Abstract
Over the course of evolution, the acquisition of novel structures has ultimately led to wide variation in morphology among extant multicellular organisms. Thus, the origins of genetic systems for new morphological structures are a subject of great interest in evolutionary biology. The larval skeleton is a novel structure acquired in some echinoderm lineages via the activation of the adult skeletogenic machinery. Previously, VEGF signaling was suggested to have played an important role in the acquisition of the larval skeleton. In the present study, we compared expression patterns of Alx genes among echinoderm classes to further explore the factors involved in the acquisition of a larval skeleton. We found that the alx1 gene, originally described as crucial for sea urchin skeletogenesis, may have also played an essential role in the evolution of the larval skeleton. Unlike those echinoderms that have a larval skeleton, we found that alx1 of starfish was barely expressed in early larvae that have no skeleton. When alx1 overexpression was induced via injection of alx1 mRNA into starfish eggs, the expression patterns of certain genes, including those possibly involved in skeletogenesis, were altered. This suggested that a portion of the skeletogenic program was induced solely by alx1. However, we observed no obvious external phenotype or skeleton. We concluded that alx1 was necessary but not sufficient for the acquisition of the larval skeleton, which, in fact, requires several genetic events. Based on these results, we discuss how the larval expression of alx1 contributed to the acquisition of the larval skeleton in the putative ancestral lineage of echinoderms.
Highlights
The current diversity in animal morphology has resulted from the gradual acquisition of novel structures and, occasionally, the loss of existing structures
Two adjacent alx genes have been identified in the sea urchin Strongylocentrotus purpuratus genome [31], suggesting that the genes were derived via tandem duplication
We searched for genes involved in the acquisition of the larval skeleton by identifying genes expressed in sea urchin larval skeletogenic cells that were essential for the development of the larval skeleton but whose starfish orthologs were expressed only in adult skeletogenic cells and not at the embryonic stage
Summary
The current diversity in animal morphology has resulted from the gradual acquisition of novel structures and, occasionally, the loss of existing structures. Sea cucumber larvae have small spicules, a larval skeleton is generally accepted to be a derived structure, and the common ancestors of echinoderms are thought not to have possessed such a skeleton; the ancestral condition is retained by crinoids and (possibly) starfish [7]. This idea is consistent with the absence of a larval skeleton in hemichordate acorn worms, the sister group to the echinoderms [8,9,10]
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