A part‐dependent account of biological individuality: why holobionts are individuals and ecosystems simultaneously

Given one conception of biological individuality (evolutionary, physiological, etc.), can a holobiont – that is the host + its symbiotic (mutualistic, commensalist and parasitic) microbiome – be simultaneously a biological individual and an ecological community? Herein, we support this possibility by arguing that the notion of biological individuality is part‐dependent. In our account, the individuality of a biological ensemble should not only be determined by the conception of biological individuality in use, but also by the biological characteristics of the part of the ensemble under investigation. In the specific case of holobionts, evaluations of their individuality should be made either host‐relative or microbe‐relative. We support the claim that biological individuality is part‐dependent by drawing upon recent empirical evidence regarding the physiology of hosts and microbes, and the recent characterization of the ‘demibiont’. Our account shows that contemporary disagreements about the individuality of the holobiont derive from an incorrect understanding of the ontology of biological individuality. We show that collaboration between philosophers and biologists can be very fruitful in attempts to solve some contemporary biological debates.     

The animal sensorimotor organization: a challenge for the environmental complexity thesis

Godfrey-Smith’s environmental complexity thesis (ECT) is most often applied to multicellular animals and the complexity of their macroscopic environments to explain how cognition evolved. We think that the ECT may be less suited to explain the origins of the animal bodily organization, including this organization’s potentiality for dealing with complex macroscopic environments. We argue that acquiring the fundamental sensorimotor features of the animal body may be better explained as a consequence of dealing with internal bodily—rather than environmental complexity. To press and elucidate this option, we develop the notion of an animal sensorimotor organization (ASMO) that derives from an internal coordination account for the evolution of early nervous systems. The ASMO notion is a reply to the question how a collection of single cells can become integrated such that the resulting multicellular organization becomes sensitive to and can manipulate macroscopic features of both the animal body and its environment. In this account, epithelial contractile tissues play the central role in the organization behind complex animal bodies. In this paper, we relate the ASMO concept to recent work on epithelia, which provides empirical evidence that supports central assumptions behind the ASMO notion. Second, we discuss to what extent the notion applies to basic animal architectures, exemplified by sponges and jellyfish. We conclude that the features exhibited by the ASMO are plausibly explained by internal constraints acting on and within this multicellular organization, providing a challenge for the role the ECT plays in this context.     

Can't see the colony for the bees: behavioural perspectives of biological individuality

The question ‘what is an individual’ does not often arise in studies within the field of behavioural ecology. Generally behavioural ecologists do not think about what makes an individual because they tend to use intuitive working concepts of individuality. Rarely do they explicitly mention how individuality affects their experimental design and interpretation of results. By contrast, the concept of individuality continues to intrigue philosophers of biology. It is interesting that while philosophers of biology debate definitions of individuality, biologists generally use the concept of individuality every day without much thought. Here we review the philosophical approaches to defining biological individuality, and illustrate how the biological individuality concepts used by biologists are affected by their study question and choice of organism. We clarify the behavioural perspective of biological individuality by introducing the concept of the behavioural individual. The notion of the behavioural individual is particularly interesting when explored in less‐conventional study organisms. By including less‐conventional organisms, it becomes clear why the concept of biological individuality is usually intuitive in behavioural ecology.     

Error management,reliability and cognitive evolution

The paper offers a partial vindication of Sterelny’s view on the role of error rates and reliability in his theory of decoupled representation based on modelling techniques borrowed from the biological literature on evolution in stochastic environments. In the case of a tight link between tracking states and behaviour, I argue that in its full generality Sterelny’s account instantiates the base-rate fallacy. With regard to non-tightly linked behaviour, I show that Sterelny’s account can be vindicated subject to an adequate evolutionary model and a suitable notion of reliability.     

Moving Past the Systematics Wars

It is time to escape the constraints of the Systematics Wars narrative and pursue new questions that are better positioned to establish the relevance of the field in this time period to broader issues in the history of biology and history of science. To date, the underlying assumptions of the Systematics Wars narrative have led historians to prioritize theory over practice and the conflicts of a few leading theorists over the less-polarized interactions of systematists at large. We show how shifting to a practice-oriented view of methodology, centered on the trajectory of mathematization in systematics, demonstrates problems with the common view that one camp (cladistics) straightforwardly “won” over the other (phenetics). In particular, we critique David Hull’s historical account in Science as a Process by demonstrating exactly the sort of intermediate level of positive sharing between phenetic and cladistic theories that undermines their mutually exclusive individuality as conceptual systems over time. It is misleading, or at least inadequate, to treat them simply as holistically opposed theories that can only interact by competition to the death. Looking to the future, we suggest that the concept of workflow provides an important new perspective on the history of mathematization and computerization in biology after World War II.     

