Biological Individuality

Integrating Scientific, Philosophical, and Historical Perspectives

Scott Lidgard, Lynn K. Nyhart, Scott Lidgard, Lynn K. Nyhart

• Publisher: University of Chicago Press
• Year: 2017
• Print ISBN: 9780226446455, 9780226446318
• eBook ISBN: 9780226446592
• Topic: Biological Sciences
• Subtopic: Evolution
• Index: Biological Sciences

Individuals are things that everybody knows—or thinks they do. Yet even scholars who practice or analyze the biological sciences often cannot agree on what an individual is and why. One reason for this disagreement is that the many important biological individuality concepts serve very different purposes—defining, classifying, or explaining living structure, function, interaction, persistence, or evolution. Indeed, as the contributors to Biological Individuality reveal, nature is too messy for simple definitions of this concept, organisms too quirky in the diverse ways they reproduce, function, and interact, and human ideas about individuality too fraught with philosophical and historical meaning.

Bringing together biologists, historians, and philosophers, this book provides a multifaceted exploration of biological individuality that identifies leading and less familiar perceptions of individuality both past and present, what they are good for, and in what contexts. Biological practice and theory recognize individuals at myriad levels of organization, from genes to organisms to symbiotic systems. We depend on these notions of individuality to address theoretical questions about multilevel natural selection and Darwinian fitness; to illuminate empirical questions about development, function, and ecology; to ground philosophical questions about the nature of organisms and causation; and to probe historical and cultural circumstances that resonate with parallel questions about the nature of society. Charting an interdisciplinary research agenda that broadens the frameworks in which biological individuality is discussed, this book makes clear that in the realm of the individual, there is not and should not be a direct path from biological paradigms based on model organisms through to philosophical generalization and historical reification.

1

The Work of Biological Individuality: Concepts and Contexts

SCOTT LIDGARD AND LYNN K. NYHART

The whole question seems to turn upon the meaning of the word “individual.”

THOMAS HENRY HUXLEY (1852, 185)

There is, indeed, as already implied, no definition of individuality that is unobjectionable.

HERBERT SPENCER (1864, 206)

Between them, Huxley and Spencer got it right. Individuality is a basic concept in biology, yet there is no broad agreement on its meaning. Not unlike other wide-ranging concepts, biological individuality is a nomadic chameleon, “subject to constant reification and change while crossing and turning across disciplines and non-scientific domains” (Surman et al. 2014, 127). Not only biologists, but also historians and philosophers of biology adopt and reanalyze the concept. Why is it so difficult to isolate a meaning for biological individuality, yet so useful to biologists that they continually put different versions of an individuality concept to work?

Put to work on specific biological problems, individuality concepts provide structure and buttress generality, predictability, and explanatory power—though seldom all together (J. Wilson 1999). They do their work in the contexts of biologists’ questions and epistemic practices, in a historically contingent yet continually changing landscape of biological knowledge and theoretical interpretation, and in philosophical views biologists draw upon. We suggest that biologists, historians, and philosophers need to appreciate all of these. In this chapter, we first show that a broad spectrum of definitional criteria of individuality has been integral to biological studies for at least 170 years. We then argue that this work is necessarily contextualized by specific problems, and lay out the notion of a problem space as a way to think about such contextualization and the place of individuality concepts within it. Our next section shows how many (if not most) specific problems concerning individuality can be seen as distributed across four stable and continuous kinds of problems: individuation, hierarchy, temporality, and constitution. We then briefly consider individuality from perspectives of relationality and interaction—systems, networks, and processes. In closing, we advocate a rethinking of what biological individuality concepts are meant to do in biology. Rather than arguing over whether this or that specific concept and definitional criterion is right or best, a more promising way forward is to recast biological individuality as a broad, stable domain of problems, a “problem agenda” (Love 2014, forthcoming).

