PERSPECTIVE PERSPECTIVE Processes and patterns of interaction as units of selection: An introduction to ITSNTS thinking W. Ford Doolittlea,1 and S. Andrew Inkpena,b Edited by Douglas Futuyma, Stony Brook University, Stony Brook, NY, and approved March 7, 2018 (received for review December 22, 2017) Many practicing biologists accept that nothing in their discipline makes sense except in the light of evolution, and that natural selection is evolution’s principal sense-maker. But what natural selection actu- ally is (a force or a statistical outcome, for example) and the levels of the biological hierarchy (genes, organisms, species, or even ecosystems) at which it operates directly are still actively disputed among philosophers and theoretical biologists. Most formulations of evolution by natural selection emphasize the differential reproduction of entities at one or the other of these levels. Some also recognize differential persistence, but in either case the focus is on lineages of material things: even species can be thought of as spatiotemporally restricted, if dispersed, physical beings. Few consider—as “units of selection” in their own right—the processes implemented by genes, cells, species, or communities. “It’s the song not the singer” (ITSNTS) theory does that, also claiming that evolution by natural selection of processes is more easily understood and explained as differential persistence than as differential reproduction. ITSNTS was formulated as a response to the observation that the collective functions of microbial communities (the songs) are more stably conserved and ecologically relevant than are the taxa that implement them (the singers). It aims to serve as a useful corrective to claims that “holobionts” (microbes and their animal or plant hosts) are aggregate “units of selection,” claims that often conflate meanings of that latter term. But ITSNS also seems broadly applicable, for example, to the evolution of global biogeochemical cycles and the definition of ecosystem function. evolution | natural selection | process | persistence | microbiome Our purpose here is to introduce and justify ITSNTS Lewontin (3) summarized the collective wisdom of (“It’s the song, not the singer”) theory as a way of con- neoDarwinian theorists in a three-part recipe for what ceptualizing evolution by natural selection (ENS) that we here are calling “standard ENS.” allows processes as well as things to be “units of selec- tion,” selected for persistence and re-produced but not (i) There is variation in morphological, physio- reproducing (1, 2). We see this as a legitimate and logical, and behavioral traits among members broadly useful application of Darwinian principles in a of a species (the principle of variation). (ii)The broad area (community evolution) currently in want of variation is in part heritable, so that individuals such theory. ITSNTS makes it sensible to talk about resemble their relations more than they re- semble unrelated individuals and, in particular, adaptations and functions as relevant to (if not proper- offspring resemble their parents (the principle ties of) multispecies collectives, while standard ENS of heredity). (iii) Different variants leave dif- formulations do not. Whenever what is remarkable ferent numbers of offspring either in immedi- about a biological or cultural phenomenon is the per- ate or remote generations (the principle of sistence of a process or pattern of interactions (a song) differential fitness). that can be carried out by a variety of cooperating entities (singers), each of these having evolved because Lewontin (3) claimed that these conditions are nec- individual participation has (as in standard ENS) favored essary and sufficient for ENS, and here we take as one its differential reproduction, that is ITSNTS. type of ENS that which will likely occur given them, aDepartment of Biochemistry and Molecular Biology, Dalhousie University, Halifax, NS B3H 4R2, Canada; and bDepartment of Philosophy, Dalhousie University, Halifax, NS B3H 4R2, Canada Author contributions: W.F.D. and S.A.I. wrote the paper. The authors declare no conflict of interest. This article is a PNAS Direct Submission. Published under the PNAS license. 1To whom correspondence should be addressed. Email: [email protected]. Published online March 26, 2018. 4006–4014 | PNAS | April 17, 2018 | vol. 115 | no. 16 www.pnas.org/cgi/doi/10.1073/pnas.1722232115 Downloaded by guest on September 25, 2021 regardless of the nature of the evolving entity. But as commonly If p = 1, it is meaningful to think of communities as reproducing understood, these principles entail differential reproduction of (ar- and forming parent–offspring lineages. The pool has a single guably) material entities producing parent–offspring lineages. contributing parent community and is the exclusive contributor to ITSNTS questions this requirement, seeing Lewontin’s conditions one or more “offspring” communities. The situation would be like as sufficient but not necessary for ENS, which we take to be any that of a lichen, whose dispersal structures include individuals reiterated causal process resulting in greater relative representa- from both fungus and phycobiont or, as we envision here, of a tion at time tn later than t1 of certain types of entities by virtue of multispecies biofilm that “reproduces” by budding off a fragment those types’ possession of certain traits, those traits for that reason containing a random sample of the organisms present in it, this to being adaptations (2). reattach and grow at a new site. If fragments are large enough to Godfrey-Smith (4) describes the more limited, traditional view overcome “ecological drift” (10), each offspring community will when he writes that: likely resemble its parent or siblings in species composition more than it resembles unrelated communities. Lewontin’s conditions Evolution by natural selection is change in a population ow- would apply and community-level properties, such as the ten- ing to variation, heredity and differential reproductive dency to form more robust propagules more often (community- success. This is usually seen as a micro-evolutionary process reproductive traits that might depend on species make-up) could acting on organisms, but the criteria required are abstract; be selected for. genes, cells, social groups and species can all, in principle, However, suppose instead that all parental communities re- enter into change of this kind. For any objects to be units of lease the individual organisms they contain into a common pool, selection in this sense, however, they must be connected by parent–offspring relations; they must have the capacity to from which n are randomly chosen to form each community in the reproduce. Units of selection in this sense can be called next generation of communities. In this case, the species com- Darwinian individuals. An evolutionarily relevant case of positions of the offspring communities will reflect only that of the reproduction can take many forms. There need not be rep- common pool and will, sampling error aside, resemble each other. lication, the faithful production of copies. Replicators are By the “law of large numbers,” such intercommunity resemblance Darwinian individuals with high-fidelity, asexual reproduc- will get closer and closer as n increases, just as the frequency of tion, and it is possible to have evolution by natural selection heads flipped with an honest coin gets closer and closer to 50% on units where reproduction is sexual and heredity is weak the longer one flips. (emphasis ours). Of necessity, n cannot be less than p, the number of parents Although sexual heredity is weaker because each parent’s con- contributing at least one individual to a new community. In many tribution is diluted by half, children usually resemble parents and real microbial communities assembled by de novo recruitment siblings more than they do “unrelated individuals,” and this is all from multiple sources, such as multispecies biofilms, the micro- that Lewontin’s second condition actually demands. But the more biomes of many animals and plants, and environmental sites like parents, the more the dilution, and Godfrey-Smith (4) cautions hydrothermal vents or whale carcasses on the sea bottom, p and n that “... there must be some parent–offspring similarity, and the will both often be very large—dozens to thousands, perhaps— clarity of a ‘parent-offspring’ relation of the relevant kind is in- and new recruits can also come from lineages of organisms pre- versely related to the number of parents—if there are too many viously only loosely associated with circumscribable communities. parents there are no parents at all.” (It is important to remember that it is the number of parent communities that contribute individuals to each offspring com- How There Can Be “Too Many Parents” munity that matters in this model, not the number of different What ITSNTS theory aims to undermine and supplant are claims species that these individuals might represent.) that multispecies groups comprise material units of selection even So, the relevance of Godfrey-Smith’s (4) “too many parents” when in violation of Lewontin’s recipe, in violation because there warning is this. When p is large, n is as large and usually larger. It are too many parents. Such claims (5–9) made with respect to might in principle be possible to identify all parental communities microbial communities (symbioses, “holobionts,” biofilms, and contributing at least one individual organism to any particular