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Reproductive strategies and their consequences for divergence, gene flow, and genetic diversity in three taxa of Clarkia

Heredity volume 131, pages 338–349 (2023)Cite this article

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Abstract

Differences in reproductive strategies can have important implications for macro- and micro-evolutionary processes. We used a comparative approach through a population genetics lens to evaluate how three distinct reproductive strategies shape patterns of divergence among as well as gene flow and genetic diversity within three closely related taxa in the genus Clarkia. One taxon is a predominantly autonomous self-fertilizer and the other two taxa are predominantly outcrossing but vary in the primary pollinator they attract. In genotyping populations using genotyping-by-sequencing and comparing loci shared across taxa, our results suggest that differences in reproductive strategies in part promote evolutionary divergence among these closely related taxa. Contrary to expectations, we found that the selfing taxon had the highest levels of heterozygosity but a low rate of polymorphism. The high levels of fixed heterozygosity for a subset of loci suggests this pattern is driven by the presence of structural rearrangements in chromosomes common in other Clarkia taxa. In evaluating patterns within taxa, we found a complex interplay between reproductive strategy and geographic distribution. Differences in the mobility of primary pollinators did not translate to a difference in rates of genetic diversity and gene flow within taxa – a pattern likely due to one taxon having a patchier distribution and a less temporally and spatially reliable pollinator. Taken together, this work advances our understanding of the factors that shape gene flow and the distribution of genetic diversity within and among closely related taxa.

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Fig. 1: Distribution, sampling, and reproductive strategy for the three study taxon of Clarkia collected from twelve populations across California.
Fig. 2: Genetic divergence and diversity among C. concinna subsp. automixa (blue), Clarkia concinna subsp. concinna (green), and C. breweri (yellow) collected from twelve populations across northern California.
Fig. 3: Within taxa measures of genetic diversity, inbreeding, and effective population size for Clarkia concinna subsp. automixa, Clarkia concinna subsp. concinna, and Clarkia breweri collected from twelve populations across northern California.
Fig. 4: Within taxa measures of population genetic structure for Clarkia concinna subsp. automixa, Clarkia concinna subsp. concinna, and Clarkia breweri collected from twelve populations across northern California.

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Data availability

Relevant data and code have been uploaded to a Dryad repository: https://doi.org/10.5061/dryad.sxksn038b.

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Acknowledgements

We thank Matt Rhodes, Shelley Sianta, Tim Miller, Rick Overson, Tania Jogesh, Evan Hilpman, and Pedro Juárez for assistance with data collection and Rick Overson for assistance with genomic library preparation. We are also grateful to Elinor Gates, Kostas Chloros, and Joseph Halay for facilitating plant collections on the grounds of the UC Lick Observatory. Permission was granted by the National Park Service to collect data and samples at Pinnacles National Park. This work was supported by US National Science Foundation DEB 1342873 to JF and KS and DBI 1461007 to JF. Samples were collected under permits FS-2400-8 and PIN-2014-SCI-003.

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Authors and Affiliations

  1. Department of Biology, Spelman College, Atlanta, GA, 30314, USA

    Zoe Diaz-Martin

  2. Negaunee Institute for Plant Conservation Science and Action, Chicago Botanic Garden, Glencoe, IL, 60035, USA

    Zoe Diaz-Martin, Anita Cisternas-Fuentes, Krissa Skogen & Jeremie Fant

  3. Plant Biology and Conservation, Northwestern University, 2205 Tech Drive, Evanston, IL, 60208, USA

    Anita Cisternas-Fuentes, Krissa Skogen & Jeremie Fant

  4. Departamento de Botánica, Facultad de Ciencias Naturales y Oceanográficas, Universidad de Concepción, Concepción, Chile

    Anita Cisternas-Fuentes

  5. Department of Ecology and Evolutionary Biology, University of California, 130 McAllister Way, Santa Cruz, CA, 95060, USA

    Kathleen M. Kay

  6. Department of Neurobiology and Behavior, Cornell University, Ithaca, NY, 14853, USA

    Robert A. Raguso

  7. Department of Biological Sciences, Clemson University, 132 Long Hall, Clemson, SC, 29631, USA

    Krissa Skogen

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Contributions

ZDM, ACF, KS, KK, RR, JF conceived and designed the study. ACF, KS, KK, and JF collected the data and determined the methodology. Investigation and visualization were conducted by ZDM. Funding was acquired by KS and JF. Writing of the original draft was completed by ZDM and JF. Writing, review, and editing of the further drafts were completed by ZDM, ACF, KS, KK, RR, and JF.

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Correspondence to Zoe Diaz-Martin.

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Diaz-Martin, Z., Cisternas-Fuentes, A., Kay, K.M. et al. Reproductive strategies and their consequences for divergence, gene flow, and genetic diversity in three taxa of Clarkia. Heredity 131, 338–349 (2023). https://doi.org/10.1038/s41437-023-00649-y

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