Does Biology Need an Organism Concept?

Among biologists, there is no general agreement on exactly what entities qualify as ‘organisms’. Instead, there are multiple competing organism concepts and definitions. While some authors think this is a problem that should be corrected, others have suggested that biology does not actually need an organism concept. We argue that the organism concept is central to biology and should not be abandoned. Both organism concepts and operational definitions are useful. We review criteria used for recognizing organisms and conclude that they are not categorical but rather continuously variable. Different organism concepts are useful for addressing different questions, and it is important to be explicit about which is being used. Finally, we examine the origins of the derived state of organismality, and suggest that it may result from positive feedback between natural selection and functional integration in biological entities.     

Cancer Development and Progression: A Non-Adaptive Process Driven by Genetic Drift

The current mainstream in cancer research favours the idea that malignant tumour initiation is the result of a genetic mutation. Tumour development and progression is then explained as a sort of micro-evolutionary process, whereby an initial genetic alteration leads to abnormal proliferation of a single cell that leads to a population of clonally derived cells. It is widely claimed that tumour progression is driven by natural selection, based on the assumption that the initial tumour cells acquire some properties that endow such cells with a selective advantage over the normal cells from which the tumour cells are derived. The standard view assumes that the transformed bodily cell somehow acquires "responsiveness" to natural selection independently of the whole organism to which the cell belongs. Yet, it is never explained where such an acquired capacity to respond to natural selection by the individual bodily cell comes from. This situation poses many difficult questions that so far have been left unanswered. For example, there is no explanation why some cells belonging to an organised whole and as such having no independent capacity for survival, apparently become 'independent' entities, able to respond to selective pressures in an autonomous fashion and then to be evaluated by natural selection. Hereunder it is argued that such a qualitative change cannot be the consequence of specific genetic mutations. Moreover, it is shown that natural selection is unlikely to be acting within the organism during tumour development and progression and that tumour evolution is a random, non-adaptive process, driven by no fundamental biological principle. Thus, mutations in the so-called oncogenes and tumour suppressor genes observed in epithelial cancers (that constitute more than 90% of all cancers) are not the result of selection for better cellular growth or survival under restrictive conditions. Instead, here it is suggested that they are the consequence of genetic drift acting upon gene functions that become non-relevant, either for the individual or the species fitness, once the organism is past its reproductive prime and as such, they also become superfluous for cell survival in the short term. It is proposed that the origin of cancer is epigenetic and it is a consequence of the need for a continued turnover of the individuals that constitute a species.     

What is an organism? An immunological answer

The question, "What is an organism?," formerly considered as essential in biology, has now been increasingly replaced by a larger question, "What is a biological individual?" On the grounds that i) individuation is theory-dependent, and ii) physiology does not offer a theory, biologists and philosophers of biology have claimed that it is the theory of evolution by natural selection that tells us what counts as a biological individual. Here I show that one physiological field, immunology, offers a theory that makes possible a biological individuation based on physiological grounds. I give a new answer to the question of the individuation of an organism by linking together the evolutionary and the immunological approaches to biological individuation.     

Evolution without speciation but with selection: LUCA, the Last Universal Common Ancestor in Gilbert's RNA world

This is not an attempt to analyze the Last Universal Common Ancestor (LUCA) to understand the origin of living systems. We do not know what came before Gilberts' RNA world. Our analysis starts with the RNA world and with genes (biological replicators alla Dawkings) made up of RNA proteins with enzymatic catalytic functions within units that are not yet modern cells. We offer a scenario where cellular entities are very simple and without individuality; they are only simple primary units of selection (the first level of selection) in which replicators compete in the most Darwinian manner, totally deprived of cooperation and interactions among genes. The information processing system of this RNA world is inaccurate and inefficient when compared to that found in organisms that came later. Among the "genes" and the entities that harbor them, high mutation rate was the most prevalent source of variability and the only inheritance was through lateral gene transfer of mobile elements. There were no chromosomes or any other genomic organization. As millions of years accumulated, complex and organized biological structures and processes evolved thanks to the variability mustered up mostly by lateral gene transfers and mutations. With micro- and mini-satellites, lateral gene transfers became indispensable devices of selection to mold variability. Competition and Darwinian selection gave way to a new transition in evolution, one I consider ineluctable, in which cooperation among interactive genes prevailed for the sake of higher fitness. Compartmentalization constituted a major transition in evolution that spurted new types of genome organization. Minichromosomes is one of these; cellular membranes and cytoplasmic structures completed the picture of the primitive cell. However, the much talked about phylogenetic tree does not exit in that ancient LUCA. The tree has no organism at its base; only clusters of genes evoke a fragile beginning for the increasingly complex cell types that were to emerge later.     

