Journal
DEVELOPMENT
Volume 132, Issue 1, Pages 89-104Publisher
COMPANY OF BIOLOGISTS LTD
DOI: 10.1242/dev.01547
Keywords
Zebrafish; Pigment pattern; morphogenesis; neural crest; fms; Csflr; xanthophore; melanophore; phylogeny; evolution
Categories
Funding
- NATIONAL INSTITUTE OF GENERAL MEDICAL SCIENCES [R01GM062182] Funding Source: NIH RePORTER
- NIGMS NIH HHS [R01 GM62182, R01 GM062182] Funding Source: Medline
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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 melarrophores and cells of the xanthophore lineage that depend on the fms receptor tyrosine kinase; zebrafish fins 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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