A holobiont is a composite organism consisting of a host together with its microbiome, such as a coral with its zooxanthellae. To explain the often intimate integration between hosts and their microbiomes, some investigators contend that selection operates on holobionts as a unit and view the microbiome’s genes as extending the host’s nuclear genome to jointly comprise a hologenome. Because vertical transmission of microbiomes is uncommon, other investigators contend that holobiont selection cannot be effective because a holobiont’s microbiome is (...) an acquired condition rather than an inherited trait. This disagreement invites a simple mathematical model to see how holobiont selection might operate and to assess its plausibility as an evolutionary force. This paper presents two variants of such a model. In one variant, juvenile hosts obtain microbiomes from their parents (vertical transmission). In the other variant, microbiomes of juvenile hosts are assembled from source pools containing the combined microbiomes of all parents (horizontal transmission). According to both variants, holobiont selection indeed causes evolutionary change in holobiont traits. Therefore, holobiont selection is plausibly an effective evolutionary force with either mode of microbiome transmission. The modeling employs two distinct concepts of inheritance, depending on the mode of microbiome transmission: collective inheritance whereby juveniles inherit a sample of the collected genomes from all parents, as contrasted with lineal inheritance whereby juveniles inherit the genomes from only their own parents. A distinction between collective and lineal inheritance also features in theories of multilevel selection. (shrink)

Holobionts are symbiotic assemblages composed by a macrobe host plus its symbiotic microbiota. In recent years, the ontological status of holobionts has created a great amount of controversy among philosophers and biologists: are holobionts biological individuals or are they rather ecological communities of independent individuals that interact together? Chiu and Eberl have recently developed an eco-immunity account of the holobiont wherein holobionts are neither biological individuals nor ecological communities, but hybrids between a host and its microbiota. (...) According to their account, the microbiota is not a proper part of the holobiont. Yet, it should be regarded as a set of scaffolds that support the individuality of the host. In this paper, we approach Chiu and Eberl’s account from a metaphysical perspective and argue that, contrary to what the authors claim, the eco-immunity account entails that the microorganisms that compose the host’s microbiota are proper parts of the holobiont. Second, we argue that by claiming that holobionts are hybrids, and therefore, not biological individuals, the authors seem to be assuming a controversial position about the ontology of hybrids, which are conventionally characterized as a type of biological individual. In doing so, our paper aligns with the contemporary tendency to incorporate metaphysical resources to shed light on current biological debates and builds on that to provide additional support to the consideration of holobionts as biological individuals from an eco-immunity perspective. (shrink)

Holobionts are symbiotic assemblages composed by a host plus its microbiome. The status of holobionts as individuals has recently been a subject of continuous controversy, which has given rise to two main positions: on the one hand, holobiont advocates argue that holobionts are biological individuals; on the other, holobiont detractors argue that they are just mere chimeras or ecological communities, but not individuals. Both parties in the dispute develop their arguments from the framework of the philosophy of (...) biology, in terms of what it takes for a “conglomerate” to be considered an interesting individual from a biological point of view. However, the debates about holobiont individuality have important ontological implications that have remained vaguely explored from a metaphysical framework. The purpose of this paper is to cover that gap by presenting a metaphysical approach to holobionts individuality. Drawing upon a conception of natural selection that puts the focus on the transgenerational recurrence of the traits and that supports the thesis that holobionts are units of selection, we argue that holobionts bear emergent traits and exert downward powers over the entities that compose them. In this vein, we argue, a reasonable argument can be made for conceiving holobionts as emergent biological individuals. (shrink)

The units or levels of selection debate concerns the question of what kind of biological systems are stable enough that part of their evolution is a result of the process of natural selection acting at their level. Traditionally, the debate has concerned at least two different, though related, questions: the question of the level at which interaction with the environment occurs, and the question of the level at which reproduction occurs. In recent years, biologists and philosophers have discussed a new (...) aspect of this debate, namely the possibility that certain multi-species consortia formed by a host and its microbiome may act as a unit of selection. This thesis, however, has not been without criticism, as it is doubtful that such consortia could meet the conditions required to achieve the degree of stability that would allow them to experience natural selection. The purpose of this paper is to systematically examine such criticisms and to defend the thesis that the holobiont/hologenome can act as a genuine level of selection both in the form of an interactor and in the form of a reproducer. To do so, it will be argued that the microbiome should be characterized in functional rather than taxonomic terms. (shrink)

