Capsicum Phylogeny and Domestication Brian Walsh Family Subfamily

Capsicum Phylogeny and Domestication Brian Walsh

Family: Subfamily: Tribe: Solanaceae Solanoideae Capsicinae (since 1999) • Estimated 25 species (my count =37) • Native to South and Central America • Current distribution is global • One of the most utilized spice in the world • Part of human diet for 9000 years • All diploid • Typically self-fertilize • Most n=12 (some n=13)

One of the most diversely utilized plants • • • Spice • Food • Dye Medicine • Weapons • Poison Drinks Deterrent Insecticide/Pesticide Preservative Snuff Rituals Tribute Town Names Punishment

Domestication • Davenport (1970) proposes all five domesticated species arose from a single ancestor (C. frutescens L. ) (Lumper) (based on morphology) • Heiser (1971) proposes each domesticated species arose from its own unique wild ancestor (Splitter) (hybridization studies) Pickersgill (1972) agrees with Heiser - different cultivated species show a combination of characters suggesting domestication by different groups of people living in different areas. • Eshbaugh (1983) argues at least three distinct domesticated lineages based on morphology, plant breeding and enzyme analysis (C. chacoense is plesiomorphic)

Agricultural Centers of the New World and theoretical flow of speciation View from 1000000 km above 5° 18’S 63° 55’W Based on C. chacoense

Domesticated Characters in Capsicum Domesticated • Gigantism of fruit • Altered fruit shape • Fruit color other than red • Retained on peduncle a maturity • Variable capsaicin levels Wild • small fruit • Fruit round • Red fruit • Peduncle dehiscence at maturity • High capsaicin levels

Capsicum annuum

Eshbaugh’s breakdown into flower color categories (why? ) Capsicum annuum complex C. annuum var. annuum C. annuum var. avicular C. frutescens white flowers C. chinense C. chacoense Capsicum baccatum group C. baccatum var. praetermissum C. baccatum var. pendulum C. baccatum var. baccatum white flowers with yellow spots Capsicum eximium complex C. pubescens C. eximium C. cardenasii Total species=8 purple flowers

C. frutescens Tabasco

C. baccatum var. praetermissum

Capsicum eximium

Capsicum eximium C. baccatum var. praetermissum

Capsicum cardenasii Only species that strictly outcrosses

Flower color classification of Capsicum • Color categories inaccurate (too many exceptions) • Only a fraction of total species included • Doesn’t agree with molecular data

Current phylogenetic questions • Monophyly of genus • Resolving species relationships

Capsicum Monophyletic? Modified from Bohs & Olmstead 1997

A B C A A C = Monophyletic A A C = Not Monophyletic

Walsh 2001 (chloroplast atp. B-rbc. L spacer data)

Walsh 2001 combined atp. B-rbc. L spacer and waxy data n=12/13

Walsh 2001 (chloroplast atp. B-rbc. L spacer data)

Capsicum monophyly • Intact for the time being • Odd C. ciliatum seems to be the weak link (n=13)

Mascone’s missing tree Mascone 2003 Flow cytometry and Feulgen densitometry 1 C-value of DNA = an equation for calculating genome size in absolute units Genome size in Mbp

Visualization of Mascone’s results Capsicum anuum complex C. annuum var. annuum C. annuum var. avicular C. frutescens white flowers C. chinense C. chacoense United by similar DNA amount and little heterochromatin

1 C G C. chacoense 3. 35 3273 C. annuum var. annuum 3. 38 3312 C. frutescens 3. 40 3332 C. chinense 3. 42 3352

Capsicum baccatum group C. baccatum var. praetermissum C. baccatum var. pendulum C. baccatum var. baccatum C. baccatum var. umbilicatum white flowers with yellow spots New variety described in 1998 Domesticated status unknown Similar DNA amounts – not surprising

1 C G C. chacoense 3. 35 3273 C. annuum var. annuum 3. 38 3312 C. frutescens 3. 40 3332 C. chinense 3. 42 3352 C. baccatum var. pendulum 3. 69 3621 C. baccatum var. baccatum 3. 71 3636 C. baccatum var. umbilicatum 3. 76 3636 Interpreted from data – not explicitly stated

Capsicum eximium complex C. pubescens C. eximium purple flowers C. cardenasii C. parvifolium synonym with C. cardenasii? (but description is off – tree? ) C. parvifolium only compared to C. campylopodium points out distantly related and nothing more C. campylopodium groups with C. pubescens – large genome size, and large amounts of heterochromatin forming complex patterns (tone implies trepidation) C. eximium has DNA content intermediate between C. baccatum and C. pubescens, but genome size supports close relationship to C. pubescens as well as isozyme and cross studies

1 C ? ? G C. chacoense 3. 35 3273 C. annuum var. annuum 3. 38 3312 C. frutescens 3. 40 3332 C. chinense 3. 42 3352 C. baccatum var. pendulum 3. 69 3621 C. baccatum var. baccatum 3. 71 3636 C. baccatum var. umbilicatum 3. 76 3636 C. eximium 4. 06 3979 C. pubescens 4. 47 4381 C. campylopodium 5. 14 5032 C. parvifolium/cardenasii 5. 77 5655

However, Mascone claims his data supports his hypothesis • Increase in DNA amount is evolutionary advancement • C. chacoense most plesiomorphic (ancestral) • C. campylopodium most advanced • n=13 in more recently evolved

Mascone tree rooted Least DNA C. chacoense C. annuum var. annuum C. frutescens C. chinense C. baccatum var. pendulum C. baccatum var. baccatum C. baccatum var. umbilicatum C. eximium C. pubescens Most DNA C. campylopodium x=13 ? C. parvifolium/cardenasii

Mascone Least DNA molecular C. chacoense C. annuum var. annuum C. frutescens C. chinense C. baccatum var. pendulum C. baccatum var. baccatum C. baccatum var. umbilicatum C. eximium C. pubescens Most DNA C. campylopodium x=13 ? C. parvifolium/cardenasii ? ancestral

X=13 species • • • C. ciliatum C. buforum C. campylopodium C. cornutum C. schottianum C. villosum C. pereirae * C. friburguense * 3 unnamed Capsicum

Capsicum flexuosum

n = 13 n = 12

Conclusion • Capsicum needs more research • Appears to be an x=12/x=13 split in distant past • research hindered by incomplete sampling • Difficult to study domestication when phylogeny unresolved • 6 new species identified in last 8 years