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Home , Blending inheritance, Ernst Mayr, George Gaylord Simpson, Motoo Kimura, Particulate inheritance, Sewall Wright

History of Evolutionary Thought:

The Grand Evolutionary Synthesis

Considered one of the most important Biological Revolutions of the Century Dr. Carol Eunmi Lee University of Wisconsin, Madison Copyright ©2020; do not upload without permission Today’s OUTLINE:

(1) The Sources of Confusion

(2) Reconciling Mendel and Darwin

(3) The Main Tenets of the Evolutionary

Synthesis

(4) Key Developments since the Synthesis

(5) Gaps in our Understanding Today (1809-1882)

Last time we discussed Darwin’s contributions to evolutionary thinking Darwin’s contribution:

“Population as a result of ”

■ More offspring are produced than can survive

■ Limited resources and competition for resources

■ There is heritable variation in a population

■ Individuals better adapted to environment survive

■ Survivors leave more offspring (“Survival of the Fittest”)

■ Thus, average character of population is altered But, Darwin’s theory was not complete

■ Because Darwin knew nothing about , he had no idea how variation was generated in populations

■ Because Darwin knew nothing about or , he had no idea how variation was passed on to offspring

■ Darwin did not know about nonadaptive evolutionary forces, such as Question:

■ What body of knowledge provided Darwinian theory with the concept of “genes” and inheritance? Mendel’s work held part of the key to what was missing in Darwin’s Theory

■ Mendel published in 1865… was ignored until 1900

■ Presented a mechanism for how traits got passed on

“Individuals pass on to their offspring intact”

(the idea of particulate (genes) inheritance) Rediscovery of Mendel’s laws of inheritance

■ In 1900, Mendel’s laws of inheritance were “rediscovered” ◆ Dutch , German plant Carl Correns, and Austrian plant breeder Erich von Tschermak-Seysenegg ✦ Worked out laws of inheritance independently ✦ Discovered Mendel’s work as they were publishing their own

■ These rediscoveries formed the beginning of the foundation of Genetics: Mendel is considered the “Father of Genetics” Hardy-Weinburg Equilibrium (Lecture 4) ◆ Wilhem Weinberg ✦ January 13, 1908 ◆ G. H. Hardy ✦ July 10, 1908 in Science

■ Mathematical description of : Could mathematically show expectations of Mendelian inheritance and whether Mendelian expectations are realized in nature ■ Did the Darwinists accept Mendelian Genetics?

■ Why or Why Not? PROBLEMS! BUT… Mendel and Darwin’s ideas seemed Incompatible

■ Mendel’s principles: dealt with particulate (discrete) traits (e.g. yellow vs. green, wrinkled vs. smooth)

■ BUT, Darwin observed continuous traits (e.g. beak size, body length)

Q: So, how would continuous traits get passed on? Selection vs

■ Mutations discovered after 1900

Q: If mutations are arising, why need selection... … if things are just mutating? Controversy between Mutationists vs Darwinists

Mutationists (+ Mendelianism)

■ They thought that required only mutations and passing on of discrete traits

Darwinists

■ They thought that evolution required only Natural Selection on continuous variation Problem

■ Darwin did not understand the unit of inheritance (what is being inherited, genes)

■ Mendelism provide that (), but Darwinian traits did not seem to be inherited in a Mendelian fashion

■ Discrete vs. Quantitative Traits: Darwin was unable to clearly see the pattern of inheritance because he studied quantitative variation Discrete vs Quantitative Traits

■ Darwin was unable to clearly see the pattern of inheritance because he studied quantitative variation • Discrete trait: a trait that has distinct values, rather than a range of , usually Frequency encoded by one or a few genes. Examples: number of fingers, color of Mendel’s , sickle cell anemia, ABO blood type, number of eggs in a clutch, presence/absence of human widow’s peak, presence/absence of dimples, etc. Type • Quantitative (continuous) trait: a trait that has Frequency a continuum of phenotypes and is encoded by multiple genes. Examples: body size, height, weight, intelligence (IQ), Running speed, beak shape, color, skin color, milk yield of cows, lifespan, etc. Type Discrete vs Quantitative Traits