Bourrat and Griffiths :33, 2018) have recently argued that most of the evidence presented by holobiont defenders to support the thesis that holobionts are evolutionary individuals is not to the point and is not even adequate to discriminate multispecies evolutionary individuals from other multispecies assemblages that would not be considered evolutionary individuals by most holobiont defenders. They further argue that an adequate criterion to distinguish the two categories is fitness alignment, presenting the notion of fitness boundedness as a criterion (...) that allows divorcing true multispecies evolutionary individuals from other multispecies assemblages and provides an adequate criterion to single out genuine evolutionary multispecies assemblages. A consequence of their criterion is that holobionts, as conventionally defined by hologenome defenders, are not evolutionary individuals except in very rare cases, and for very specific host-symbiont associations. This paper is a critical response to Bourrat and Griffiths’ arguments and a defence of the arguments presented by holobiont defenders. Drawing upon the case of the hologenomic basis of the evolution of sanguivory in vampire bats, I argue that Bourrat and Griffiths overlook some aspects of the biological nature of the microbiome that justifies the thesis that holobionts are evolutionarily different to other multispecies assemblages. I argue that the hologenome theory of evolution should not define the hologenome as a collection of genomes, but as the sum of the host genome plus some traits of the microbiome which together constitute an evolutionary individual, a conception I refer to as the stability of traits conception of the hologenome. Based on that conception I argue that the evidence presented by holobiont defenders is to the point, and supports the thesis that holobionts are evolutionary individuals. In this sense, the paper offers an account of the holobiont that aims to foster a dialogue between hologenome advocates and hologenome critics. (shrink)

Over the last three decades, studies in microbiology have exposed a world of diverse and dynamic interactions. Through metagenomic sequencing, complex bacterial communities became visible and proved important for many biological phenomena. As a result of discovering the connection between microorganisms and organisms’ survival, the notion of the holobiont has become prominent and has been suggested as a biological individual. The view of the holobiont as an individual, commonly known as the Hologenome Theory, focuses on the interactions and relations between (...) the host and its symbionts in the host’s development and evolution. Today, the holobiont is at the heart of the debate on the nature of the biological individual, a debate which is connected to the same question about the nature of the individual organism. (shrink)

How does microbiota research impact our understanding of biological individuality? We summarize the interdisciplinary summer school on "Microbiota, Symbiosis and Individuality: Conceptual and Philosophical Issues" (July 2019), which was supported by a European Research Council starting grant project "Immunity, DEvelopment, and the Microbiota" (IDEM). The summer school centered around interdisciplinary group work on four facets of microbiota research: holobionts, individuality, causation, and human health. The conceptual discussion of cutting-edge empirical research provided new insights into microbiota and highlights the value (...) of incorporating into meetings experts from other disciplines, such as philosophy and history of science. (shrink)

Symbiosis plays a fundamental role in contemporary biology, as well as in recent thinking in philosophy of biology. The discovery of the importance and universality of symbiotic associations has brought new light to old debates in the field, including issues about the concept of biological individuality. An important aspect of these debates has been the formulation of the hologenome concept of evolution, the notion that holobionts are units of natural selection in evolution. This review examines the philosophical assumptions that (...) underlie recent proposal of the hologenome concept of evolution, and traces those debates back in time to their historical origins, to the moment when the connection between the topics of symbiosis and biological individuality first caught the attention of biologists. The review is divided in two parts. The first part explores the historical origins of the connection between the notion of symbiosis and the concept of biological individuality, and emphasizes the role of A. de Bary, R. Pound, A. Schneider and C. Merezhkowsky in framing the debate. The second part examines the hologenome concept of evolution and explores four parallelisms between contemporary debates and the debates presented in the first part of the essay, arguing that the different debates raised by the hologenome concept were already present in the literature. I suggest that the novelty of the hologenome concept of evolution lies in the wider appreciation of the importance of symbiosis for maintaining life on Earth as we know it. Finally, I conclude by suggesting the importance of exploring the connections among contemporary biology, philosophy of biology and history of biology in order to gain a better understanding of contemporary biology. (shrink)

This is an article in Thomas J.J. McCloughlin (Ed.) The Nature of Science in Biology: A Resource for Educators. Graphikon Teo, Dublin. -/- Abstract: Philosophers usually tend to think of animals when they think about life, plants often only appear in their works as on the margins, in the background; they are rarely in the centre. However, plant life involves unique processes, including remarkable modes of interaction between plants and their environments. Needless to say, plants are vital parts of ecosystems. (...) Serious attention to plants provides novel and interesting perspectives on many topics in philosophy of biology, including individuality, organisation and disease. Plant biology should have a substantial part in philosophy education. To support this assertion, this paper briefly describes three topics related to plant-environment interaction and explains some of their philosophical implications. These topics are growth, plant hormones and plant-plant microbiota interactions, all of which present crucial aspects related to some prevalent topics in philosophy of biology such as individuality, systems thinking, and holobiont. (shrink)

