W. Doolittle

Understanding community-level selection using Lewontin’s criteria requires both community-level inheritance and community-level heritability, and in the discipline of community and ecosystem genetics, these are often conflated. While there are existing studies that show the possibility of both, these studies impose community-level inheritance as a product of the experimental design. For this reason, these experiments provide only weak support for the existence of community-level selection in nature. By contrast, treating communities as interactors (in line with Hull’s replicator-interactor framework or Dawkins’s idea of the “extended phenotype”) provides a more plausible and empirically supportable model for the role of ecological communities in the evolutionary process.

Many contemporary biologists and philosophers of biology admit that selection occurs at any level of the biological hierarchy at which entities showing heritable variation in fitness are found, while insisting that fitness at any level entails differential reproduction, not differential persistence. Those who allow that persistence can be selected doubt that selection on nonreproducing entities can be reiterated, to produce “complex adaptations.” We present here a verbal model of subclones evolving in a simple idealized chemostat that calls into question these suppositions and is usefully explanatory when taken as an analogy to selection for persistence of clades.

To date, no definition of life has been unequivocally accepted by the scientific community. In frustration, some authors advocate alternatives to standard definitions. These include using a list of characteristic features, focusing on life’s effects, or categorizing biospheres rather than life itself; treating life as a fuzzy category, a process or a cluster of contingent properties; or advocating a ‘wait-and-see’ approach until other examples of life are created or discovered. But these skeptical, operational, and pluralistic approaches have intensified the debate, rather than settled it. Given the failure of even these approaches, we advocate a new strategy. In this paper, we reverse the usual line of reasoning and argue that the “life problem” arises from thinking incorrectly about the nature of life. Scientists most often conceptualize life as a class or kind, with earthly life as a single instance of it. Instead, we advocate thinking about Earth’s Life as an individual, in the way that species are now thought to be. In this view, Life is a monophyletic clade that originated with a last universal common ancestor, and includes all its descendants. We can continue to use the category ‘life’ pragmatically to refer to similarities between various phenomena and Life. But the relevant similarities are a matter of interest and preference, not a matter of fact. The search for other life in the Universe, then, is merely a search for entities that resemble parts of Life in whatever sense astrobiologists find most appealing. This does not mean that the search for evolved complexity elsewhere in the universe or its creation in the lab are futile endeavors, but that debates over whether they count as ‘life’ are. Ironically, finally abandoning the concept ‘life’ may make our searches for evolved complexity more fruitful. We explain why.

The origin and prevalence of transposable elements may best be understood as resulting from “selfish” evolutionary processes at the within-genome level, with relevant populations being all members of the same TE family or all potentially mobile DNAs in a species. But the maintenance of families of TEs as evolutionary drivers, if taken as a consequence of selection, might be better understood as a consequence of selection at the level of species or higher, with the relevant populations being species or ecosystems varying in their possession of TEs. In 2015, Brunet and Doolittle made the case for legitimizing claims for an evolutionary role for TEs by recasting such claims as being about species selection. Here I further develop this “how possibly” argument. I note that with a forgivingly broad construal of evolution by natural selection we might come to appreciate many aspects of Life on earth as its products, and TEs as—possibly—contributors to the success of Life by selection at several levels of a biological hierarchy. Thinking broadly makes this proposition a testable Darwinian one.

Diverse living systems possess the capacity for regeneration; that is, they can under some circumstances repair, re-produce, and maintain themselves in the face of disturbance or damage. Think of systems as diverse as forests, microbial biofilms, corals, salamanders, hydra, and human skin cells. This capacity is fundamental to life—without it, many biological systems would be too fragile to cope with stress and would frequently collapse—but because it is multiply realized in wildly different living systems at many scales, finding a common understanding may seem futile, and in fact research has proceeded along independent lines. For example, the sciences of organismal regeneration and ecological regeneration appear to have little more than a nominal relationship. Progress towards unification can be made, we think, by turning to evolutionary theory, specifically by synthesizing recent discussions of the evolution of individuals versus collectives with older literature about replicators versus interactors. This allows us to provide a partial answer in response to MacCord and Maienschein’s call for “basic units and mechanisms” of regeneration, relevant when that process is “adaptive.” We argue that the basics of adaptive regeneration can be understood and generalized through a modification of David Hull’s replicator-interactor framework.

