Skip to main content
SpringerLink
Log in

The proximate-ultimate distinction and the active role of the organism in evolution

  • Published:
Biology & Philosophy Aims and scope Submit manuscript

Abstract

The validity and utility of the proximate-ultimate distinction in biology have recently been under debate. Opponents of the distinction argue that it rules out individual-level organismic processes from evolutionary explanations, thereby leading to an unfounded separation between organismic (developmental, behavioral, etc.) causation and evolutionary causation. Proponents of the proximate-ultimate distinction, on the other hand, argue that it serves an important epistemological role in forming different kinds of explanation-seeking questions in biology. In this paper we offer an interpretation the proximate-ultimate distinction not only as a means of forming explanation-seeking questions, but also as a distinction that can help highlight the way in which individual-level organismic processes can be evolutionary causes. We do this by interpreting the distinction between proximate and ultimate causes as a distinction between structuring and triggering causes.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

Notes

  1. Mayr uses the German word ‘fragestellung’ (which roughly translates to something like “way of asking/posing a question”) to emphasize that the distinction captures two different research methodologies (Mayr 1961, 1501).

  2. Calcott (2013) offers a different reason to discard the PUD than an appeal to the active role of the organisms and reciprocal causation. He argues that lineage explanations—the explanation of how individual-level developmental mechanisms can produce different phenotypic effects in individuals of a shared linage—points to a class of questions that address individual-level mechanisms (typical for proximate questions), yet are addressed in a diachronic temporal context (typical for ultimate questions). Lineage explanations point to an interesting challenge for the integration of evo-devo in evolutionary theory. However, as Calcott neither appeals to the active role of the organisms nor reciprocal causation to make his argument (in fact he argues that in many lineage explanations, an appeal to reciprocal causation is not part of the explanation), we have elected to leave the problem of lineage explanations in relation to the PUD unaddressed in this paper.

  3. ‘Neglected’ might not be an ideal word to use here, as it may carry the connotation that these additional evolutionary causes have not been researched or have otherwise been “swept under the rug.” This is of course not true. Attention to these additional “nonstandard” causes and their relation to evolutionary theory have been pursued by evolutionary theorist in the twentieth century and earlier (e.g., Baldwin 1896a, 1896b; Waddington 1953; see also West-Eberhard 2003, ch. 2). ‘Neglected’ can here be understood as something along the lines of: “treated as non-standard or special causes of evolution.”.

  4. Sholl and Piglucci (2015) and Pigliucci (2019) are notable exceptions. Pigliucci is one of those that have spearheaded the debate on an extended evolutionary synthesis (e.g., Pigliucci and Müller 2010), yet still defends the validity and utility of the PUD.

  5. We are not claiming that this is the only motivation behind Mayr’s use of the PUD. See Beatty (1994) for an excellent discussion on the many different roles the PUD served for Mayr throughout his career.

  6. In some cases, a trait may be present in a population through the action of drift, which could be invoked as an ultimate cause in the explanation of trait distributions (Ramsey 2013).

  7. Reciprocal causation is widespread and instances can be found in niche construction, cases of coevolution, sexual selection (e.g., mate-choice), frequency-dependent selection, social evolution, maternal effects, and so on. Even Darwin seems to have appreciated the importance of reciprocal causation in his work on earthworms (Darwin 1881). See Laland et al. (2009, 2011, 2013a, 2013b) and Uller and Laland (2019) for a more in-depth discussion of these examples. See also Svensson (2018) for a critical examination of these arguments.

  8. See Buskell (2019) for an excellent discussion of the different ways reciprocal causation is used to challenge “standard” evolutionary theory.

  9. One quibble with Mayr’s explanation: The New World warbler (Parulidae) is a family of tropical birds thought to have originated in Central America, which is where they reach their greatest extant diversity (Curson et al. 1994). Thus, it is best to think of them not as temperate birds that fly south to avoid starvation and freezing during winter, but as tropical birds that fly north to nest in regions with fewer predators and a seasonal abundance of insects.

  10. In cases of phenotypic underdetermination due to developmental plasticity, norms of reaction can play the same role as Mayr’s open behavioral programs. The norm of reaction is a central concept in evolutionary theory, and it thus seems unlikely that Mayr, or indeed anybody else, would argue that the phenotype is predetermined, or overdetermined, by the genotype. See Dickins and Dickins (2018) for discussion.

  11. See below. See also Dickins and Dickins (2018), Dickins and Barton (2013) and Scott-Phillips et al. (2011).

  12. This is a vastly oversimplified description of his account, which merits more attention than we can give it here. See Otsuka (2014, 2016) and Okasha and Otsuka (2020).

  13. An average—understood as an arithmetic mean—is not, it turns out, the best way of quantifying fitness. See Pence and Ramsey (2013) for a discussion of the mathematical foundation of fitness.

