A New Evoluonary Populaon Genec Theory of Plant and Animal Domescaon

Greger Larson Joachim Burger Trends in Genet. 2013 Sunny San Diego • 2013 Sunny San Diego • 2001 Sunny San Diego • 1999 Sunny San Diego Sunny San Diego • 1995 We aren’t good at origins

• Bill Bryson - Notes From a Small Island We aren’t good at origins

• Bill Bryson - Notes From a Small Island “Among the many thousands of things I have never been able to understand, one in parcular stands out. That is the queson of who was the first person who stood by a pile of sand and said, ‘You know, I bet if we took some of this and mixed it with a lile potash and heated it, we could make a material that would be solid and yet transparent. We could call it ‘glass.’ Call me obtuse, but you could stand me on a beach ll the end of me and never would it occur to me to try and make it into windows.” We aren’t good at origins • Opposites

Complementaries

True False Dead Alive We aren’t good at origins • Opposites

Complementaries Antonyms

True False Fast Slow Dead Alive Good Bad We aren’t good at process • Fascinaon with the impossible middle We aren’t good at process • Fascinaon with the impossible middle We aren’t good at process • Fascinaon with the impossible middle We aren’t good at process • Fascinaon with the impossible middle

Larson declares zombie apocolypse upon us #PAGXXI We aren’t good at process • “Never occur to me...”

Not Glass Glass We aren’t good at process • “Never occur to me...”

Not Glass Glass

Not Glass Glass We aren’t good at origins •Actual glass origins: non-linear, accidents 4th-3rd millennium BC Faience a pre-glass vitreous material made by a process similar to glazing. ‘Glass’ beads were an accidental byproduct of process We aren’t good at origins •Actual glass origins - Advances in producon

1226 – "Broad Sheet" 1330 – "Crown Glass" 1620 – "Blown Plate" 1678 – "Crown Glass" 1688 – "Polished Plate" 1773 – "Polished Plate" 1834 – "Improved Cylinder Sheet" 1843 – Early form of "Float Glass" 1847 – "Rolled Plate" 1888 – "Machine Rolled" 1898 – "Wired Cast" 1903 – "Machine Drawn Cylinder" 1913 – "Flat Drawn Sheet" 1923 – "Polished Plate" 1938 – "Polished Plate" 1959 – "Float Glass" Roman glass 4th century AD We aren’t good at origins • You cannot infer origins from finished products We aren’t good at origins • You cannot infer origins from finished products We aren’t good at origins • You cannot infer origins from finished products We aren’t good at origins • You cannot infer origins from finished products So what about domescaon

Finished Products So what about domescaon

Finished Products Origin So what about domescaon • Either impossible or “eureka moment”

Wolf Dog So what about domescaon • Either impossible or “eureka moment”

Wolf Dog

Galton 1907 Thinking about the process • Belyaev’s fox farm experiment Breaking the dichotomy

Vigne 2011 Breaking the dichotomy

“Using this theorecal framework it appears that the concept of (process of) domescaon must be disassociated from that of the domesc animal.” Vigne 2011 Breaking the dichotomy

1930 1 male 3 females Breaking the dichotomy

1930 1 male 3 females

Larson insists ‘hamsters are cute’ #PAGXXI Breaking the dichotomy

• Commensal

Zeder 2012 Breaking the dichotomy

• Commensal Dog Cat Rat Mouse Guinea pig Birds: Chicken, Pigeon, Duck, Turkey Zeder 2012 Breaking the dichotomy

• Prey

Zeder 2012 Breaking the dichotomy

• Prey Sheep Goat Llama, Alpaca Reindeer Bovids: Taurine cows, Indicine cows, Bali Cale, Yak, Water Buffalo Zeder 2012 Breaking the dichotomy