Individuals,groups, fitness and utility: multi-level selection meets social choice theory

In models of multi-level selection, the property of Darwinian fitness is attributed to entities at more than one level of the biological hierarchy, e.g. individuals and groups. However, the relation between individual and group fitness is a controversial matter. Theorists disagree about whether group fitness should always, or ever, be defined as total (or average) individual fitness. This paper tries to shed light on the issue by drawing on work in social choice theory, and pursuing an analogy between fitness and utility. Social choice theorists have long been interested in the relation between individual and social utility, and have identified conditions under which social utility equals total (or average) individual utility. These ideas are used to shed light on the biological problem.     

A note on frequency dependence and the levels/units of selection

On the basis of distinctions between those properties of entities that can be defined without reference to other entities and those that (in different ways) cannot, this note argues that non-trivial forms of frequency-dependent selection of entities should be interpreted as selection occurring at a level higher than that of those entities. It points out that, except in degenerately simple cases, evolutionary game-theoretic models of selection are not models of individual selection. Similarly, models of genotypic selection such as heterosis cannot be legitimately interpreted as models of genic selection. The analysis presented here supports the views that: (i) selection should be viewed as a multi-level process; (ii) upper-level selection is ubiquitous; (iii) kin selection should be viewed as a type of group selection rather than individual selection; and (iv) inclusive fitness is not an individual property.

The genetical theory of multilevel selection

The theory of multilevel selection (MLS) is beset with conceptual difficulties. Although it is widely agreed that covariance between group trait and group fitness may arise in the natural world and drive a response to ‘group selection’, ambiguity exists over the precise meaning of group trait and group fitness and as to whether group selection should be defined according to changes in frequencies of different types of individual or different types of group. Moreover, the theory of MLS has failed to properly engage with the problem of class structure, which greatly limits its empirical application to, for example, social insects whose colonies are structured into separate age, sex, caste and ploidy classes. Here, I develop a genetical theory of MLS, to address these problems. I show that taking a genetical approach facilitates a decomposition of group‐level traits – including reproductive success – into the separate contributions made by each constituent individual, even in the context of so‐called emergence. However, I uncover a novel problem with the group‐oriented approach: in many scenarios, it may not be possible to express a meaningful covariance between trait and fitness at the level of the social group, because the group's constituents belong to separate, irreconcilable classes.     

What is an "organism"? On the occurrence of a new term and its conceptual transformations 1680-1850

The essay reconstructs the occurrence of the term "organism" and the transformations of its concept from around 1680 to the middle of the nineteenth century. The different sections refer to individual authors who used the word "organism" and situate its usage in specific historical contexts. After earlier uses of the word in medieval sources, the Latin word "organismus" appeared in 1684 in Stahl's medico-physiological writings. Around 1700, it can be found in French (organisme), English (organism), Italian (organismo) and later also in German (Organismus). During the eighteenth century, the word "organism" generally referred to a specific principle or form of order, often in opposition to the order of "mechanism," that could be applied to plants, animals or the entire world. At the end of the eighteenth century, the term became a generic name for individual living entities with inside-outside-interfaces and an inner "organization" of parts. From around 1830, the word "organism" replaced the expressions "organic" or "organized body" as a recurrent technical term in the emerging biological disciplines.     

