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Populations and Individuals in Heterokaryotic Fungi: A Multilevel Perspective

Published online by Cambridge University Press:  01 January 2022

Abstract

Among mycologists, questions persist about what entities should be treated as the fundamental units of fungal populations. This article articulates a coherent view about populations of heterokaryotic fungi and the individuals that comprise them. Using Godfrey-Smith’s minimal concept of a Darwinian population, I argue that entities at two levels of the biological hierarchy satisfy the minimal concept in heterokaryotic fungi: mycelia and nuclei. I provide a preliminary answer to the question of how to understand the relation between these two populations. This article contributes to discussions about the nature of biological individuality, organismality, and evolutionary transitions.

Type
Research Article
Copyright
Copyright © The Philosophy of Science Association

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Footnotes

Thanks to Henri Folse III, Patrick Forber, Peter Godfrey-Smith, Anne Pringle, and members of the Pringle Lab, Kolea Zimmerman, and three anonymous reviewers for valuable comments on earlier drafts of this article.

References

Aanen, Duur K., Debets, Alfons J. M., Arjan, J. de Visser, G. M., and Hoekstra, Rolf F.. 2008. “The Social Evolution of Somatic Fusion.” Bioessays 30 (11–12): 11931203.CrossRefGoogle ScholarPubMed
Anderson, James B., and Kohn, Linda M.. 1998. “Genotyping, Gene Genealogies and Genomics Bring Fungal Population Genetics Above Ground.” Trends in Ecology and Evolution 13 (11): 444–49.. doi:10.1016/S0169-5347(98)01462-1.CrossRefGoogle ScholarPubMed
Anderson, James B., and Kohn, Linda M. 2007. “Dikaryons, Diploids, and Evolution.” In Sex in Fungi: Molecular Determination and Evolutionary Implications, ed. Heitman, J., Casselton, L., Taylor, J., and Kronstad, J.. Washington, DC: ASM.Google Scholar
Buller, A. H. Reginald. 1931. “Social Organisation in Coprinus Sterquilinus and Other Fungi.” In Researches on Fungi, Vol. 4, chap. 1. London: Longmans, Green.Google Scholar
Burnett, J. H. 2003. Fungal Populations and Species. Oxford Biology Readers. Oxford: Oxford University Press.Google Scholar
Buss, Leo W. 1982. “Somatic Cell Parasitism and the Evolution of Somatic Tissue Compatibility.” Proceedings of the National Academy of Sciences of the USA 79 (17): 5337–41.CrossRefGoogle ScholarPubMed
Buss, Leo W. 1987. The Evolution of Individuality. Princeton, NJ: Princeton University Press.Google Scholar
Calcott, Brett, and Sterelny, Kim. 2011. The Major Transitions in Evolution Revisited. Cambridge, MA: MIT Press.CrossRefGoogle Scholar
Clarke, Ellen. 2011a. “Plant Individuality and Multilevel Selection Theory.” In The Major Transitions Revisited, ed. Sterelny, Kim and Calcott, Brett. Cambridge, MA: MIT Press.Google Scholar
Calcott, Brett 2011b. “The Problem of Biological Individuality.” Biological Theory 5 (4): 312–25.Google Scholar
Calcott, Brett 2012. “Plant Individuality: A Solution to the Demographer’s Dilemma.” Biology and Philosophy 27 (3): 321–61.. doi:10.1007/s10539-012-9309-3.Google Scholar
Darwin, Charles. 1859/1859. On the Origin of Species: A Facsimile of the 1st Edition. Cambridge, MA: Harvard University Press.Google Scholar
Davis, Rowland. 1966. “Heterokaryosis.” In The Fungi: An Advanced Treatise, Vol. 2, The Fungal Organism, ed. Ainsworth, G. C., Sussman, Alfred S., and Sparrow, F. K., 567–88. New York: Academic Press.Google Scholar
Dawkins, Richard. 1976/1976. The Selfish Gene: 30th Anniversary Edition—with a New Introduction by the Author. New York: Oxford University Press.Google Scholar
Dawkins, Richard 1982. The Extended Phenotype: The Gene as the Unit of Selection. Oxford: Freeman.Google Scholar
Ereshefsky, Marc, and Pedroso, Makmiller. 2013. “Biological Individuality: The Case of Biofilms.” Biology and Philosophy 28 (2): 331–49.. doi:10.1007/s10539-012-9340-4.CrossRefGoogle Scholar
Folse, Henri J. IIIrd, and Roughgarden, Joan. 2010. “What Is an Individual Organism? A Multilevel Selection Perspective.” Quarterly Review of Biology 85 (4): 447–72.CrossRefGoogle ScholarPubMed
Glass, N. Louise, and Kaneko, Isao. 2003. “Fatal Attraction: Nonself Recognition and Heterokaryon Incompatibility in Filamentous Fungi.” Eukaryotic Cell 2 (1): 18.. doi:10.1128/EC.2.1.1-8.2003.CrossRefGoogle ScholarPubMed
Godfrey-Smith, Peter. 2009. Darwinian Populations and Natural Selection. Oxford: Oxford University Press.CrossRefGoogle Scholar
Godfrey-Smith, Peter 2011a. “Agents and Acacias: Replies to Dennett, Sterelny, and Queller.” Biology and Philosophy 26 (4): 501–15.. doi:10.1007/s10539-011-9246-6.CrossRefGoogle Scholar
