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Problems of multi-species organisms: endosymbionts to holobionts

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Abstract

The organism is one of the fundamental concepts of biology and has been at the center of many discussions about biological individuality, yet what exactly it is can be confusing. The definition that we find generally useful is that an organism is a unit in which all the subunits have evolved to be highly cooperative, with very little conflict. We focus on how often organisms evolve from two or more formerly independent organisms. Two canonical transitions of this type—replicators clustered in cells and endosymbiotic organelles within host cells—demonstrate the reality of this kind of evolutionary transition and suggest conditions that can favor it. These conditions include co-transmission of the partners across generations and rules that strongly regulate and limit conflict, such as a fair meiosis. Recently, much attention has been given to associations of animals with microbes involved in their nutrition. These range from tight endosymbiotic associations like those between aphids and Buchnera bacteria, to the complex communities in animal intestines. Here, starting with a reflection about identity through time (which we call “Theseus’s fish”), we consider the distinctions between these kinds of animal–bacteria interactions and describe the criteria by which a few can be considered jointly organismal but most cannot.

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Acknowledgments

We thank Thomas Pradeu for encouraging this work and for stimulating discussion and helpful comments. We also thank Judie Bronstein and two anonymous referees for their helpful comments on the manuscript. This is a Tyson Research Center of Washington University in St. Louis contribution. Our research is funded by the John Templeton Foundation #43667 and the USA National Science Foundation Grants #IOS1256416 and #DEB1146375.

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  1. Department of Biology, CB 1137, Washington University in St Louis, One Brookings Drive, St Louis, MO, 63130-4899, USA

    David C. Queller & Joan E. Strassmann

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  1. David C. Queller
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Correspondence to David C. Queller.

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Queller, D.C., Strassmann, J.E. Problems of multi-species organisms: endosymbionts to holobionts. Biol Philos 31, 855–873 (2016). https://doi.org/10.1007/s10539-016-9547-x

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