Natural Selection: A Misnomer Concept

Charles Robert Darwin hypothesized that the mechanism of evolution and the diversity of life on earth are because of natural selection. That is, which biological entity would thrive on earth is a matter of selection by the nature. But, in the present article it is hypothesized that the process of appearance of different types of biological entities and the orientation of these organisms in the space in respect to time are the effects of ‘will force’ of the organisms concerned. That is, the mechanism of evolution is a process of self selection, not natural selection.     

Causal Regularities in the Biological World of Contingent Distributions

Former discussions of biological generalizations have focused on the question of whether there are universal laws of biology. These discussions typically analyzed generalizations out of their investigative and explanatory contexts and concluded that whatever biological generalizations are, they are not universal laws. The aim of this paper is to explain what biological generalizations are by shifting attention towards the contexts in which they are drawn. I argue that within the context of any particular biological explanation or investigation, biologists employ two types of generations. One type identifies causal regularities exhibited by particular kinds of biological entities. The other type identifies how these entities are distributed in the biological world.     

Gene name ambiguity of eukaryotic nomenclatures

MOTIVATION: With more and more scientific literature published online, the effective management and reuse of this knowledge has become problematic. Natural language processing (NLP) may be a potential solution by extracting, structuring and organizing biomedical information in online literature in a timely manner. One essential task is to recognize and identify genomic entities in text. 'Recognition' can be accomplished using pattern matching and machine learning. But for 'identification' these techniques are not adequate. In order to identify genomic entities, NLP needs a comprehensive resource that specifies and classifies genomic entities as they occur in text and that associates them with normalized terms and also unique identifiers so that the extracted entities are well defined. Online organism databases are an excellent resource to create such a lexical resource. However, gene name ambiguity is a serious problem because it affects the appropriate identification of gene entities. In this paper, we explore the extent of the problem and suggest ways to address it. RESULTS: We obtained gene information from 21 organisms and quantified naming ambiguities within species, across species, with English words and with medical terms. When the case (of letters) was retained, official symbols displayed negligible intra-species ambiguity (0.02%) and modest ambiguities with general English words (0.57%) and medical terms (1.01%). In contrast, the across-species ambiguity was high (14.20%). The inclusion of gene synonyms increased intra-species ambiguity substantially and full names contributed greatly to gene-medical-term ambiguity. A comprehensive lexical resource that covers gene information for the 21 organisms was then created and used to identify gene names by using a straightforward string matching program to process 45,000 abstracts associated with the mouse model organism while ignoring case and gene names that were also English words. We found that 85.1% of correctly retrieved mouse genes were ambiguous with other gene names. When gene names that were also English words were included, 233% additional 'gene' instances were retrieved, most of which were false positives. We also found that authors prefer to use synonyms (74.7%) to official symbols (17.7%) or full names (7.6%) in their publications. CONTACT: lifeng.chen@dbmi.columbia.edu     

The influence of neighbor relatedness on multilevel selection in the Great Lakes sea rocket

Natural selection can operate at the individual and group level in natural populations. This study investigates the ecological factors that determine the relative importance of individual versus group selection. In particular, it determines how the relatedness of interacting neighbors influences multilevel natural selection in a population of the Great Lakes sea rocket. Focal plants were grown in groups of siblings, groups of plants that were themselves siblings but unrelated to the focal plants, and groups of plants with mixed genotypes. Significant group selection on plant size was observed only when the neighbors were siblings but not when they were unrelated. In sibling groups, individuals with heavier stems had higher fitness, and individuals growing with heavier but shorter neighbors also had higher fitness. Thus, individual and group selection on stem weight operated in the same direction. The detection of group selection in sibling groups can be attributed in part to an increased opportunity for group selection in these groups since sibling groups differed more from one another than the other group types. In addition, the quality of the selective environment in sibling groups may have differed from that for the other group types. Group selection was therefore more prevalent in the most genetically structured sample, in which responses to group selection are also most likely to occur.     