■ Darwin was unable to clearly see the pattern of inheritance because he studied quantitative variation

Frequency • Quantitative (continuous) trait: a trait that has a continuum of phenotypes and is encoded by multiple genes. Examples: body size, height, weight, intelligence (IQ), Running speed, beak shape, hair color, skin color, milk yield of cows, lifespan, etc. Type

Example: human height encoded by ~423 genes: http://www.nature.com/ng/journal/v46/n11/full/ng.3097.html Proponents of the Darwinist Theory

■ Proponents of were correct about mechanisms of Natural Selection, but they did not understand what Selection was acting on, as they were unaware of the unit of inheritance (genes) or how the variation was passed on to the next generation

■ They came up with the idea of “” where offspring gain characteristics of both parents, like mixing colors of paint… but, this was a vague idea that was incorrect

■ Many of them were Biometricians (statistical types) that thought that evolution was gradually acting on continuous traits Proponents of the Mutationist/Mendelist Theory

■ Many Prominent at the time supported the Mutationist/Mendelist theory

■ Proponents of the mutationist theory included Hugo de Vries, among those who “discovered” Mendel’s 1900 paper and Thomas Hunt Morgan, founder of Drosophila genetics

■ Thought that evolution arose through genetic changes (mutations) that were discrete and sudden

■ New originated when they mutated from pre-existing species, but this process was independent of natural selection Controversy between Mutationists vs Darwinists

Controversy persisted for ~30 years up till the 1930s, during which little progress was made Problems to Resolve:

■ At the heart was the question of whether Mendelian genetics and Mutation could be reconciled with mechanisms of Natural Selection.

■ A second issue was whether the broad-scale changes () seen by palaeontologists could be explained by changes seen in local populations (). Problem caused by:

■ Binary thinking (Black or White thinking): it’s this or that… “if I’m right, you must be wrong” à When in fact the two or more factors might interact

■ Inability to see overarching mechanism that could explain a wide range of phenomena: “How could your Hardy-Weinberg (Mendel) explain the inheritance of 5.1 cm, 5.5 cm beak length (continuous characters)?” à When in fact, one principle might govern and explain the different patterns Genetic Drift

■ A concept as important as Natural Selection

■ But, not as prominent on people’s minds

■ 1872 Gulick: Neutral theory (Genetic Drift)

■ 1921 A.C. Hagedoorn produced data to support Neutral Theory Genetic Drift The Modern Synthesis 1930s ~ 1940s

Also called the “Synthesis of Evolution and Genetics” The synthesis of (integrate the roles of mutation, selection, genetic drift, , )

Darwin and Mendel Reconciled The Modern Synthesis 1930s ~ 1940s

Also called the “Synthesis of Evolution and Genetics”

Among the Greatest Scientific Revolutions of the Century Three of the "architects" of the evolutionary synthesis: G. Ledyard Stebbins, Jr., ,

Photograph from Smocovitis, V. B. 1997. G. Ledyard Stebbins, Jr. and the evolutionary synthesis (1924-1950). American Journal of Botany 84: 1625-1637. The Evolutionary Synthesis was important because many scientists from different fields convened to discuss the evolutionary mechanisms and clear up confusion and inconsistencies Some Key Tenets of the Modern Synthesis

■ Populations are the units of Evolution

■ Mendel vs Darwin: continuous traits are also coded by particulate genes, but many genes

■ Mutation vs Selection: Mutations are sources of upon which Selection acts

■ Natural Selection and Mutation are not the only evolutionary forces. Examples: Genetic Drift, Migration

■ Microevolutionary processes, such as Drift, Selection, Mutation, lead to Macroevolutionary changes Some Tenets of the Evolutionary Synthesis ■ The is different from the

