Evolutionary diversification of pigment pattern in Danio fishes:differential fms dependence and stripe loss in D.albolineatus
2004
The developmental bases for species differences in adult phenotypes remain
largely unknown. An emerging system for studying such variation is the adult
pigment pattern expressed by Danio fishes. These patterns result from
several classes of pigment cells including black melanophores and yellow
xanthophores, which differentiate during metamorphosis from latent stem cells
of presumptive neural crest origin. In the zebrafish D. rerio ,
alternating light and dark horizontal stripes develop, in part, owing to
interactions between melanophores and cells of the xanthophore lineage that
depend on the fms receptor tyrosine kinase; zebrafish fms
mutants lack xanthophores and have disrupted melanophore stripes. By contrast,
the closely related species D. albolineatus exhibits a uniform
pattern of melanophores, and previous interspecific complementation tests
identified fms as a potential contributor to this difference between
species. Here, we survey additional species and demonstrate marked variation
in the fms -dependence of hybrid pigment patterns, suggesting
interspecific variation in the fms pathway or fms
requirements during pigment pattern formation. We next examine the cellular
bases for the evolutionary loss of stripes in D. albolineatus and
test the simplest model to explain this transformation, a loss of fms
activity in D. albolineatus relative to D. rerio . Within
D. albolineatus , we demonstrate increased rates of melanophore death
and decreased melanophore migration, different from wild-type D.
rerio but similar to fms mutant D. rerio . Yet, we also
find persistent fms expression in D. albolineatus and
enhanced xanthophore development compared with wild-type D. rerio ,
and in stark contrast to fms mutant D. rerio . These findings
exclude the simplest model in which stripe loss in D. albolineatus
results from a loss of fms -dependent xanthophores and their
interactions with melanophores. Rather, our results suggest an alternative
model in which evolutionary changes in pigment cell interactions themselves
have contributed to stripe loss, and we test this model by manipulating
melanophore numbers in interspecific hybrids. Together, these data suggest
evolutionary changes in the fms pathway or fms requirements,
and identify changes in cellular interactions as a likely mechanism of
evolutionary change in Danio pigment patterns.
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