Gb_PGCs_merge_flat

Animal germ cells can be specified during embryogenesis by inheriting maternal determinants present in the egg, by receiving inductive signals from neighbouring cells, or potentially by some complex combination of the two mechanisms. Many well-established laboratory model organisms use the inheritance mechanism. However, our literature survey of the entire animal tree of life, and our empirical work developing and applying new genetic resources to a broad range of non-traditional model organisms, showed that genes encoding maternal germ line determinants in Drosophila, Caenorhabditis elegans, zebrafish and Xenopus, were entirely dispensable for germ line establishment in many animals.

We showed that the cricket Gryllus bimaculatus establishes its germ line not with inherited determinants like Drosophila, but with the same inductive mechanism as mice, namely BMP-mediated activation of a germ line regulatory program driven by the transcription factor Blimp-1. This provided the first experimental evidence for inductive germ cell specification in any invertebrate.

Ultimately, we propose that the inductive mechanism was much more prevalent across animals than previously believed, and that such a mechanism likely specified germ cells in the last common animal ancestor. This work shows that developmental mechanisms used by popular model organisms are not necessarily ancestral nor generalizable, but rather may be independently evolved and highly derived. Only by continuing to expand taxon sampling and perform functional genetic experiments across more organisms, will we be able to understand the evolutionary origins and diversification patterns of such crucial developmental processes.

Current ongoing work in this area includes examining the functional evolution of multiple genes involved in animal germ line formation and function, from germ cell specification through migration and gametogenesis.

References

oskar acts with the transcription factor Creb to regulate long-term memory in crickets. Arpita Kulkarni, Ben Ewen-Campen, Kanta Terao, Yukihisa Matsumoto, Yaolong Li, Takayuki Watanabe, Jonchee A. Kao, Swapnil S. Parhad, Guillem Ylla, Makoto Mizunami and Cassandra G. Extavour PNAS, 120 (21) e2218506120 (2023). [PubMed]
Null hypotheses for developmental evolution. Church, S.H. and Extavour, C.G. Development, 147(8):dev178004 (2020). [PubMed]
Hox genes limit germ cell formation in the short germ insect Gryllus bimaculatus. Barnett, A.A., Nakamura, T. and Extavour, C.G.* PNAS, 116(33):16430-16435 (2019). [PubMed]
Convergent evolution of germ granule nucleators: a hypothesis. Kulkarni, A. and Extavour, C.G. Stem Cell Research, 24: 188-194 (2017). [PubMed]
Causes and evolutionary consequences of primordial germ cell specification mode in metazoans. Whittle, C.A. and Extavour, C.G. Proceedings of the National Academy of Sciences of the USA, 114(23): 5784-5791 (2017). [PubMed]
Refuting the hypothesis that the acquisition of germ plasm accelerates animal evolution. Whittle, C.A. and Extavour, C.G. Nature Communications, 7, 12637 (2016). [PubMed]
A premeiotic function for boule in the planarian Schmidtea mediterranea. Iyer, H., Issigonis, M., Sharma, P.P., Extavour, C.G. and Newmark, P.A. PNAS, 113(25): E3509-18 (2016). [PubMed]
The transcriptional repressor Blimp-1 acts downstream of BMP signaling to generate primordial germ cells in the cricket Gryllus bimaculatus.. Nakamura, T. and Extavour, C.G. Development 143(2), 255-263 (2016). [PubMed]
vasa and piwi are required for mitotic integrity in early embryogenesis in the spider Parasteatoda tepidariorum. Schwager, E.E., Meng, Y. and Extavour, C.G. Developmental Biology, 402(2): 276-290 (2015). [PubMed]
The significance and scope of evolutionary developmental biology: a vision for the 21st century. Moczek, A., Sears, K., Stollewerk, A., Wittkopp, P., Diggle, P., Dworkin, I., Ledon-Rettig, C., Matus, D., Roth, S., Abouheif, E., Brown, F. Chiu, C.-H., Cohen, C.S., De Tomaso, T., Gilbert, S., Hall, B., Love, A., Lyons, D., Sanger, T., Smith, J., Specht, C., Vallejo-Marin, M. and Extavour, C.G. Evolution and Development, 17(3): 198-219 (2015). [PubMed]
BMP signaling is required for generation of primordial germ cells in an insect. Donoughe, S., Nakamura, T., Ewen-Campen, B., Green II, D.A., Henderson, L. and Extavour, C.G Proceedings of the National Academy of Sciences of the USA, 111(11): 4133-4138 (2014). [PubMed]
Identification of a putative germ plasm in the crustacean Parhyale hawaiensis. Gupta, T. and Extavour, C.G. EvoDevo, 4(1): 34 (2013). [PubMed]
Evidence against a germ plasm in the milkweed bug Oncopeltus fasciatus, a hemimetabolous insect. Ewen-Campen, B.*, Jones, T.E.*. and Extavour, C.G. Biology Open, 2(6): 556-568 (2013). [PubMed]
Germ Cell Specification Requires Zygotic Mechanisms Rather Than Germ Plasm in a Basally Branching Insect. Ewen-Campen, B., Donoughe, S., Clarke, D.N., and Extavour, C.G Current Biology, 23(10): 835-842 (2013). [PubMed]