Microbes, mutualism, and range margins: testing the fitness consequences of soil microbial communities across and beyond a native plant's range

John W. Benning, David A. Moeller

Research output: Contribution to journalArticlepeer-review

22 Scopus citations

Abstract

Interactions between plants and soil fungi and bacteria are ubiquitous and have large effects on individual plant fitness. However, the degree to which spatial variation in soil microbial communities modulates plant species’ distributions remains largely untested. Using the California native plant Clarkia xantiana ssp. xantiana we paired glasshouse and field reciprocal transplants of plant populations and soils to test whether plant–microbe interactions affect the plant’s geographic range limit and whether there is local adaptation between plants and soil microbe communities. In the field and glasshouse, one of the two range interior inocula had a positive effect on plant fitness. In the field, this benefit was especially pronounced at the range edge and beyond, suggesting possible mutualist limitation. In the glasshouse, soil inocula from beyond-range tended to increase plant growth, suggesting microbial enemy release beyond the range margin. Amplicon sequencing revealed stark variation in microbial communities across the range boundary. Plants dispersing beyond their range limit are likely to encounter novel microbial communities. In C. x. xantiana, our results suggest that range expansion may be facilitated by fewer pathogens, but could also be hindered by a lack of mutualists. Both negative and positive plant–microbe interactions will likely affect contemporary range shifts.

Original languageEnglish (US)
Pages (from-to)2886-2900
Number of pages15
JournalNew Phytologist
Volume229
Issue number5
DOIs
StatePublished - Dec 18 2020

Bibliographical note

Funding Information:
The authors thank Lana Bolin, Haley Branch, Alexai Faulkner, Adam Kostanecki, Sarah Tran, Amanda Gorton, and Anna Peschel for assistance with field and lab work. The authors appreciate insightful comments from Peter Kennedy, Ruth Shaw, and Peter Tiffin on experimental design, analyses, and interpretation of results. The UMN UMGC Microbiome team was invaluable in helping us process and analyze the microbial community data. Feedback from three anonymous reviewers and the associate editor greatly improved the manuscript. Our work was generously supported by grants from the National Science Foundation (DEB‐1701072 to JWB and DAM and DEB‐1255141 to DAM) and the Society for the Study of Evolution (JWB). Any opinions, findings, and conclusions expressed in this material are those of the authors and do not necessarily reflect the views of the National Science Foundation.

Publisher Copyright:
© 2020 The Authors New Phytologist © 2020 New Phytologist Foundation

Keywords

  • Clarkia xantiana ssp. xantiana
  • biotic interaction
  • geographic range limit
  • local adaptation
  • plant–soil feedbacks
  • reciprocal transplant
  • species distributions

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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