Abstract
The Wnt genes represent a large family of secreted glycoprotein ligands that date back to early animal evolution. Multiple duplication events generated a set of 13 Wnt families of which 12 are preserved in protostomes. Embryonic Wnt expression patterns (Wnt-patterning) are complex, representing the plentitude of functions these genes play during development. Here, we comprehensively investigated the embryonic expression patterns of Wnt genes from three species of spiders covering both main groups of true spiders, Haplogynae and Entelegynae, a mygalomorph species (tarantula), as well as a distantly related chelicerate outgroup species, the harvestman Phalangium opilio. All spiders possess the same ten classes of Wnt genes, but retained partially different sets of duplicated Wnt genes after whole genome duplication, some of which representing impressive examples of sub- and neo-functionalization. The harvestman, however, possesses a more complete set of 11 Wnt genes but with no duplicates. Our comprehensive data-analysis suggests a high degree of complexity and evolutionary flexibility of Wnt-patterning likely providing a firm network of mutational protection. We discuss the new data on Wnt gene expression in terms of their potential function in segmentation, posterior elongation, and appendage development and critically review previous research on these topics. We conclude that earlier research may have suffered from the absence of comprehensive gene expression data leading to partial misconceptions about the roles of Wnt genes in development and evolution.
Highlights
Wnt genes are important for the regulation of many aspects of animal development
Loss of Wnt genes is common among arthropods [21, 30, 39], which is most obvious in model insects like Drosophila melanogaster and Tribolium castaneum that have only retained seven and nine Wnt genes, respectively
The apparent loss of a second Wnt4 gene in Pholcus may be representative for Haplogynae as a whole as we could not identify a second copy in the published genome of another basally branching haplogyne spider, the recluse Loxosceles reclusa
Summary
Wnt genes are important for the regulation of many aspects of animal development They encode secreted glycoprotein ligands that bind to different families of transmembrane receptors such as Frizzled and LRP5/6 Binding of Wnt molecules to their dedicated receptors activates intracellular signaling cascades that regulate target gene transcription (reviewed in e.g., [69, 88, 78]). The last common ancestor of arthropods possessed 12 Wnt genes. Other arthropods have retained representatives of most (e.g., the myriapods Glomeris marginata and Strigamia maritima, and the spider Parasteatoda tepidariorum) or all (the crustacean Daphnia pulex) of the 12 Wnt families found in arthropods [22, 39]. Some Wnt genes are represented by two paralogs, the result of a whole genome duplication (WGD) that took place in the lineage
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