Proceedings of the Royal Society B: Biological Sciences
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Why are not all chilies hot? A trade-off limits pungency

David C. Haak

David C. Haak

Department of Biology, University of Washington, PO Box 351800, 24 Kincaid Hall, Seattle, WA 98195-1800, USA

[email protected]

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Leslie A. McGinnis

Leslie A. McGinnis

Department of Biology, University of Washington, PO Box 351800, 24 Kincaid Hall, Seattle, WA 98195-1800, USA

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,
Douglas J. Levey

Douglas J. Levey

Department of Biology, University of Florida, PO Box 118525, Gainesville, FL 32611-8525, USA

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and
Joshua J. Tewksbury

Joshua J. Tewksbury

Department of Biology, University of Washington, PO Box 351800, 24 Kincaid Hall, Seattle, WA 98195-1800, USA

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Published:https://doi.org/10.1098/rspb.2011.2091

    Evolutionary biologists increasingly recognize that evolution can be constrained by trade-offs, yet our understanding of how and when such constraints are manifested and whether they restrict adaptive divergence in populations remains limited. Here, we show that spatial heterogeneity in moisture maintains a polymorphism for pungency (heat) among natural populations of wild chilies (Capsicum chacoense) because traits influencing water-use efficiency are functionally integrated with traits controlling pungency (the production of capsaicinoids). Pungent and non-pungent chilies occur along a cline in moisture that spans their native range in Bolivia, and the proportion of pungent plants in populations increases with greater moisture availability. In high moisture environments, pungency is beneficial because capsaicinoids protect the fruit from pathogenic fungi, and is not costly because pungent and non-pungent chilies grown in well-watered conditions produce equal numbers of seeds. In low moisture environments, pungency is less beneficial as the risk of fungal infection is lower, and carries a significant cost because, under drought stress, seed production in pungent chilies is reduced by 50 per cent relative to non-pungent plants grown in identical conditions. This large difference in seed production under water-stressed (WS) conditions explains the existence of populations dominated by non-pungent plants, and appears to result from a genetic correlation between pungency and stomatal density: non-pungent plants, segregating from intra-population crosses, exhibit significantly lower stomatal density (p = 0.003), thereby reducing gas exchange under WS conditions. These results demonstrate the importance of trait integration in constraining adaptive divergence among populations.

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