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.     

Biological individuality: the case of biofilms

This paper examines David Hull’s and Peter Godfrey-Smith’s accounts of biological individuality using the case of biofilms. Biofilms fail standard criteria for individuality, such as having reproductive bottlenecks and forming parent-offspring lineages. Nevertheless, biofilms are good candidates for individuals. The nature of biofilms shows that Godfrey-Smith’s account of individuality, with its reliance on reproduction, is too restrictive. Hull’s interactor notion of individuality better captures biofilms, and we argue that it offers a better account of biological individuality. However, Hull’s notion of interactor needs more precision. We suggest some ways to make Hull’s notion of interactor and his account of individuality more precise. Generally, we maintain that biofilms are a good test case for theories of individuality, and a careful examination of biofilms furthers our understanding of biological individuality.     

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.     

Cellular differentiation and individuality in the ‘minor’ multicellular taxa

Biology needs a concept of individuality in order to distinguish organisms from parts of organisms and from groups of organisms, to count individuals and compare traits across taxa, and to distinguish growth from reproduction. Most of the proposed criteria for individuality were designed for ‘unitary’ or ‘paradigm’ organisms: contiguous, functionally and physiologically integrated, obligately sexually reproducing multicellular organisms with a germ line sequestered early in development. However, the vast majority of the diversity of life on Earth does not conform to all of these criteria. We consider the issue of individuality in the ‘minor’ multicellular taxa, which collectively span a large portion of the eukaryotic tree of life, reviewing their general features and focusing on a model species for each group. When the criteria designed for unitary organisms are applied to other groups, they often give conflicting answers or no answer at all to the question of whether or not a given unit is an individual. Complex life cycles, intimate bacterial symbioses, aggregative development, and strange genetic features complicate the picture. The great age of some of the groups considered shows that ‘intermediate’ forms, those with some but not all of the traits traditionally associated with individuality, cannot reasonably be considered ephemeral or assumed transitional. We discuss a handful of recent attempts to reconcile the many proposed criteria for individuality and to provide criteria that can be applied across all the domains of life. Finally, we argue that individuality should be defined without reference to any particular taxon and that understanding the emergence of new kinds of individuals requires recognizing individuality as a matter of degree.     

Quality prevails over identity in the sexually selected vocalisations of an ageing mammal

Background

Male sexually selected vocalisations generally contain both individuality and quality cues that are crucial in intra- as well as inter-sexual communication. As individuality is a fixed feature whereas male phenotypic quality changes with age, individuality and quality cues may be subjected to different selection pressures over time. Individuality (for example, morphology of the vocal apparatus) and quality (for example, body size and dominance status) can both affect the vocal production mechanism, inducing the same components of vocalisations to convey both kinds of information. In this case, do quality-related changes to the acoustic structure of calls induce a modification of vocal cues to identity from year to year? We investigated this question in fallow deer (Dama dama), in which some acoustic parameters of vocalisations (groans) code for both individuality and quality.

Results

We carried out a longitudinal analysis of groan individuality, examining the effects of age and dominance rank on the acoustic structure of groans of the same males recorded during consecutive years. We found both age- and rank-related changes to groans; the minimum values of the highest formant frequencies and the fundamental frequency increased with the age of males and they decreased when males became more dominant. Both age- and rank-related acoustic parameters contributed to individuality. Male quality changed with age, inducing a change in quality-related parameters and thus, a modification of vocal cues to male individuality between years.

Conclusions

The encoding of individuality and quality information in the same components of vocalisations induces a tradeoff between these two kinds of signals over time. Fallow deer vocalisations are honest signals of quality that are not fixed over time but are modified dynamically according to male quality. As they are more reliable cues to quality than to individuality, they may not be used by conspecifics to recognize a given male from one year to another, but potentially used by both sexes to assess male quality during each breeding season.

     

The role of vocal individuality in conservation

Identifying the individuals within a population can generate information on life history parameters, generate input data for conservation models, and highlight behavioural traits that may affect management decisions and error or bias within census methods. Individual animals can be discriminated by features of their vocalisations. This vocal individuality can be utilised as an alternative marking technique in situations where the marks are difficult to detect or animals are sensitive to disturbance. Vocal individuality can also be used in cases were the capture and handling of an animal is either logistically or ethically problematic. Many studies have suggested that vocal individuality can be used to count and monitor populations over time; however, few have explicitly tested the method in this role. In this review we discuss methods for extracting individuality information from vocalisations and techniques for using this to count and monitor populations over time. We present case studies in birds where vocal individuality has been applied to conservation and we discuss its role in mammals.     

Individuality in male songs of wild black crested gibbons (Nomascus concolor)

This is the first study of vocal individuality in male songs of black crested gibbons. The sound recordings were carried out at two field sites, Pinghe, Ailao Mountains, and Dazhaizi, Wuliang Mountains, both located in Yunnan province, China. A total of 127 coda phrases of 38 male songs bouts of eight individual male gibbons were analyzed. Stepwise discriminant function analysis was used to examine the acoustic individuality of the males. We found that individuality among neighbors was very pronounced. Moreover, individuality within a site (i.e. among neighbors) is higher than among individuals between sites. Our finding suggests that black crested gibbons may actively increase their degree of vocal individuality against that of their immediate neighbors by vocal adjustment.     

