Assortative mating by an obliquely transmitted local cultural trait promotes divergence

Justin Yeh University of North Carolina at Chapel Hill Do learned birdsong dialects lead to ? • Molecular similarity might correlate with dialect similarity (Baker 1975; Baker & Thompson 1982; Zink & Barrowclough 1984) • Genetic cline overlap with cultural cline, but at lower steepness, and the birdsong does not predict genotype (Kenyon et al. 2016) • Bird lineage with song learning has more species than that without (Lachlan & Servedio 2004)

Justin Yeh 2 correlation ⇏ causation no correlation ⇏ no causation

Justin Yeh 3 Oblique learning: from unrelated individual of the previous generation • Juvenile songbirds learn from adult neighbors • Obliquely transmitted traits are immune to (Yeh & Servedio 2015) • If any juvenile can learn from any adult, there should not be correlation between gene and culture

Justin Yeh 4 Spatial structure creates gene- culture association • Learning is spatially restricted • Cultural traits can be locally adapted – High-freq vocal signals in cities (Luther & Derryberry 2012) – Tonal languages in humid environment (Everett et al. 2014)

Justin Yeh 5 Hypothesis

Local genes & Local song & local local oblique reproduction learning

Justin Yeh 6 Hypothesis

Local genes & Local song & local local oblique reproduction learning

Gene-culture association

Justin Yeh 7 Hypothesis

Local genes & Local song & local local oblique reproduction learning

Divergent selection Gene-culture & sexual selection association on song

Genetic divergence

Justin Yeh 8 Hypothesis

Local genes & Local song & local local oblique reproduction learning

Divergent selection Gene-culture & sexual selection association on song

Genetic divergence

Justin Yeh 9 Population genetic model

m

Justin Yeh 10 Population genetic model

m A B a b

Justin Yeh 11 Population genetic model

m A B a b

s H sH

Justin Yeh 12 Population genetic model

C1 C2 m A B a b

s H sH

Justin Yeh 13 Population genetic model

sD , α sD , α

C1 C2 m A B a b

s H sH

Justin Yeh 14 Population genetic model

sD , α sD , α

C1 C2 m A B a b

s H sH

Justin Yeh 15 Population genetic model

sD , α, μ sD , α , μ

N C1 C2 m N A B a b

s H sH

Justin Yeh 16 Simulation conditions

• All genes and cultural traits start diverged – Contact zone • 5000 generations

Justin Yeh 17 Both sexual and divergent selection promote LD

Local gene Local song

Gene-culture Selection on association song (α, sD)

Genetic divergence (LD)

Justin Yeh 18 Both sexual and divergent selection promote LD

m=0.01, sH=0.09, μ=0, no drift

Local gene Local song LD s Gene-culture Selection on D association song (α, sD)

0.01 0.1 1 10 100 Female preference strength (α) Genetic divergence (LD) Note: Intermediate α maximizes sexual selection in phenotype-matching models (Servedio 2011)

Justin Yeh 19 Drift and mutation just make things messy Drift & mutation

Local gene Local song

Gene-culture Selection on association song (sD, α)

Genetic divergence (LD)

Justin Yeh 20 Drift and mutation just make things messy

-3 Drift & mutation m=0.01; sH=0.1; α=1; μ=10 ; N=1000

Local gene Local song LD

Gene-culture Selection on sD association song (sD, α)

Cultural trait divergence (calculated like Nei’s genetic distance) Genetic divergence (LD)

Justin Yeh 21 and viability give better evidence than gene-culture correlation • Correlation can be caused by geography • Correlation can be difficult to observe – Oblique learning temporarily and locally removes gene-culture association – Stochastic process may lead to high cultural variation within patches

Justin Yeh 22 Why should cultural care about speciation? • group formation, ideological divide, radicalization, etc. • Reduced genetic exchange <--> reduced memetic exchange • Genetic divergence <--> cultural divergence

Justin Yeh 23 Acknowledgement

• Maria Servedio • Marc Feldman • Courtney Fitzpatrick • National Science Foundation (USA)

Justin Yeh 24 Life cycle

Drift

Oblique learning with Migration cultural mutation

Viability Sexual selection selection & reproduction

Justin Yeh 25 Drift

Migration Oblique learning w/ cultural mutation

Sexual selection & Viability selection reproduction

• D-M incompatibility for A and B (sH)

• Divergent selection on C (sD)

Genotype Culture Patch 1 Patch 2

AB & ab C1, C3… 1 1-sD

Ab & aB C1, C3… 1-sH (1-sH)(1-sD)

AB & ab C2, C4… 1-sD 1

Ab & aB C2, C4… (1-sH)(1-sD) 1-sH

Justin Yeh 26 Drift

Migration Oblique learning w/ cultural mutation

Viability Sexual selection & selection reproduction • Polygyny (sexual selection on males) • Preference (α) to mate with individuals of the same cultural trait (phenotype-matching) ♂ ♀ C1 C2 C3 …

C1 1+α 1 1 1

C2 1 1+α 1 1

C3 1 1 1+α 1 … 1 1 1 … 27 Drift Oblique learning w/ Migration cultural mutation

Viability Sexual selection selection & reproduction • From the previous generation in the same patch

f(ABC1)juvenile=f(AB)juvenile((1- μ) f(C1)adult + μ f(C2)adult)

• Gene-culture association becomes 0 within each patch!

Justin Yeh 28 Life cycle order & number of possible cultural traits

-3 m=0.01; sH=0.1; α=1; μ=10 ; N=1000

m=0.01; sH=0.1; sD=0-0.5; α=1 # of C alleles

LD

sD

Cultural trait divergence

Drift

Viability Oblique learning selection

Migration Sexual selection

29 sD selection

Local gene Local song Local gene Local song migration migration

Gene-culture Gene-culture α, s α association D association selection

Genetic divergence (LD) Genetic divergence (LD)

Justin Yeh 30 Scientific Empirical Proof-of-concept method research models

Observe nature and build hypothesis

Choose Design protocol Gather evidence assumptions and gather data and build model

Analyze evidence Analyze data Analyze model

Evaluate hypothesis and propose new directions

Servedio et al. (2014) Not Just a Theory—The Utility of Mathematical Models in . PLoS Biol 12(12): e1002017