The developmental basis for the recurrent evolution of deuterostomy and protostomy

Abstract

The mouth opening of bilaterian animals develops either separate from (deuterostomy) or connected to (protostomy) the embryonic blastopore, the site of endomesoderm internalization. Although this distinction preluded the classification of bilaterian animals in Deuterostomia and Protostomia, and has influenced major scenarios of bilaterian evolution, the developmental basis for the appearance of these different embryonic patterns remains unclear. To identify the underlying mechanisms, we compared the development of two brachiopod species that show deuterostomy (Novocrania anomala) and protostomy (Terebratalia transversa), respectively. We show that the differential activity of Wnt signalling, together with the timing and location of mesoderm formation, correlate with the differential behaviour and fate of the blastopore. We further assess these principles in the spiral-cleaving group Annelida, and propose that the developmental relationships of mouth and blastoporal openings are secondary by-products of variations in axial and mesoderm development. This challenges the previous evolutionary emphasis on extant blastoporal behaviours to explain the origin and diversification of bilaterian animals.

Cleavage modification did not alter blastomere fates during bryozoan evolution

“…This molecular map is similar not only to the typical spiral-cleaving embryos, but also to brachiopod embryos [87, 129], whose embryos have a much greater number of cells and no stereotypic cleavage pattern [164]. Thus, a single cell in the bryozoan embryo expressing gata456 might be homologous to a whole region of gata456 expression in the brachiopod embryo [87], as suggested by Hejnol [5].…”

“…The anterior/foregut markers nk2.1 , foxa , and gsc are expressed in a region opposed to posterior/hindgut markers bra , cdx , evx , and wnt1 , which are generally restricted to the D quadrant. Transcripts of nk2.1 are restricted to the B quadrant in a comparable position, in relation to the cyphonautes anteroposterior axis, to the anterior/ventral expression found in other bilaterians [62, 71, 122, 129, 130]. In a similar fashion, transcripts of wnt1 , a gene commonly expressed at the posterior end of bilaterians [131–134], occur at the posterior region of the vegetal ectoderm of M. membranacea (see also Additional file 18: Table S2 for a comparison of spiralian-specific gene expression patterns).…”

Clustered brachiopod Hox genes are not expressed collinearly and are associated with lophotrochozoan novelties

“…Single colorimetric whole-mount in situ hybridization was carried out following an established protocol (detailed protocol available in Protocol Exchange, 2008; www.nature.com/protocolexchange/ protocols/480) (96,97). Double fluorescence in situ hybridization was conducted as described elsewhere (98,99).…”

Ground plan of the larval nervous system in phoronids: Evidence from larvae of viviparous phoronid

“…The phylogenetic tree is based on the most recent analysis of brachiozoan phylogeny (Cohen, 2013). Furthermore within Brachiopoda, both protostomic and deuterostomic developmental modes are present in relatively closely related genera of brachiopods (e.g., Martín-Durán, Passamaneck, Martindale, & Hejnol, 2016) in stark contrast to the traditional division of animal phylogeny based on this feature of early development, highlighting the probable homoplastic nature of development within this group of organisms and thus consequently caution against the use of this character as phylogenetically informative at the level of resolving deep animal phylogenetic relationships as also pointed out to be the case by the other reviewer with regard to neural development. The bilobed stage has been described in all groups of the Brachiozoa and can be regarded as having the ground plan of larvae in this clade.…”