Flatfish: An Asymmetric Perspective on Metamorphosis - Current Topics in Developmental Biology - page 168

morphology ( Policansky, 1982b ). The higher incidences of reversal in
the above flounders in cultured versus wild populations may suggest that
in at least some populations and ecological settings reversed flounder may
be selected against in nature for reasons that still remain unknown.
During embryogenesis, all vertebrates display directional asymmetry in
the placement of internal organs ( Hamada et al., 2002; Levin, 2005 ), as well
as morphological asymmetries in the paired habenulae, pineal, and par-
apineal glands of the brain's dorsal diencephalon (epithalamus) ( Concha &
Wilson, 2001 ). Asymmetric development of the epithalamus, heart, and
gut during embryogenesis has been shown to be controlled by expression
of the nodal-lefty-pitx2 (NLP) pathway on the left side of their embryonic
primordia in both the zebrafish ( Danio rerio ) (see reviews by Concha,
Signore, & Colombo, 2009 and Snelson & Gamse, 2009 ) and the Japanese
flounder ( P. olivaceus )( Hashimoto et al., 2002, 2007; Suzuki et al., 2009 ).
Interestingly, about 2 weeks following embryogenesis, pitx2 has been found
to be re-expressed asymmetrically on the left side of the habenulae of nearly
metamorphic flounder larvae in both P. olivaceus (a sinistral flatfish) and the
spotted halibut ( Verasper variegatus , a dextral flatfish) ( Suzuki et al., 2009 ).
The same study observed that during metamorphosis flatfish habenulae un-
dergo two distinct forms of asymmetric morphological development: (1)
volumetric asymmetry, where the right habenula grows larger than the left
in both sinistral and dextral flatfish species and (2) positional asymmetry,
where in sinistral species the migration of the right eye is accompanied by
a rightward movement of the habenulae along the ventral diencephalon,
and in dextral species the migration of the left eye is accompanied by a left-
ward movement of the habenulae (refer to Fig. 6.4 A-D). Whereas many fish
species are known to display volumetric asymmetry of the habenulae
( Concha & Wilson, 2001 ), the metamorphic development of such a dra-
matic positional asymmetry of the habenulae has to date only been reported
for flatfish. It is not yet clear whether asymmetric positional development of
the habenulae plays an active or a permissive role in facilitating metamorphic
skull remodeling and eye migration.
Hashimoto et al. (2002) have isolated a Japanese flounder clonal line,
reversed ( rev ), in which more than half of homozygous offspring derived from
rev expressed the normally left-specific marker pitx2 bilaterally in the
lateral plate mesoderm (LPM) of embryos ( Fig. 6.5 ). As reversal of gut
coiling was observed at a high frequency in rev juveniles, and also consider-
ing that abnormal pitx2 expression in the LPM has been shown to corre-
spond with reversed visceral organ asymmetry in other vertebrates