Godfrey-Smith, Peter 2011b. “Darwinian Populations and Transitions in Individuality.” In The Major Transitions in Evolution Revisited, ed. Calcott, Brett and Sterelny, Kim, 6581. Cambridge, MA: MIT Press.CrossRefGoogle Scholar
Grosberg, Richard K., and Strathmann, Richard R.. 2007. “The Evolution of Multicellularity: A Minor Major Transition?Annual Review of Ecology, Evolution, and Systematics 38 (1): 621–54.. doi:10.1146/annurev.ecolsys.36.102403.114735.CrossRefGoogle Scholar
Hardin, Garrett. 1968. “The Tragedy of the Commons.” Science 162 (3859): 1243–48.. doi:10.1126/science.162.3859.1243.CrossRefGoogle ScholarPubMed
Harper, John L. 1977. Population Biology of Plants. London: Academic Press.Google Scholar
Hull, David L. 1980. “Individuality and Selection.” Annual Review of Ecology and Systematics 11 (1): 311–32.. doi:10.1146/annurev.es.11.110180.001523.CrossRefGoogle Scholar
Hull, David L. 1992. “Individual.” In Keywords in Evolutionary Biology, ed. Keller, Evelyn Fox. Cambridge, MA: Harvard University Press.Google Scholar
Hull, David L., Langman, Rodney E., and Glenn, Sigrid S.. 2001. “A General Account of Selection: Biology, Immunology, and Behavior.” Behavioral and Brain Sciences 24 (3): 511–28.CrossRefGoogle ScholarPubMed
Hutchings, M. J., and Booth, D.. 2004. “Much Ado about Nothing … So Far?Journal of Evolutionary Biology 17 (6): 1184–86.. doi:10.1111/j.1420-9101.2004.00812.x.CrossRefGoogle Scholar
Huxley, Julian. 1912. The Individual in the Animal Kingdom. Cambridge: Cambridge University Press.CrossRefGoogle Scholar
Huxley, Thomas Henry. 1852. “Upon Animal Individuality.” Proceedings of the Royal Institute of Great Britain 11:184–89.Google Scholar
James, Timothy Y., Stenlid, Jan, Olson, Ake, and Johannesson, Hanna. 2008. “Evolutionary Significance of Imbalanced Nuclear Ratios within Heterokaryons of the Basidiomycete Fungus Heterobasidion Parviporum.” Evolution: International Journal of Organic Evolution 62 (9): 2279–96.. doi:10.1111/j.1558-5646.2008.00462.x.CrossRefGoogle ScholarPubMed
Janzen, Daniel H. 1977. “What Are Dandelions and Aphids?American Naturalist 111 (979): 586–89.CrossRefGoogle Scholar
Johannesson, Hanna, and Stenlid, Jan. 2004. “Nuclear Reassortment between Vegetative Mycelia in Natural Populations of the Basidiomycete Heterobasidion Annosum.” Fungal Genetics and Biology 41 (5): 563–70.. doi:10.1016/j.fgb.2004.01.002.CrossRefGoogle ScholarPubMed
Lewontin, Richard C. 1970. “The Units of Selection.” Annual Review of Ecology and Systematics 1 (1): 118.. doi:10.1146/annurev.es.01.110170.000245.CrossRefGoogle Scholar
Michod, Richard E. 1999. Darwinian Dynamics: Evolutionary Transitions in Fitness and Individuality. Princeton, NJ: Princeton University Press.Google Scholar
Okasha, Samir. 2006. Evolution and the Levels of Selection. Oxford: Clarendon.CrossRefGoogle Scholar
Otto, Sarah P., and Hastings, Ian M.. 1998. “Mutation and Selection within the Individual.” Genetica 102–3 (1–6): 507–24.Google Scholar
Otto, Sarah P., and Orive, Maria E.. 1995. “Evolutionary Consequences of Mutation and Selection within an Individual.” Genetics 141 (3): 1173–87.CrossRefGoogle ScholarPubMed
Pawlowska, Teresa E. 2005. “Genetic Processes in Arbuscular Mycorrhizal Fungi.” FEMS Microbiology Letters 251 (2): 185–92.. doi:10.1016/j.femsle.2005.08.007.CrossRefGoogle ScholarPubMed
Pineda-Krch, Mario, and Lehtilä, Kari. 2004. “Costs and Benefits of Genetic Heterogeneity within Organisms.” Journal of Evolutionary Biology 17 (6): 1167–77.. doi:10.1111/j.1420-9101.2004.00808.x.CrossRefGoogle ScholarPubMed
Pontecorvo, G. 1946. “Genetic Systems Based on Hetero Caryosis.” Cold Spring Harbor Symposia on Quantitative Biology 11 (January): 193201. doi:10.1101/SQB.1946.011.01.021.Google Scholar
Pradeu, Thomas. 2012. The Limits of the Self: Immunology and Biological Identity. Trans. Vitanza, Elizabeth. New York: Oxford University Press.CrossRefGoogle Scholar
Rayner, Alan D. M. 1991. “The Challenge of the Individualistic Mycelium.” Mycologia 83 (1): 4871.. doi:10.2307/3759832.CrossRefGoogle Scholar
Santelices, B. 1999. “How Many Kinds of Individual Are There?Trends in Ecology and Evolution 14 (4): 152–55.CrossRefGoogle Scholar
Sterelny, Kim. 2011. “Darwinian Spaces: Peter Godfrey-Smith on Selection and Evolution.” Biology and Philosophy 26 (February): 489500. doi:10.1007/s10539-010-9244-0.CrossRefGoogle Scholar
Stout, A. B. 1929. “The Clon in Plant Life.” Journal of the New York Botanical Garden 30:2537.Google Scholar
Tuomi, J. 2004. “Genetic Heterogeneity within Organisms and the Evolution of Individuality.” Journal of Evolutionary Biology 17 (6): 1182–83.. doi:10.1111/j.1420-9101.2004.00811.x.CrossRefGoogle ScholarPubMed
Webster, John, and Weber, Roland. 2007. Introduction to Fungi. 3rd ed. Cambridge: Cambridge University Press.CrossRefGoogle Scholar