Definitions and Criteria of Biological Individuality

There is now a sprawling definitional diversity of biological individuality concepts, constituted by dozens of old and new criteria defining “individual” or its contained subset “organism.” These definitions and criteria don’t always agree in picking out the same biological objects (Clarke 2010), and perhaps agree even less when some of their theory-driven underpinnings are compared. This section presents some of the definitional criteria that have been proposed for either biological “individuals” or “organisms” (Table 1.1), before moving on to the four kinds of problems we introduced earlier. Our compilation includes some 146 publications from 1800 to the present that have offered definitions or criteria for either one or both of these terms. While the terms are not equivalent, they have been used interchangeably in many publications, precluding a simple separation here. We have attempted to parse the references into groups by approximate criteria in order to facilitate comparisons.

Table 1.1. Some definitional criteria for “biological individuals” or “organisms” in biology

Definitional Criteria	References
Propagation and capacity for reiterating a qualified sameness, irrespective of means of propagation	E. Darwin 1800; C. Darwin 1839; Gaudichaud 1841; Steenstrup 1845; Owen 1849, 1851; Leuckart 1851; Braun 1853, 1855–56; Hofmeister 1862; Spencer 1864; Haeckel 1866; Weismann 1889, 1893; Bailey 1906; Bergson 1911; Geddes and Mitchell 1911; W. Wheeler 1911; Child 1912, 1915; J. Huxley 1912, 1949; Thomson 1920; Arber 1930, 1941; Agar 1948; Bell 1982; Vuorisalo and Tuomi 1986; Tuomi and Vuorisalo 1989; Margulis 1993; Gould and Lloyd 1999; Griesemer 2000; R. Wilson 2005; Dupré and O’Malley 2009; Godfrey-Smith 2009, 2011, 2013; A. Hamilton et al. 2009; Wilson and Barker 2013; Hamilton and Fewell 2013; Booth 2014b; Moreno and Mossio 2015a and b; L. Ma et al. 2016
Sex or sexually demarcated life cycle, excluding other means of propagation	Gallesio 1814; Carpenter 1848; T. H. Huxley 1852; Burnett 1854; Cobbold 1869; Janzen 1977; de Sousa 2005
Demarcated life cycle or phases of life cycle, irrespective of means of propagation	Steenstrup 1845; Owen 1849, 1851; Leuckart 1851; Braun 1853, 1855–56; Hofmeister 1862; Haeckel 1866; Bonner 1974; Dawkins 1982; R. Wilson 2005; Rainey and Kerr 2011; Wilson and Barker 2013
Causal integration, cohesion, collaboration, or agency of parts (often functional, sometimes metabolic, developmental, or related to division of labor)	Milne-Edwards 1827; Leuckart 1851; Spencer 1864; Bergson 1911; Geddes and Mitchell 1911; W. Wheeler 1911; J. Huxley 1912, 1949; Montgomery 1880; Child 1915; Thomson 1920; Fisher 1934; Emerson 1939; Agar 1948; Jeuken 1952; Vuorisalo and Tuomi 1986; Tuomi and Vuorisalo 1989; Wilson and Sober 1989; Margulis and Guerrero 1991; Sober 1991; Zylstra 1992; Margulis 1993; Baum 1998; Bolker 2000; Korn 2002; R. Wilson 2005; Dupré and O’Malley 2009; Gardner and Grafen 2009; Godfrey-Smith 2009, 2011, 2013; A. Hamilton et al. 2009; Folse and Roughgarden 2010; Wolfe 2010; Gilbert et al. 2012; Bouchard 2013; Haber 2013; Hamilton and Fewell 2013; Turner 2013; Wilson and Barker 2013; Arnellos et al. 2014; Booth 2014b; Gilbert 2014; Huneman 2014a and b; O’Malley 2014; Schneider and Winslow 2014; Boon et al. 2015; Bordenstein and Theis 2015; Moreno and Mossio 2015a and b; West et al. 2015; Guay and Pradeu 2016
Constituting or a part of a biological hierarchy (generally formed by a process at one level and contributing to another process forming an object at a higher level)	Gaudichaud 1841; Owen 1849; Leuckart 1851; Braun 1853, 1855–56; Haeckel 1866; Geddes and Mitchell 1911; Child 1915; Arber 1930, 1941; Tuomi and Vuorisalo 1989; Wilson and Sober 1989; Zylstra 1992; Korn 2002; Huneman 2014a and b; Schneider and Winslow 2014; Moreno and Mossio 2015a and b
Exhibiting adaptation(s)	Spencer 1864; Gardner and Grafen 2009; Queller and Strassmann 2009; West and Kiers 2009; Folse and Roughgarden 2010
Partition of germ and somatic cell lineages (and division of labor in some views)	Weismann 1889, 1893; Buss 1987; Michod and Roze 2001; Michod and Nedelcu 2003; de Sousa 2005; Michod 2007; Godfrey-Smith 2009, 2011, 2013; Folse and Roughgarden 2010