■ Acquired characters () are not inherited

■ Traits are inherited via genes, and they do not “blend” with other genes (Darwin was wrong about this one)

■ Genes mutate, resulting in different alleles

■ Evolution occurs at the population level, due to a change in proportions of individuals with different

■ Changes in proportion in a population could occur via random genetic drift () or Natural Selection… the rate of mutation is usually too low to cause large changes in proportions

■ Even very weak natural selection could cause substantial changes over a longer time scale

■ Mutations generate the genetic variation upon which natural selection acts

■ Microevolutionary processes lead to Macroevolutionary changes (speciation)

■ All organisms on the planet are related to one another in a great “tree of ”, and have diverged by branching from common ancestors

■ Gaps in the fossil record are likely due to incompleteness of the fossil record. Gradual changes seen in many parts of the fossil record suggest gradual changes over time ■ With which of these tenets do you agree?

■ With which do you not agree? Mutation vs Selection

and Reconciling Mendel and Darwin Mutation vs Selection

■ And Reconciling Mendel and Darwin ◆ continuous and discrete traits could follow the same principles of inheritance (Mendel), just that continuous traits are coded by many genes (loci)

■ If there are many genes (loci) coding for a trait, rather than one, the offspring look intermediate between the parents (looks like “blending inheritance”)

■ BUT, the SAME Mendelian patterns of inheritance apply for multi-locus traits, it’s just that you don’t see the particulate inheritance of each in the offspring, but the average effect across all the genes affecting the trait How do you deal with multi-locus quantitative traits? (2nd point below)

■ Hardy Weinberg: multiple alleles at a single locus: ◆ 3 alleles: (p + q + r)2 which expands to... p2 + 2pq + q2 + 2pr + 2qr + r2 =1.0 ◆ 4 alleles: (p + q + r + s)2

■ Hardy Weinberg: multiple loci ◆ HW principle still applies to each locus independently ◆ Need to use principles of to examine effects of multiple loci The Population Geneticists

JBS Haldane Sewall Wright

Mathematical theory of population genetics showed that mutation and selection TOGETHER cause adaptive evolution: Mutation is NOT an alternative to Natural Selection, but the raw material RA Fisher upon which natural selection acts. Fisher vs Wright Both appreciated the importance of Natural Selection AND Genetic Drift But they argued about the relative importance Ronald Aylmer Fisher (1890-1962)

Background in math, , astronomy, and genetics

Made key contributions to the field of

Developed the Foundations for the of Natural Selection Ronald Aylmer Fisher (1890-1962) • Natural selection occurs in large populations

• Many genes are involved

• Mutations are the main substrate for selection

Other Contributions:

• Adding mathematical rigor into the theory of selection • Elegant synthesis of Mendelian inheritance into the Theory of Selection • Important developments in Statistics (ANOVA) Sewall Wright (1889-1988)

Heavily influenced by examples from agriculture

Worked for the US Dept of Agriculture: breeding in guinea pigs and cattle

Became a professor at UW-Madison in Genetics Sewall Wright (1889-1988)

• and Genetic Drift are important for creating new gene interactions

• These new gene interactions (epistasis caused by new recombinations) are the main substrate for selection

I’ll talk a lot about Sewall Wright in the lecture on Genetic Drift The Population Geneticists

If you want to read more about this topic, this book is a good read Reconciling Microevolutionary Mechanisms and Macroevolutionary processes Microevolution à Macroevolution

Ernst Mayr George Gaylord Simpson G. Ledyard Stebbins and others George Gaylord Simpson Microevolutionary processes within species account for macroevolution among species That is, mutation, genetic drift, natural selection, and other processes that act within species (microevolution) are the SAME mechanisms that account for the origin of new species and major long term evolution (macroevolution) James F. Crow (1916-2012) University of Wisconsin, Madison

