Reinvestigating the early embryogenesis in the flatworm Maritigrella crozieri highlights the unique spiral cleavage program found in polyclad flatworms

Johannes Girstmair,Maximilian J Telford

doi:10.1186/s13227-019-0126-5

Abstract

BackgroundSpiral cleavage is a conserved, early developmental mode found in several phyla of Lophotrochozoans resulting in highly diverse adult body plans. While the cleavage pattern has clearly been broadly conserved, it has also undergone many modifications in various taxa. The precise mechanisms of how different adaptations have altered the ancestral spiral cleavage pattern are an important ongoing evolutionary question, and adequately answering this question requires obtaining a broad developmental knowledge of different spirally cleaving taxa. In flatworms (Platyhelminthes), the spiral cleavage program has been lost or severely modified in most taxa. Polyclad flatworms, however, have retained the pattern up to the 32-cell stage. Here we study early embryogenesis of the cotylean polyclad flatworm Maritigrella crozieri to investigate how closely this species follows the canonical spiral cleavage pattern and to discover any potential deviations from it.ResultsUsing live imaging recordings and 3D reconstructions of embryos, we give a detailed picture of the events that occur during spiral cleavage in M. crozieri. We suggest, contrary to previous observations, that the four-cell stage is a product of unequal cleavages. We show that that the formation of third and fourth micromere quartets is accompanied by strong blebbing events; blebbing also accompanies the formation of micromere 4d. We find an important deviation from the canonical pattern of cleavages with clear evidence that micromere 4d follows an atypical cleavage pattern, so far exclusively found in polyclad flatworms.ConclusionsOur findings highlight that early development in M. crozieri deviates in several important aspects from the canonical spiral cleavage pattern. We suggest that some of our observations extend to polyclad flatworms in general as they have been described in both suborders of the Polycladida, the Cotylea and Acotylea.

Highlights

Spiral cleavage is a conserved, early developmental mode found in several phyla of Lophotrochozoans resulting in highly diverse adult body plans
We noted that second cleavages were slightly asynchronous, which explains the occasional observation of embryos in a three-cell stage before the formation of four sized blastomeres takes place
We have been able to look at connections between nuclear movements and cell divisions and link them with cellular dynamics such as cell blebbing, and pinpoint important developmental events like symmetry breaking

Summary

Introduction

Spiral cleavage is a conserved, early developmental mode found in several phyla of Lophotrochozoans resulting in highly diverse adult body plans. The Lophotrochozoa is one of two major clades of protostomes, sister group of the Ecdysozoa [1, 14, 23, 27, 59] It contains approximately a dozen morphologically diverse and mostly marine phyla. Representative lophotrochozoan phyla with spiral cleavage comprise annelids, molluscs, nemerteans, flatworms, phoronids and entoprocts [30, 40], and recent phylogenetic results show that these spirally cleaving phyla form a clade within the Lophotrochozoa [49]. The fact that spiral cleavage has been maintained in these animals since they diverged in the early Cambrian, over half a billion years ago, argues that selection for maintaining spiral cleavage exists

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