In defense of the organism

Thomas Pradeu’s The Limits of the Self provides a precise account of biological identity developed from the central concepts of immunology. Yet the central concepts most relevant to this task (self and nonself) are themselves deemed inadequate, suffering from ambiguity and imprecision. Pradeu seeks to remedy this by proposing a new guiding theory for immunology, the continuity theory. From this, an account of biological identity is provided in terms of uniqueness and individuality, ultimately leading to a defense of the heterogeneous organism as expressing the highest degree of individuality.     

Symbiosis as the way of eukaryotic life: The dependent co-origination of the body

Molecular analyses of symbiotic relationships are challenging our biological definitions of individuality and supplanting them with a new notion of normal part–whole relationships. This new notion is that of a ‘holobiont’, a consortium of organisms that becomes a functionally integrated ‘whole’. This holobiont includes the zoological organism (the ‘animal’) as well as its persistent microbial symbionts. This new individuality is seen on anatomical and physiological levels, where a diversity of symbionts form a new ‘organ system’ within the zoological organism and become integrated into its metabolism and development. Moreover, as in normal development, there are reciprocal interactions between the ‘host’ organism and its symbionts that alter gene expression in both sets of cells. The immune system, instead of being seen as functioning solely to keep microbes out of the body, is also found to develop, in part, in dialogue with symbionts. Moreover, the immune system is actively involved in the colonization of the zoological organism, functioning as a mechanism for integrating microbes into the animal-cell community. Symbionts have also been found to constitute a second mode of genetic inheritance, providing selectable genetic variation for natural selection. We develop, grow and evolve as multi-genomic consortia/teams/ecosystems.     

‘The importance of symbiosis in philosophy of biology: an analysis of the current debate on biological individuality and its historical roots’

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.     

Biofilms and Planktonic Cells of Pseudomonas aeruginosa Have Similar Resistance to Killing by Antimicrobials

Biofilms are considered to be highly resistant to antimicrobial agents. Strictly speaking, this is not the case-biofilms do not grow in the presence of antimicrobials any better than do planktonic cells. Biofilms are indeed highly resistant to killing by bactericidal antimicrobials, compared to logarithmic-phase planktonic cells, and therefore exhibit tolerance. It is assumed that biofilms are also significantly more tolerant than stationary-phase planktonic cells. A detailed comparative examination of tolerance of biofilms versus stationary- and logarithmic-phase planktonic cells with four different antimicrobial agents was performed in this study. Carbenicillin appeared to be completely ineffective against both stationary-phase cells and biofilms. Killing by this beta-lactam antibiotic depends on rapid growth, and this result confirms the notion of slow-growing biofilms resembling the stationary state. Ofloxacin is a fluoroquinolone antibiotic that kills nongrowing cells, and biofilms and stationary-phase cells were comparably tolerant to this antibiotic. The majority of cells in both populations were eradicated at low levels of ofloxacin, leaving a fraction of essentially invulnerable persisters. The bulk of the population in both biofilm and stationary-phase cultures was tolerant to tobramycin. At very high tobramycin concentrations, a fraction of persister cells became apparent in stationary-phase culture. Stationary-phase cells were more tolerant to the biocide peracetic acid than were biofilms. In general, stationary-phase cells were somewhat more tolerant than biofilms in all of the cases examined. We concluded that, at least for Pseudomonas aeruginosa, one of the model organisms for biofilm studies, the notion that biofilms have greater resistance than do planktonic cells is unwarranted. We further suggest that tolerance to antibiotics in stationary-phase or biofilm cultures is largely dependent on the presence of persister cells.     