His work has touched on nearly every area of evolutionary genetics -will discuss some of his contributions in Lecture on Mutations http://www.genetics.wisc.edu/CATG/crow/index.html Professor James Crow Lecture:

Selection on Quantitative Traits (multi-locus traits):

video.wpt.org/video/1811393836/ Moral of the Story

■ Scientists from different fields should talk to each other

■ Should avoid binary thinking (this vs. that, right vs. wrong), as different mechanisms might work together in an integrated fashion

■ We are often biased by what we study (example of continuous vs. discrete traits) After the Evolutionary Synthesis The Importance of Natural Selection vs Genetic Drift

Ongoing debate after the Evolutionary Synthesis Even after the synthesis the relative importance of Natural Selection and Genetic Drift was debated

• During the Evolutionary Synthesis, Sewall Wright focused more on importance of Genetic Drift, whereas RA Fisher focused on Natural Selection • Shortly after the Evolutionary Synthesis many focused on selection to the point of assuming that most phenotypes were the result of Natural Selection • Emphasis on Genetic Drift resurged in the 1970s, 80s with Kimura’s “Neutral Theory”

• Then in the 2000s and 2010s interest in Selection increased with the ability to detect signatures of Natural Selection in sequence dataà much of the genome is under selection (1924-1994)

The Neutral Theory of

Classic Paper: Kimura, Motoo. 1968. Evolutionary rate at the molecular level. Nature. 217: 624–626.

Classic Book: Kimura, Motoo (1983). The neutral theory of molecular evolution. Cambridge University Press. The Neutral Theory of Molecular Evolution (Lecture #6)

• The Neutral theory posits that the vast majority of evolutionary change at the molecular level is caused by random genetic drift rather than natural selection. Motoo Kimura • Neutral theory is not incompatible with Darwin's theory of evolution by natural selection: adaptive changes are acknowledged as present and important, but hypothesized to be a small minority evolutionary change. • Purifying selection (negative selection) could still be acting to remove deleterious mutations from the genome. But, the idea here is that most of the genetic variation within and between populations is due to neutral variation (mutations and genetic drift).

• **Ongoing debate on the extent to which variation across the genome is caused by genetic drift vs. natural selection While the Evolutionary Synthesis was a HUGE leap in the right direction, there were a few tenets that required modification (as a result of new discoveries in Genetics) Some Tenets of the Evolutionary Synthesis ■ The phenotype is different from the genotype

■ Acquired characters (phenotypic plasticity) are not inherited –not always true

■ Traits are inherited via genes, and they do not “blend” with other genes (Darwin was wrong about this one)

■ Genes mutate, resulting in different alleles

■ Evolution occurs at the population level, due to a change in proportions of individuals with different genotypes

■ Changes in proportion in a population could occur via random genetic drift (Sewall Wright) or Natural Selection… the rate of mutation is usually too low to cause large changes in proportions

■ Even very weak natural selection could cause substantial changes over a longer time scale

■ Mutations generate the genetic variation upon which natural selection acts

■ Microevolutionary processes lead to Macroevolutionary changes (speciation)

■ All organisms on the planet are related to one another in a great “”, and have diverged by branching from common ancestors

■ Gaps in the fossil record are likely due to incompleteness of the fossil record. Gradual changes seen in many parts of the fossil record suggest gradual changes over time –not always true Completing the Synthesis Advances in Genetics

■ Epigenetic Inheritance

■ Some genetic changes could lead to radical changes in phenotype ◆ Polyploidization, through polyploid hybridization or Whole Genome Duplication ◆ Regulatory Evolution (e.g. transcription factor evolution, as TFs regulate many genes) à often leads to radical evolution of development ◆ Transposons The role of Epigenetics

■ Lamarck Revisited

■ Lamarck was incorrect in thinking that the inheritance of acquired characters is the main mechanism of evolution

■ However, we now know that the inheritance of acquired characters does happen sometimes, through the inheritance of epigenetic modifications (Epigenetic Inheritance)

