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. (shrink)

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. (shrink)

Both physiological and evolutionary criteria of biological individuality are underpinned by the idea that an individual is a functionally integrated whole. However, a precise account of functional integration has not been provided so far, and current notions are not developed in the details, especially in the case of composite systems. To address this issue, this paper focuses on the organisational dimension of two representative associations of prokaryotes: biofilms and the endosymbiosis between prokaryotes. Some critical voices have been raised against the (...) thesis that biofilms are biological individuals. Nevertheless, it has not been investigated which structural and functional obstacles may prevent them from being fully integrated physiological or evolutionary units. By contrast, the endosymbiotic association of different species of prokaryotes has the potential for achieving a different type of physiological integration based on a common boundary and interlocked functions. This type of association had made it possible, under specific conditions, to evolve endosymbionts into fully integrated organelles. This paper therefore has three aims: first, to analyse the organisational conditions and the physiological mechanisms that enable integration in prokaryotic associations; second, to discuss the organisational differences between biofilms and prokaryotic endosymbiosis and the types of integration they achieve; finally, to provide a more precise account of functional integration based on these case studies. (shrink)

Available evidence suggests that two prokaryotes, an archaeon and a bacterium, collaborated in the eventual formation of nucleated cells with arguably increased complexity of form and function. However, the mechanisms by which bacteria and archaea cooperated in the formation of eukaryotes, and the selective pressures that promoted this partnership, remain a mystery. Mitochondria are eukaryotic organelles thought to be derived from respiring, alpha-proteobacterial endosymbionts capable of generating ATP by oxidative phosphorylation. The earliest eukaryote likely harbored mitochondria, since all characterized eukaryotic (...) lineages show evidence of containing, or having once contained, these organelles. Consequently, it has been argued that mitochondria, and particularly the ATP that can be generated by these compartments, allowed for evolution toward an expanded number of proteins, an increase in overt specialization achievable by eukaryotic cells, and the eventual formation of complex multicellular organisms. However, the relationship between mitochondrial ATP generation and its potency in allowing genome expansion has been a matter of debate. Moreover, how and why an endosymbiont not yet converted to an organelle might purposefully provide ATP to its host is not clear. Here, I propose that the initial driving force for integration of the proto-mitochondrial endosymbiont within the proto-eukaryotic host may not have been provision of ATP to its archaeal partner, but rather that heat generated by the endosymbiont allowed the archaeal host to endure lower temperatures at the outset of eukaryogenesis. I discuss how this arrangement may have led to the increased apparent complexity that is characteristic of eukaryotes. (shrink)

Protistology, and evolutionary protistology in particular, is experiencing a golden research era. It is an extended one that can be dated back to the 1970s, which is when the molecular rebirth of microbial phylogeny began in earnest. John Archibald, a professor of evolutionary microbiology at Dalhousie University, focuses on the beautiful story of endosymbiosis in his book, John Archibald, One Plus One Equals One: Symbiosis and the Origin of Complex Life. However, this historical narrative could be treated as synecdochal of (...) how the molecular revolution has changed evolutionary biology forever, and that is how Archibald has structured his book. I will address the encompassing theme of molecular methods in detail, but also pay careful attention to the endosymbiosis thread in its own right. (shrink)

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”. (shrink)

Both paleobiology and investigations of ‘major evolutionary transitions’ are intimately concerned with the macroevolutionary shape of life. It is surprising, then, how little studies of major transitions are informed by paleontological perspectives and. I argue that this disconnect is partially justified because paleobiological investigation is typically ‘phenomena-led’, while investigations of major transitions are ‘theory-led’. The distinction turns on evidential relevance: in the former case, evidence is relevant in virtue of its relationship to some phenomena or hypotheses concerning those phenomena; in (...) the latter, evidence is relevant in virtue of providing insights into, or tests of, an abstract body of theory. Because paleobiological data is by-and-large irrelevant to the theory which underwrites the traditional conception of major transitions, it is of limited use to that research program. I suggest that although the traditional conception of major transitions is neither ad-hoc or problematically incomplete, its promise of providing unificatory explanations of the transitions is unlikely to be kept. Further, examining paleobiological investigations of mass extinctions and organogenesis, I further argue that whether or not transitions in paleobiology count as ‘major’ turns on how we conceive of major transitions ; although major transitions potentially have a unified theoretical basis, recent developments suggest that investigations are becoming increasingly phenomena-led; adopting phenomena-led investigations maximizes the evidence available to paleobiologists. (shrink)

Philosophers have usually highlighted how the weakness and paucity of historical evidence underdetermine the choice between rival historical explanations. Focusing underdetermination on the link between theory and evidence comes, I argue, with three assumptions: competing hypotheses are easy to generate, investigators agree on the constitution and interpretation of the evidence and a plurality of hypotheses is a useful evil to reach consensus. The last assumption implies that the sustained coexistence of incompatible hypotheses is considered as a scientific failure. I argue (...) that this negative vision of sustained disagreement has monistic undertones. By drawing from a case study in evolutionary biology, this paper defends a form of scientific pluralism. Firstly, I show that underdetermination is not only found at the inferential level but also at the level of the constitution and interpretation of the evidence, on the choice of investigative scaffolds and when interpreting background theories. Because of that, competing hypotheses exhibit a degree of methodological incommensurability. While catastrophic from a monistic standpoint, I defend that scientific pluralism gives a different, and I think richer, account of such situations. On the plus side, competing approaches benefit from their sustained coexistence and interaction. I argue that this generates direct and indirect epistemic goods independently of whether the controversy is solved. Scientific pluralism also shifts our attention from achieving consensus to managing disagreement. The challenge becomes to maintain the conditions for fruitful interactions in a community with incommensurable approaches and heterogeneous expertise. (shrink)