Evolutionary diversification of pigment pattern inDaniofishes:differentialfmsdependence and stripe loss inD. albolineatus

Abstract

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 fmsmutants 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 fmsrequirements 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 fmsactivity 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. albolineatusresults 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.

Phylogenetic relationships of Danio within the order Cypriniformes: a framework for comparative and evolutionary studies of a model species

“…''panther,'' D. roseus, D. sp. ''hikari,'' D. choprai, and D. erythromicron (Quigley et al, 2004(Quigley et al, , 2005. Our phylogenetic analyses indicate that comparisons of Danio with species of Devario and/or Esomus may be misleading because they are not as closely related as once thought.…”

Evolution of danio pigment pattern development

“…This approach was applied recently to D. albolineatus, in which an adult stripe pattern has been lost evolutionarily (Figure 1, 4d). This species has far fewer melanophores than D. rerio particularly during late stages of metamorphosis, when the kit-independent melanophores develop in D. rerio (Quigley et al, 2005). Moreover, interspecific complementation tests identified csf1r or its pathway as candidates for contributing to this difference in melanophore number and patterning between species (Parichy and Johnson, 2001).…”

“…The same principle can be applied to species differences (Long et al, 1996;Sucena et al, 2003). Hybrids between D. rerio and other danios typically resemble D. rerio (Figure 1) (Parichy and Johnson, 2001;Quigley et al, 2005); this result is especially dramatic for species with uniform pigment patterns, or vertical bars, in which hybrids instead develop horizontal stripes! Alleles of pigment pattern genes in other species thus are often recessive to those of D. rerio, a fact that can be exploited to test whether a gene identified as a D. rerio mutant might also differ in its activity between species.…”

“…For studies of pigment pattern development and evolution, D. rerio also is convenient because its relatives have a diverse array of pigment patterns (Fang, 1998;McClure, 1999;Fang and Kottelat, 2000;Quigley and Parichy, 2002;Quigley et al, 2004;Quigley et al, 2005). Figures 1 and 2 show examples of some of these pigment patterns as well as inferred phylogenetic relationships among some of the many species within the group.…”

“…Teleost pigment patterns thus reflect the spatial arrangements of the different chromatophore classes themselves, and the pigments serve as cell autonomous markers of their respective cell types. Interestingly, erythrophores are present in some but not all danio species and appear to have arisen or been lost independently across taxa (McClure, 1999;Quigley et al, 2005). The cell lineage relationships among different pigment cell classes are only poorly understood.…”