Duplicated FoxA genes in the leech Helobdella: Insights into the evolution of direct development in clitellate annelids

• Published in: Developmental dynamics 2018-05, Vol.247 (5), p.763-778
• Main Authors: Kuo, Dian‐Han, Hsiao, Yu‐Hsiang
• Format: Article
• Language: English
• Subjects: Animals; annelid; Annelida - embryology; Annelida - metabolism; Biological evolution; Ectoderm; Ectoderm - embryology; Ectoderm - metabolism; Embryo, Nonmammalian - metabolism; Embryogenesis; Embryos; Endoderm; Endoderm - embryology; Endoderm - metabolism; evolution of direct development; Evolutionary genetics; Foregut; Forkhead Transcription Factors - genetics; Forkhead Transcription Factors - metabolism; FoxA; Ganglia; ganglion morphogenesis; Gene duplication; Gene expression; gut development; Leeches - embryology; Leeches - metabolism; Midgut; Morphogenesis; Morphogenesis - genetics; Morphogenesis - physiology; Reproduction (copying)
• ISSN: 1058-8388; 1097-0177
• DOI: 10.1002/dvdy.24621

Background: As an adaptation to the land, the clitellate annelid had reorganized its embryogenesis to develop “directly” without the ancestral planktonic larval stage. To study the evolution of gut development in the directly developing clitellates, we characterized the expression pattern of the conserved gut gene, FoxA, in the embryonic development of the leech. Results: The leech has three FoxA paralogs. Hau‐FoxA1 is first expressed in a subset of endoderm cells and then in the foregut and the midgut. Hau‐FoxA2 is expressed in the stomodeum, which is secondarily derived from the anterior ectoderm in the clitellates rather than the tissue around the blastopore, the ancestral site of mouth formation in Phylum Annelida. Hau‐FoxA3 is expressed during the morphogenesis of segmental ganglia from the ectodermal teloblast lineages, a clitellate‐specific trait. Hau‐FoxA1 and Hau‐FoxA2 are also expressed during the morphogenesis of the leech‐specific front sucker. Conclusions: The expression patterns suggested that Hau‐FoxA1 carries out most of the conserved function in the endoderm and gut development, while the other two duplicates appear to have evolved unique novel functions in the directly developing clitellate embryos. Therefore, neofunctionalization and co‐option of FoxA might have made a significant contribution to the evolution of direct development in Clitellata. Developmental Dynamics 247:763–778, 2018. © 2018 Wiley Periodicals, Inc. Key Findings FoxA has experienced a series of lineage‐specific duplication events in the leech. Hau‐FoxA1 maintains the ancestral function in gut development. The earliest site of Hau‐FoxA1 expression suggests a novel pathway of endoderm development in the clitellate annelids. Hau‐FoxA2 and Hau‐FoxA3 acquired novel functions and are involved in the development of clitellate‐specific traits.