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Background  Gene duplication provides opportunities for lineage diversification and evolution of developmental novelties. Duplicated genes generally either disappear by accumulation of mutations (nonfunctionalization), or are preserved either by the origin of positively selected functions in one or both duplicates (neofunctionalization), or by the partitioning of original gene subfunctions between the duplicates (subfunctionalization). The Pax2/5/8 family of important developmental regulators has undergone parallel expansion among chordate groups. After the divergence of urochordate and vertebrate lineages, two rounds of independent gene duplications resulted in the  Pax2, Pax5 , and  Pax8  genes of most vertebrates (the sister group of the urochordates), and an additional duplication provided the  pax2a  and  pax2b  duplicates in teleost fish. Separate from the vertebrate genome expansions, a duplication also created two  Pax2/5/8  genes in the common ancestor of ascidian and larvacean urochordates.    Results  To better understand mechanisms underlying the evolution of duplicated genes, we investigated, in the larvacean urochordate  Oikopleura dioica , the embryonic gene expression patterns of  Pax2/5/8  paralogs. We compared the larvacean and ascidian expression patterns to infer modular subfunctions present in the single pre-duplication  Pax2/5/8  gene of stem urochordates, and we compared vertebrate and urochordate expression to infer the suite of  Pax2/5/8  gene subfunctions in the common ancestor of olfactores (vertebrates + urochordates). Expression pattern differences of larvacean and ascidian Pax2/5/8 orthologs in the endostyle, pharynx and hindgut suggest that some ancestral gene functions have been partitioned differently to the duplicates in the two urochordate lineages. Novel expression in the larvacean heart may have resulted from the neofunctionalization of a  Pax2/5/8  gene in the urochordates. Expression of larvacean  Pax2/5/8  in the endostyle, in sites of epithelial remodeling, and in sensory tissues evokes like functions of  Pax2 ,  Pax5  and  Pax8  in vertebrate embryos, and may indicate ancient origins for these functions in the chordate common ancestor.    Conclusion  Comparative analysis of expression patterns of chordate Pax2/5/8 duplicates, rooted on the single-copy  Pax2/5/8  gene of amphioxus, whose lineage diverged basally among chordates, provides new insights into the evolution and development of the heart, thyroid, pharynx, stomodeum and placodes in chordates; supports the controversial conclusion that the atrial siphon of ascidians and the otic placode in vertebrates are homologous; and backs the notion that  Pax2/5/8  functioned in ancestral chordates to engineer epithelial fusions and perforations, including gill slit openings.

Evolution of developmental roles of Pax2/5/8paralogs after independent duplication in urochordate and vertebrate lineages