MBE Advance Access originally published online on July 26, 2006
Molecular Biology and Evolution 2006 23(11):2008-2016; doi:10.1093/molbev/msl071
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Research Articles |
A Genomic Fossil Reveals Key Steps in Hemoglobin Loss by the Antarctic Icefishes


* Department of Ecology and Evolutionary Biology, Yale University
Department of Biology, Northeastern University
E-mail: iceman{at}neu.edu.
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
- and ß-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 ß-globin gene but retain a truncated
-globin pseudogene. Surprisingly, a phylogenetically derived icefish species, Neopagetopsis ionah, possesses a complete, but nonfunctional, adult
ß-globin complex. This cluster contains 2 distinct ß-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
ß-globin cluster prior to the diversification of the extant species in the clade. Through lineage sorting of ancestral polymorphism, 2 types of alleles became fixed in the clade: 1) the
-globin pseudogene of the majority of species and 2) the inactive
ß-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.
Key Words: hemoglobin loss by icefishes genomic instability genetic introgression interspecific hybridization Channichthyidae Notothenioidei
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