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Early blastomere determines embryo proliferation and caste fate in a polyembryonic wasp

Abstract

Polyembryonic development is a unique mode of metazoan development in which a single zygote generates multiple embryos by clonal proliferation1. The polyembryonic parasitic insect Copidosoma floridanum shows one of the most extreme cases of polyembryony, producing up to 2,000 embryos from a single egg. In addition, this wasp exhibits an unusual polyphenism, producing two morphologically distinct larval castes, termed precocious and reproductive, that develop clonally from the same zygote2. This form of development seems incompatible with a model of insect development in which maternal pre-patterning of the egg specifies embryonic axial polarity3. Here we show that maternal pre-patterning in the form of germ plasm creates cellular asymmetry at the four-cell stage embryo of Copidosoma that is perpetuated throughout development. Laser ablations of cells show that the cell inheriting the germ plasm regulates both the fate and proliferation of the reproductive caste. Thus, we have uncovered a new mechanism of caste specification, mediated by the regulatory capacity of a single cell. This study shows that the evolution of mammalian-like regulative development of an insect embryo relies on a novel cellular context that might ultimately enhance developmental plasticity.

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Figure 1: Life cycle of Copidosoma, alignment and phylogram of CfVasa amino acid sequences.
Figure 2: Cfvasa mRNA and protein expression patterns during Copidosoma embryogenesis.
Figure 3: Cfvasa mRNA and protein expression patterns during Copidosoma precocious larvae morphogenesis (purple, mRNA; red, Vasa protein; green, tubulin).
Figure 4: Cell ablation of four-cell stage Copidosoma embryo.

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Acknowledgements

We are thankful to L. Nagy for the idea of performing embryo transplantation into host eggs; E. Zhurov for expert embryo transplantation; P. Lasko, L. Nagy, L. Dickinson, T. Reavell, T. Drysdale, P. Wigge and G. Velicer for critical reading of the manuscript; E. Zhurov and I. Craig for the artwork; J. Whistlecraft, L. Verdon and N. Terzin for Copidosoma rearing; and R. Kulperger for the statistical analysis. M.G. thanks V. Grbić and Ž. Srdić for introducing him to parasitic wasps. This work was supported by grants from the Canadian Foundation of Innovation, Premier's Research Excellence Award and National Science and Engineering Research Council to M.G.

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Correspondence to Miodrag Grbić.

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Supplementary information

Copidosoma embryo movements: in vitro embryo culture

Time-lapse of early Copidosoma primary morula movement in in vitro embryo culture. Digital image capture was performed every 1 minute over 2 hours. (MOV 1331 kb)

Multiple sequence alignment of Vasa proteins

Multiple sequence alignment of Vasa proteins used for phylogenetic analysis of Copidosoma Vasa amino acid sequence in CLUSTAL W format. Below the compared sequences, identical amino acids are denoted by an asterisk (*), conserved amino acids are denoted by a colon (:), and semi-conserved amino acids by a period (.). Alignment was manually edited. (PDF 10 kb)

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Zhurov, V., Terzin, T. & Grbić, M. Early blastomere determines embryo proliferation and caste fate in a polyembryonic wasp. Nature 432, 764–769 (2004). https://doi.org/10.1038/nature03171

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