Whole-Genome Duplication and the Functional Diversification of Teleost FishHemoglobins

摘要

Subsequent to the two rounds of whole-genome duplication that occurred in the common ancestor of vertebrates, a third genome duplication occurred in the stem lineage of teleost fishes. This teleost-specific genome duplication (TGD) is thought to have provided genetic raw materials for the physiological, morphological, and behavioral diversification of this highly speciose group. The extreme physiological versatility of teleost fish is manifest in their diversity of blood–gas transport traits, which reflects the myriad solutions that have evolved to maintain tissue O2 delivery in the face of changing metabolic demands and environmental O2 availability during different ontogenetic stages. During the course of development, regulatory changes in blood–O2 transport are mediated by the expression of multiple, functionally distinct hemoglobin (Hb) isoforms that meet the particular O2-transport challenges encountered by the developing embryo or fetus (in viviparous or oviparous species) and in free-swimming larvae and adults. The main objective of the present study was to assess the relative contributions of whole-genome duplication, large-scale segmental duplication, and small-scale gene duplication in producing the extraordinary functional diversity of teleost Hbs. To accomplish this, we integrated phylogenetic reconstructions with analyses of conserved synteny to characterizethe genomic organization and evolutionary history of the globin gene clusters of teleosts.These results were then integrated with available experimental data on functionalproperties and developmental patterns of stage-specific gene expression. Our resultsindicate that multiple α- and β-globin geneswere present in the common ancestor of gars (order Lepisoteiformes) and teleosts. Thecomparative genomic analysis revealed that teleosts possess a dual set of TGD-derivedglobin gene clusters, each of which has undergone lineage-specific changes in gene contentvia repeated duplication and deletion events. Phylogenetic reconstructions revealed thatparalogous genes convergently evolved similar functional properties in different teleostlineages. Consistent with other recent studies of globin gene family evolution invertebrates, our results revealed evidence for repeated evolutionary transitions in thedevelopmental regulation of Hb synthesis.