Skip to main content
Log in

Back to the fundamentals: a reply to Basener and Sanford 2018

  • Published:
Journal of Mathematical Biology Aims and scope Submit manuscript

“…you can’t have a paradigm shift if there’s no paradigm to be shifted. You can, however, have a paradigm shaft—that’s when people create a false view of the field and claim that new discoveries have overthrown the standard paradigm.”

–Laurence A. Moran (2023), What’s in Your Genome?

Abstract

Fisher’s fundamental theorem of natural selection has haunted theoretical population genetic literature since it was proposed in 1930, leading to numerous interpretations. Most of the confusion stemmed from Fisher’s own obscure presentation. By the 1970s, a clearer view of Fisher’s theorem had been achieved and it was found that, regardless of its utility or significance, it represents a general theorem of evolutionary biology. Basener and Sanford (J Math Biol 76:1589–1622, 2018) writing in JOMB, however, paint a different picture of the fundamental theorem as one hindered by its assumptions and incomplete due to its failure to explicitly incorporate mutational effects. They argue that Fisher saw his theorem as a “mathematical proof of Darwinian evolution”. In this reply, we show that, contrary to Basener and Sanford, Fisher’s theorem is a general theorem that applies to any evolving population, and that, far from their assertion that it needed to be expanded, the theorem already implicitly incorporates ancestor–descendant variation. We also show that their numerical simulations produce unrealistic results. Lastly, we argue that Basener and Sanford’s motivations were in undermining not merely Fisher’s theorem, but the concept of universal common descent itself.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Basener WF, Sanford JC (2018) The fundamental theorem of natural selection with mutations. J Math Biol 76:1589–1622

    MathSciNet  Google Scholar 

  • Basener WF, Cordova S, Hössjer O, Sanford JC (2021) Dynamics systems and fitness maximization in evolutionary biology. In: Sriraman B (ed) Handbook of the mathematics of the arts and sciences. Springer, Switzerland, pp 2097–2169

    Google Scholar 

  • Bulmer M (1989) Maintenance of genetic variability by mutation-selection balance: a child’s guide through the jungle. Genome 31:761–767

    Google Scholar 

  • Bürger R (2000) The mathematical theory of selection, recombination, and mutation. John Wiley and Sons, Chichester

    Google Scholar 

  • Chou H, Chiu H, Delaney NF, Segrè D, Marx CJ (2011) Diminishing returns epistasis among beneficial mutations decelerates adaptation. Science 332(6034):1190–1192

    Google Scholar 

  • Coltman DW, O’Donoghue P, Hogg JT, Festa-Bianchet M (2005) Selection and genetic (co)variance in bighorn sheep. Evolution 59(6):1372–1382

    Google Scholar 

  • Couce A, Magnan M, Lenski RE, Tenaillon O (2022) Predictability shifts from local to globe rules during bacterial adaptation. bioRxiv. https://doi.org/10.1101/2022.05.17.492360

    Article  Google Scholar 

  • Crow J (1997) The high spontaneous mutation rate: Is it a health risk? PNAS 94(16):8380–8386

    Google Scholar 

  • Crow J, Kimura M (1970) An introduction to population genetic theory. Harper & Row Publishers, New York

    Google Scholar 

  • Edwards AWF (1969) Review of Ewens (1969). Heredity 24:672–673

    Google Scholar 

  • Ewens WJ (1989) An interpretation and proof of the fundamental theorem of natural selection. Theo Pop Biol 36:167–180

    MathSciNet  Google Scholar 

  • Eyre-Walker A, Keightley PD (2007) The distribution of fitness effects of new mutations. Nat Rev Genet 8:610–618

    Google Scholar 

  • Eyre-Walker A, Woolfit M, Phelps T (2006) The distribution of fitness effects of new deleterious amino acid mutations in humans. Genetics 173:891–900

    Google Scholar 

  • Fisher RA (1930) The genetical theory of natural selection. Clarendon Press, Oxford

