Journal Article

Craniofacial development of hagfishes and the evolution of vertebrates

Kuraku, Shigehiro, Ota, Kinya G., Fujimoto, Satoko, Kuratani, Shigeru, Oisi, Yasuhiro

2013

Overview

Cyclostomes, the living jawless vertebrates including hagfishes and lampreys, represent the most basal lineage of vertebrates. Although the monophyly of cyclostomes has been supported by recent molecular analyses, the phenotypic traits of hagfishes, especially the lack of some vertebrate-defining features and the reported endodermal origin of the adenohypophysis, have been interpreted as hagfishes exhibiting a more ancestral state than those of all other vertebrates. Furthermore, the adult anatomy of hagfishes cannot be compared easily with that of lampreys. Here we describe the craniofacial development of a series of staged hagfish embryos, which shows that their adenohypophysis arises ectodermally, consistent with the molecular phylogenetic data. This finding also allowed us to identify a pan-cyclostome pattern, one not shared by jawed vertebrates. Comparative analyses indicated that many of the hagfish-specific traits can be explained by changes secondarily introduced into the hagfish lineage. We also propose a possibility that the pan-cyclostome pattern may reflect the ancestral programme for the craniofacial development of all living vertebrates. An analysis of staged hagfish embryos shows that the hagfish adenohypophysis is ectodermal in origin, revealing it to be a developmental quirk unique to hagfishes that was hitherto misleading; from this and other observations a ‘pan-cyclostome’ developmental pattern is derived, indicating that it was primitive for all vertebrates. The face of early vertebrate evolution The hagfish is the most primitive extant vertebrate. Its anatomy and development hold clues to understanding the evolution of that most enigmatic of structures, the vertebrate head. Hagfish embryos are notoriously hard to obtain, but a few years ago Shigeru Kuratani and colleagues managed to prepare some, and — for the first time since 1899 — significant work on hagfish embryology began. This paper presents the first detailed report on the craniofacial development of a hagfish species, Eptatretus burgeri . The authors identify an embryonic development pattern shared only by the jawless lampreys and hagfish that may have been primitive for all vertebrates.

• Publisher: Nature Publishing Group UK,Nature Publishing Group
• Subject: 631/136 / 631/181/735 / 631/181/757 / Animals / Biological Evolution / Embryo, Nonmammalian - anatomy & histology / Embryo, Nonmammalian - embryology / Embryo, Nonmammalian - ultrastructure / Embryonic Development / Embryos / Gene Expression Regulation, Developmental - genetics / Hagfishes / Hagfishes - anatomy & histology / Hagfishes - embryology / Hagfishes - genetics / Hagfishes - physiology / Head - anatomy & histology / Head - embryology / Humanities and Social Sciences / Lampreys - anatomy & histology / Lampreys - embryology / Models, Biological / Molecular Sequence Data / multidisciplinary / Musculoskeletal system / Phylogenetics / Phylogeny / Physiological aspects / Science / Vertebrates