Abstract
BackgroundThe digestive systems of animals can become highly specialized in response to their exploration and occupation of new ecological niches. Although studies on different animals have revealed commonalities in gut formation, the model systems Caenorhabditis elegans and Drosophila melanogaster, which belong to the invertebrate group Ecdysozoa, exhibit remarkable deviations in how their intestines develop. Their morphological and developmental idiosyncrasies have hindered reconstructions of ancestral gut characters for the Ecdysozoa, and limit comparisons with vertebrate models. In this respect, the phylogenetic position, and slow evolving morphological and molecular characters of marine priapulid worms advance them as a key group to decipher evolutionary events that occurred in the lineages leading to C. elegans and D. melanogaster.ResultsIn the priapulid Priapulus caudatus, the gut consists of an ectodermal foregut and anus, and a mid region of at least partial endodermal origin. The inner gut develops into a 16-cell primordium devoid of visceral musculature, arranged in three mid tetrads and two posterior duplets. The mouth invaginates ventrally and shifts to a terminal anterior position as the ventral anterior ectoderm differentially proliferates. Contraction of the musculature occurs as the head region retracts into the trunk and resolves the definitive larval body plan. Despite obvious developmental differences with C. elegans and D. melanogaster, the expression in P. caudatus of the gut-related candidate genes NK2.1, foxQ2, FGF8/17/18, GATA456, HNF4, wnt1, and evx demonstrate three distinct evolutionarily conserved molecular profiles that correlate with morphologically identified sub-regions of the gut.ConclusionsThe comparative analysis of priapulid development suggests that a midgut formed by a single endodermal population of vegetal cells, a ventral mouth, and the blastoporal origin of the anus are ancestral features in the Ecdysozoa. Our molecular data on P. caudatus reveal a conserved ecdysozoan gut-patterning program and demonstrates that extreme morphological divergence has not been accompanied by major molecular innovations in transcriptional regulators during digestive system evolution in the Ecdysozoa. Our data help us understand the origins of the ecdysozoan body plan, including those of C. elegans and D. melanogaster, and this is critical for comparisons between these two prominent model systems and their vertebrate counterparts.Electronic supplementary materialThe online version of this article (doi:10.1186/s12915-015-0139-z) contains supplementary material, which is available to authorized users.
Highlights
The digestive systems of animals can become highly specialized in response to their exploration and occupation of new ecological niches
In P. caudatus, gastrulation occurs at the vegetal pole [35], and after endomesoderm ingression, the embryo shows an obliterated archenteron, and a narrowed blastopore that corresponds to the future anal opening of the digestive tract [34]
Anteroposterior patterning of the digestive tract of P. caudatus To characterize in greater detail the specification and formation of the different gut regions, we identified and studied the expression patterns of the anterior/foregut markers NK2.1, foxQ2, and FGF8/17/18; the midgut markers GATA456 and hepatocyte nuclear factor 4 (HNF4); and the posterior/hindgut markers wnt1 and evx (Figure 5)
Summary
The digestive systems of animals can become highly specialized in response to their exploration and occupation of new ecological niches. Studies on different animals have revealed commonalities in gut formation, the model systems Caenorhabditis elegans and Drosophila melanogaster, which belong to the invertebrate group Ecdysozoa, exhibit remarkable deviations in how their intestines develop Their morphological and developmental idiosyncrasies have hindered reconstructions of ancestral gut characters for the Ecdysozoa, and limit comparisons with vertebrate models. Jaws, and proboscides to capture and grind food, stomachs and digestive glands to process nutrients, and cloacae to release excretory products are just a few examples of the specializations exhibited by animal digestive systems Despite this diversity in gut architecture and complexity, the comparative study of different bilaterian animals has revealed commonalities in the early ontogenetic stages of gut formation, and a handful of genes have been related to the specification and initial development of the digestive system [3,4,5,6]. The way in which the gut forms may significantly change as organisms undergo developmental adaption in response to de novo habitat colonization [8,9,10]
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