Inhere we expand the concept of Holobiont to incorporate niche construction theory in order to increase our understanding of the current planetary crisis. By this, we propose a new ontology, the Ecobiont, as the basic evolutionary unit of analysis. We make the case of Homo Sapiens organized around modern cities (technobionts) as a different Ecobiont from classical Homo Sapiens (i.e. Hunter- gatherers Homo Sapiens). We consider that Ecobiont ontology helps to make visible the coupling of Homo Sapiens with other biological (...) entities under processes of natural and cultural evolution. Not to see this coupling hidden systemic risks and enhance the probability of catastrophic events. So Ecobiont ontology is necessary to understand and respond to the current planetary crisis. -/- . (shrink)

This paper addresses the question of what organisms are and therefore what kinds of biological entities qualify as organisms. For some time now, the concept of organismality has been eclipsed by the notion of individuality. Biological individuals are those systems that are units of selection. I develop a conception of organismality that does not rely on evolutionary considerations, but instead draws on development and ecology. On this account, organismality and individuality can come apart. Organisms, in my view, are as Godfrey-Smith (...) puts it “essentially persisters.” I argue that persistence is underpinned by differentiation, integration, development, and the constitutive embeddedness of organisms in their worlds. I examine two marginal cases, the Portuguese Man O’ War and the honey bee colony, and show that both count as organisms in light of my analysis. Next, I examine the case of holobionts, hosts plus their microsymbionts, and argue that they can be counted as organisms even though they may not be biological individuals. Finally, I consider the question of whether other, less tightly integrated biological systems might also be treated as organisms. (shrink)

The hologenome concept of evolution is a hypothesis about the evolution of animals and plants. It asserts that the evolution of animals and plants was partially triggered by their interactions with their symbiotic microbiomes. In that vein, the hologenome concept posits that the holobiont (animal host + symbionts of the microbiome) is a unit of selection. -/- The hologenome concept has been severely criticized on the basis that selection on holobionts would only be possible if there were a tight (...) transgenerational host-genotype-to-symbiont-genotype connection. As our current evidence suggests that this is not the case for most of the symbiont species that compose the microbiome of animals and plants, the opportunity for holobiont selection is very low in relation to the opportunity for selection on each of the species that compose the host microbiome. Therefore, holobiont selection will always be disrupted ‘from below’, by selection on each of the species that compose the microbiome. -/- This thesis constitutes a conceptual effort to defend philosophically the hologenome concept. I argue that the criticism according to which holobiont selection requires tight transgenerational host-genotype-to-symbiont-genotype connection is grounded on a metaphysical view of the world according to which the biological hierarchy needs to be nested, such that each new level of selection includes every entity from below. Applied to hologenomes, it entails that the hologenome is a collection of genomes, and selection of hologenomes is assumed to entail cospeciation of the host with the species that constitute its microbiome. -/- Against that interpretation, I propose the ‘stability of traits’ account, according to which hologenome evolution is the result of the action of natural selection in a non-nested hierarchical world. In that vein, hologenome evolution does not entail cospeciation, and thus it does not require tight transgenerational host-genotype-to-symbiont-genotype connection. By embracing a multilevel selection perspective, I argue that hologenome evolution results from the simultaneous action of natural selection on each of the lineages that compose the microbiome, and on the assemblage composed by the host genome plus the functional traits of its microbiome. Hologenome selection occurs when the evolution of the traits of the microbiome result from their effects on the fitness of the host, and it can take the form of multilevel selection 1, or multilevel selection 2. In both cases, hologenome selection entails the evolution of microbiome traits, as well as evolution of the host genome, rather than cospeciation of lineages. (shrink)

A biographical sketch of the Hologenome Theory.