    Google Scholar 

  • Fleming WH (1979) Equilibrium distributions of continuous polygenic traits. SIAM J App Math 36:148–168

    MathSciNet  Google Scholar 

  • Gillespie JH (1984) A simple stochastic gene substitution model. Theor Popul Biol 23:202–215

    MathSciNet  Google Scholar 

  • Grafen A (2015) Biological fitness and the fundamental theorem of natural selection. Am Nat 186(1):1–14

    Google Scholar 

  • Gustafsson L (1986) Lifetime reproductive success and heritability: empirical support for Fisher’s fundamental theorem. Am Nat 128(5):761–764

    Google Scholar 

  • Haller BC, Messer PW (2023) SLiM 4: multispecies eco-evolutionary modeling. Am Nat 201(5):E127–E139

    Google Scholar 

  • Hamilton WD (1975) Innate social aptitudes of man: an approach from evolutionary genetics. In: Fox R (ed) ASA Studies 4: biological anthropology. Malaby Press, London, pp 133–153

    Google Scholar 

  • Hartl DL, Taubes CH (1996) Compensatory nearly neutral mutations: Selection without adaptation. J Theor Biol 192:303–309

    Google Scholar 

  • Hirsch CN, Flint-Garcia SA, Beissinger TM, Eichten SR, Deshpande S, Barry K, McMullen MD, Holland JB, Buckler ES, Springer N, Buell CR, de Leon N, Kaeppler SM (2014) Insights into the effects of long-term artificial selection on seed size in maize. Genetics 198(1):409–421

    Google Scholar 

  • Houle D (1992) Comparing evolvability and variability of quantitative traits. Genetics 130(1):195–204

    Google Scholar 

  • Houle D, Morikawa B, Lynch M (1996) Comparing mutational variabilities. Genetics 143(3):1467–1483

    Google Scholar 

  • Huber CD, Durvasula A, Hancock AM, Lohmueller KE (2018) Gene expression drives the evolution of dominance. Nat Comm 9(2750):1–11

    Google Scholar 

  • Istock CA (1978) Fitness variation in a natural population. In: Dingle H (ed) Evolution of insect migration and diapause. Springer-Verlag, New York, pp 171–190

    Google Scholar 

  • Keightley PD, Lynch M (2003) Toward a realistic model of mutations affecting fitness. Evolution 57(3):683–685

    Google Scholar 

  • Kempthorne O (1957) An introduction to genetical statistics. Chapman and Hall, London

    Google Scholar 

  • Kimura M (1964) Diffusion models in population genetics. J App Prob 1:177–232

    MathSciNet  Google Scholar 

  • Kimura M (1979) Model of effectively neutral mutations in which selective constraint is incorporated. Proc Natl Acad Sci USA 76(7):3440–3444

    Google Scholar 

  • Kimura M (1983) The neutral theory of molecular evolution. Cambridge Univ Press, Cambridge

    Google Scholar 

  • Kingman JFC (1978) Simple model for balance between selection and mutation. J Appl Probab 15:1–12

    MathSciNet  Google Scholar 

  • Kondrashov AS (1995) Contamination of the genome by very slightly deleterious mutations: why have we not died 100 times over? J Theo Biol 175(4):583–594

    Google Scholar 

  • Kruuk LEB, Clutton-Brock TH, Slate J, Pemberton JM, Brotherstone S, Guinness FE (2000) Heritability of fitness in a wild mammal population. PNAS 97(2):698–703

    Google Scholar 

  • Lande R (1975) The maintenance of genetic variability by mutation in a polygenic character with linked loci. Gen Res 26:221–235

    Google Scholar 

  • Lande R (1976) Natural selection and random genetic drift in phenotypic evolution. Evolution 30:314–334

    Google Scholar 

  • Lederberg J, Lederberg E (1952) Replica plating and indirect selection of bacterial mutants. J Bacteriol 63(3):399–406

