Genetic trade-offs underlie divergent life history strategies for local adaptation in white clover

Sara J. Wright, David M. Goad, Briana L. Gross, Patricio R. Muñoz, Kenneth M. Olsen

Research output: Contribution to journalArticlepeer-review

13 Scopus citations

Abstract

Local adaptation is common in plants, yet characterization of its underlying genetic basis is rare in herbaceous perennials. Moreover, while many plant species exhibit intraspecific chemical defence polymorphisms, their importance for local adaptation remains poorly understood. We examined the genetic architecture of local adaptation in a perennial, obligately-outcrossing herbaceous legume, white clover (Trifolium repens). This widespread species displays a well-studied chemical defence polymorphism for cyanogenesis (HCN release following tissue damage) and has evolved climate-associated cyanogenesis clines throughout its range. Two biparental F2 mapping populations, derived from three parents collected in environments spanning the U.S. latitudinal species range (Duluth, MN, St. Louis, MO and Gainesville, FL), were grown in triplicate for two years in reciprocal common garden experiments in the parental environments (6,012 total plants). Vegetative growth and reproductive fitness traits displayed trade-offs across reciprocal environments, indicating local adaptation. Genetic mapping of fitness traits revealed a genetic architecture characterized by allelic trade-offs between environments, with 100% and 80% of fitness QTL in the two mapping populations showing significant QTL×E interactions, consistent with antagonistic pleiotropy. Across the genome there were three hotspots of QTL colocalization. Unexpectedly, we found little evidence that the cyanogenesis polymorphism contributes to local adaptation. Instead, divergent life history strategies in reciprocal environments were major fitness determinants: selection favoured early investment in flowering at the cost of multiyear survival in the southernmost site versus delayed flowering and multiyear persistence in the northern environments. Our findings demonstrate that multilocus genetic trade-offs contribute to contrasting life history characteristics that allow for local adaptation in this outcrossing herbaceous perennial.

Original languageEnglish (US)
Pages (from-to)3742-3760
Number of pages19
JournalMolecular ecology
Volume31
Issue number14
DOIs
StatePublished - Jul 2022

Bibliographical note

Funding Information:
We thank Drs Justin Fay (U Rochester), Christy Edwards (Missouri Botanical Garden), Stephanie Spielman (Rowan U), Nicholas Kooyers (U Louisiana-Lafayette), and Ken Quesenberry (U Florida) for experimental design suggestions, statistical advice, and manuscript feedback. Special thanks to Mike Dyer and the Washington University greenhouse staff for supporting plant breeding, maintenance, and propagation. Thank you to Linda Small, Samantha Myers, and Maya Dutta for assistance with DNA extractions, genotyping, and phenotyping. Field experiments were made possible by the help of numerous field coordinators and assistants. In particular, we thank Haley Reeves and María José Gómez-Quijano (DMN field coordinators); Kenneth Wright, Julien Weinstein, Amy Kuhle and Bailee Warsing (STL assistants); Dr Yolanda Lopez (GFL assistant); and Lindsey Brush and Dr Luis Inostroza (GFL field coordinators). We also thank two anonymous reviewers for feedback. This work was supported by the following funding sources: NSF CAREER Award to KMO (DEB-0845497); NSF Integrated Organismal Systems award to KMO, BLG and PRM (IOS-1557770); NSF Graduate Research Fellowship to SJW (DGE-1745038); NSF Doctoral Dissertation Improvement Grant (DDIG) to SJW and KMO (DEB-1601641); and William H. Danforth Plant Science Fellowship to DMG.

Funding Information:
We thank Drs Justin Fay (U Rochester), Christy Edwards (Missouri Botanical Garden), Stephanie Spielman (Rowan U), Nicholas Kooyers (U Louisiana‐Lafayette), and Ken Quesenberry (U Florida) for experimental design suggestions, statistical advice, and manuscript feedback. Special thanks to Mike Dyer and the Washington University greenhouse staff for supporting plant breeding, maintenance, and propagation. Thank you to Linda Small, Samantha Myers, and Maya Dutta for assistance with DNA extractions, genotyping, and phenotyping. Field experiments were made possible by the help of numerous field coordinators and assistants. In particular, we thank Haley Reeves and María José Gómez‐Quijano (DMN field coordinators); Kenneth Wright, Julien Weinstein, Amy Kuhle and Bailee Warsing (STL assistants); Dr Yolanda Lopez (GFL assistant); and Lindsey Brush and Dr Luis Inostroza (GFL field coordinators). We also thank two anonymous reviewers for feedback. This work was supported by the following funding sources: NSF CAREER Award to KMO (DEB‐0845497); NSF Integrated Organismal Systems award to KMO, BLG and PRM (IOS‐1557770); NSF Graduate Research Fellowship to SJW (DGE‐1745038); NSF Doctoral Dissertation Improvement Grant (DDIG) to SJW and KMO (DEB‐1601641); and William H. Danforth Plant Science Fellowship to DMG.

Publisher Copyright:
© 2021 John Wiley & Sons Ltd.

Keywords

  • QTL×E interactions
  • adaptive polymorphism
  • antagonistic pleiotropy
  • chemical defence
  • cyanogenesis
  • local adaptation

PubMed: MeSH publication types

  • Journal Article
  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, Non-P.H.S.

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