Quigley Ian K, Turner Jessica M, Nuckels Richard J, Manuel Joan L, Budi Erine H, MacDonald Erin L, Parichy David M
Section of Integrative Biology, Section of Molecular, Cell and Developmental Biology, Institute for Cellular and Molecular Biology, University of Texas at Austin, 1 University Station C0930, Austin, TX 78712, USA.
Development. 2004 Dec;131(24):6053-69. doi: 10.1242/dev.01526. Epub 2004 Nov 10.
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.
神经嵴起源的潜伏前体细胞或干细胞存在于多种胚胎后组织中。尽管这些细胞因其在人类健康和疾病中的作用而具有生物医学研究价值，但其潜在的进化意义却一直未得到充分重视。作为阐明此类细胞对脊椎动物形态进化贡献的第一步，我们研究了斑马鱼成体色素模式进化多样化过程中神经嵴细胞和胚胎后潜伏前体细胞的相对作用。这些色素模式源于源自胚胎神经嵴细胞的胚胎黑素细胞的数量和排列，以及源自假定神经嵴起源的潜伏前体细胞的胚胎后变态黑素细胞。在斑马鱼（Danio rerio）中，幼虫到成体转变期间，通过从潜伏前体细胞募集变态黑素细胞，形成了黑素细胞条纹模式。在新的系统发育数据背景下采用比较方法，我们表明另外五个物种的成体色素模式也源自变态黑素细胞，将其确定为成体色素模式发育的一种祖先模式。相比之下，黑纹斑马（D. nigrofasciatus，斑马鱼的姐妹物种）表面上类似的成体条纹是由胚胎阶段分化的黑素细胞重新组织形成的，变态黑素细胞的贡献较小。遗传镶嵌和分子标记分析揭示了黑纹斑马黑素细胞谱系外部的进化变化，包括变态黑素细胞前体的显著减少。最后，种间互补试验确定了一个候选遗传途径，该途径有助于变态黑素细胞的进化减少以及早期幼虫黑素细胞对黑纹斑马成体色素模式发育的贡献增加。这些结果证明了潜伏前体细胞在斑马鱼色素模式多样化中的重要作用。更普遍地说，胚胎后神经嵴衍生干细胞或其特定后代的部署差异可能对脊椎动物成体形态的进化多样化有重大贡献，特别是在经历变态的物种中。
