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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.