Environmental complexity,adaptability and bacterial cognition: Godfrey-Smith’s hypothesis under the microscope

The paper presents evidence in bacteria for the utility of Godfrey-Smith’s environmental complexity thesis (ECT), using certain kinds of signal transduction systems as proxies for cognitive/behavioral complexity. Microbiologists already accept that the number of signal transduction proteins in a bacterial genome indicates the level of ecological complexity to which the organism is subject: the more signalling proteins, the greater the complexity. Sheer numbers are not always a reliable indicator of behavioral complexity, however. The paper proposes a new, ECT-based procedure for identifying, from genomic sequence and signalling repertoire, novel bacterial candidates likely to exhibit behavioral complexity in response to a complex ecological niche.     

Slow axoplasmic transport: a fiction?

Ribosomes have not been observed in axoplasm. This had led to the notions that the perikaryon is the only source of neuronal proteins and that the axoplasm is supplied by a (slow) transport mechanism. However, we question these two notions because they are unable to give an account of real neurones in accordance with the body of biological knowledge. We point out, for example, that the synthetic rate of perikarya or the life span of axoplasmic proteins should be beyond known ranges for animal cells and that a uniform axon is unlikely to result if it is fed from one end. We propose an alternative view for the maintenance of the axon which accepts the controversial idea of axoplasmic synthesis of proteins; as a result, the slow transport becomes unnecessary. Our view gives a qualitative account of the observations dealing with the maintenance of the axoplasm. To account for the phenomenology in a more quantitative fashion, a computer simulation was carried out where the equations of the program provided only for axoplasmic synthesis of proteins; the set of curves retrieved were in good agreement with experimental findings believed so far to support the notion of slow transport. In conclusion, we think that the notion of "slow axoplasmic transport" has been a misinterpretation of good observations because the frame of reference was incomplete in not providing for axoplasmic synthesis of proteins.     

The adaptive importance of cognitive efficiency: an alternative theory of why we have beliefs and desires

Finding out why we have beliefs and desires is important for a thorough understanding of the nature of our minds (and those of other animals). It is therefore unsurprising that several accounts have been presented that are meant to answer this question. At least in the philosophical literature, the most widely accepted of these are due to Kim Sterelny and Peter Godfrey-Smith, who argue that beliefs and desires evolved due to their enabling us to be behaviourally flexible in a way that reflexes do not—which, they claim, is beneficial in epistemically complex environments. However, as I try to make clear in this paper, upon closer consideration, this kind of account turns out to be theoretically implausible. In the main, this is because it fails to give due credit to the powers of reflex-driven organisms, which can in fact be just as flexible in their behaviour as ones that are belief/desire-driven. In order to improve on this account, I therefore propose that beliefs and desires evolved, not due to their enabling us to do something completely different from what reflexive organisms can do, but rather due to their enabling us to do the same things better. Specifically, I argue that beliefs and desires evolved for making the generation of behaviour more efficient, since they can simplify the necessary cognitive labour considerably. I end by considering various implications of this account.     

Synthetic biology and its alternatives. Descartes,Kant and the idea of engineering biological machines

The engineering-based approach of synthetic biology is characterized by an assumption that ‘engineering by design’ enables the construction of ‘living machines’. These ‘machines’, as biological machines, are expected to display certain properties of life, such as adapting to changing environments and acting in a situated way. This paper proposes that a tension exists between the expectations placed on biological artefacts and the notion of producing such systems by means of engineering; this tension makes it seem implausible that biological systems, especially those with properties characteristic of living beings, can in fact be produced using the specific methods of engineering. We do not claim that engineering techniques have nothing to contribute to the biotechnological construction of biological artefacts. However, drawing on Descartes’s and Kant’s thinking on the relationship between the organism and the machine, we show that it is considerably more plausible to assume that distinctively biological artefacts emerge within a paradigm different from the paradigm of the Cartesian machine that underlies the engineering approach. We close by calling for increased attention to be paid to approaches within molecular biology and chemistry that rest on conceptions different from those of synthetic biology’s engineering paradigm.     

Niche construction,adaptive preferences,and the differences between fitness and utility

A number of scholars have recently defended the claim that there is a close connection between the evolutionary biological notion of fitness and the economic notion of utility: both are said to refer to an organism’s success in dealing with its environment, and both are said to play the same theoretical roles in their respective sciences. However, an analysis of two seemingly disparate but in fact structurally related phenomena—‘niche construction’ (the case where organisms change their environment to make it fit to their needs) and ‘adaptive preferences’ (the case where agents change their wants to make them fit to what the world has given them)—shows that one needs to be very careful about the postulation of this sort of fitness–utility connection. Specifically, I here use the analysis of these two phenomena to establish when connecting fitness and utility is and is not possible.     