Biological science uses multiple species concepts. Order can be brought to this diversity if we recognize two key features. First, any given species concept is likely to have a patchwork structure, generated by repeated application of the concept to new domains. We illustrate this by showing how two species concepts (biological and ecological) have been modified from their initial eukaryotic applications to apply to prokaryotes. Second, both within and between patches, distinct species concepts may interact and hybridize. We thus defend a semantic picture of the species concept as a collection of interacting patchwork structures. Thus, although not all uses of the term pick out the same kind of unit in nature, the diversity of uses reflects something more than mere polysemy. We suggest that the emphasis on the use of species to pick out natural units is itself problematic, because that is not the term’s sole function. In particular, species concepts are used to manage inquiry into processes of speciation, even when these processes do not produce clearly delimited species.

In the half century since the formulation of the prokaryote : eukaryote dichotomy, many authors have proposed that the former evolved from something resembling the latter, in defiance of common (and possibly common sense) views. In such ‘eukaryotes first’ (EF) scenarios, the last universal common ancestor is imagined to have possessed significantly many of the complex characteristics of contemporary eukaryotes, as relics of an earlier ‘progenotic’ period or RNAworld. Bacteria and Archaea thus must have lost these complex features secondarily, through ‘streamlining’. If the canonical three-domain tree in which Archaea and Eukarya are sisters is accepted, EF entails that Bacteria and Archaea are convergently prokaryotic.We ask what this means and how it might be tested.

Here we endorse Hull’s replicator/interactor framework as providing the overarching understanding sought by MacCord and Maienschein. We suggest that difficulties in seeing the regeneration of limbs by salamanders and of forest ecosystems after fires as similar evolutionary processes can be overcome in this framework. In generalizing Dawkins’s “selfish gene” perspective, Hull defined natural selection as “a process in which the differential extinction and proliferation of interactors causes the differential perpetuation of the replicators that produced them”. Although genes and bacteria are simultaneously both replicators and interactors, communities and ecosystems are generally only interactors. As reproducers, members of sexual species are intermediate. Within such species, organisms are indeed the interactors whose “differential extinction and proliferation” causes the “differential perpetuation” of replicators. But sexually-reproducing organisms do not individually replicate, persist, or recur as interactors, and in consequence it is only those genes causing an interactor differential that are specifically perpetuated in the long run. Higher-level interactors may seldom if ever reproduce, but their recurrence does enable the “differential perpetuation” of replicators specifically responsible for their “differential extinction and proliferation”. In offering answers to the question “What are the replicators specifically responsible for the differential extinction and proliferation of such higher-level entities?” we hope to unify adaptive regeneration across scales, from organisms to ecosystems.

This paper investigates the complexity hypothesis in microbial evolutionary genetics from a philosophical vantage. This hypothesis, in its current version, states that genes with high connectivity are likely to be resistant to being horizontally transferred. We defend four claims. There is an important distinction between two different ways in which a gene family can persist: vertically and horizontally. There is a trade-off between these two modes of persistence, such that a gene better at achieving one will be worse at achieving the other. At least some genes are likely to experience selection favoring increased transferability. One consequence of this can be encapsulated as the “simplicity hypothesis”: horizontally persisting genes will experience selection favoring reduced connectivity. In order to make sense of the simplicity hypothesis, we need to consider evolutionary populations that transcend species boundaries. Vertical and horizontal persistence are therefore not two competing ways of succeeding at the same game, but involve playing two different games altogether. The complexity hypothesis can be understood in terms of two related notions: entrenchment and Cuvierian functionalism. This framing reveals previously unrecognized and philosophically interesting connections between reasoning about deep conservation and horizontal transfer.

