Pigment pattern evolution by differential deployment of neural crest and post-embryonic melanophore lineages inDaniofishes

Abstract

Latent precursors or stem cells of neural crest origin are present in a variety of post-embryonic tissues. Although these cells are of biomedical interest for roles in human health and disease, their potential evolutionary significance has been underappreciated. As a first step towards elucidating the contributions of such cells to the evolution of vertebrate form, we investigated the relative roles of neural crest cells and post-embryonic latent precursors during the evolutionary diversification of adult pigment patterns in Danio fishes. These pigment patterns result from the numbers and arrangements of embryonic melanophores that are derived from embryonic neural crest cells, as well as from post-embryonic metamorphic melanophores that are derived from latent precursors of presumptive neural crest origin. In the zebrafish D. rerio, a pattern of melanophore stripes arises during the larval-to-adult transformation by the recruitment of metamorphic melanophores from latent precursors. Using a comparative approach in the context of new phylogenetic data, we show that adult pigment patterns in five additional species also arise from metamorphic melanophores, identifying this as an ancestral mode of adult pigment pattern development. By contrast, superficially similar adult stripes of D. nigrofasciatus (a sister species to D. rerio) arise by the reorganization of melanophores that differentiated at embryonic stages, with a diminished contribution from metamorphic melanophores. Genetic mosaic and molecular marker analyses reveal evolutionary changes that are extrinsic to D. nigrofasciatus melanophore lineages, including a dramatic reduction of metamorphic melanophore precursors. Finally, interspecific complementation tests identify a candidate genetic pathway for contributing to the evolutionary reduction in metamorphic melanophores and the increased contribution of early larval melanophores to D. nigrofasciatus adult pigment pattern development. These results demonstrate an important role for latent precursors in the diversification of pigment patterns across danios. More generally, differences in the deployment of post-embryonic neural crest-derived stem cells or their specified progeny may contribute substantially to the evolutionary diversification of adult form in vertebrates, particularly in species that undergo a metamorphosis.

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.…”

The genetic covariance between life cycle stages separated by metamorphosis

“…Since the early development of the adaptive decoupling hypothesis, empirical studies have been designed to prove or disprove adaptive decoupling by examining genetic correlations for traits on the same side of metamorphosis and traits separated by metamorphosis [9,10,54], or by examining the stage, or stages in which genes with specific functions are expressed [11,12,55]. Although these studies show that adaptive decoupling and developmental constraints across the metamorphic boundary exist, the evolutionary consequences of genetic associations across metamorphosis still remain uncertain.…”

“…Accordingly, the adaptive decoupling hypothesis for the benefits of metamorphosis [4] predicts that traits separated by metamorphosis should be genetically uncorrelated, thereby allowing evolutionary change to occur within each stage, without corresponding effects on phenotypes expressed in other stages. Studies that have tested this prediction by examining genetic associations across metamorphosis have found contradictory results [9][10][11][12], and so the relevance of the & 2014 The Author(s) Published by the Royal Society. All rights reserved.…”

Evolution of danio pigment pattern development

“…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.…”

“…By contrast, adult D. rerio have 4-6 stripes of melanophores that do not correspond topologically to the earlier larval stripes; xanthophores are abundant between melanophore stripes and iridophores are found across the entire flank. That other danios have larval patterns virtually indistinguishable from D. rerio despite their very different adult pigment patterns (Quigley et al, 2004) suggests that pigment patterns are uncoupled both evolutionarily and developmentally across stages.…”