Organisms or biological individuals? Combining physiological and evolutionary individuality

The definition of biological individuality is one of the most discussed topics in philosophy of biology, but current debate has focused almost exclusively on evolution-based accounts. Moreover, several participants in this debate consider the notions of a biological individual and an organism as equivalent. In this paper, I show that the debates would be considerably enriched and clarified if philosophers took into account two elements. First, physiological fields are crucial for the understanding of biological individuality. Second, the category of biological individuals should be divided into two subcategories: physiological individuals and evolutionary individuals, which suggests that the notions of organism and biological individual should not be used interchangeably. I suggest that the combination of an evolutionary and a physiological perspective will enable biologists and philosophers to supply an account of biological individuality that will be both more comprehensive and more in accordance with scientific practices.     

Integrated But Not Whole? Applying an Ontological Account of Human Organismal Unity to the Brain Death Debate

As is clear in the 2008 report of the President's Council on Bioethics, the brain death debate is plagued by ambiguity in the use of such key terms as ‘integration’ and ‘wholeness’. Addressing this problem, I offer a plausible ontological account of organismal unity drawing on the work of Hoffman and Rosenkrantz, and then apply that account to the case of brain death, concluding that a brain dead body lacks the unity proper to a human organism, and has therefore undergone a substantial change. I also show how my view can explain hard cases better than one in which biological integration (as understood by Alan Shewmon and the President's Council) is taken to imply ontological wholeness or unity.     

Capsule shields the function of short bacterial adhesins

Bacterial surface structures such as capsules and adhesins are generally regarded as important virulence factors. Here we demonstrate that capsules block the function of the self-recognizing protein antigen 43 through physical shielding. The phenomenon is not restricted to Escherichia coli but can occur in other gram-negative bacteria. Likewise, we show that other short adhesins exemplified by the AIDA-I protein are blocked by the presence of a capsule. The results support the notion that capsule polysaccharides sterically prevent receptor-target recognition of short bacterial adhesins. This negative interference has important biological consequences, such as affecting the ability of bacteria to form biofilms.     

γ-Alkylidene-γ-lactones and isobutylpyrrol-2(5H)-ones analogues to rubrolides as inhibitors of biofilm formation by Gram-positive and Gram-negative bacteria

Several molecules have been discovered that interfere with formation of bacterial biofilms, opening a new strategy for the development of more efficient treatments in case of antibiotic resistant bacteria. Amongst the most active compounds are some natural brominated furanones from marine algae Delisea pulchra that have proven to be able to control pathogenic biofilms. We have recently reported that some rubrolide analogues are able to inhibit biofilm formation of Enterococcus faecalis. In the present Letter we describe results of the biological evaluation of a small library of 28 compounds including brominated furanones and the corresponding lactams against biofilm formation of Staphylococcus aureus, Pseudomonas aeruginosa, Staphylococcus epidermidis and Streptococcus mutans. Our results showed that in general these compounds were more active against biofilms of S. epidermidis and P. aeruginosa, with little or no inhibition of planktonic bacterial growth. In some cases they were able to prevent biofilm formation of P. aeruginosa at concentrations as low as 0.6 μg/mL (1.3 μM, compound 3d) and 0.7 μg/mL (1.3 μM, 3f). Results also indicate that, in general, lactams are more active against biofilms than their precursors, thus designating this class of molecules as good candidates for the development of a new generation of antimicrobial drugs targeted to biofilm inhibition.     

Crossing scales,crossing disciplines: collective motion and collective action in the Global Commons

Two conflicting tendencies can be seen throughout the biological world: individuality and collective behaviour. Natural selection operates on differences among individuals, rewarding those who perform better. Nonetheless, even within this milieu, cooperation arises, and the repeated emergence of multicellularity is the most striking example. The same tendencies are played out at higher levels, as individuals cooperate in groups, which compete with other such groups. Many of our environmental and other global problems can be traced to such conflicts, and to the unwillingness of individual agents to take account of the greater good. One of the great challenges in achieving sustainability will be in understanding the basis of cooperation, and in taking multicellularity to yet a higher level, finding the pathways to the level of cooperation that is the only hope for the preservation of the planet.