  14. The reader might object here and argue that since we use contrastive questions to highlight the difference between structuring and triggering causes, our suggestion fares no better in uncovering the ontological implications and commitments than an epistemological interpretation of the PUD. However, we think it is important to highlight two different classes of questions one might pose: clarificatory and explanation-seeking questions. We are using contrastive clarificatory questions in order to uncover what makes structuring and triggering causes distinct kinds of causes, while the epistemological interpretation of the PUD takes the PUD to be a tool for formulating different contrastive explanation-seeking questions we may ask of biological phenomena. Of course, an answer to a clarificatory question might overlap with an answer to a related explanation-seeking answer, but they should not be treated as identical kinds of questions.

References

  • Aaby BH,. Ramsey G (2019) Three Kinds of Niche Construction. Br J Philos Sci. First online 05 December 2019. Doi:https://doi.org/10.1093/bjps/axz054

  • Amundson R (2005) The Changing role of the embryo in evolutionary thought: roots of Evo-Devo. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Ariew A (2003) Ernst Mayr’s ‘ultimate/proximate’ distinction reconsidered and reconstructed. Biol Philos 18:553–565

    Article  Google Scholar 

  • Baldwin JM (1896a) A new factor in evolution. Am Nat 30:441–451

    Article  Google Scholar 

  • Baldwin JM (1896b) A New factor in evolution (continued). Am Nat 30:536–553

    Article  Google Scholar 

  • Bateson P (2004) The active role of behaviour in evolution. Biol Philos 19:283–298

    Article  Google Scholar 

  • Bateson P (2017a) Adaptability and evolution. Interface Focus, 7

  • Bateson P (2017b) Behaviour, development and evolution. Open Book Publishers, Cambridge

    Book  Google Scholar 

  • Bateson P, Gluckman P (2011) Plasticity, robustness, development and evolution. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Beatty J (1994) The proximate/ultimate distinction in the multiple careers of Ernst Mayr. Biol Philos 9:333–356

    Article  Google Scholar 

  • Birch J (2017) The Philosophy of social evolution. Oxford University Press, Oxford

    Book  Google Scholar 

  • Buskell A (2019) Reciprocal Causation and the Extended Evolutionary Synthesis. Biol Theory 14:267–279

    Article  Google Scholar 

  • Calcott B (2013) Why how and why aren’t enough: more problems with Mayr’s proximate-ultimate distinction. Biol Philos 28:767–780

    Article  Google Scholar 

  • Curson J, Quinn D, Beadle D (1994) New world warblers. Helm Identification Guides. Christopher Helm Publishers, London

    Google Scholar 

  • Darwin CR (1881) The Formation of vegetable mould through the actions of worms, with observations on their habits. John Murray, London.

  • Dawkins R (1976) The selfish gene. Oxford University Press, Oxford

    Google Scholar 

  • Dawkins R (1982) The Extended phenotype: the gene as the unit of selection. Oxford University Press, Oxford

    Google Scholar 

  • Dawkins R (2004) Extended phenotype—but not too extended. a reply to laland, Turner and Jablonka. Biol Philosophy 19:377–396

    Article  Google Scholar 

  • Dickins TE, Barton RA (2013) Reciprocal causation and the proximate-ultimate distinction. Biol Philos 28:747–756

    Article  Google Scholar 

  • Dickins TE, Dickins BJA (2018) The extent of the modern synthesis: the foundational framework for evolutionary biology. In: Burggren W, Dubansky B (eds) Development and evolution. Springer, Cham, CH, pp 155–176

    Google Scholar 

  • Dretske F (1988) Explaining behavior: reasons in a world of causes. The MIT Press, Cambridge, MA

    Google Scholar 

  • Dretske F (2004) Psychological vs. biological explanations of behavior. Biol Philos 32:167–177

    Google Scholar 

  • Duckworth RA (2009) The role of behavior in evolution: a search for mechanism. Evol Ecol 23:513–531

    Article  Google Scholar 

  • Futuyma DJ, Kirkpatrick M (2017) Evolution. Sinauer Associates Inc., Sunderland, MA

    Google Scholar 

  • Gilbert SF (2012) Ecological developmental biology: environmental signals for normal animal development. Evol Dev 14:20–28

    Article  Google Scholar 

  • Gilbert SF, Epel D (2015) Ecological developmental biology: the environmental regulation of development, health, and evolution. Sinauer Associates Inc., Sunderland, MA

    Google Scholar 

  • Griffiths PE, Gray RD (1994) Developmental systems and evolutionary explanation. Journal of Philosophy 91(6):277–304

    Article  Google Scholar 

  • Haig D (2013) Proximate and ultimate causes: How Come? And what for? Biol Philos 28:781–786