This paper investigates the complexity hypothesis in microbial evolutionary genetics from a philosophical vantage. This hypothesis, in its current version, states that genes with high connectivity are likely to be resistant to being horizontally transferred. We defend four claims. There is an important distinction between two different ways in which a gene family can persist: vertically and horizontally. There is a trade-off between these two modes of persistence, such that a gene better at achieving one will be worse at achieving the other. At least some genes are likely to experience selection favoring increased transferability. One consequence of this can be encapsulated as the “simplicity hypothesis”: horizontally persisting genes will experience selection favoring reduced connectivity. In order to make sense of the simplicity hypothesis, we need to consider evolutionary populations that transcend species boundaries. Vertical and horizontal persistence are therefore not two competing ways of succeeding at the same game, but involve playing two different games altogether. The complexity hypothesis can be understood in terms of two related notions: entrenchment and Cuvierian functionalism. This framing reveals previously unrecognized and philosophically interesting connections between reasoning about deep conservation and horizontal transfer.

Constructive Neutral Evolution is an evolutionary mechanism that can explain much molecular inter-dependence and organismal complexity without assuming positive selection favoring such dependency or complexity, either directly or as a byproduct of adaptation. It differs from but complements other non-selective explanations for complexity, such as genetic drift and the Zero Force Evolutionary Law, by being ratchet-like in character. With CNE, purifying selection maintains dependencies or complexities that were neutrally evolved. Preliminary treatments use it to explain specific genetic and molecular structures or processes, such as retained gene duplications, the spliceosome, and RNA editing. Here we aim to expand the scope of such explanation beyond the molecular level, integrating CNE with Multi-Level Selection theory, and arguing that several popular higher-level selection scenarios are in fact instances of CNE. Suitably contextualized, CNE occurs at any level in the biological hierarchy at which natural selection as normally construed occurs. As examples, we focus on modularity in protein–protein interaction networks or “interactomes,” the origin of eukaryotic cells and the evolution of co-dependence in microbial communities—a variant of the “Black Queen Hypothesis” which we call the “Gray Queen Hypothesis”.

Microbiologists are transitioning from the study and characterization of individual strains or species to the profiling of whole microbiomes and microbial ecology. Equipped with high-throughput methods for studying the taxonomic and functional characteristics of diverse samples, they are just beginning to encounter the conceptual, theoretical, and experimental problems of comparing taxonomy to function, and extracting useful measures from such comparisons. Although still unresolved, these problems are well studied in macro-ecology and are reiterated here as an historical precautionary for microbial ecologists. Beyond expected and unresolved terminological vagueness, we argue that assessments and comparisons of taxonomic and functional profiles in micro-ecology suffer from theoretically unresolvable arbitrariness and ambiguities. We divide these into problems of scale, individuation, and commensurability. We argue that there is no technically/theoretically “correct” scale, individuation, or comparison of taxonomy and function, but there are nonetheless better and worse methodologies for profiling.

Lateral gene transfer, the exchange of genetic information between lineages, not only makes construction of a universal Tree of Life difficult to achieve, but calls into question the utility and meaning of any result. Here I review the science of prokaryotic LGT, the philosophy of the TOL as it figured in Darwin’s formulation of the Theory of Evolution, and the politics of the current debate within the discipline over how threats to the TOL should be represented outside it. We could encourage a more realistic and supportive public understanding of evolution by admitting that what we believe in is not a unified meta-theory but a versatile and well-stocked explanatory toolkit.

That holobionts are units of selection squares poorly with the observation that microbes are often recruited from the environment, not passed down vertically from parent to offspring, as required for collective reproduction. The taxonomic makeup of a holobiont’s microbial community may vary over its lifetime and differ from that of conspecifics. In contrast, biochemical functions of the microbiota and contributions to host biology are more conserved, with taxonomically variable but functionally similar microbes recurring across generations and hosts. To save what is of interest in holobiont thinking, we propose casting metabolic and developmental interaction patterns, rather than the taxa responsible for them, as units of selection. Such units need not directly reproduce or form parent-offspring lineages: their prior existence has created the conditions under which taxa with the genes necessary to carry out their steps have evolved in large numbers. These taxa or genes will reconstruct the original interaction patterns when favorable conditions occur. Interaction patterns will vary in ways that affect the likelihood of and circumstances under which such reconstruction occurs. Thus, they vary in fitness, and evolution by natural selection will occur at this level. It is on the persistence, reconstruction, and spread of such interaction patterns that students of holobiosis should concentrate, we suggest. This model also addresses other multi-species collectively beneficial interactions, such as biofilms or biogeochemical cycles maintaining all life.

