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Nascent multicellular life and the emergence of individuality

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Abstract

The evolution of multicellular organisms from unicellular ancestors involves a shift in the level at which selection operates. It is usual to think about this shift in terms of the emergence of traits that cause heritable differences in reproductive output at the level of nascent collectives. Defining these traits and the causes of their origin lies at the heart of understanding the evolution of multicellular life. In working toward a mechanistic, take-nothing-for-granted account, we begin by recognizing that the standard Lewontin formulation of properties necessary and sufficient for evolution by natural selection does not necessarily encompass Darwinian evolution in primitive collectives where parent-offspring relationships may have been poorly defined. This, we suggest, limits the ability to conceptualize and capture the earliest manifestations of Darwinian properties. By way of solution we propose a relaxed interpretation of Lewontin’s conditions and present these in the form of a set of necessary requirements for evolution by natural selection based upon the establishment of genealogical connections between recurrences of collectives. With emphasis on genealogy – as opposed to reproduction – it is possible to conceive selection acting on collectives prior to any manifestation of heritable variance in fitness. Such possibility draws attention to the evolutionary emergence of traits that strengthen causal relationships between recurrences – traits likely to underpin the emergence of forms of multiplication that establish parent-offspring relationships. Application of this framework to collectives of marginal status, particularly those whose recurrence is not defined by genealogy, makes clear that change at the level of collectives need not arise from selection acting at the higher level. We conclude by outlining applicability of our framework to loosely defined collectives of cells, such as those comprising the slugs of social amoeba and microbes that constitute the human microbiome.

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Acknowledgements

We are indebted to Ellen Clarke for long hours of enjoyable discourse out of which this article grew – the background being provided by the stimulating ‘Individuals and Groups’ meeting in Almora, India. In addition to Ellen, we give our thanks to the anonymous referees who endured the frustration of a too preliminary draft and to Vidyanand Nanjundiah. Our thanks also to support provided by the Kavli Institute for Theoretical Physics, University of California, Santa Barbara, and to the participants of the 2013 workshop on cooperation and the evolution of multicellularity. PBR gratefully acknowledges financial support from the Marsden Fund Council administered by the Royal Society of New Zealand, grant RFP-12-20 from the Foundational Questions in Evolutionary Biology Fund, and a KITP Simons Distinguished Visiting Scholarship.

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Authors and Affiliations

  1. Institut de Biologie de l’École Normale Supérieure (IBENS), CNRS UMR 8197 INSERM U1024, 46 rue d’Ulm, 75005, Paris, France

    Silvia De Monte

  2. New Zealand Institute for Advanced Study and Allan Wilson Centre for Molecular Ecology & Evolution, Massey University, Private Bag 102904, Auckland, 0745, New Zealand

    Paul B Rainey

  3. Max Planck Institute for Evolutionary Biology, August Thienemann Strasse 2, 24306, Plön, Germany

    Paul B Rainey

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  1. Silvia De Monte
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Correspondence to Silvia De Monte or Paul B Rainey.

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[De Monte S and Rainey PB 2014 Nascent multicellular life and the emergence of individuality. J. Biosci. 39 1–12] DOI 10.1007/s12038-014-9420-5

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De Monte, S., Rainey, P.B. Nascent multicellular life and the emergence of individuality. J Biosci 39, 237–248 (2014). https://doi.org/10.1007/s12038-014-9420-5

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