    Google Scholar 

  • Leigh EG (1987) Ronald Fisher and the development of evolutionary theory. II. Influences of new variation on evolutionary process. Oxford Surv Evol Biol 4:212–264

    Google Scholar 

  • Luque VJ (2017) One equation to rule them all: a philosophical analysis of the Price equation. Biol Philos 32:97–125

    Google Scholar 

  • Lynch M (2016) Mutation and human exceptionalism: our future genetic load. Genetics 202(3):869–875

    Google Scholar 

  • Lynch M, Hill W (1986) Phenotypic evolution by neutral mutation. Evolution 40:915–935

    Google Scholar 

  • MacLean RC, Buckling A (2009) The distribution of fitness effects of beneficial mutations in Pseudomonas aeruginosa. PLoS Genet 5(3):e1000406

    Google Scholar 

  • Manalil S, Busi R, Renton M, Powles SB (2011) Rapid evolution of herbicide resistance by low herbicide dosages. Weed Sci 59(2):210–217

    Google Scholar 

  • Maynard Smith J (1962) The scientist speculates: an anthology of partly-baked ideas. Ed. Good IJ, Basic Books, NY, pp 252–256

  • McCleery RH, Pettifor RA, Armbruster P, Meyer K, Sheldon BC, Perrins CM (2004) Components of variance underlying fitness in a natural population of the Great Tit Parus major. Am Nat 164(3):E63–E72

    Google Scholar 

  • Merilä J, Sheldon C (1999) Lifetime reproductive success and heritability in nature. Am Nat 155(3):301–310

    Google Scholar 

  • Messina FJ (1993) Heritability and ‘evolvability’ of fitness components in Callosobruchus maculatus. Heredity 71:623–629

    Google Scholar 

  • Muller HJ (1950) Our load of mutations. Am J Hum Genet 2(2):111–176

    MathSciNet  Google Scholar 

  • Mustonen V, Lässig M (2009) From fitness landscapes to seascapes: non-equilibrium dynamics of selection and adaptation. Trends Genet 25(3):111–119

    Google Scholar 

  • Ohta T (1977) Molecular evolution and polymorphism. Natl Inst Genet Mishima Japan 76:148–167

    Google Scholar 

  • Ohta T, Tachida H (1990) Theoretical study of near neutrality. I. Heterozygosity and rate of mutation substitution. Genetics 126:219–229

    Google Scholar 

  • Orr HA (1998) The population genetics of adaptation: the distribution of factors fixed during adaptive evolution. Evolution 52(4):935–949

    Google Scholar 

  • Orr HA (2000) Adaptation and the cost of complexity. Evolution 54:13–20

    Google Scholar 

  • Orr HA (2005) The genetic theory of adaptation: a brief history. Nat Rev Genet 6:119–127

    Google Scholar 

  • Palmer AC, Kishony R (2013) Understanding, predicting and manipulating the genotypic evolution of antibiotic resistance. Nat Rev Genet 14:243–248

    Google Scholar 

  • Price GR (1970) Selection and covariance. Nature 227:520–521

    Google Scholar 

  • Price GR (1972a) Extension of covariance selection mathematics. Ann Hum Genet Lond 35:485–490

    Google Scholar 

  • Price GR (1972b) Fisher’s ‘fundamental theorem’ made clear. Ann Hum Genet Lond 36:129–140

    MathSciNet  Google Scholar 

  • Provine WB (1971) The origins of theoretical population genetics. University of Chicago Press, Chicago

    Google Scholar 

  • Queller DC (2017) Fundamental theorems of evolution. Am Nat 189(4):345–353

    Google Scholar 

  • Rice S (1990) A geometric model for the evolution of development. J Theo Biol 143(3):319–342

    MathSciNet  Google Scholar 

  • Rice S (2004) Evolutionary theory: mathematical and conceptual foundations. Sinauer Associates, Oxford University Press, Oxford

    Google Scholar 

  • Robertson A (1955) Selection in animals: synthesis. Cold Spring Harbor Symp Quant Biol 20:225–229