Biological lineages move through time, space, and each other. As they do, they diversify, diverge, and grade away from and into one another. One result of this is genealogical discordance; i.e., the lineages of a biological entity may have different histories. We see this on numerous levels, from microbial networks, to holobionts, to population-level lineages. This paper considers how genealogical discordance impacts our study of species. More specifically, I consider this in the context of three framing questions: (1) How, (...) if at all, does genealogical discordance challenge, modify, or revise how we conceive of species? (2) How has growing appreciation of genealogical discordance impacted scientific practice? Of systematics in particular? (3) How do lineages at different levels diverge and diversify? All told, genealogical discordance enriches and complicates our taxonomic ontology, as well as the practice of reconstructing phylogenies. This presents both challenges and opportunities for the study of divergence and diversification. (shrink)

Contemporary biological research has suggested that some host–microbiome multispecies systems (referred to as “holobionts”) can in certain circumstances evolve as unique biological individual, thus being a unit of selection in evolution. If this is so, then it is arguably the case that some biological adaptations have evolved at the level of the multispecies system, what we call hologenomic adaptations. However, no research has yet been devoted to investigating their nature, or how these adaptations can be distinguished from adaptations at (...) the species-level (genomic adaptations). In this paper, we cover this gap by investigating the nature of hologenomic adaptations. By drawing on the case of the evolution of sanguivory diet in vampire bats, we argue that a trait constitutes a hologenomic adaptation when its evolution can only be explained if the holobiont is considered the biological individual that manifests this adaptation, while the bacterial taxa that bear the trait are only opportunistic beneficiaries of it. We then use the philosophical notions of emergence and inter-identity to explain the nature of this form of individuality and argue why it is special of holobionts. Overall, our paper illustrates how the use of philosophical concepts can illuminate scientific discussions, in the trend of what has recently been called metaphysics of biology. (shrink)

The article proposes to further develop the ideas of the Extended Evolutionary Synthesis by including into evolutionary research an analysis of phenomena that occur above the organismal level. We demonstrate that the current Extended Synthesis is focused more on individual traits (genetically or non-genetically inherited) and less on community system traits (synergetic/organizational traits) that characterize transgenerational biological, ecological, social, and cultural systems. In this regard, we will consider various communities that are made up of interacting populations, and for which the (...) individual members can belong to the same or to different species. Examples of communities include biofilms, ant colonies, symbiotic associations resulting in holobiont formation, and human societies. The proposed model of evolution at the level of communities revises classic theorizing on the major transitions in evolution by analyzing the interplay between community/social traits and individual traits, and how this brings forth ideas of top-down regulations of bottom-up evolutionary processes (collaboration of downward and upward causation). The work demonstrates that such interplay also includes reticulate interactions and reticulate causation. In this regard, we exemplify how community systems provide various non-genetic ‘scaffoldings’, ‘constraints’, and ‘affordances’ for individual and sociocultural evolutionary development. Such research complements prevailing models that focus on the vertical transmission of heritable information, from parent to offspring, with research that instead focusses on horizontal, oblique and even reverse information transmission, going from offspring to parent. We call this reversed information transfer the ‘offspring effect’ to contrast it from the ‘parental effect’. We argue that the proposed approach to inheritance is effective for modelling cumulative and distributed developmental process and for explaining the biological origins and evolution of language. (shrink)

To enable microbial colonisation of the gut mucosa, the intestinal immune system must not only react to danger signals but also recognize cues that indicate safety. Safety recognition, paradoxically, is mediated by the same environmental sensors that are involved in signalling danger. Indeed, in addition to their well established role in inducing inflammation in response to stress signals, pattern recognition receptors (PRRs) and a variety of metabolic sensors also promote gut-microbiota symbiosis by responding to "microbial symbiosis factors", "resolution-associated molecular patterns", (...) markers of energy extraction and other signals indicating the absence of pathogenic infection and tissue damage. Here we focus on how the paradoxical role of immune receptors and other environmental sensors define the microbiota signature of the individual. (shrink)

This paper introduces the reconstitutor as a comprehensive unit of heredity within the context of evolutionary research. A reconstitutor is the structure resulting from a set of relationships between different elements or processes that are actively involved in the recreation of a specific phenotypic variant in each generation regardless of the biomolecular basis of the elements or whether they stand in a continuous line of ancestry. Firstly, we justify the necessity of introducing the reconstitutor by showing the limitations of other (...) evolutionary conceptions of the unit of heredity, such as the replicator, the reproducer, and the Darwinian individual. We argue that these conceptions are based on the requirement of lineage formation, which we argue to be unnecessary for the existence of evolutionary heredity. In the second part, we introduce the reconstitutor, which we base on the concept of Stability of Traits, and illustrate how it covers cases of hereditary phenomena not covered by the previous accounts. Secondly, we illustrate how the reconstitutor could serve as a platform to rethink ecological inheritance and other forms of inheritance that have been recently introduced under the song/singer model of evolution. (shrink)