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Inner ear development in cyclostomes and evolution of the vertebrate semicircular canals
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Journal Article
Inner ear development in cyclostomes and evolution of the vertebrate semicircular canals
2019
Overview
Jawed vertebrates have inner ears with three semicircular canals, the presence of which has been used as a key to understanding evolutionary relationships. Ostracoderms, the jawless stem gnathostomes, had only two canals and lacked the lateral canal
1
–
3
. Lampreys, which are modern cyclostomes, are generally thought to possess two semicircular canals whereas the hagfishes—which are also cyclostomes—have only a single canal, which used to be regarded as a more primitive trait
1
,
4
. However, recent molecular and developmental analyses have strongly supported the monophyly of cyclostomes
5
–
7
, which has left the evolutionary trajectory of the vertebrate inner ear unclear
8
. Here we show the differentiation of the otic vesicle of the lamprey
Lethenteron camtschaticum
and inshore hagfish
Eptatretus burgeri
. This is the first time, to our knowledge, that the development of the hagfish inner ear is reported. We found that canal development in the lamprey starts with two depressions—which is reminiscent of the early developmental pattern of the inner ear in modern gnathostomes. These cyclostome otic vesicles show a pattern of expression of regulatory genes, including OTX genes, that is comparable to that of gnathosomes. Although two depressions appear in the lamprey vesicle, they subsequently fuse to form a single canal that is similar to that of hagfishes. Complete separation of the depressions results in anterior and posterior canals in gnathostomes. The single depression of the vesicle in hagfishes thus appears to be a secondarily derived trait. Furthermore, the lateral canal in crown gnathostomes was acquired secondarily—not by de novo acquisition of an OTX expression domain, but by the evolution of a developmental program downstream of the OTX genes.
The differentiation of the inner ear in the lamprey
Lethenteron camtschaticum
and hagfish
Eptatretus burgeri
sheds light on the evolution of the semicircular canals of jawed vertebrates.
Publisher
Nature Publishing Group UK,Nature Publishing Group
Subject
/ 14
/ 14/19
/ 38
/ 38/1
/ 38/77
/ Analysis
/ Animals
/ Canals
/ Cysts
/ Ear
/ Fish
/ Gene Expression Regulation, Developmental
/ Genes
/ Hagfishes - anatomy & histology
/ Humanities and Social Sciences
/ Lampreys - anatomy & histology
/ Letter
/ Myxini
/ Science
/ Semicircular Canals - anatomy & histology
/ Semicircular Canals - embryology
/ Sharks - anatomy & histology
/ Vertebrates - anatomy & histology