    Google Scholar 

  • Roth FP, Wakeley J (2016) Taking exception to human eugenics. Genetics 204(2):821–823

    Google Scholar 

  • Rupe CL, Sanford JC (2013) Using numerical simulation to better understand fixation rates, and establishment of a new principle: Haldane’s ratchet. Proc Int Conf Creat 7(1):32

    Google Scholar 

  • Sanford JC (2005) Genetic entropy and the mystery of the genome. Elim Publishing, NY

    Google Scholar 

  • Sanford JC, Carter RW, Brewer W, Baumgardner J, Potter B, Potter J (2018) Adam and eve, designed diversity, and allele frequencies. Proc Int Conf Creat 8(1):8

    Google Scholar 

  • Sanjuán R, Moya A, Elena SF (2004) The distribution of fitness effects caused by single-nucleotide substitutions in an RNA virus. PNAS 101(22):8396–8401

    Google Scholar 

  • Schrempf A, Giehr J, Röhrl R, Steigleder S, Heinze J (2017) Royal Darwinian demons: enforced changes in reproductive efforts do not affect the life expectancy of ant queens. Am Nat 189(4):436–442

    Google Scholar 

  • Stuart YE, Campbell TS, Hohenlohe PA, Reynolds RG, Revell LJ, Losos JB (2014) Rapid evolution of a native species following invasion by a congener. Science 346(6208):463–466

    Google Scholar 

  • Svensson EI, Connallon T (2019) How frequency-dependent selection affects population fitness, maladaptation and evolutionary rescue. Evol Appl 12(7):1243–1258

    Google Scholar 

  • Tataru P, Mollion M, Glémin S, Bataillon T (2017) Inference of distribution of fitness effects and proportion of adaptive substitutions from polymorphism data. Genetics 207(3):1103–1119

    Google Scholar 

  • Teplitsky C, Mills JA, Yarrall JW, Merilä J (2009) Heritability of fitness components in a wild bird population. Evolution 63(3):716–726

    Google Scholar 

  • Thatcher JW, Shaw JM, Dickinson WJ (1998) Marginal fitness contributions of nonessential genes in yeast. PNAS 95(1):253–257

    Google Scholar 

  • Turelli M (1984) Heritable genetic-variation via mutation selection balance: Lerch’s zeta meets the abdominal bristle. Theo Pop Biol 25:138–193

    Google Scholar 

  • Van Noordwijk AJ, Balen JH, Scharloo W (1980) Heritability of ecological important traits in the great tit Parus major. Ardea 68:193–203

    Google Scholar 

  • Wade MJ (1985) Soft selection, hard selection, kin selection, and group selection. Am Nat 125:61–73

    Google Scholar 

  • Walsh B, Lynch M (2018) Evolution and selection of quantitative traits. Oxford University Press, Oxford

    Google Scholar 

  • Wright S (1937) The distribution of gene frequencies in populations. PNAS 23(6):307–320

    Google Scholar 

  • Wright S (1978) Evolution and the genetics of populations. Vol. 4, Variability within and among natural populations. University of Chicago Press, Chicago

    Google Scholar 

  • Wright SI, Bi IV, Schroeder SG, Yamasaki M, Doebley JF, McMullen MD, Gaut BS (2005) The effects of artificial selection on the maize genome. Science 308(5726):1310–1314

    Google Scholar 

Download references

Acknowledgements

We thank Jonathan L. Baker for helpful comments on this manuscript. We also thank Donny Budinsky and Paul Price for bringing B&S to our attention, as well as their continued encouragement in addressing confusion in the field.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Zachary B. Hancock.

Additional information

Publisher's Note

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

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Hancock, Z.B., Cardinale, D.S. Back to the fundamentals: a reply to Basener and Sanford 2018. J. Math. Biol. 88, 54 (2024). https://doi.org/10.1007/s00285-024-02077-w

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s00285-024-02077-w

Keywords

Navigation