Genetic homogeneity or near-homogeneity, and genetic distinctness or uniqueness	Weismann 1889, 1893; Todd and Rayner 1980; Dawkins 1982; Vuorisalo and Tuomi 1986; Smith et al. 1992; G. Williams 1992; Santelices 1999; de Sousa 2005
Immunological or allorecognition system integration (including tolerance and symbiotic microorganism integration in some views)	Ehrlich and Morgenroth 1900; Metchnikoff 1905; Loeb 1921, 1937; Todd 1930; Medawar 1957; Burnet 1959, 1969; Todd and Rayner 1980; Gilbert et al. 2012; Pradeu 2012, 2013; Brusini et al. 2013; Anderson and McKay 2014; Tauber 2015a and b; Guay and Pradeu 2016
Autonomy or discreteness: functional, metabolic, physiological, or otherwise	Sutton 1902; Bailey 1906; W. Wheeler 1911; J. Huxley 1912, 1949; Jeuken 1952; Buss 1987; G. Williams 1992; Santelices 1999; R. Wilson 2005; Wilson and Barker 2013; Arnellos et al. 2014; Booth 2014b
Spatial and temporal continuity	Sutton 1902; J. Huxley 1912, 1949; Hull 1978, 1980, 1992; Bell 1982; Zylstra 1992; Gould and Lloyd 1999; de Sousa 2005; A. Hamilton et al. 2009; Haber 2013; Hamilton and Fewell 2013; Guay and Pradeu 2016
Spatial and temporal boundedness	J. Huxley 1912, 1949; Emerson 1939; Jeuken 1952; Ghiselin 1974; Hull 1978, 1980, 1992; Todd and Rayner 1980; Bell 1982; Margulis and Guerrero 1991; Zylstra 1992; Baum 1998; Gould and Lloyd 1999; de Sousa 2005; A. Hamilton et al. 2009; Haber 2013; Hamilton and Fewell 2013
Indivisible without losing character or function	Montgomery 1880; J. Huxley 1912; Michod and Roze 2001; Michod 2007, 2011
Bottleneck in life cycle, or accompanying some forms of propagation (a narrowing of material constituents between generations, typically unicellular)	J. Huxley 1912; Dawkins 1982; Fagerström 1992; Grosberg and Strathmann 1998; Godfrey-Smith 2009, 2013
Unit of selection or capacity to undergo selection (often with a common evolutionary fate)	Emerson 1939; Tuomi and Vuorisalo 1989; Wilson and Sober 1989; Gould and Lloyd 1999; Michod and Roze 2001; Michod and Nedelcu 2003; Michod 2007, 2011; Bouchard 2008, 2013; A. Hamilton et al. 2009; Leigh 2010; Gilbert et al. 2012; Clarke 2012, 2013; Goodnight 2013; Hamilton and Fewell 2013; Booth 2014b; Gilbert 2014; Boon et al. 2015; Bordenstein and Theis 2015; L. Ma et al. 2016
Fitness maximization or alignment	Janzen 1977; Grafen 2006; Gardner 2009; Gardner and Grafen 2009; Folse and Roughgarden 2010; Leigh 2010; Niklas and Kutschera 2014; West et al. 2015
High cooperation and low or restrained conflict among cell lineages or other contituents	Wilson and Sober 1989; Michod and Roze 2001; Michod and Nedelcu 2003; Michod and Herron 2006; Michod 2007, 2011; Queller and Strassmann 2009; West and Kiers 2009; Strassmann and Queller 2010; West et al. 2015
Particular genetic/epigenetic regulatory interaction and integration that generates and retains phenotype structure (often as genetic or, more broadly, developmental modules)	Wagner 1989a and b, 2014; Gass and Hall 2007; Arnellos et al. 2014
Persistence	Thomson 1920; Van Valen 1989; Bouchard 2008, 2013; Haber 2013; Turner 2013
Mechanisms of policing or diminishing cell lineage conflict or cheating (sometimes stipulating reduced within-object selection)	Grosberg and Strathmann 1998; Michod and Roze 2001; Michod and Nedelcu 2003; Godfrey-Smith 2009; Clarke 2013
Non-genetic microbial interaction or integration, and microbial phenotypic heterogeneity among cells or among groups of like cells, in either isoclonal or mixed populations	Avery 2006; Davidson and Surette 2008; Huang 2009; Ackerman 2013; Doolittle 2013; Martins and Locke 2015; Van Gestel et al. 2015
Factors that provide heritable variation in fitness in populations of objects, together with factors that mediate interactions among parts of objects, constraining variation at that level	Clarke 2012, 2013
Cognition or self-awareness	Turner 2013
High relative interaction strengths among groups of living entities (as in ecological communities or sub-communities)	Huneman 2014a and b
Note: The terms “biological individuals” and “organisms” are not distinguished in this compilation. References from the beginning of the nineteenth century onward are listed adjacent to the respective criteria. Some criteria overlap, and the same reference may specifiy more than one criterion. See text for explanation and discussion.