Alternative formulations of multilevel selection

Hierarchical expansions of the theory of natural selection exist in two distinct bodies of thought in evolutionary biology, the group selection and the species selection traditions. Both traditions share the point of view that the principles of natural selection apply at levels of biological organization above the level of the individual organism. This leads them both to considermultilevel selection situations, where selection is occurring simultaneously at more than one level. Impeding unification of the theoretical approaches of the multilevel selection traditions are the different goals of investigators in the different subdisciplines and the different types of data potentially available for analysis. We identify two alternative approaches to multilevel situations, which we termmultilevel selection [1] andmultilevel selection [2]. Of interest in the former case are the effects of group membership onindividual fitnesses, and in the latter the tendencies for the groups themselves to go extinct or to found new groups (i.e., group fitnesses). We argue that: neither represents the entire multilevel selection process; both are aspects of any multilevel selection situation; and both are legitimate approaches, suitable for answering different questions. Using this formalism, we show that: multilevel selection [2] does not require emergent group properties in order to provide an explanatory mechanism of evolutionary change; multilevel selection [1] is usually more appropriate for neontological group selection studies; and species selection is most fruitfully considered from the point of view of multilevel selection [2]. Finally we argue that the effect hypothesis of macroevolution, requiring, in selection among species, both the absence of group effects on organismic fitness (multilevel selection [1]), and the direct determination of species fitnesses by those of organisms, is untestable with paleontological data. Furthermore, the conditions for the effect hypothesis to hold are extremely restrictive and unlikely to apply to the vast majority of situations encountered in nature.     

Organisms as Functional Machines: A Connectivity Explanation

Living organisms exist as a complex set of levels of organizationarranged in a pattern of strong ordering with none of theselevels being more important than others for a full understandingof life. Central to biological strong ordering is the organismallevel. Individual organisms are of special interest to biologistsbecause they are relevant to all biological processes regardlessof the operational level of the process. This is especiallytrue for investigations of the morphological-physiological propertiesof organisms. For such studies, living organisms must be consideredas complex machines with all of the sophisticated integrationand multifarious interactions of component parts typical ofcomplex systems. Understanding of the properties of any individualfeature in an organism depends as much, or possibly even more,on an appreciation of its connections and interactions withother features of that organism than on an understanding ofits intrinsic attributes. Learning the connectivity skills,including the modes of thinking, needed to comprehend the integrationof diverse components of any complex system requires a differenttraining than that needed to determine the detailed attributesof individual parts; both are necessary, however, to achieveproper advances in biological knowledge. Case studies of severalvertebrate features will be used to illustrate types of interactionswhich exist between structural/functional attributes, and howtheir recognition can lead to new and interesting questions.This "feeling for the organism" may be the major factor separatingthose biologists who are able to make important discoveriesfrom those who will only provide the subsequent, less excitingdetails of normal science.     

The Mastodon in the room: how Darwinian is neo-Darwinism?

Failing to acknowledge substantial differences between Darwinism and neo-Darwinism impedes evolutionary biology. Darwin described evolution as the outcome of interactions between the nature of the organism and the nature of the conditions, each relatively autonomous but both historically and spatially intertwined. Furthermore, he postulated that the nature of the organism was more important than the nature of the conditions, leading to natural selection as an inevitable emergent product of biological systems. The neo-Darwinian tradition assumed a creative rather than selective view of natural selection, with the nature of the organism determined by the nature of the conditions, rendering the nature of the organism and temporal contingency unnecessary. Contemporary advances in biology, specifically the phylogenetics revolution and evo-devo, underscore the significance of history and the nature of the organism in biology. Darwinism explains more biology better, and better resolves apparent anomalies between living systems and more general natural laws, than does neo-Darwinism. The "extended" or "expanded" synthesis currently called for by neo-Darwinians is Darwinism.     

