Genomic evidence for independent origins of β-like globin genes in monotremes and therian mammals

Abstract

Phylogenetic reconstructions of the ␤-globin gene family in vertebrates have revealed that developmentally regulated systems of hemoglobin synthesis have been reinvented multiple times in independent lineages. For example, the functional differentiation of embryonic and adult ␤-like globin genes occurred independently in birds and mammals. In both taxa, the embryonic ␤-globin gene is exclusively expressed in primitive erythroid cells derived from the yolk sac. However, the '' -globin'' gene in birds is not orthologous to the -globin gene in mammals, because they are independently derived from lineage-specific duplications of a proto ␤-globin gene. Here, we report evidence that the early and late expressed ␤-like globin genes in monotremes and therian mammals (marsupials and placental mammals) are the products of independent duplications of a proto ␤-globin gene in each of these two lineages. Results of our analysis of genomic sequence data from a large number of vertebrate taxa, including sequence from the recently completed platypus genome, reveal that the -and ␤-globin genes of therian mammals arose via duplication of a proto ␤-globin gene after the therian/monotreme split. Our analysis of genomic sequence from the platypus also revealed the presence of a duplicate pair of ␤-like globin genes that originated via duplication of a proto ␤-globin gene in the monotreme lineage. This discovery provides evidence that, in different lineages of mammals, descendent copies of the same proto ␤-globin gene may have been independently neofunctionalized to perform physiological tasks associated with oxygen uptake and storage during embryonic development.

Differential loss of embryonic globin genes during the radiation of placental mammals

“…3). In combination with the results for the atlantogenatan taxa (see above) and marsupials (16,19), these results indicate that the HBE genes of therian mammals originated via duplication of a proto-HBB gene after the therian/prototherian split (Ϸ220 Mya), and that HBG and HBH are the products of two successive rounds of duplication that occurred after the eutherian/metatherian split (Ϸ170 Mya). For the adult portion of the cluster, phylogeny reconstructions of flanking and intronic sequence demonstrated that the HBB genes of laurasiatherian species are 1:1 orthologs of the HBB gene in humans, and likewise for the HBD genes (Fig.…”

“…Remarkably, the early-and late-expressed ␤-like globin genes in monotremes and therian mammals (marsupials and eutherians) are the products of independent duplications of a proto ␤-globin gene in each of these two lineages (19). Whereas the ␤-globin gene cluster of marsupials has retained the ancestral two-gene structure, the addition of new early-and late-expressed genes to the ␤-globin gene cluster of eutherian mammals is attributable to several successive rounds of duplication and divergence after the eutherian/marsupial split, which is thought to have occurred Ϸ170 Mya (20).…”

Hemoglobin–oxygen affinity in high-altitude vertebrates: is there evidence for an adaptive trend?

“…In comparative studies of Hb evolution involving orthologous genes from a diversity of species, it may often be the case that phylogenies of the α-and β-globin genes are not congruent with one another or with the assumed species tree Hoffmann et al, 2008a,b;Opazo et al, 2008aOpazo et al, ,b, 2009Runck et al, 2009Runck et al, , 2010Gaudry et al, 2014;Natarajan et al, 2015a). This genealogical discordance can have multiple biological causes, including ectopic gene conversion (a form of non-reciprocal recombinational exchange between duplicated genes), introgressive hybridization (incorporation of allelic variants from one species into the gene pool of another species by means of hybridization and repeated back-crossing) and incomplete lineage sorting (the retention of ancestral polymorphism from one split between populations to the next, followed by stochastic sorting of allelic lineages among the descendant species).…”

Developmental regulation of hemoglobin synthesis in the green anole lizard Anolis carolinensis

“…Each of the main lineages of tetrapods inherited an ortholog of the same proto -globin gene, which then underwent one or more rounds of duplication and divergence to produce distinct repertoires of -like globin genes in each descendant lineage ( Fig.1B) (Opazo et al, 2008a;Opazo et al, 2008b;Patel et al, 2008;Hoffmann et al, 2010). For example, an inventory of globin genes in the green anole genome revealed that this species possesses a pair of highly distinct -like globin genes,  I and …”