What changes when an evolutionary transition in individuality takes place? Many different answers have been given, in respect of different cases of actual transition, but some have suggested a general answer: that a major transition is a change in the extent to which selection acts at one hierarchical level rather than another. The current paper evaluates some different ways to develop this general answer as a way to characterise the property ‘evolutionary individuality’; and offers a justification of the option taken in Clarke (J Philos 110(8):413–435, 2013)—to define evolutionary individuality in terms of an object’s capacity to undergo selection at its own level. In addition, I suggest a method by which the property can be measured and argue that a problem which is often considered to be fatal to that method—the problem of ‘cross-level by-products’—can be avoided.
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The phylogeny of multicellularity is very hard to unpick, but a popular theory is that metazoans evolved by heterochrony from an ancestor that was closely related to a sponge, descended from a choanoflagellate, around 780 million years ago (Valentine and Marshall 2015).
Note that transitions are not inevitable or unidirectional. For example, various fungal lineages are thought to have gained multicellularity and then later transitioned back to unicellularity (Sharpe et al. 2015, 9).
I will argue in section five that, thanks to the action of individuating mechanisms, much of the time we will get the same result regardless of which trait we choose.
Even those authors who dissent will concur that there is a fact of the matter about which of two hierarchical levels is dominant, in any case (Sober 2011).
ANOVA of fitness would fail in respect of cases, such as germ separated cases, in which some parts of the individual exhibit much higher fitness than others.
Another alternative would be to simply compare the levels of genetic variance at the different hierarchical levels. However, genetic variance is neither necessary nor sufficient for evolution by natural selection. It is not necessary because there can be non-genetic sources of heritable variance in fitness, such as differential vertically transmitted symbionts. It is not sufficient because genetic variants can be prevented from passing their traits onto offspring, as in the case of sterile worker insects.
Although, as Birch points out, the extent to which a population is group-structured versus network-structured may itself be continuous, so that groups may have an intermediate level of groupishness (Birch Forthcoming).
This characterisation of evolutionary individuals is far from universal. For example, when Hull discusses the individuality of species he is concerned with their particularity, rather than with whether selection acts at the level of species (Hull 1978).
It is unlikely, however that this variable can be empirically measured. Shelton and Michod introduce a notion of ‘counterfactual fitness’ in which we try to make informed judgments about how a unit would fare if it was removed from its social setting (Shelton and Michod 2014).
More precisely, facts about how a lineage of the unit in question will respond to selection in the future.
Which include but are not limited to ‘policing mechanisms’ (Reeve and Keller 1999), and ‘conflict modifiers’ (Michod and Roze 2001).’ Individuating mechanism’ forms a broader class, because it includes what I call ‘demarcation mechanisms’, which enhance focal-level selection, in addition to policing mechanisms, which suppress lower-level selection.
The full definition which is defended in Clarke (2013) says that an individuating mechanism is a mechanism that either limits an object’s capacity to undergo within-object selection, by decreasing the availability of within-object heritable variance in fitness (Policing kind), or increases its capacity to participate in a between-object selection process, by increasing the availability of object-level heritable variance in fitness (Demarcation kind).
To avoid circularity, we will need to appeal to cases in which there is actual selection at the focal level to justify consideration of a particular mechanism as an individuating mechanisms—as grounding the capacity, in other words.
Rare exceptions have been known (Rong et al 1988).
Another is to abandon the Price analysis in favour of the contextual approach. This technique of regression analysis avoids the problem of cross level by products, but it has problems of its own. In particular, it yields the counterintuitive result that group selection can occur even in the absence of variation between groups (Okasha 2006).
