Asymmetrical development of bones and soft tissues during eye migration of metamorphosing Japanese flounder, Paralichthys olivaceus

Abstract

The symmetrical body of flatfish larvae dramatically changes into an asymmetrical form after metamorphosis. Eye migration results in the most significant asymmetrical development seen in any vertebrate. To understand the mechanisms involved in eye migration, bone and cartilage formation was observed during metamorphosis in laboratory-reared Japanese flounder, Paralichthys olivaceus, by using whole-body samples and histological sections. Most of the hard tissues of the cranium (parasphenoid, trabecular cartilage, supraorbital canal, and supraorbital bar) exist symmetrically in the larval period before metamorphosis and develop by twisting in the same direction as that in which the eye migrates. An increase in skin thickness beneath the eye was observed only on the blind side at the beginning of eye migration; this was the first definitive difference between the right and left sides of the body. The pseudomesial bar, a peculiar bone present only in flatfishes, developed from this thick skin and grew dorsad. Novel sac-like structures were found and named retrorbital vesicles. The retrorbital vesicle of the blind side grew larger and faster than that of the ocular side when the right eye moved most dramatically, whereas no difference was observed between the volume of right and left connective tissue in the head. The asymmetrical presence and growth of the pseudomesial bar together with inflation of the retrorbital vesicle on the blind side may be responsible for right eye migration during metamorphosis in the Japanese flounder.

Embryonic and larval staging of summer flounder (paralichthys dentatus)

“…At this stage resorption of soft tissues and of the supraorbital bar that initially separates the two eyes, as well as thickening of the skin under the migrating eye, have already begun (Okada et al, 2001). Asymmetry of the head skeleton appears remarkably late in its development (Wagemans et al, 1998;Okada et al, 2001). We saw no structural asymmetry in cleared and stained summer flounder before Stage F, in accordance with recent observations in Japanese flounder larvae (Okada et al, 2001).…”

“…However, length and age do not consistently correlate with degree of development, or with the maturation of particular organ systems (Norman, 1934;Brewster, 1987;Seikai, 1992;Okada et al, 2001). Environmental effects on developmental timing and size in flatfishes are well-documented even under relatively uniform hatchery conditions (Bisbal and Bengtson, 1995b;Bengtson, 1999;Bengtson and Gleason, 1999;van Maaren and Daniels, 2000).…”

“…The earliest developmental events in preparation for eye migration occur at Stage E, before the migrating eye has begun to move. At this stage resorption of soft tissues and of the supraorbital bar that initially separates the two eyes, as well as thickening of the skin under the migrating eye, have already begun (Okada et al, 2001). Asymmetry of the head skeleton appears remarkably late in its development (Wagemans et al, 1998;Okada et al, 2001).…”

“…When the fish are approximately a month old, they undergo a massive morphological reorganization that includes the development of profound differences between the right and left sides of the body (Norman, 1934;Brewster, 1987;Seikai, 1992;Okada et al, 2001).…”

Asymmetric craniofacial remodeling and lateralized behavior in larval flatfish

“…It has generally been assumed that the unique asymmetries characteristic of adult flatfish develop during metamorphosis (Youson, 1988), and the phenomenology of asymmetric flatfish skull development and eye migration during this period has been widely documented (Brewster, 1987;Okada et al, 2001;Okada et al, 2003a;Okada et al, 2003b;Saele et al, 2004;Wagemans et al, 1998). However, the possibility that metamorphic laterality is preceded by subtle larval asymmetry has not been explored.…”