The first complete sequence of an archaebacterial genome, that of Methanococcus jannaschii, has recently been published(1). Less than half of the open reading frames (ORFs) can be assigned a function based on similarity to known sequences in databases. These assignable ORFs fall into two general classes; those involved in transcription, translation and replication are more similar to eukaryotic homologs, while those determining metabolic processes are more similar to eubacterial versions. The immense but very rewarding task of making biological and evolutionary sense of all this information has only just begun.

In fact, nearly every scientist who has written on the general subject of evolution has felt compelled to show how deftly he can skate toward the abyss of teleology without falling in.J.H. Campbell, 163Molecular biology has as its primary objective the elucidation of the coupling between genotype and phenotype. This goal has so far been pursued within a neoDarwinian theoretical framework which is relatively limited. Within this framework we can indeed understand remarkably well the mechanisms of replication and expression of genes and the means by which replication and expression are regulated in cells; we know how genotype determines phenotype at the molecular level, in single cells. We are also close to an understanding of the relationship between genes and development in muticellular animals and plants.

Our understanding of what microbes are and how they evolve has undergone many radical shifts since the late nineteenth century, when many still believed that bacteria could be spontaneously generated and most thought microbial “species” (if any) to be unstable and interchangeable in form and function (pleomorphic). By the late twentieth century, an ontology based on single cells and definable species with predictable properties, evolving like species of animals or plants, was widely accepted. Now, however, genomic and metagenomic data show that lateral gene transfer compromises this picture of stability and predictability, and refocuses our attention on multilineage communities. Treating such communities as unstable but identifiable evolving “individuals” makes us again pleomorphists, of a sort

Clade selection is unpopular with philosophers who otherwise accept multilevel selection theory. Clades cannot reproduce, and reproduction is widely thought necessary for evolution by natural selection, especially of complex adaptations. Using microbial evolutionary processes as heuristics, I argue contrariwise, that (1) clade growth (proliferation of contained species) substitutes for clade reproduction in the evolution of complex adaptation, (2) clade-level properties favoring persistence – species richness, dispersal, divergence, and possibly intraclade cooperation – are not collapsible into species-level traits, (3) such properties can be maintained by selection on clades, and (4) clade selection extends the explanatory power of the theory of evolution.

In fact, nearly every scientist who has written on the general subject of evolution has felt compelled to show how deftly he can skate toward the abyss of teleology without falling in.J.H. Campbell, 163Molecular biology has as its primary objective the elucidation of the coupling between genotype and phenotype. This goal has so far been pursued within a neoDarwinian theoretical framework which is relatively limited. Within this framework we can indeed understand remarkably well the mechanisms of replication and expression of genes and the means by which replication and expression are regulated in cells; we know how genotype determines phenotype at the molecular level, in single cells. We are also close to an understanding of the relationship between genes and development in muticellular animals and plants.

Here I advance two related evolutionary propositions. (1) Natural selection is most often considered to require competition between reproducing “individuals”, sometimes quite broadly conceived, as in cases of clonal, species or multispecies-community selection. But differential survival of non-competing and non-reproducing individuals will also result in increasing frequencies of survival-promoting “adaptations” among survivors, and thus is also a kind of natural selection. (2) Darwinists have challenged the view that the Earth’s biosphere is an evolved global homeostatic system. Since there is only one biosphere, reproductive competition cannot have been involved in selection for such survival-promoting adaptations, they claim. But natural selection through survival could reconcile Gaia with evolutionary theory