blood. These startling phenotypes are associated in several icefish species with deletions of juvenile and adult globin loci, which in red-blooded teleosts are typically composed of tightly linked pair...

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Bibliographic Details
Published in:Molecular Biology and Evolution
Main Authors: Near, Thomas J., Parker, Sandra K., William Detrich, H.
Format: Text
Language:English
Published: Oxford University Press 2006
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Online Access:http://mbe.oxfordjournals.org/cgi/content/short/msl071v1
https://doi.org/10.1093/molbev/msl071
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Summary:Antarctic icefishes are the only vertebrates that do not have hemoglobin and erythrocytes in their blood. These startling phenotypes are associated in several icefish species with deletions of juvenile and adult globin loci, which in red-blooded teleosts are typically composed of tightly linked pairs of α- and β-globin genes. It is unknown if the loss of hemoglobin expression in icefishes was the direct result of such deletions, or if other mutational events compromised globin chain synthesis prior to globin gene loss. In this study we show that 15 of the 16 icefish species have lost the adult β-globin gene but retain a truncated α-globin pseudogene. Surprisingly, a phylogenetically derived icefish species, Neopagetopsis ionah , possesses a complete, but non-functional, adult αβ-globin complex. This cluster contains two distinct β-globin pseudogenes whose phylogenetic origins span the entire Antarctic notothenioid radiation, consistent with an origin via introgression. Maximum likelihood ancestral state reconstruction supports a scenario of icefish globin gene evolution that involves a single loss of the transcriptionally active adult αβ-globin cluster prior to the diversification of the extant species in the clade. Through lineage sorting of ancestral polymorphism, two types of alleles became fixed in the clade, 1) the α-globin pseudogene of the majority of species, and 2) the inactive αβ-globin complex of N. ionah . We conclude that the globin pseudogene complex of N. ionah is a "genomic fossil" that reveals key intermediate steps on the pathway to loss of hemoglobin expression by all icefish species.