Crop domestication and its impact on naturally selected trophic interactions

Yolanda H. Chen1, Rieta Gols2, Chase Stratton1, Kristian Brevik1, and Betty Benrey3

1University of Vermont, USA2Wageningan University, The Netherlands

3Université de Neuchâtel, Switzerland

IRRI Images

CIAT 2004)

Origin of all of the major phytophagous insect orders and families (Grimaldi and Engel 2005)

Origin of domesticated crops, ~13,000 year ago (Hillman et al. 2001)

(IRRI Images)

Where?

Rice, pigeon pea, jack bean, winged bean, yams, taro, Coconut, orange, lime, tangerine, grapefruit, mango, banana, cucumber, nutmeg, eggplant, plantain, coconut, jute

Rice, soybean, turnip, yams, chestnut, quince; persimmon

litchi, apricot, peach

African rice, sorghum, tef, yam, castor bean, watermelon, melon, okra, coffee

wheat, barley, rye, oat, pea, chickpea, lentil, turnip, carrot, radish, safflower, flax, olive,

fig, walnut, date palm, almond, grape, onion, lettuce,

peanut, Phaseolus beans, potato, peanut, cotton, cashew, pineapple, papaya, avocado, pepper, squash, coca

Maize, Phaseolus beans, Cotton,

Papaya, peppers, squash,

tomato,

Sunflower, cranberry, blueberrypecan

Brassica crops

Where?Apple

pear

Insect herbivores appear to be more abundant and possibly less attacked in agroecosystems than in wild systems (Elton 1958, Pimental 1961, Root 1973, and Risch 1987).

What is the role of crop domestication in altering species interactions?

(T. Degen)

(T. Degen)

Crop domestication

Wild Agricultural

Domestication

The process of genetic change that crops undergo to increase their adaptedness to cultivation and human tastes.

ChemicalPhysicalSemiochemical

(Meyer et al. 2012)

Questions

1) Does domestication favor herbivores and/or select against natural enemy activity?

2) What are the general consequences of selection for particular types of plant traits?

Methods

Domestication gradient (meet the criteria)• Extensive searches through Web of Science

and CAB Abstracts• Yield of >50 papers, Database of 1325 papers

General tritrophic responses (any relevant papers)• Tritrophic responses to plant traits targeted by

domestication• 275 papers

Plant traits targeted by domesticationPhysical• Enlargement of plant structures• Simpler plant architecture• Change in trichome density• Reduction in glumes• Decreased tissue toughness• Greater phenological uniformityChemical• Decreased secondary metabolites• Decreased inducibilityNutritional• Increased protein• Increased sugar

Herbivore feeding guilds

Chewers

Piercing/sucking insectsPredispersal seed predators

BorersLeaf minersGalling

Natural Enemies

ParasitoidsPredators

Geography matters

• The majority of crops (88% of 203 reviewed) were domesticated within the native range of their wild progenitors (Meyer et al. 2012).

We used studies that:• Lab comparing domesticated crops with their

wild ancestor - endemic insect species • Field studies conducted within the geographic

range of the wild ancestor.• Or secondary contact with previously interacting

species= 25 papers

• Insect diversity

• Dominance for a subset of species

∆ Community composition(Chen & Welter, 2002; Chao et al., 2011; Michaud, 2011; Chen et al., 2013)

Natural ecosystems Agroecosystems

(~50% decline, Chen et al. 2013)

Domestication gradient

Domestication gradient

(N = 25)

Natural ecosystems

(N = 179)Plant traits Herbivores N.E. Herbivores N.E. Enlargement + - + -?

Reduction in glumes and spines + ? +, - ?Decreased branching + - ~ ?

Greater phenological uniformity + ? ~ ?Decrease tissue toughness + ? + +?

Decreased secondary metabolites + + ~ +Decreased inducibility? ? ? +? +?Increased protein ? ? + -?Increased sugar ? ? + ?

Does domestication favor herbivores and select against natural enemy activity?

Favoring N. E. • ↑ parasitoid survival and performance (Campan and

Benrey 2004, Harvey et al. 2007, Gols et al. 2008) - But may not increase parasitoid densities in the field.

Selecting against N. E.• ↑ parasitoid encapsulation (Bukovinszky et al. 2009)• ↓ parasitoid efficacy and impact (Chen and Welter 2003,

2005, and 2007)• ↓ keystone predator abundance (Chen and Bernal 2011)

Only 9 studies on domestication effects on N. E

Domestication -a spotty record

• Emphasis on plant resistance to economically-important herbivores

• G x E interactions are likely very important shaping the community interactions

• Effects of domestication on infochemicals were not consistent

• Access to geographic centers of crop origin have been a major barrier

A trade-off between yield and defense?

• ~30% of the studies documented crop selection on yield (but all crops have higher yields than wild ancestors)

• 44% of the studies documented a decline in chemical defenses

- Not all studies focused on chemistry• No relationship between yield and defense

across 29 crops (Turcotte et al. 2014)

Does domestication favor herbivores and/or select against natural enemy activity?

• The directionality of selection on plant traits benefits herbivores

• Natural enemies have been more poorly studied, but show more negative effects of domestication

What are the general consequences of selection for particular types of plant traits?

• Selection for gigantism allows boring herbivores to escape from their natural enemies

• Decline in chemical defenses is associated with increased herbivore preference and performance

• Increased nutrients and decreased tissue toughness is associated with faster larval development

Outstanding questions

• How does crop domestication alter arthropod community structure and function?

• Does crop domestication alter predator-prey dynamics and natural control?

• Are the disruptive effects of domestication fixed or can we breed traits back into the crops to improve their ecological function?

Different groups of people have different preferences for foodSelection differs by ethnic group (Brush and Perales 2007)- Color, taste, storage, yield, etc.

Thanks! Julio BernalRaul MedinaJ. P. MichaudAndrew MichelAndrew NortonCesar Rodriguez-SaonaShawn SteffanSteve Welter…our research labs