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Necessity is the mother of invention Yoav Ram School of Computer Science IDC Herzliya TAU Theory-Fest, 1 Jan 2020 1

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Collaborators 2 University of Hawai‘i Lee Altenberg Stanford University Marcus W. Feldman Tel Aviv University Lilach Hadany Uri Liberman

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My main interest Evolution of mechanisms for generation and transmission of phenotypic and genetic variation

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Generation of variation “Some authors believe it to be as much the function of the reproductive system to produce individual differences… as to make the child like its parents.” -- Charles Darwin On the Origin of Species, 1872 4

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Produce individual differences Make the child like its parents Balance 5

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Variation Fidelity Balance 6

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“favorable mutations... The only raw material for evolution.” “high frequency of new mutant genes that cause an appreciable reduction in viability” Balance: Mutation -- A.H. Sturtevant Quar Rev Biol, 1937 7

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Beneficial mutations Deleterious mutations Balance: Mutation 8

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Migrating Homing Balance: Migration 9

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Innovating Imitating Balance: Learning 10

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Exploration Exploitation Balance: Learning 11

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Models Ram, Altenberg, Liberman & Feldman, TPB 2018 12

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General Model • Types A1 , A2 , …, An (mutants, sites, behaviors) • Frequencies f1 , f2 , …, fn • Fitness w1 , w2 , …, wn A3 A4 A1 A2 13

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General Model • Type Ak transition probability is Ck • Ak transitions to Aj with probability Mj,k # → % = C( ⋅ %,# A3 A4 A1 A2 * Type transmission is vertical & uni-parental 14

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General Model The change in f=(f1 , f2 , …, fn ) is given by , / = − + where D and C is a positive diagonal matrices: = 8 0 0 0 ⋱ 0 0 0 ; = 8 0 0 0 ⋱ 0 0 0 ; M is an irreducible column-stochastic matrix, , is a normalizing factor to ensure ∑#>8 ; # / = 1 (1) 15

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Mutation Model 1 n possible alleles of a specific locus, A1 , …, An wk fitness of allele Ak Ck mutation rate with allele Ak , = 1/: mutations are equally probable to any allele 16

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Mutation Model 2 Ak : individual with k deleterious mutations wk fitness with k deleterious mutations Ck mutation rate with k deleterious mutations Mutations are deleterious or beneficial with probability δ and β: E,EF8 = , E,EH8 = , E,E = 1 − − 17

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Migration Model Ak individual in deme (site) k wk fitness in deme k Ck probability of leaving deme k Different migration schemes can apply (Karlin 1982) 18 , = K 1 − , = , = + 1 0, ℎ , = K 1 − , = , = ± 1 0, ℎ

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Learning Model Ak phenotype\behavior k e.g. number of hours to invest in foraging, etc. wk fitness of phenotype k Ck exploration rate of phenotype k i.e. 1-Ck exploitation rate Exploration breadth is modeled with M: Mj,k is the probability that an exploring individual with phenotype j will switch to phenotype k. 19

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Models • Mutation: single locus • Mutation: multilocus • Migration • Learning … 20

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21 Results

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Equilibrium Looking for the equilibrium: , ∗∗ = − + ∗ ∗ 22

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Math details… , ∗∗ = − + ∗ • , ∗ and ∗ are eigenvalue and eigenvector of − + • … which is non-negative primitive matrix • So , ∗ and ∗ exist, unique, non-negative • Perron-Frobenius theory • So… 23

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Long-term mean fitness ∗: stable equilibrium frequency vector , ∗: stable equilibrium population mean fitness , ∗∗ = − + ∗ ∗ Globally stable 24

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Result 1: Modified mean fitness principle If: fitness wk of Ak is below the mean fitness , ∗ Then: increasing Ck transition from Ak will increase mean fitness , ∗ 25

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Result 1: Modified mean fitness principle If: fitness wk of Ak is below the mean fitness , ∗ Then: increasing Ck transition from Ak will increase mean fitness , ∗ , ∗ = , ∗ − 26

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Result 1: Modified mean fitness principle If: fitness wk of Ak is below the mean fitness , ∗ Then: increasing Ck transition from Ak will increase mean fitness , ∗ , ∗ = , ∗ − 27

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Math details… Analysis uses Caswell’s formula for sensitivity of the population growth rate to changes in life history parameters ^ = = ⇒ = Caswell, TPB 1978 Hermisson et al, TPB 2002 Reproduced in appendix A of Ram et al., TPB 2018 28

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Stress-induced mutation Increasing the mutation rate Ck of individuals with below average fitness wk increases the population mean fitness , Ram & Hadany, Evolution 2012 Ram & Hadany, PRSB 2014 Modified mean fitness principle in action. 29

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Fisher’s Reproductive value Relative contribution to long-term population 30 Fisher, 1930 pg 27 Hermisson et al, TPB 2002 Appendix B of Ram et al., TPB 2018

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Corollary 2: Reproductive value principle If: fraction of long-term population descending from Ak will increase, on average, from transitions Then: increasing Ck transition from Ak will increase mean fitness , ∗ 32

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Increased transition from below-average individuals increases the population mean fitness… But will it evolve? 34

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Evolutionary genetic stability* • Modifier locus that modifies Ck • Start with resident allele b with {C1 , …, Cn } • Introduce invader allele B with {C’1 , …, C’n } • Can allele B increase in frequency and invade? • Allele b that cannot be invaded is evolutionary stable *Liberman, JMB 1988 35

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Modifier model , / = − − , / = − ′ − ′ is the frequency vector for resident allele b is the frequency vector for resident allele B , is the total population mean fitness 36

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Math details… , / = − − , / = − ′ − ′ Set to equilibrium (, ) = (∗, ) (B is absent) Check external stability of (∗, ) to increase in g Using eigenvalue of Jacobian of system at (∗, ) 37

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Reduction principle If transition rate is uniform: Ck =C doesn’t depend on k Then according to the Reduction principle*: Invader allele B invades the population if and only if it decreases transition rate C. * Altenberg, Liberman & Feldman, PNAS 2017 38

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Result 2: Evolution of increased genetic variation Invader allele B invades the population if it increases transition from types with below- average fitness. 39

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Result 2: Evolution of increased genetic variation Invader allele B invades the population if it increases transition from types with below- average fitness. j / k > = , ∗ − 40

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Summary 41

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Summary • Increased transition from below-average types: • Increases population mean fitness • Expected to evolve • Assuming M is irreducible! • Applications to mutation, migration, learning… 42

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Outlook Cultural transmission Frequency-dependent transmission , / = − − Preliminary result in Liberman, Ram, Altenberg & Feldman, TPB 2019 Recombination and sex Preliminary result in Ram & Hadany, AmNat 2019 Transmission of social traits 43

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Ram Lab @ IDC 66 yoav@yoavram.com @yoavram www.yoavram.com Now recruiting grad students and postdocs Interdisciplinary Center Herzliya