It is important to recognize that a number of these criteria overlap, and that a reference may endorse a definition using either a single criterion or several. Also, many definitional criteria allow for degrees of individuality and degrees of organismality (Verworn 1899; Bergson 1911; Conklin 1916; J. Huxley 1926, 1949; Sober 1991; Godfrey-Smith 2009; Queller and Strassmann 2009; Strassmann and Queller 2010; Herron et al. 2013; Wolfe 2014), although some references don’t endorse this view. A few authors have combined multiple criteria into higher definitional categories or factors that abstract away from some of the more material criteria in Table 1.1. For instance, the criterion of high cooperation and low conflict could be considered to subsume germ-soma separation, policing, and bottlenecks (Herron et al. 2013). Godfrey-Smith (2011) discusses two categories that may overlap in different senses of individuality, “Darwinian individuals” and (in a non-Darwinian sense) organisms. Clarke (2012) subsumes a range of different criteria within each of two factors, one that ensures variation among biological objects in a population and another that acts to constrain variation within each object. These factors attempt to combine the effects of certain other criteria listed in Table 1.1 that could influence heritable variation in fitness, her overriding concern. Goodnight (2013) offers three definitions of individuality in terms of fitness, with an informed discussion of models, criteria, or fitness proxies that could actualize them: units of fitness at a chosen organizational level, objects at the lowest level experiencing natural selection, and objects at the lowest level displaying an evolutionary response to natural selection. He states clearly that it is the observer who imposes an abs...

Table of contents

• Cover
• Title Page
• Copyright Page
• Contents
• Introduction: Working Together on Individuality
• 1  The Work of Biological Individuality: Concepts and Contexts
• 2  Cells, Colonies, and Clones: Individuality in the Volvocine Algae
• 3  Individuality and the Control of Life Cycles
• 4  Discovering the Ties That Bind: Cell-Cell Communication and the Development of Cell Sociology
• 5  Alternation of Generations and Individuality, 1851
• 6  Spencer’s Evolutionary Entanglement: From Liminal Individuals to Implicit Collectivities
• 7  Biological Individuality and Enkapsis: From Martin Heidenhain’s Synthesiology to the Völkisch National Community
• 8  Parasitology, Zoology, and Society in France, ca. 1880–1920
• 9  Metabolism, Autonomy, and Individuality
• 10  Bodily Parts in the Structure-Function Dialectic
• Commentaries: Historical, Biological, and Philosophical Perspectives
• Acknowledgments
• List of Contributors
• Index