• Directed

Zeder 2012 Breaking the dichotomy

• Directed Pack, Transport: Horse, Donkey, Camels (Bactrian and Dromedary) New World bovid: Buffalo Small Pets: Ferret, Hamster, Rabbit, Turtle, Mink, Chinchilla, Gerbil Birds: Ostrich, Emu, Parrot, Goose, Canary Acquac: Hermit crabs, Fish (Goldfish, Koi, Tuna), Crustaceans (shrimp) , Molluscs (abalone), Echinoderms (sea urchins / cucumbers), Algae (seaweed) Zeder 2012 Admixture: Pigs Admixture: Pigs

Tepe zen ruchlo b ü -A öyük D öyük a öyük ğacı yük yük rda şe H ö ö Pe te dion menia hti en agalassos- or rkeli H eilan r ac ran (others) 1. Ulucak H 2. Malkayası3. M 4. Badema 5. S 6. G 7. Çamlıbel Tarlası8. Si 9. Lidar H 10. Hassek H11. Çayönü 12. L 13. A 14. T 15. Kohneh Tepesi-Haftavan16. I

Medieval 5th cent AD-15th cent AD * * Hellenistic-Roman * * * 500 BC-5th cent AD * * Iron Age * * * * 1,200-600 BC * * Late Bronze Age 1,600-1,200 BC *

Middle Bronze Age ! 2,000-1,600 BC

Early Bronze Age 3,100-2,000 BC * Chalcolithic * 6,000-3,100 BC * Neolithic 7,000-6,000 BC

14 3 6 7 13 1 2 4 5 8 9 1011 15 12 16 16 16 16

Y1 Y2 Arm1T Arm2T European

Ooni et al 2013 Admixture: Pigs

Tepe zen ruchlo b ü -A öyük D öyük a öyük ğacı yük yük rda şe H ö ö Pe te dion menia hti en agalassos- or rkeli H eilan r ac ran (others) 1. Ulucak H 2. Malkayası3. M 4. Badema 5. S 6. G 7. Çamlıbel Tarlası8. Si 9. Lidar H 10. Hassek H11. Çayönü 12. L 13. A 14. T 15. Kohneh Tepesi-Haftavan16. I

Medieval 5th cent AD-15th cent AD * * Hellenistic-Roman * * * 500 BC-5th cent AD * * Iron Age * * * * 1,200-600 BC * * Late Bronze Age 1,600-1,200 BC *

Middle Bronze Age ! 2,000-1,600 BC

Early Bronze Age 3,100-2,000 BC * Chalcolithic * 6,000-3,100 BC * Neolithic 7,000-6,000 BC

14 3 6 7 13 1 2 4 5 8 9 1011 15 12 16 16 16 16

Y1 Y2 Arm1T Arm2T European

Ooni et al 2013 Admixture: Pigs

Larson et al 2007 Admixture: Pigs

Larson et al 2007 Admixture: Pigs

Larson et al 2007 Admixture: Pigs

Larson won’t stop self-cing #PAGXXI Larson et al 2007 Admixture: Pigs 1) Pigs domescated in Near East & East Asia Admixture: Pigs 1) Pigs domescated in Near East & East Asia 2) Domesc pigs moved by people Admixture: Pigs 1) Pigs domescated in Near East & East Asia 2) Domesc pigs moved by people 3) Domesc pigs interbreed with, and take on the genec appearance of local wild boar Admixture: Pigs 1) Pigs domescated in Near East & East Asia 2) Domesc pigs moved by people 3) Domesc pigs interbreed with, and take on the genec appearance of local wild boar

What is domescaon? Need to differenate between: 1) inial process - Cayonu 2) subsequent admixture - W Turkey / Europe What is true for pigs...

• Chickens

Eriksson et al 2008 What is true for pigs...

• Cows Taurine

Indicine

Hybrid

Hanoe et al 2000 What is true for pigs...

• Cats What is true for pigs...

• Horses

Warmuth et al 2012 What is true for pigs...

• Horses

“...the spread of horse domescaon out of the western Eurasian steppe was characterized by high levels of introgression from local wild populaons.”

Warmuth et al 2012 What is true for pigs...

• Bees What is true for pigs...

• Bees

“We found that managed honey bees actually have higher levels of genec diversity compared with their progenitors in East and West Europe, providing an unusual example whereby human management increases genec diversity by promong admixture.” What is true for animals...