The many faces of biological individuality

Biological individuality is a major topic of discussion in biology and philosophy of biology. Recently, several objections have been raised against traditional accounts of biological individuality, including the objections of monism (the tendency to focus on a single individuality criterion and/or a single biological field), theory-centrism (the tendency to discuss only theory-based individuation), ahistoricity (the tendency to neglect what biologists of the past and historians of biology have said about biological individuality), disciplinary isolationism (the tendency to isolate biological individuality from other scientific and philosophical domains that have investigated individuality), and the multiplication of conceptual uncertainties (the lack of a precise definition of “biological individual” and related terms). In this introduction, I will examine the current philosophical landscape about biological individuality, and show how the contributions gathered in this special issue address these five objections. Overall, the aim of this issue is to offer a more diverse, unifying, and scientifically informed conception of what a biological individual is.     

Individuality,subjectivity, and minimal cognition

The paper links discussions of two topics: biological individuality and the simplest forms of mentality. I discuss several attempts to locate the boundary between metabolic activity and ‘minimal cognition.’ I then look at differences between the kinds of individuality present in unicellular life, multicellular life in general, and animals of several kinds. Nervous systems, which are clearly relevant to cognition and subjectivity, also play an important role in the form of individuality seen in animals. The last part of the paper links these biological transitions to the evolutionary history of subjective experience.     

Individuality and the existence of species through time

The individuality of species provides the basis for linking practical taxonomy with evolutionary and ecological theory. An individual is here defined as a collection of parts (lower-level entities) that are mutually connected. Different types of species individual exist, based on different types of connection between organisms. An interbreeding species is a group of organisms connected by the potential to share common descendants, whereas a genealogical species is integrated by the sharing of common ancestors. Such species definitions serve to set the limits of species at a moment of time and these slices connect through time to form time-extended lineages. This perspective on the nature of individuality has implications that conflict with traditional views of species and lineages: (1) Several types of connections among organisms may serve to individuate species in parallel (species pluralism); (2) each kind of species corresponds to a distinct kind of lineage; (3) although lineage branching is the most obvious criterion to break lineages into diachronic species, it cannot be justified simply by reference to species individuality; (4) species (like other individuals) have fuzzy boundaries; (5) if we wish to retain a species rank, we should focus on either the most- or least-inclusive individual in a nested series; (6) not all organisms will be in any species; and (7) named species taxa are best interpreted as hypotheses of real species. Although species individuality requires significant changes to systematic practice and challenges some preconceptions we may have about the ontology of species, it provides the only sound basis for asserting that species exist independently of human perception.     

Leibnizian organisms,nested individuals,and units of selection

Summary Leibniz developed a new notion of individuality, according to which individuals are nested one within another, thereby abandoning the Aristotelian formula at the heart of substantialist metaphysics, ‘one body, one substance’. On this model, the level of individuality is determined by the degree of activity, and partly defined by its relations with other individuals. In this article, we show the importance of this new notion of individuality for some persisting questions in theoretical biology. Many evolutionary theorists presuppose a model of individuality that will eventually reduce to spatiotemporal mechanisms, and some still look for an exclusive level or function to determine a unit of selection. In recent years, a number of alternatives to these exclusive approaches have emereged, and no consensus can be foreseen. It is for this reason that we propose the model of nested individuals. This model supports pluralistic multi-level selection and rejects an exclusive level or function for a unit of selection. Since activity is essential to the unity of an individual, this model focuses on integrating processes of interaction and replication instead of choosing between them. In addition, the model of nested individuals may also be seen as a distinct perspective among the various alternative models for the unit of selection. This model stresses activity and pluralism: it accepts simultaneuous co-existence of individuals at different levels, nested one within the other. Our aim in this article is to show now a chapter of the history of metaphysics may be fruitfully brought to bear on the current debate over the unit of selection in evolutionary biology.     

The individuality of artifacts and organisms

Is there any genuine difference between organisms and artifacts? Where and how would we identify such a difference? This paper argues the difference involves the character of their individuality. Unlike an organism, an artifact's individuality is (for the most part) determined by the function that the designer selected in the artifact's production rather than the functional interdependence of its parts. In both cases, individuality is a historical property and in both cases the parts may be functionally interdependent to some extent. However, for artifacts, this interdependence is not what makes it the individual that it is. Instead, the interdependence of its parts is in the service of the functions for which the spear was designed. No such additional purpose or function exists for an organism.     

The individuality thesis (3 ways)

I spell out and update the individuality thesis, that species are individuals, and not classes, sets, or kinds. I offer three complementary presentations of this thesis. First, as a way of resolving an inconsistent triad about natural kinds; second, as a phylogenetic systematics theoretical perspective; and, finally, as a novel recursive account of an evolved character (individuality). These approaches do different sorts of work, serving different interests. Presenting them together produces a taxonomy of the debates over the thesis, and isolates ways it has been (and may continue to be) productive. This goes to the larger point of this paper: a defense of the individuality thesis in terms of its utility, and an update of it in light of recent theoretical developments and empirical work in biology.     

