The success of artificial selection for collective composition hinges on initial and target values.

Abstract

Microbial collectives can perform functions beyond the capability of individual members. Enhancing collective functions through artificial selection is, however, challenging. Here, we explore the 'rafting-a-waterfall' metaphor where achieving a target population composition depends on both target and initial compositions. Specifically, collectives comprising fast-growing (F) and slow-growing (S) individuals were grown for 'maturation' time, and the collective with S-frequency closest to the target value is chosen to 'reproduce' via inoculating offspring collectives. During collective maturation, intra-collective selection acts like a waterfall, relentlessly driving the S-frequency to lower values, while during collective reproduction, inter-collective selection resembles a rafter striving to reach the target frequency. Using simulations and analytical calculations, we show that intermediate target S frequencies are the most challenging, akin to a target within the vertical drop of a waterfall, rather than above or below it. This arises because intra-collective selection is the strongest at intermediate S-frequencies, which can overpower inter-collective selection. While achieving a low target S frequencies is consistently feasible, attaining high target S-frequencies requires an initially high S-frequency - much like a raft that can descend but not ascend a waterfall. As Newborn size increases, the region of achievable target frequency is reduced until no frequency is achievable. In contrast, the number of collectives under selection plays a less critical role. In scenarios involving more than two populations, the evolutionary trajectory must navigate entirely away from the metaphorical 'waterfall drop.' Our findings illustrate that the strength of intra-collective evolution is frequency-dependent, with implications in experimental planning.