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MBE Advance Access originally published online on March 30, 2009
Molecular Biology and Evolution 2009 26(7):1469-1478; doi:10.1093/molbev/msp064
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© The Author 2009. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. All rights reserved. For permissions, please e-mail: journals.permissions@oxfordjournals.org

Research Articles

Origin and Ascendancy of a Chimeric Fusion Gene: The β/{delta}-Globin Gene of Paenungulate Mammals

Juan C. Opazo*,{dagger}, Angela M. Sloan{ddagger}, Kevin L. Campbell{ddagger},1 and Jay F. Storz*,1

* School of Biological Sciences, University of Nebraska
{dagger} Instituto de Ecología y Evolución, Facultad de Ciencias, Universidad Austral de Chile, Valdivia, Chile
{ddagger} Department of Biological Sciences, University of Manitoba, Winnipeg, MB, Canada

E-mail: jstorz2{at}unl.edu.

Accepted for publication March 15, 2009.

The {delta}-globin gene (HBD) of eutherian mammals exhibits a propensity for recombinational exchange with the closely linked β-globin gene (HBB) and has been independently converted by the HBB gene in multiple lineages. Here we report the presence of a chimeric β/{delta} fusion gene in the African elephant (Loxodonta africana) that was created by unequal crossing-over between misaligned HBD and HBB paralogs. The recombinant chromosome that harbors the β/{delta} fusion gene in elephants is structurally similar to the "anti-Lepore" duplication mutant of humans (the reciprocal exchange product of the hemoglobin Lepore deletion mutant). However, the situation in the African elephant is unique in that the chimeric β/{delta} fusion gene supplanted the parental HBB gene and is therefore solely responsible for synthesizing the β-chain subunits of adult hemoglobin. A phylogenetic survey of β-like globin genes in afrotherian and xenarthran mammals revealed that the origin of the chimeric β/{delta} fusion gene and the concomitant inactivation of the HBB gene predated the radiation of "Paenungulata," a clade of afrotherian mammals that includes three orders: Proboscidea (elephants), Sirenia (dugongs and manatees), and Hyracoidea (hyraxes). The reduced fitness of the human Hb Lepore deletion mutant helps to explain why independently derived β/{delta} fusion genes (which occur on an anti-Lepore chromosome) have been fixed in a number of mammalian lineages, whereas the reciprocal {delta}/β fusion gene (which occurs on a Lepore chromosome) has yet to be documented in any nonhuman mammal. This illustrates how the evolutionary fates of chimeric fusion genes can be strongly influenced by their recombinational mode of origin.

Key Words: chimeric fusion gene • gene duplication • gene family evolution • globin genes • hemoglobin • nonallelic homologous recombination

1 These authors contributed equally to this work.

Scott Edwards, Associate Editor


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