Wnt gene expression in sea urchin development: heterochronies associated with the evolution of developmental mode.
The Wnt genes encode a large family of conserved secreted proteins that are widely involved in animal development. The variety and ubiquity of this ancient family suggest that Wnt genes may have been important in the evolution of animal development, including early development. To test this hypothesis, we have characterized the expression of several Wnt genes in closely related sea urchins that exhibit radically different modes of early development. Wnt-1, -4, and -5 genes exhibit several conserved molecular and developmental characteristics, both within sea urchins and with Wnt genes examined in other animals (Ferkowicz et al. 1998). Here, we demonstrate that sea urchin Wnt-5 transcripts are specifically detected by in situ hybridization in discrete embryonic, larval, and developing adult tissues and processes: (1) in a band of vegetal ectoderm in mesenchyme blastula stage embryos, (2) in the larval ciliary bands, (3) in tissues that form the early adult rudiment (left coelomic pouch and overlying vestibular ectoderm), and (4) in the developing adult radial nervous system. We find that the sites of Wnt-5 transcript accumulation are conserved in species exhibiting either indirect- or direct-developmental modes, suggesting that Wnt-5 function(s) have been conserved in sea urchin development. However, dramatic heterochronic changes in Wnt-5 gene expression have occurred in the direct-developing species that parallel the accelerated morphological changes that occur during direct development. These results suggest that heterochronic changes in the expression of conserved developmental regulatory genes, such as the Wnt family members, are agents of evolutionary change in animal development.
Ferkowicz
M J
MJ
Indiana Molecular Biology Institute and Department of Biology, Indiana University, Bloomington 47405, USA.
Raff
R A
RA
D000818:Animals; D005075:Biological Evolution; D004527:Egg Proteins / Q000096:biosynthesis; D015870:Gene Expression; D007091:Image Processing, Computer-Assisted; D017403:In Situ Hybridization; D005810:Multigene Family; D009420:Nervous System / Q000196:embryology; D011518:Proto-Oncogene Proteins / Q000096:biosynthesis*; D012333:RNA, Messenger / Q000302:isolation & purification; D012617:Sea Urchins / Q000196:embryology* / Q000235:genetics*; D013045:Species Specificity; D013997:Time Factors; D051153:Wnt Proteins; D051155:Wnt1 Protein; D060528:Wnt4 Protein; D029961:Zebrafish Proteins
D004527:Egg Proteins; D011518:Proto-Oncogene Proteins; D012333:RNA, Messenger; D051153:Wnt Proteins; C491963:Wnt-5 protein, sea urchin; D051155:Wnt1 Protein; D060528:Wnt4 Protein; D029961:Zebrafish Proteins