Anatomy of the lamprey ear: morphological evidence for occurrence of horizontal semicircular ducts in the labyrinth of Petromyzon marinus

Abstract

In jawed (gnathostome) vertebrates, the inner ears have three semicircular canals arranged orthogonally in the three Cartesian planes: one horizontal (lateral) and two vertical canals. They function as detectors for angular acceleration in their respective planes. Living jawless craniates, cyclostomes (hagfish and lamprey) and their fossil records seemingly lack a lateral horizontal canal. The jawless vertebrate hagfish inner ear is described as a torus or doughnut, having one vertical canal, and the jawless vertebrate lamprey having two. These observations on the anatomy of the cyclostome (jawless vertebrate) inner ear have been unchallenged for over a century, and the question of how these jawless vertebrates perceive angular acceleration in the yaw (horizontal) planes has remained open. To provide an answer to this open question we reevaluated the anatomy of the inner ear in the lamprey, using stereoscopic dissection and scanning electron microscopy. The present study reveals a novel observation: the lamprey has two horizontal semicircular ducts in each labyrinth. Furthermore, the horizontal ducts in the lamprey, in contrast to those of jawed vertebrates, are located on the medial surface in the labyrinth rather than on the lateral surface. Our data on the lamprey horizontal duct suggest that the appearance of the horizontal canal characteristic of gnathostomes (lateral) and lampreys (medial) are mutually exclusive and indicate a parallel evolution of both systems, one in cyclostomes and one in gnathostome ancestors.

Development and Functional Organization of the Cranial Nerves in Lampreys

“…The octaval nerve carries information from the labyrinth sensory organs, which in lampreys mostly consist of two semicircular canal crests, the macula communis and a small macula neglecta (Lowenstein et al, ); nevertheless, in a recent paper (Maklad et al, ), two sets of horizontal semicircular canals were reported in the labyrinth of the adult sea lamprey. However, these canals appear not to be homologous to the gnathostome canals as they are located medially rather than laterally.…”

Gene, cell, and organ multiplication drives inner ear evolution

“…However, while the ear of hagfish is a simple torus with two canal cristae and an elongated gravity sensing common macula (Fig. 3), lampreys have evolved a complicated labyrinth with several unique features including two medial canals that together seem to serve the function of the single lateral canal of jawed vertebrates (Maklad et al, 2014). It appears that several genes drive lateral canal development, as a canal is missing in null mutants of these genes, Otx1 (Fritzsch et al, 2001; Morsli et al, 1999), N-Myc (Domínguez-Frutos et al, 2011; Kopecky et al, 2011) and Lmx1a (Koo et al, 2009; Nichols et al, 2008).…”

Development of the Mammalian ‘Vestibular’ System

“…This ear change seems to coincide with the evolution of lateral fins and neck muscle attachments to the ear (Trinajstic et al, 2013) but also with the reorganization of the lamprey-like organization of eye muscles (Fritzsch et al, 1990) into jawed vertebrate muscles (Young, 2008). Recent evidence suggests that lampreys may have independently evolved a medially located horizontal canal system distinct from the jawed vertebrate lateral horizontal canal system (Maklad et al, 2014). The advantages of one VOR system over the other remain unclear, given that lampreys are very effective predators of bony fish.…”