    Article  Google Scholar 

  • Hansell M (2007) Built by animals: the natural history of animal architecture. Oxford University Press, Oxford

    Google Scholar 

  • John RM, Rougeulle C (2018) Developmental epigenetics: phenotype and the flexible genome. Front Cell Develop Biol. Published online 11 October 2018

  • Laland KN, Odling-Smee J, Feldman MW (2005) On the breadth and significance of niche construction: a reply to Griffiths, Okasha and Sterelny Biol Philos 20:37–55

    Article  Google Scholar 

  • Laland KN, Odling-Smee J, Feldman MW, Kendal J (2009) Conceptual barriers to progress within evolutionary theory. Found Sci 14:195–216

    Article  Google Scholar 

  • Laland KN, Sterelny K, Odling-Smee J, Hoppitt W, Uller T (2011) Cause and effect in biology revisited: Is Mayr’s proximate-ultimate dichotomy still useful? Science 334:1512–1516

    Article  Google Scholar 

  • Laland KN, Odling-Smee J, Hoppitt W, Uller T (2013a) More on how and why: Cause and effect in biology revisited’. Biol Philos 28:719–745

    Article  Google Scholar 

  • Laland KN, Odling-Smee J, Hoppitt W, Uller T (2013b) More on how and why: A response to commentaries. Biol Philos 28:793–810

    Article  Google Scholar 

  • Laland KN, Feldman MW, Müller GB, Jablonka E, Uller T, Sterelny K, Moczek A, Odling-Smee J (2014) Does evolutionary theory need a rethink? Yes, Urgently. Nature 514(7521):161–164

    Article  Google Scholar 

  • Laland KN, Uller T, Feldman MW, Sterelny K, Müller GB, Moczek A, Jablonka E, Odling-Smee J (2015) The extended evolutionary synthesis: its structure, assumptions and predictions. Proc R Soc B 282:20151019

    Article  Google Scholar 

  • Laland KN, Matthews B, Feldman MW (2016) An introduction to niche construction theory. Evol Ecol 30:191–202

    Article  Google Scholar 

  • Laland KN, Odling-Smee J, Feldman MW (2019) Understanding Niche construction as an evolutionary process. In: Laland KN, Uller T (eds) Evolutionary causation: biological and philosophical reflections. The MIT Press, Cambridge, pp 127–152

    Google Scholar 

  • Levins R, Lewontin RC (1985) The dialectical biologist. Harvard University Press, Cambridge

    Google Scholar 

  • Levis NA, Pfennig DW (2016) Evaluating ‘plasticity first’ evolution in nature: key criteria and empirical approaches. Trends Ecol Evol 31(7):563–574

    Article  Google Scholar 

  • Lewontin RC (1983) Gene, Organism, and Environment. In: Bendall DS (ed) Evolution: from molecules to men. Cambridge University Press, Cambridge, pp 273–285

    Google Scholar 

  • Lewontin RC (2000) The triple Helix: gene, organism, and environment. Harvard University Press, Cambridge

    Google Scholar 

  • Mayr E (1961) Cause and effect in biology. Science 134:1501–1506

    Article  Google Scholar 

  • Mayr E (1963) Animal species and evolution. The Belknap Press of Harvard University Press, Cambridge, MA

    Book  Google Scholar 

  • Mayr E (1974) Behavior programs and evolutionary strategies. Am Sci 62:650–659

    Google Scholar 

  • Mayr E (1980) Some thoughts on the history of the evolutionary synthesis. In: Mayr E, Provine WB (eds) The evolutionary synthesis. Harvard University Press, Cambridge, MA, Cambridge, pp 1–48

    Chapter  Google Scholar 

  • Mayr E (1984) The triumph of the modern synthesis. Times Literary Suppl 2:1261–1262

    Google Scholar 

  • Moczek AP, Sultan SE, Foster S, Ledón-Rettig C, Dworkin I, Nijhout HF, Abouheif E, Pfennig DW (2011) The Role of Developmental plasticity in evolutionary innovation. Proc R Soc B 278:2705–2713

    Article  Google Scholar 

  • Moczek AP (2019) The Shape of things to come: Evo Devo perspective on causes and consequences in evolution. In: Uller T, Laland K (eds) Evolutionary causation: biological and philosophical reflections. The MIT Press, Cambridge, MA, pp 63–80

    Google Scholar 

  • Nijhout HF (2003) Development and evolution of adaptive polyphenisms. Evol Dev 5:9–18

    Article  Google Scholar 

  • Odling-Smee J, Laland KN, Feldman MW (2003) Niche construction: the neglected process in evolution. Princeton University Press, Princeton, NJ

    Google Scholar 

  • Okasha S, Otsuka J (2020) The price equation and the causal analysis of evolutionary change. Philos Trans R Soc Lond B Biol Sci 375(1797):20190365

