Reproduction of mats via the cheat-embracing (CE) regime, in conjunction with selection among collectives, decoupled fitness, effected a shift in selection to the higher level, and fostered initial steps toward the emergence of development. The causative factor is of central interest. While it is possible that a life cycle of two phases is key, reproduction via a bottleneck phase, combined with between-collective selection, may be sufficient. For example, it is conceivable that the fitness of WS mats propagated via a bottleneck without requirement to pass through an alternate (SM) phase could improve as a consequence of the production of more substantive adhesive polymers that come at the expense of individual cell performance. To test for such a possibility we performed a control experiment in which WS mats were propagated under a “cheat-purging” (CP) regime. The sole difference between the CP and CE regimes is the cell that passes through the bottleneck: under the CP regime the cell passing through the bottleneck is a WS cell (Figure 4.1, righthand panel). Reproduction via the CP regime is analogous to fragmentation.
Conventional wisdom predicts the CP regime to have greatest evolutionary potential. Indeed, after 10 generations of lineage selection (Figure 3.1) fitness of evolved collectives improved significantly (χ2=15.737, df=1, P<0.0001; Figure 4.12; Appendix 8.2.1). However, this was accompanied by a similar improvement in the fitness of single cells (t86=2.132, P=0.036; Figure 4.12; Appendix 8.2.1). Improvement in the fitness of evolved collectives is thus explained by improvement in individual cell performance. The striking response observed under the CE regime can therefore be attributed to a life cycle of alternating phases.
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Figure 4.12 Fitness of evolved CP collectives and their single cell constituents relative to ancestral types. Both collective and cell-level fitness increased significantly. Error bars are SEM, based on N=15.
To explore adaptations of the CP regime that contributed to increased collective performance, life history properties were determined relative to ancestral types, as for the CE regime. No improvement was seen in the capacity for WS types to transition to SM. A significantly lower proportion of the evolved collectives produced SM (χ2=8.199, df=1, P=0.0042): SM types took longer to arise (Figure 4.13a) hinting at the possibility that cheater suppression might have begun to evolve under this regime (Figure 4.13b-d).
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Figure 4.13 Life history traits under the CP regime. (a) Proportion of collectives producing SM (note that this data is identical to panel (a) of Figure 3.5) (b) Total cell density. (c) Cell density of the new type. (d) Proportion of SM cell types/total cells. Each circle represents the mean of 45 collectives (i.e. 3 replicates for each of the 15 collectives), however, for c and d collectives that failed to produce SM were excluded. Ancestral = grey, evolved = black. Error bars are SEM, based on N≤15. * represents a significance level of P<0.05.
Regression and correlation analyses summarising the relationship between traits of collectives evolved under the CP regime and the single cells of which they are comprised are shown in Figure 4.11c and d (Appendix 8.2.3). Under the CP regime enhanced collective fitness is explained by changes in traits that improve the competitive ability of individual cells. Enhanced collective fitness under the CP regime is thus most likely a by-product of selection at the lower (cell) level.
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4.4. Perspective
Multicellular organisms are descendants of once free-living cells (Buss, 1987; Maynard Smith & Szathmáry, 1995; Bonner, 1998; Grosberg & Strathmann, 2007). By virtue of their capacity for differential reproduction, ancestral free-living cells were units of selection (Lewontin, 1970). As such they evolved by Darwinian processes (Okasha, 2006; Godfrey-Smith, 2009). During the transition to multicellularity, collectives of cells emerged that came to participate in Darwinian processes in their own right (Maynard Smith, 1988; Michod, 1999; Okasha, 2006; Godfrey-Smith, 2009). The essential ingredient was a means of collective reproduction (Maynard Smith, 1988; Godfrey-Smith, 2009). This most seminal of Darwinian properties emerges afresh at each transition and requires evolutionary explanation(Griesemer, 2000). Here we have shown that cheating cells – those types seemingly most detrimental to the persistence of newly formed cooperative entities – can function as a germ line to facilitate reproduction of collectives. In assuming the role of germ line, cheats not only solve the very problem they pose, but underpin the emergence of a new level of biological organisation – a level comprised of collectives with properties sufficient to participate in Darwinian evolution (Lewontin, 1970; Michod, 1999; Okasha, 2006; Godfrey-Smith, 2009).
While emphasising distinctive roles for cooperating and cheating cells, similar two-phase life cycles could conceivably emerge from a variety of simple founding states in which the nascent multicellular organism comprises both group-forming and individually-acting cell types (Libby & Rainey, 2013). Such founding states have implications for understanding the origins of complex life cycles, including those that involve development of a new organism from a single cell (Godfrey-Smith, 2009; Libby
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& Rainey, 2013, 2013), and where the single cell is derived from a dedicated germ line that is distinct from soma (Buss, 1987).
Mode of reproduction also has profound implications for how selection sees nascent multicellular organisms (Stearns, 2007; Libby & Rainey, 2013). When collectives reproduce via a two-phase life cycle, success depends on the existence of both collective and individual cell states. Each state is in effect a different attribute of a single and altogether new kind of organism whose evolution stands to be unified through a developmental programme (Wolpert, 1990). Selection acting at the higher level favours those collectives most able to perpetuate the life cycle (Libby & Rainey, 2013). Because the properties that engender success at the higher level are not equivalent to properties yielding successful individual cells, improvement of the collective comes at a cost to the cell. Decoupling of fitness between levels is a signature of this conflict. When reproduction of collectives is via fragmentation (a single phase life cycle), the traits that yield success at the higher level are largely those that determine success at the lower level. The focus of selection remains, at both collective and single cell phases, the individual cooperating cell. This offers limited opportunity for the emergence of new kinds of biological individuality because properties of higher and lower levels remain aligned. It is possible that the prevalence of complex life cycles among extant multicellular organisms reflects the fact that such cycles, on first emergence, delivered to selection collectives with greatest propensity to participate in Darwinian evolution.
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