Abstract
The diverse and complex developmental mechanisms of segmentation have been more thoroughly studied in arthropods, vertebrates and annelids—distantly related animals considered to be segmented. Far less is known about the role of “segmentation genes” in organisms that lack a segmented body. Here we investigate the expression of the arthropod segment polarity genes engrailed, wnt1 and hedgehog in the development of brachiopods—marine invertebrates without a subdivided trunk but closely related to the segmented annelids. We found that a stripe of engrailed expression demarcates the ectodermal boundary that delimits the anterior region of Terebratalia transversa and Novocrania anomala embryos. In T. transversa, this engrailed domain is abutted by a stripe of wnt1 expression in a pattern similar to the parasegment boundaries of insects—except for the expression of hedgehog, which is restricted to endodermal tissues of the brachiopod embryos. We found that pax6 and pax2/5/8, putative regulators of engrailed, also demarcate the anterior boundary in the two species, indicating these genes might be involved in the anterior patterning of brachiopod larvae. In a comparative phylogenetic context, these findings suggest that bilaterians might share an ancestral, non-segmental domain of engrailed expression during early embryogenesis.
Highlights
Referred to as segment polarity genes[21,22,23], and their expression and function is conserved among the body segments of other arthropods[7,24,25,26]
To investigate the developmental and molecular features of the boundaries in brachiopod embryos, we studied the trilobed larva of Terebratalia transversa[36], and the bilobed larva of Novocrania anomala[33,37], species that belong to distinct brachiopod lineages (Fig. 1b)
It has been hypothesized that planktotrophy is ancestral for the Brachiopoda[48] and that larvae of rhynchonelliforms and craniiforms might have evolved a lecithotrophic mode of development independently[49,50]
Summary
Referred to as segment polarity genes[21,22,23], and their expression and function is conserved among the body segments of other arthropods[7,24,25,26]. The discovery of a brachiopod larvae with serially arranged coelomic sacs[33] has revived the idea that brachiopods had a segmented ancestor[34,35] These putative segmented structures, and the closer phylogenetic position to annelids, place brachiopods as an interesting group to test the involvement of the segment polarity genes in other developmental boundaries, and to better comprehend the evolution of segmentation mechanisms in protostomes. To investigate the developmental and molecular features of the boundaries in brachiopod embryos, we studied the trilobed larva of Terebratalia transversa[36], and the bilobed larva of Novocrania anomala[33,37], species that belong to distinct brachiopod lineages (Fig. 1b) In these two species, we analyzed the expression of the segment polarity genes en, wnt[1], and the core components of the Hedgehog signaling pathway to test whether their expression correlate with the development of the ectodermal and mesodermal boundaries of T. transversa and N. anomala larvae. We examined upstream control genes of en and discovered similarities between the molecular profile of a brachiopod larval boundary and the embryonic patterning of anterior boundaries in deuterostomes, such as the hemichordate collar/trunk boundary and the vertebrate fore/midbrain boundary, further suggesting a non-segmental ancestral role of en for bilaterians
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