The Definition and Recognition of Biological Adaptation

Biological adaptation is a property of phenotypic features oforganisms relative to selection demands of the environment.Adaptive features are ones having properties of form and functionwhich permit the organism to maintain successfully the synergbetween a biological role of that feature and a stated selectionforce. The degree of goodness of the adaptation can be measuredby means of the amount of energy needed to maintain the synergwith less energy indicating better adaptation. Adaptation doesnot apply to a close fit between different features or betweenthe form and function of a feature or to the mutual interactionsbetween features of a structural network. The state of beingadapted is independent of the process of becoming adapted asadaptations need not evolve under the control of selection forcesto which they are now adapted. Selection is here consideredas the demands placed on the organism by the environment withwhich the organism must cope to continue surviving as an individual.Adapted features have been judged using three methods—thecomparative the correlative and the synthetic—of whichonly the last is valid. The synthetic method requires studyof the forms and functions of the feature in the laboratoryand of the biological roles of the feature and the selectiondemands of the environment in the field. It is suggested thatthe best approach for the study of adaptations is a team effortwith constant feedback between the laboratory and field phasesof study. It is urged that attention be given to the developmentof an ecological morphology to supplement functional morphologyand provide the necessary foundation for proper elucidationof biological adaptations.     

Redefining viruses: lessons from Mimivirus

Viruses are the most abundant living entities and probably had a major role in the evolution of life, but are still defined using negative criteria. Here, we propose to divide biological entities into two groups of organisms: ribosome-encoding organisms, which include eukaryotic, archaeal and bacterial organisms, and capsid-encoding organisms, which include viruses. Other replicons (for example, plasmids and viroids) can be termed 'orphan replicons'. Based on this suggested classification system, we propose a new definition for a virus--a capsid-encoding organism that is composed of proteins and nucleic acids, self-assembles in a nucleocapsid and uses a ribosome-encoding organism for the completion of its life cycle.     

Morphological interpretation of darwinism

The development of evolutionary theory requires the resolution of the problem of relationships between random and regular processes in historical development of biological systems. According to the theory of natural selection, ecological factors play a leading role in evolution. Variations are nondirectional, unpredictable, and provide chaotic diversity of variants, only some of which are potentially useful. However, based on random processes, new variants that are useful for organisms and remain adaptive significance in various ecological situations are infrequent. At the same time, morphology demonstrates certain evolutionary patterns. The morphological approach takes into account the role in evolution of structural features of organism and social systems and evolutionary significance of “constructive technologies,” which distinguish morphological interpretation of evolutionary processes. The constructive and evolutionary patterns revealed in biological systems provide the basis for morphological interpretation of the principle of natural selection: both natural and artificial selection is interaction between social systems (populations, ecosystems, biogeocoenoses) and organisms composing them.     

Mirror imagery and biological selection

Lake Tanganiyka has lefty and righty cichlid fish that show there can be natural selection for a trait over its mirror image counterpart.This raises the question ‘Can there be biological selection of a whole organism over its mirror image counterpart?’ That is, could the fitness of a fish be altered by simply changing it into its own enantaniomorph? My answer is no. I present Flatlander thought experiment to demonstrate that mirror imagecounterparts are duplicates because they only differ in how they happen to be oriented in space. The counterparts have the same intrinsic properties and are in the same environment,so there can be no difference in fitness.     

Genomic imprinting and the units of adaptation

Two guiding principles identify which biological entities are able to evolve adaptations. Williams'' principle holds that, in order for an entity to evolve adaptations, there must be selection between such entities. Maynard Smith''s principle holds that, in order for an entity to evolve adaptations, selection within such entities must be absent or negligible. However, although the kinship theory of genomic imprinting suggests that parent-of-origin-specific gene expression evolves as a consequence of natural selection acting between—rather than within—individuals, it evades adaptive interpretation at the individual level and is instead viewed as an outcome of an intragenomic conflict of interest between an individual''s genes. Here, I formalize the idea that natural selection drives intragenomic conflicts of interest between genes originating from different parents. Specifically, I establish mathematical links between the dynamics of natural selection and the idea of the gene as an intentional, inclusive-fitness-maximizing agent, and I clarify the role that information about parent of origin plays in mediating conflicts of interest between genes residing in the same genome. These results highlight that the suppression of divisive information may be as important as the suppression of lower levels of selection in maintaining the integrity of units of adaptation.