    Article  Google Scholar 

  • Otsuka J (2014) Using causal models to integrate proximate and ultimate causation. Biol Philos 30:19–37

    Article  Google Scholar 

  • Otsuka J (2016) Causal foundations of evolutionary genetics. Br J Philos Sci 67(1):247–269

    Article  Google Scholar 

  • Oyama S, Griffiths PE, Gray RD (2001) Cycles of contingency: developmental systems and evolution. The MIT Press, Cambridge, MA

    Google Scholar 

  • Pigliucci M, Müller GB (2010) Evolution: the extended synthesis. The MIT Press, Cambridge, MA

    Book  Google Scholar 

  • Pigliucci M (2019) Causlity and the role of philosophy of science. In: Laland KN, Uller T (eds) Evolutionary causation: biological and philosophical reflections. The MIT Press, Cambridge, MA, pp 13–28

    Google Scholar 

  • Pence C, Ramsey G (2013) A new foundation for the propensity interpretation of fitness. Br J Philos Sci 64:851–881

    Article  Google Scholar 

  • Ramsey G (2013) Driftability. Synthese 190:3909–3928

    Article  Google Scholar 

  • Ramsey G (2016) The causal structure of evolutionary theory. Australas J Philos 94:421–434

    Article  Google Scholar 

  • Ramsey G, Bastian ML, van Schaik C (2007) Animal innovation defined and operationalized. Behav Brain Sci 30:393–437

    Article  Google Scholar 

  • Scholl R, Pigliucci M (2015) The proximate-ultimate distinction and evolutionary biology: causal irrelevance versus explanatory abstraction. Biol Philos 30:653–670

    Article  Google Scholar 

  • Scott-Phillips TC, Dickins TE, West SA (2011) Evolutionary theory and the ultimate-proximate distinction in the human behavioral sciences. Perspect Psychol Sci 6(1):38–47

    Article  Google Scholar 

  • Sultan SE (2015) Organism and environment: ecological development, niche construction, and adaptation. Oxford University Press, Oxford

    Book  Google Scholar 

  • Sultan SE (2019) Genotype-environment interaction and the unscripted reaction norm. In: Uller T, Laland K (eds) Evolutionary causation: biological and philosophical reflections. The MIT Press Cambridge, MA, pp 109–126

    Google Scholar 

  • Sullivan KA (1989) Predation and starvation: age-specific mortality in Juvenile Juncosm (Junco phaenotus). J Anim Ecol 58:275–286

    Article  Google Scholar 

  • Svensson EI (2018) On reciprocal causation in the evolutionary process. Evol Biol 45:1–14

    Article  Google Scholar 

  • Turner JS (2000) The extended organism: the physiology of animal-built structures. Harvard University Press, Cambridge, MA

    Google Scholar 

  • Waddington CH (1953) Genetic assimilation of an acquired character. Evolution 7(2):118–126

    Article  Google Scholar 

  • Warner DA, Shine R (2008) The adaptive significance of temperature-dependent sex determination in a reptile. Nature 451(7178):566–568

    Article  Google Scholar 

  • Watt WB (2013) Causal mechanisms and the capacity for Niche construction. Biol Philos 28(5):757–766

    Article  Google Scholar 

  • West-Eberhard MJ (1983) Sexual selection, social competition, and speciation. Q Rev Biol 58:155–183

    Article  Google Scholar 

  • West-Eberhard MJ (2003) Developmental plasticity and evolution. Oxford University Press, Oxford

    Book  Google Scholar 

  • Yackel-Adams AA, Skagen SK, Savidge JA (2006) Modeling post-fledging survival of lark buntings in response to ecological and biological factors. Ecology 87:178–188

    Article  Google Scholar 

Download references

Acknowledgements

This article arose out of an invitation to give a talk at the 2020 “Niche Construction and Other Mechanisms in Ecology and Evolution” workshop. We thank the organizers of the workshop, Marie I. Kaiser and Rose Trappes from Bielefeld University and Ulrich Krohs and Behzad Nematipour from the University of Münster. We also thank Jan Baedke, James DiFrisco, Rose Trappes, and the anonymous reviewers for their feedback on earlier drafts of this paper.

Author information

Authors and Affiliations

  1. Institute of Philosophy, KU Leuven, Leuven, Belgium

    Grant Ramsey & Bendik Hellem Aaby

Authors
  1. Grant Ramsey
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Bendik Hellem Aaby
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Grant Ramsey.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ramsey, G., Aaby, B.H. The proximate-ultimate distinction and the active role of the organism in evolution. Biol Philos 37, 31 (2022). https://doi.org/10.1007/s10539-022-09863-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s10539-022-09863-0

Keywords

Search

Navigation