Opinion
Rethinking heredity, again

https://doi.org/10.1016/j.tree.2012.02.003Get rights and content

The refutation of ‘soft’ inheritance and establishment of Mendelian genetics as the exclusive model of heredity is widely portrayed as an iconic success story of scientific progress. Yet, we are witnessing a re-emergence of debate on the role of soft inheritance in heredity and evolution. I argue that this reversal reflects not only the weight of new evidence but also an important conceptual change. I show that the concept of soft inheritance rejected by 20th-century genetics differs fundamentally from the current concept of ‘nongenetic inheritance’. Moreover, whereas it has long been assumed that heredity is mediated by a single, universal mechanism, a pluralistic model of heredity is now emerging, based on a recognition of multiple, parallel mechanisms of inheritance.

Section snippets

A scientific revolution undone?

A fundamental assumption of classical Mendelian genetics and the evolutionary Modern Synthesis is that heredity is ‘hard’ – that is, mediated by the transmission of gene alleles that are impervious to environmental influence. By the standard historical narrative, the exclusive validity of the Mendelian model of heredity was established through the culmination of a lengthy scientific debate 1, 2, 3. According to Mayr's authoritative history [3], the possibility of ‘soft’ or ‘Lamarckian’

The hard/soft dichotomy

The roots of the scientific study of heredity, the attempt to understand why and how traits such as personality, facial features and certain diseases run in families, can be traced back to the 18th century [13]. Of the many competing ideas from this early period, two views of heredity – hard versus soft [14] – crystallized, by the late 19th century, into a dichotomy that has been at the center of the inheritance debate ever since (Box 2). Proponents of hard heredity believed that parents

Nongenetic inheritance

Over the past three decades, several research programs have explored various nongenetic mechanisms of inheritance that operate in parallel with Mendelian-genetic inheritance. Nongenetic inheritance comprises all vertical (i.e. parent–offspring) mechanisms of inheritance (other than the transmission of DNA sequence variation), including transgenerational epigenetic inheritance, somatic inheritance, environmental inheritance, and behavioral or cultural inheritance 6, 7, 8, 10. A common feature of

A pluralistic model of heredity

The model of heredity now emerging is pluralistic [12], or ‘inclusive’ [8] or ‘extended’ [60], in that it combines genetic and nongenetic mechanisms of inheritance 7, 8, 10. The pluralistic model therefore recognizes the reality of both hard and soft inheritance, and the potential for a range of intermediate phenomena.

A corollary of the pluralistic model is variation in the nature of inheritance among different traits and taxa, spanning a continuum from purely genetic to purely nongenetic.

Concluding remarks

I argue that the rejection of soft inheritance by influential 20th-century geneticists reflected two key ideas: a narrowed definition of heredity as the transmission of DNA sequences at conception, and the belief that heredity is mediated by a single, universal mechanism of transmission. As a corollary of these ideas, many leading geneticists assumed that soft inheritance, if it occurs, must involve the modification of germ-line DNA sequences by environmental or somatic factors – a process that

Glossary

Acquired trait
a phenotypic character (trait) induced by the environment or arising spontaneously during an individual's lifetime.
Behavioral/cultural inheritance
the transmission from parents to offspring of variation in behavior or culture via imitation or learning by offspring (and, in some cases, teaching by parents).
Biased mutation
mutation that is non-random in that particular environmental factors tend to induce particular changes in the DNA sequence.
Environmental inheritance
the transmission

References (85)

  • G.M. Cook

    Neo-Lamarckian experimentalism in America: origins and consequences

    Q. Rev. Biol.

    (1999)
  • O.E. Landman

    The inheritance of acquired characteristics

    Ann. Rev. Genet.

    (1991)
  • E. Mayr

    The Growth of Biological Thought: Diversity, Evolution, and Inheritance

    (1982)
  • T.S. Kuhn

    The Structure of Scientific Revolutions

    (1970)
  • E. Avital et al.

    Animal Traditions: Behavioural Inheritance in Evolution

    (2000)
  • E. Jablonka et al.

    Transgenerational epigenetic inheritance

  • R. Bonduriansky et al.

    Nongenetic inheritance and its evolutionary implications

    Annu. Rev. Ecol. Evol. Syst.

    (2009)
  • E. Danchin

    Beyond DNA: integrating inclusive inheritance into an extended theory of evolution

    Nat. Rev. Genet.

    (2011)
  • E. Jablonka et al.

    Epigenetic Inheritance and Evolution

    (1995)
  • E. Jablonka et al.

    Evolution in Four Dimensions

    (2005)
  • J. Sapp

    Beyond the Gene: Cytoplasmic Inheritance and the Struggle for Authority in Genetics

    (1987)
  • M. Mameli

    The inheritance of features

    Biol. Philos.

    (2005)
  • C. López-Beltrán

    The medical origins of heredity

  • E. Mayr

    Prologue: some thoughts on the history of the evolutionary synthesis

  • P.J. Bowler

    The Mendelian Revolution: the Emergence of Hereditarian Concepts in Modern Science and Society

    (1989)
  • F.B. Churchill

    Rudolf Virchow and the pathologist's criteria for the inheritance of acquired characteristics

    J. Hist. Med.

    (1976)
  • F.B. Churchill

    From heredity theory to vererbung: the transmission problem, 1850–1915

    ISIS

    (1987)
  • W. Johannsen

    The genotype conception of heredity

    Am. Nat.

    (1911)
  • J. Huxley

    Soviet Genetics and World Science

    (1949)
  • F.H.C. Crick

    The Croonian Lecture: The Genetic Code

    Proc. R. Soc. Lond. B

    (1966)
  • S.S. Chetverikov

    O nekotrikh momentakh evolutsionnovo protsessa s tochki zrenija sovremennoj genetiki (On certain aspects of the evolutionary process from the perspective of modern genetics)

    Zhurnal Eksperimentalnoj Biologii (A)

    (1926)
  • E.M. East et al.

    Inbreeding and outbreeding: their genetic and sociological significance

  • T.H. Morgan

    The Physical Basis of Heredity

    (1919)
  • S. Wright

    Systems of mating. I. The biometric relations between parent and offspring

    Genetics

    (1921)
  • T. Dobzhansky

    Genetics and the Origin of Species

    (1951)
  • E.J. Steele

    Somatic Selection and Adaptive Evolution: on the Inheritance of Acquired Characters

    (1979)
  • E.J. Steele

    Lamarck's Signature: How Retrogenes are Changing Darwin's Natural Selection Paradigm

    (1998)
  • R. Boyd et al.

    Culture and the Evolutionary Process

    (1985)
  • A. Mesoudi

    Cultural Evolution: How Darwinian Theory can Explain Human Culture and Synthesize the Social Sciences

    (2011)
  • L.L. Cavalli-Sforza et al.

    Cultural Transmission and Evolution: a Quantitative Approach

    (1981)
  • M.W. Feldman et al.

    On the theory of evolution under genetic and cultural transmission with application to the lactose absorption problem

  • P.J. Richerson et al.

    Not by Genes Alone: How Culture Transforms Human Evolution

    (2005)
  • Cited by (145)

    • Organization and Inheritance in Twenty-First-Century Evolutionary Biology

      2024, History, Philosophy and Theory of the Life Sciences
    View all citing articles on Scopus
    View full text