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The placenta as a model for understanding the origin and evolution of vertebrate organs

Nature Ecology & Evolution volume 1, Article number: 0072 (2017) Cite this article

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Abstract

How organs originate and evolve is a question fundamental to understanding the evolution of complex multicellular life forms. Vertebrates have a relatively standard body plan with more or less the same conserved set of organs. The placenta is a comparatively more recently evolved organ, derived in many lineages independently. Using placentas as a model, we discuss the genetic basis for organ origins. We show that the evolution of placentas occurs by acquiring new functional attributes to existing tissues, changes in the patterning and development of tissues, and the evolution of novel cell types. We argue that a diversity of genomic changes facilitated these physiological transformations and that these changes are likely to have occurred during the evolution of organs more broadly. Finally, we argue that a key aspect to understanding the evolutionary origin of organs is that they are likely to result from novel interactions between distinct cell populations.

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Figure 1: Major vertebrate organs have ancient origins.
Figure 2: Phylogenetic relationships of vertebrates in lineages in which the evolution of placental structures has been studied.
Figure 3: A small selection of the diverse parental and embryonic tissues involved in placental development in vertebrates.
Figure 4: How placental intimacy can result in new signalling processes supporting the evolution and origin of an organ.

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Acknowledgements

This research was funded by the Gaylord Donnelley Postdoctoral Environmental Fellowship to O.W.G. and a John Templeton Foundation Grant to G.P.W. (no. 54860). The authors thank T. Stewart, E. Erckenbrack, A. Chavan, C. Laing and F. Stabile for useful comments on drafts of this manuscript and M. Thompson for his encouragement to write it.

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Authors and Affiliations

  1. Department of Ecology and Evolutionary Biology, Yale University, New Haven, Connecticut, 06511, USA

    Oliver W. Griffith & Günter P. Wagner

  2. Yale Systems Biology Institute, West Haven, Connecticut, 06516, USA

    Oliver W. Griffith & Günter P. Wagner

  3. Department of Obstetrics, Gynecology and Reproductive Sciences, Yale Medical School, New Haven, Connecticut, 06511, USA

    Günter P. Wagner

  4. Department of Obstetrics and Gynecology, Wayne State University, Detroit, Michigan, 48201, USA

    Günter P. Wagner

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O.W.G. wrote the manuscript. O.W.G. and G.P.W. developed ideas for, edited and approved the final version of the paper.

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Correspondence to Oliver W. Griffith.

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Griffith, O., Wagner, G. The placenta as a model for understanding the origin and evolution of vertebrate organs. Nat Ecol Evol 1, 0072 (2017). https://doi.org/10.1038/s41559-017-0072

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