Ågren JA (2014) Evolutionary transitions in individuality: insights from transposable elements. Trends Ecol Evol 29(2):90–96
Birch J (Forthcoming) The philosophy of social evolution
Bonner JT (1974) On development: the biology of form. Harvard Uni Press, Cambridge
Booth A (2014) Populations and individuals in heterokaryotic fungi: a multilevel perspective. Philos Sci 81(4):612–632
Bouchard F (2008) Causal processes, fitness, and the differential persistence of lineages. Philos Sci 75(5):560–570
Bouchard F, Huneman P (2013) From groups to individuals: evolution and emerging individuality. MIT Press, Cambridge
Bourke AF (2011) Principles of social evolution. OUP, Oxford
Bowles S, Fehr E, Gintis H (2003) Strong reciprocity may evolve with or without group selection. Theor Primatol Proj Newslett 1:12
Buss LW (1987) The evolution of individuality. Princeton University Press, Princeton
Clarke E (In review) How to count organisms
Clarke E (2010) The problem of biological individuality. Biol Theory 5(4):312–325
Clarke E (2012) Plant individuality: a solution to the demographer’s dilemma. Biol Philos 27(3):321–361
Clarke E (2013) The multiple realizability of biological individuals. J Philos 110(8):413–435
Clarke E (2014) Origins of evolutionary transitions. J Biosci 39(2):303–317
Cock JM, Collén J (2015). Independent emergence of complex multicellularity in the brown and red algae. In: Evolutionary transitions to multicellular life. Springer Netherlands, pp 335–361
Damuth J, Heisler IL (1988) Alternative formulations of multilevel selection. Biol Philos 3:407–430
Dawkins R (1982) The extended phenotype. Oxford University Press, Oxford
De Sousa R (2005) Biological individuality. Croat J Philos 14:195–218
Dupré J, O’Malley MA (2009) Varieties of living things: life at the intersection of lineage and metabolism. Philos Theory Biol 1:1–25
Ereshefsky M, Pedroso M (2015) Rethinking evolutionary individuality. Proc Natl Acad Sci 112(33):10126–10132
Fairclough SR (2015) Choanoflagellates: perspective on the origin of animal multicellularity. In: Evolutionary transitions to multicellular life. Springer Netherlands, pp 99–116
Fletcher JA, Doebeli M (2009) A simple and general explanation for the evolution of altruism. Proc R Soc Lond B Biol Sci 276(1654):13–19
Folse HJ III, Roughgarden J (2010) ‘What is an individual organism? A multilevel perspective. Q Rev Biol 85:447–472
Frank SA (1997) Models of symbiosis. Am Nat 150(S1):S80–S99
Frank SA (2012) Natural selection. III. Selection versus transmission and the levels of selection. J Evol Biol 25(2):227–243
Friesen ML (2012) Widespread fitness alignment in the legume–rhizobium symbiosis. New Phytol 194(4):1096–1111
Gardner A (2015) The genetical theory of multilevel selection. J Evol Biol 28(2):305–319
Gardner A, Grafen A (2009) Capturing the superorganism: a formal theory of group adaptation. J Evol Biol 22(4):659–671
Ghiselin M (1974) A radical solution to the species problem. Syst Biol 23(4):536–544
Godfrey-Smith P (2008) Varieties of population structure and the levels of selection. Br J Philos Sci 59(1):25–50
Godfrey-Smith P (2009) Darwinian populations and natural selection. OUP, Oxford
Goodnight C (2013) On multilevel selection and kin selection: contextual analysis meets direct fitness. Evolution 67(6):1539–1548
Goodnight CJ, Schwartz JM, Stevens L (1992) Contextual analysis of models of group selection, soft selection, hard selection, and the evolution of altruism. Am Nat 140:743–761
Gould SJ, Lloyd EA (1999) Individuality and adaptation across levels of selection: how shall we name and generalize the unit of Darwinism? Proc Natl Acad Sci 96(21):11904–11909
Guay A, Pradeu T (eds) (2015) Individuals across the sciences. Oxford University Press, Oxford
Haber M (2013) Colonies are individuals: revisiting the superorganism revival. In: From groups to individuals: evolution and emerging individuality, pp 195–217
Harper JL (1977) Plant population biology. Academic, London
Heisler IL, Damuth J (1987) A method for analyzing selection in hierarchically structured populations. Am Nat 130(4):582–602
Herron MD, Nedelcu AM (2015) Volvocine algae: from simple to complex multicellularity. In: Ruiz-Trillo IR, Nedelcu AM (eds) Evolutionary transitions to multicellular life: principle and mechanisms. Springer, New York
Hölldobler B, Wilson EO (2009) The superorganism: the beauty, elegance, and strangeness of insect societies. WW Norton & Company, New York
Hull D (1978) A matter of individuality. Philos Sci 45:335–360
Janzen DH (1977) What are dandelions and aphids? Am Nat 111(979):586–589
Keller L (ed) (1999) Levels of selection in evolution. Princeton University Press, Princeton
Lang D, Rensing SA (2015) The evolution of transcriptional regulation in the Viridiplantae and its correlation with morphological complexity. In: Evolutionary transitions to multicellular life. Springer Netherlands, pp 301–333
Lewontin RC (1970) The units of selection. Annu Rev Ecol Syst 1:1–18
Lloyd E (1995) Units and levels of selection. In: Zalta EN (ed) The Stanford encyclopedia of philosophy (Fall 2005 Edition). http://plato.stanford.edu/archives/fall2005/entries/selection-units/
Macpherson AJ, Harris NL (2004) Interactions between commensal intestinal bacteria and the immune system. Nat Rev Immunol 4:478–485
