The Origins of Population Genetics and the Evolutionary Synthesis 1894-1944

1. The Origins of Population Genetics and the Evolutionary Synthesis1894-1944 Evolution-- Summer 2007

2. Three arguments--Argument 1: Theories of inheritance and evolution are always built together… “Evo Devo”-- the relatively new field combining evolution and ontogenetic development-- must overcome the effects of the Evolutionary Synthesis. A different theory of inheritance was built in the early 20th century in order to accommodate current understandings of Evolution by Natural Selection

3. Three arguments--Argument 2: The Evolutionary Synthesis had two distinct phases: (1900-1931): methodological consolidation to produce a genetic description of evolution. (1932-1947): (apparent) theoretical and disciplinary consolidation. The second phase failed to include paleontology…and represents larger problems.

4. Argument 3: We are still paying a price for misunderstanding the scope of the Synthesis. Early mathematical models exclude certain questions and levels of evolution: Non-Mendelian groups, either extinct populations or higher taxa Any evolutionary process that works above the species level Elements of Evo-Devo, particularly the possibility of a flexible relationship between genotype and phenotype.

5. Darwin and “Incipient Adaptations” - No explanation for the initial stages of adaptations - No possibility of assigning adaptive function to any given characteristic - (Repeated courses of adaptive change) Possible solutions: 1) Heredity supplies small, adaptive variations (or ordered variations?) 2) Selection always organizes adaptation… but that’s all we can say. 3) Selection “waits” for large, adaptive variations Foundations for Population Genetics:Darwin’s Adaptation Problem

6. Foundations of Population Genetics:Incipient Adaptation and the 1896 Impasse • William Bateson (1894) Materials For the Study of Variation (argument, evidence) • Francis Galton (1890s): Biometry, “sports” and regression analysis (powerful methodology) • Debate Between August Weismann and Herbert Spencer (1894-1896) (undermining opponents but no possibility of a “crucial experiment”) • (1900: DeVries, experiment and Mendelian inheritance)

7. Three causal theories: Neo-Darwinism Mutationism/ Saltationism Neo-Lamarckism/ Orthogenesis Two methods: Biometry Mendelism All included natural selection. The problem was to explain: 1) variation 2) adaptation 3) speciation -- without a complete or even workable theory of inheritance. The Synthesis, Part I, 1900-1932: Neo-Darwinism: A theory without a method

8. Francis Galton Populations and “swamping” Interbreeding among “sports” as an explanation for adaptation and speciation Hugo DeVries - Mendel’s system as an explanation for the behavior of “sports” in populations - Mendelian characters: large, and adaptive - Evidence and experiment in Oenothera 1890-1900: Arguments for Mutation-driven evolution

9. “Stable inheritance” Gametes are impervious to outside influence Genes and morphology have in a fixed relationship (not a formal part of Weismann’s idea) Neo-Lamarckism is excluded Orthogenesis (ordered, non-Lamarckian variation) is excluded Are these methodological- or theoretical consequences? Heredity and exclusion(Method and Theory)

10. R. A. Fisher, “The Correlation between Relatives on the Supposition of Mendelian Inheritance” (1918): • A demonstration of method for biometricians: the heritable causes of human height can be better described in Mendelian terms than by regression analysis among relatives. • An argument for describing and investigating Darwinian (gradual, selection-driven) evolution within an operational description of heredity associated with mutationism/saltationism.

11. Fisher, 1922-1930: Fitting Method to a Neo-Darwinian Theory of Evolution “On the Dominance Ratio” (1922) made the effects of genes’ interaction negligible: evolution can be described in terms of changing (single) gene frequencies and in a single stochastic equation. The Genetical Theory of Natural Selection (1930) was built to express Darwin’s qualitative theory in mathematical terms: Evolution is selection-driven and gradual, but only in very large (Mendelian) populations.

12. Heredity (1914-1921) Method of Path Co-efficients: multiple regression analyses for all genes In theory: possible to represent the effects of gene interaction In practice: works only in Mendelian populations (as in pedigreed stocks) Shifting Balance Theory of Evolution More attention to population structure Evolution can happen at different rates Selection values for alleles are changeable, and selection may not be the most significant or constant force in evolution Sewall Wright,1931-1932: Alternative models of heredity and evolution, and…

13. Wright’s “Evolution in Mendelian Populations” (1931): Agreement and Disagreement with Fisher Wright’s mathematical results for single alleles in different scenarios agreed with Fisher’s results. Different heredity, different causal theory, agreement of mathematical results… why forge that agreement? Neo-Lamarckism and Mutationism remained common and viable enemies of Neo-Darwinism; as in 1900, the theory needed a method. Fisher and Wright’s methodological agreement in 1931 was the extent of their synthesis, and the (imperfect) catalyst for the Modern Synthesis.

14. Part II, 1932-1947:The Synthesis: Scale and Meaning of Wright’s Fitness Surface “Diagrammatic representation of the field of gene combinations in two dimensions instead of many thousands” (italics added) Wright- “The roles of mutation, inbreeding, crossbreeding and selection in evolution,” 1932

15. Genetics and the Origin of Species (1937) Foundational theoretical text for the Modern Synthesis. Foundational piece of disciplinary consolidation: a naturalist applying “population thinking” to the wild. “Genetics of Natural Populations” Series (1937-1975) Dobzhansky designs experiments with Wright’s help. Translation problems: natural- to Mendelian populations; genetic variability to population size Dobzhansky and Wright by 1937: The beginning of the “Modern Synthesis”

16. Scale: Equid genera Scale: Niches Dobzhansky to Simpson (1937-1944): Fitness Surfaces, Scale and “population thinking” Simpson- Tempo and Mode in Evolution, 1944

17. Part III, Post-synthesis consequences of the conflating theory and method: Paleontology’s exclusion from the Synthesis: Simpson as “(mere) consistency argument” Serious challenges to the Modern Synthesis in the 1970s and 1980s-- Punctuated Equilibrium, Hierarchical Evolution, and an argument for a genuine distinction between micro- and macroevolution “Adaptationist Programme” remains intact, along with its philosophical problems.

18. Part III, Post-synthesis consequences of the conflating theory and method: It may get even worse… Commitment to a method built in 1931 limits investigable questions: Causal theories of macro-evolution, or those attending to higher taxa are excluded. Continued and limiting oversimplification of the relationship between genotype and phenotype; resistance to some of the most interesting findings in Evo-Devo.

19. Part III, Post-synthesis consequences of the conflating theory and method “Phenotypes are, no doubt, more appropriate units for dealing with selection, whether between individuals or groups, but genotypes seem more appropriate for mutation or random drift. The choice, however, is practically irrelevant in connection with pictorial representation of changes that occur in populations.” Sewall Wright- “Surfaces of selective value revisited,” 1988

20. Lasting Questions for Evo Devo orThe continuing value of the Evolutionary Synthesis Does the framework of mathematical population genetics allow us to study all elements of evolution in nature? Did “Hox genes” evolve in a way that population genetics can describe? Will the framework established during the Evolutionary Synthesis allow us to answer questions like these?