Individuality of contact calls in the Greater Flamingo Phoenicopterus ruber and the problem of background noise in a colony

Acoustic communication has great importance in social relationships and especially in individual recognition in the Greater Flamingo Phoenicopterus ruber. However, it is constrained by the noisy environment of the colony. I performed an analysis of both the temporal and frequency patterns of contact calls and showed that the use of both is essential for discrimination between individuals. I made a search for the acoustic parameters which are used by the flamingos. It appears that the call duration, the slow amplitude modulation, the spectrum bandwidth and the repartition of energy among harmonics exhibit individuality. Recognition between the birds must be based on a multiparametric analysis, taking into account both spectral and temporal features of the calls. Indeed, no single parameter was sufficient to discriminate between individual birds used in my research. In the noisy environment of the colony, the transmission of individuality in a message is improved by this multiparametric coding, which can be considered as an adaptation to these extreme acoustic conditions. Moreover, the study revealed numerous acoustic convergences with another colonial bird species, the Emperor Penguin Aptenodytes forsteri , and both species seemed to use the same method to encode individuality in their vocalizations.     

Individuality in the vocalizations of infant and adult coppery titi monkeys (Plecturocebus cupreus)

As social animals, many primates use acoustic communication to maintain relationships. Vocal individuality has been documented in a diverse range of primate species and call types, many of which have presumably different functions. Auditory recognition of one's neighbors may confer a selective advantage if identifying conspecifics decreases the need to participate in costly territorial behaviors. Alternatively, vocal individuality may be nonadaptive and the result of a unique combination of genetics and environment. Pair-bonded primates, in particular, often participate in coordinated vocal duets that can be heard over long distances by neighboring conspecifics. In contrast to adult calls, infant vocalizations are short-range and used for intragroup communication. Here, we provide two separate but complementary analyses of vocal individuality in distinct call types of coppery titi monkeys (Plecturocebus cupreus) to test whether individuality occurs in call types from animals of different age classes with presumably different functions. We analyzed 600 trill vocalizations from 30 infants and 169 pulse-chirp duet vocalizations from 30 adult titi monkeys. We predicted that duet contributions would exhibit a higher degree of individuality than infant trills, given their assumed function for long-distance, intergroup communication. We estimated 7 features from infant trills and 16 features from spectrograms of adult pulse-chirps, then used discriminant function analysis with leave-one-out cross-validation to classify individuals. We correctly classified infants with 48% accuracy and adults with 83% accuracy. To further investigate variance in call features, we used a multivariate variance components model to estimate variance partitioning in features across two levels: within- and between-individuals. Between-individual variance was the most important source of variance for all features in adults, and three of four features in infants. We show that pulse-chirps of adult titi monkey duets are individually distinct, and infant trills are less individually distinct, which may be due to the different functions of the vocalizations.     

Social group size predicts the evolution of individuality

Discriminating among individuals is a critical social behavior in humans and many other animals and is often required for offspring and mate recognition, territorial or coalitional behaviors, signaler reliability assessment, and social hierarchies. Being individually discriminated is more difficult in larger groups, and large group size may select for increased individuality-signature information-in social signals, to facilitate discrimination. Small-scale studies suggest that more social species have greater individuality in their social signals, such as contact calls. However, this relationship has not been evaluated in a broader-scale evolutionary context or in social signals other than contact calls. It is not yet known whether social group size may be viewed as a general evolutionary driver of individuality. Here we show a strong positive evolutionary link between social group size in sciurid rodents and individuality in their social alarm calls. Social group size explained over 88% of the variation in vocal individuality in phylogenetic independent contrasts. Species living in larger groups, but not in more complex groups, had more signature information in their calls. Our results suggest that social group size may promote the evolution of individual signatures and that the sociality-individuality relationship may be a general phenomenon in nature.     

Functional Integration and Individuality in Prokaryotic Collective Organisations

Acta Biotheoretica - Both physiological and evolutionary criteria of biological individuality are underpinned by the idea that an individual is a functionally integrated whole. However, a precise...     

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.     

Evolution of the individual

This article studies the transition in evolution from single cells to multicellular organisms as a case study in the origin of individuality. The issues considered are applicable to all major transitions in the units of selection that involve the emergence of cooperation and the regulation of conflict. Explicit genetic models of mutation and selection both within and between organisms are studied. Cooperation among cells increases when the fitness covariance at the level of the organism overcomes within-organism change toward defection. Selection and mutation during development generate significant levels of within-organism variation and lead to variation in organism fitness at equilibrium. This variation selects for gem-line modifiers and other mediators of within-organism conflict, increasing the heritability of fitness at the organism level. The evolution of these modifiers is the first new function at the emerging organism level and a necessary component of the evolution of individuality.