Ecological factors influence balancing selection on leaf chemical profiles of a wildflower

Lauren N Carley; Julius P Mojica; Baosheng Wang; Chia-Yu Chen; Ya-Ping Lin; Kasavajhala V S K Prasad; Emily Chan; Che-Wei Hsu; Rose Keith; Chase L Nuñez; Carrie F Olson-Manning; Catherine A Rushworth; Maggie R Wagner; Jing Wang; Pei-Min Yeh; Michael Reichelt; Kathryn Ghattas; Jonathan Gershenzon; Cheng-Ruei Lee; Thomas Mitchell-Olds

doi:10.1038/s41559-021-01486-0

Ecological factors influence balancing selection on leaf chemical profiles of a wildflower

Nat Ecol Evol. 2021 Aug;5(8):1135-1144. doi: 10.1038/s41559-021-01486-0. Epub 2021 Jun 17.

Authors

Lauren N Carley^{1

2

3

4}, Julius P Mojica^{2

5}, Baosheng Wang^{2

6}, Chia-Yu Chen^{7

8}, Ya-Ping Lin^{7

9}, Kasavajhala V S K Prasad¹⁰, Emily Chan², Che-Wei Hsu^{7

11

12}, Rose Keith^{2

13}, Chase L Nuñez^{1

14}, Carrie F Olson-Manning^{2

15}, Catherine A Rushworth^{2

4

16

17}, Maggie R Wagner^{2

18

19}, Jing Wang^{2

6}, Pei-Min Yeh⁷, Michael Reichelt²⁰, Kathryn Ghattas², Jonathan Gershenzon²⁰, Cheng-Ruei Lee^{21

22

23}, Thomas Mitchell-Olds^{24

25}

Affiliations

¹ Duke University Program in Ecology, Durham, NC, USA.
² Biology Department, Duke University, Durham, NC, USA.
³ Rocky Mountain Biological Laboratory, Gothic, CO, USA.
⁴ Department of Plant and Microbial Biology, University of Minnesota Twin Cities, St Paul, MN, USA.
⁵ Pairwise Plants, Durham, NC, USA.
⁶ Key Laboratory of Plant Resources Conservation and Sustainable Utilization, South China Botanical Garden, Chinese Academy of Sciences, Guangzhou, China.
⁷ Institute of Ecology and Evolutionary Biology, National Taiwan University, Taipei, Taiwan.
⁸ Experimental and Clinical Research Center (ECRC) of the MDC and Charité Berlin, Berlin, Germany.
⁹ World Vegetable Center Headquarters, Tainan, Taiwan.
¹⁰ Department of Biology and Cell and Molecular Biology Program, Colorado State University, Fort Collins, CO, USA.
¹¹ Department of Biology, Humboldt Universität zu Berlin, Berlin, Germany.
¹² The Berlin Institute for Medical Systems Biology, Max Delbrück Center for Molecular Medicine, Berlin, Germany.
¹³ Biology Department, DePauw University, Greencastle, IN, USA.
¹⁴ Department for the Ecology of Animal Societies, Max Planck Institute of Animal Behavior, Baden-Württemberg, Germany.
¹⁵ Augustana University, Sioux Falls, SD, USA.
¹⁶ Evolution and Ecology Department, University of California Davis, Davis, CA, USA.
¹⁷ University and Jepson Herbaria, University of California Berkeley, Berkeley, CA, USA.
¹⁸ Department of Ecology and Evolutionary Biology, University of Kansas, Lawrence, KS, USA.
¹⁹ Kansas Biological Survey, Lawrence, KS, USA.
²⁰ Department of Biochemistry, Max Planck Institute for Chemical Ecology, Jena, Germany.
²¹ Institute of Ecology and Evolutionary Biology, National Taiwan University, Taipei, Taiwan. [email protected].
²² Institute of Plant Biology, National Taiwan University, Taipei, Taiwan. [email protected].
²³ Genome and Systems Biology Degree Program, National Taiwan University, Taipei, Taiwan. [email protected].
²⁴ Biology Department, Duke University, Durham, NC, USA. [email protected].
²⁵ Rocky Mountain Biological Laboratory, Gothic, CO, USA. [email protected].

Abstract

Balancing selection is frequently invoked as a mechanism that maintains variation within and across populations. However, there are few examples of balancing selection operating on loci underpinning complex traits, which frequently display high levels of variation. We investigated mechanisms that may maintain variation in a focal polymorphism-leaf chemical profiles of a perennial wildflower (Boechera stricta, Brassicaceae)-explicitly interrogating multiple ecological and genetic processes including spatial variation in selection, antagonistic pleiotropy and frequency-dependent selection. A suite of common garden and greenhouse experiments showed that the alleles underlying variation in chemical profile have contrasting fitness effects across environments, implicating two ecological drivers of selection on chemical profile: herbivory and drought. Phenotype-environment associations and molecular genetic analyses revealed additional evidence of past selection by these drivers. Together, these data are consistent with balancing selection on chemical profile, probably caused by pleiotropic effects of secondary chemical biosynthesis genes on herbivore defence and drought response.

Publication types

Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't

MeSH terms

Brassicaceae* / genetics
Herbivory
Plant Leaves
Polymorphism, Genetic
Selection, Genetic*

Associated data

Dryad/10.5061/dryad.7h44j0zsr

Grants and funding

R01 GM086496/GM/NIGMS NIH HHS/United States