Margulis L (1970) Origin of eukaryotic cells: evidence and research implications for a theory of the origin and evolution of microbial, plant, and animal cells on the Precambrian earth. Yale University Press, New Haven
Martens J (2010) Organisms in evolution. Hist Philos Life Sci 32(2–3):373–400
Maynard Smith J, Szathmary E (1997) The major transitions in evolution. Oxford University Press, Oxford
McShea DW (2000) Functional complexity in organisms: parts as proxies. Biol Philos 15(5):641–668
Michod RE (1999) Darwinian dynamics. Evolutionary transitions in fitness and individuality. Princeton University Press, Princeton
Michod RE (2006) The group covariance effect and fitness trade-offs during evolutionary transitions in individuality. Proc Natl Acad Sci 103(24):9113–9117
Michod RE, Roze D (2001) Cooperation and conflict in the evolution of multicellularity. Heredity 86(1):1–7
Okasha S (2001) Why won’t the group selection controversy go away? Br J Philos Sci 52(1):25–50
Okasha S (2006) Evolution and the levels of selection. Oxford University Press, Oxford
Okasha S (2016) The relation between kin and multilevel selection: an approach using causal graphs. Br J Philos Sci 67(2):435–470
Pepper JW, Herron MD (2008) Does biology need an organism concept? Biol Rev 83(4):621–627
Pradeu T (2010) What is an organism? An immunological answer. Hist Philos Life Sci 32:247–267
Price GR (1970) Selection and covariance. Nature 227:520–521
Price GR (1972) Extension of covariance selection mathematics. Ann Hum Genet 35(4):485–490
Queller DC (2000) Relatedness and the fraternal major transitions. Philos Trans R Soc Lond B Biol Sci 355(1403):1647–1655
Queller DC, Strassmann JE (2009) Beyond society: the evolution of organismality. Philos Trans R Soc Lond B Biol Sci 364(1533):3143–3155
Ratnieks FL, Visscher PK (1989) Worker policing in the honeybee. Nature 342(6251):796–797
Reeve HK, Hölldobler B (2007) The emergence of a superorganism through intergroup competition. Proc Natl Acad Sci 104(23):9736–9740
Reeve HK, Keller L (1999) Levels of selection: burying the units-of-selection debate and unearthing the crucial new issues. In: Levels of selection in evolution, pp 3–14
Rong R, Chandley AC, Song J, McBeath S, Tan PP, Bai Q, Speed RM (1988) A fertile mule and hinny in China. Cytogenet Genome Res 47(3):134–139
Ruiz-Trillo IR, Nedelcu AM (eds) (2015) Evolutionary transitions to multicellular life: principle and mechanisms. Springer, New York
Santelices B (1999) How many kinds of individual are there? Trends Ecol Evol 14(4):152–155
Sharpe SC, Eme L, Brown MW, Roger AJ (2015) Timing the origins of multicellular eukaryotes through phylogenomics and relaxed molecular clock analyses. In: Evolutionary transitions to multicellular life. Springer Netherlands, pp 3–29
Shelton DE, Michod RE (2014) Group selection and group adaptation during a major evolutionary transition: insights from the evolution of multicellularity in the volvocine algae. Biol Theory 9(4):452–469
Sober E (1994) Conceptual issues in evolutionary biology. Mit Press, Cambridge
Sober E (2011) Realism, conventionalism, and causal decomposition in units of selection: reflections on Samir Okasha’s evolution and the levels of selection. Philos Phenomenol Res 82(1):221–231
Sober E, Wilson DS (1998). Unto others: the evolution and psychology of unselfish behavior. Cembridge (Massachusetts), pp 34–36
Solé RV, Duran-Nebreda S (2015) In silico transitions to multicellularity. In: Evolutionary transitions to multicellular life. Springer Netherlands, pp 245–266
Strassmann JE, Queller DC (2010) The social organism: congresses, parties, and committees. Evolution 64(3):605–616
Szathmáry E, Jordán F, Pál C (2001) Can genes explain biological complexity? Science 292(5520):1315–1316
Valentine JW, Marshall CR (2015) Fossil and transcriptomic perspectives on the origins and success of metazoan multicellularity. In: Evolutionary transitions to multicellular life. Springer Netherlands, pp 31–46
West SA, Fisher RM, Gardner A, Kiers ET (2015) Major evolutionary transitions in individuality. Proc Natl Acad Sci 112(33):10112–10119
Williams GC (1966) Adaptation and natural selection. Princeton University Press, Princeton
Wilson DS (1975) A theory of group selection. Proc Natl Acad Sci 72(1):143–146
Wilson J (1999) Biological individuality: the identity and persistence of living entities. Cambridge University Press, Cambridge
Wilson DS (2010) Darwin’s cathedral: evolution, religion, and the nature of society. University of Chicago Press, Chicago
Wilson RA, Barker M (2013) The biological notion of individual. In: Stanford encyclopedia of philosophy. Stanford University, Stanford
Wilson DS, Sober E (1989) Reviving the superorganism. J Theor Biol 136:337–356
Wilson DS, Sober E (1994) Reintroducing group selection to the human behavioral sciences. Behav Brain Sci 17(04):585–608
With many thanks to Samuel Alizon, Pierrick Bourrat, Matthew Herron, Samir Okasha, Thomas Pradeu, Paul Ryan and two anonymous referees.
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Clarke, E. A levels-of-selection approach to evolutionary individuality. Biol Philos 31, 893–911 (2016). https://doi.org/10.1007/s10539-016-9540-4
- Levels of selection
- Evolutionary individuality
- Major transitions