• Apples What is true for animals...

• Apples

“Bidireconal gene flow between the domescated apple and the European crabapple resulted in the current M. domesca being genecally more closely related to this species than to its Central Asian progenitor, M. sieversii.” What is true for animals...

• Grapes What is true for animals...

• Grapes

“We find support for a Near East origin of vinifera and present evidence of introgression from local sylvestris as the grape moved into Europe.” What is true for animals...

• Rice

Fuller et al 2012 What is true for animals...

• Rice

“The protracted domescaon process finished around 6,500–6,000 years ago in China and about two millennia later in India, when hybridizaon with Chinese rice took place.”

Fuller et al 2012 What is true for animals...

• Rice

Fuller et al 2012 What is true for animals...

• Rice

Fuller et al 2012 What’s the problem • Admixture conceals the past and undermines our ability to infer origins using modern animals What’s the problem • Admixture conceals the past and undermines our ability to infer origins using modern animals

• Bifurcaon is easily reconstructed What’s the problem • Admixture conceals the past and undermines our ability to infer origins using modern animals

• Bifurcaon is easily reconstructed

• Reculaon, not so much What’s the problem • Admixture conceals the past and undermines our ability to infer origins using modern animals

• Bifurcaon is easily reconstructed

• Reculaon, not so much

Larson using vernacular - not so cute #PAGXXI What’s the problem • Admixture conceals the past and undermines our ability to infer origins using modern animals

Larson et al 2012 What’s the problem • Admixture conceals the past and undermines our ability to infer origins using modern animals

Larson et al 2012 What’s the problem • Admixture conceals the past and undermines our ability to infer origins using modern animals

Larson et al 2012 Problems with the soluon • Modern DNA says nothing. Ancient DNA! Problems with the soluon • Modern DNA says nothing. Ancient DNA! • Focus on mtDNA or single markers Problems with the soluon • Modern DNA says nothing. Ancient DNA! • Focus on mtDNA or single markers

“...introgression occurs almost exclusively from the local to the invading species... This paern is strongest at markers experiencing reduced gene flow (organelle genes) that are oen preferenally introgressed.” Problems with the soluon • Modern DNA says nothing. Ancient DNA! • Focus on mtDNA or single markers

“...introgression occurs almost exclusively from the local to the invading species... This paern is strongest at markers experiencing reduced gene flow (organelle genes) that are oen preferenally introgressed.” Problems with the soluon • Modern DNA says nothing. Ancient DNA! • Focus on mtDNA or single markers

Hailer et al 2012, Miller et al 2012 Problems with the soluon • Modern DNA says nothing. Ancient DNA! • Focus on mtDNA or single markers

Hailer et al 2012, Miller et al 2012 Problems with the soluon • Modern DNA says nothing. Ancient DNA! • Focus on mtDNA or single markers A beer soluon • Ancient nuclear genomes A beer soluon • Ancient nuclear genomes

ADMIXTURE! So What

• There is no one domescaon process despite phenotypic similaries in domesc animals So What

• There is no one domescaon process despite phenotypic similaries in domesc animals

• There are no domescaon ‘events’ So What

• There is no one domescaon process despite phenotypic similaries in domesc animals

• There are no domescaon ‘events’

• Role of admixture is under-appreciated in domescaon definions and ruins origins So What

• There is no one domescaon process despite phenotypic similaries in domesc animals

• There are no domescaon ‘events’

• Role of admixture is under-appreciated in domescaon definions and ruins origins • Way ahead: Sequencing genomes of wild, domesc, past, present to quanfy admixture and reveal the full history (L. Orlando horses) The coming insights • Greater resoluon, deeper insight The coming insights • Greater resoluon, deeper insight

Where / When

How The coming insights • Greater resoluon, deeper insight

Where / When

How Sunny San Diego • 1973: The fascinaon & the repulsion Sunny San Diego • 1973: The fascinaon & the repulsion

Larson was odd looking baby #PAGXXI