■ Yet, the extent to which epigenetic inheritance occurs is still not known and controversial (experimentally difficult to confirm), especially in animals C.H. Waddington --his resurgence

■ Largely dismissed during the Evolutionary Synthesisà attacked for being “Lamarckian” for his ideas on “” Conrad Hal Waddington

■ Father of Developmental ◆ Introduced the concept of “Canalization” ◆ Coined the term “Epigenetics” Interested in the interplay between phenotypic plasticity (response to stress) and selectionà “Genetic Assimilation” Why did Waddington become popular starting in the 1990’s?

■ Evo-Devo: Evolution of Development as playing an important role in the evolution of phenotypes

◆ Evolution of developmental program could cause radical phenotypic change

◆ The idea of evolution of canalization and decanalization of a developmental program

◆ Genetic Assimilation: stress could cause decanalization, and the phenotypes that are exposed could then be under selection à creation of “Hopeful Monsters” Evolution of Development (Lecture #26)

■ How small changes in developmental genes (like Hox genes) could radically cause the evolution of body plans

■ Will talk more about this when I get to lecture on Animal Diversity Evolution at the Molecular Genetic Level

Which types of mutations predominate and contribute to more often?

■ Structural vs Regulatory? ◆ Is phenotypic evolution occurring predominantly at the level of gene products (e.g. proteins) or at the level of gene regulation (e.g. transcription, RNA processing, translation, etc.)?

■ cis-Regulation vs trans-Regulation? ◆ Is regulatory evolution occurring predominantly at the level of cis-regulatory elements (e.g. promoter, enhancers) or at the level of trans-acting factors (e.g. transcription factors, etc.)?

More on Lectures on Molecular Evolution Role of Genomics (Lectures #15, 16)

■ How do whole evolve?

■ How does selection act on networks of interacting genes?

■ How many and which genes are involved in the formation of new species? Today: Genome Evolution and Systems Biology

■ How do multiple genes interact?

■ How do multiple genes affect a phenotype? (questions about the “genotype-phenotype map”)

■ Systems Biology: How does selection act on interacting gene regulatory networks?

■ Evolution of Genome Architecture Questions:

(1) What were the sources of confusion regarding evolutionary mechanisms leading up to the Evolutionary Synthesis? (2) What was the Modern (Evolutionary) Synthesis? (3) What were the main tenets of the Evolutionary Synthesis? (4) What is the relationship between natural selection, genetic drift, and mutation? (5) What were some of the limitations of the Evolutionary Synthesis? (6) What were some key developments since the Evolutionary

Synthesis?

(7) What gaps remain in our understanding today? Sample Exam Questions 1. For several decades "Darwinists" and "Mendelists" battled over the mechanisms of evolution. Which of the following did NOT contribute to this particular conflict? (a) Geneticists/Evolutionary did not understand that continuous and discrete traits follow the same principle of inheritance (b) Geneticists/Evolutionary biologists did not understand that natural selection acts on mutations in a population (c) Mendel worked with discrete traits, whereas Darwin worked with continuous traits, leading to differences in perspectives on inheritance (d) Darwin was unaware of the mechanism or unit of inheritance (e) Darwin was unaware of the mechanisms of Genetic Drift Sample Exam Question

2.Which of the following was NOT a tenet of the Evolutionary Synthesis?

(a) Evolution occurs at the level of populations, in terms of changes in frequencies, rather than changes at the individual level

(b) Selection could act on traits that are coded by multiple genes

(c) Selection acts on genetic variation in traits that are caused by mutations

(d) Natural Selection and Mutation are the only causes of evolutionary change

(e) Microevolutionary processes within populations lead to Macroevolutionary changes among populations ■ Answers:

■ 1. E (Darwin did not know about Genetic Drift, but that was not a reason for the conflict between the “Darwinists” and “Mendelists”)

■ 2. D