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Extremely low genetic diversity in the European clade of the model bryophyte Anthoceros agrestis

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Abstract

The hornwort Anthoceros agrestis is emerging as a model system for the study of symbiotic interactions and carbon fixation processes. It is an annual species with a remarkably small and compact genome. Single accessions of the plant have been shown to be related to the cosmopolitan perennial hornwort Anthoceros punctatus. We provide the first detailed insight into the evolutionary history of the two species. Due to the rather conserved nature of organellar loci, we sequenced multiple accessions in the Anthoceros agrestis–A. punctatus complex using three nuclear regions: the ribosomal spacer ITS2, and exon and intron regions from the single-copy coding genes rbcS and phytochrome. We used phylogenetic and dating analyses to uncover the relationships between these two taxa. Our analyses resolve a lineage of genetically near-uniform European A. agrestis accessions and two non-European A. agrestis lineages. In addition, the cosmopolitan species Anthoceros punctatus forms two lineages, one of mostly European accessions, and another from India. All studied European A. agrestis accessions have a single origin, radiated relatively recently (less than 1 million years ago), and are currently strictly associated with agroecosystem habitats.

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Availability of data and materials

The data set generated and analysed during the current study is available from GenBank and DRYAD [https://datadryad.org/stash/dataset/doi:10.5061/dryad.qnk98sfcb].

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Acknowledgements

We would like to acknowledge the LIFE IUCN European Red List team and Norbert Schnyder for access to population size data for European Anthoceros agrestis from the Red List work (contract number LIFE14PREBE001). Thanks to Ilia Leitch for information about the Anthoceros agrestis genome size, and to the many colleagues who improved our sampling by sending us their Anthoceros collections. We are also grateful to the anonymous reviewers of a previous version of this manuscript, whose comments have hopefully led to some beneficial changes. This study formed the research thesis element of Tom Dawes’ MSc degree at the University of Edinburgh and Royal Botanic Garden, Edinburgh.

Funding

JCVA acknowledges support from the Earl S. Tupper Fellowship (Smithsonian Tropical Research Institute) and le Conseil de recherches en sciences naturelles et en genie du Canada RGPIN/05967-2016; TD and LLF acknowledge funding from the Royal Botanic Garden, Edinburgh, which is supported by the Scottish Government’s Rural and Environment Science and Analytical Services Division. PS acknowledges funding from Swiss National Science Foundation grant nos 160004 and 131726, the Georges and Antoine Claraz Foundation, The Forschungskredit and the University Research Priority Program.

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Author notes

  1. Thomas N. Dawes and Juan Carlos Villarreal A. have contributed equally to this work.

Authors and Affiliations

  1. Royal Botanic Garden Edinburgh, Edinburgh, Scotland

    Thomas N. Dawes & Laura L. Forrest

  2. Victoria University of Wellington, Wellington, New Zealand

    Thomas N. Dawes

  3. Department of Biology, Université Laval, Quebec, Canada

    Juan Carlos Villarreal A.

  4. Smithsonian Tropical Research Institute, Panama City, Panama

    Juan Carlos Villarreal A.

  5. University of Zurich and Zurich-Basel Plant Science Center, Zurich, Switzerland

    Péter Szövényi

  6. Swedish Museum of Natural History, Stockholm, Sweden

    Irene Bisang

  7. Boyce Thompson Institute, Ithaca, NY, USA

    Fay-Wei Li & Duncan A. Hauser

  8. Plant Biology Section, Cornell University, Ithaca, NY, USA

    Fay-Wei Li & Duncan A. Hauser

  9. Nees-Institut für Biodiversität Der Pflanzen, Bonn, Germany

    Dietmar Quandt

  10. Australian National Botanic Gardens, Canberra, Australia

    D. Christine Cargill

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Contributions

LLF, JCVA and TD contributed to the study conception and design. Material preparation, data collection and analyses were performed by TD, JCVA and LLF. The first draft of the manuscript was written by LLF, JCVA and TD, and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.

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Correspondence to Laura L. Forrest.

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Online Resource 1. Voucher table for the specimens included in the multigene analyses.

Online Resource 2. PCR and Sanger sequencing primers used in this study.

Online Resource 3. Basic statistics for the three loci.

Online Resource 4. Phylogeny produced using phytochrome (a) and rbcS (b) nucleotide sequence data, and annotated with ML bootstrap values and posterior probabilities as symbols on the trees.

Online Resource 5.Anthoceros divergence dates (in Ma) from the three calibration schemes (see text). (a) UCLN “relaxed” clock with a single calibration (root calibration) of 20 Ma and sd of 3; (b) UCLN “relaxed” clock with the root calibration and the island calibration on the node of the neoendemic A. cristatus, with a normal prior with a mean of 1 and sd of 0.25; (c) UCLN “relaxed” clock (Online Resource 4) with three calibrations (Online Resource 6): a normal root calibration, the A. cristatus calibration, and the crown age of the A. punctatus–agrestis–lamellatus–venosus group from the previous study applied to the ingroup, with a mean of 6 Ma and sd of 1.

Online Resource 6. (a) Uncorrelated lognormal (UCLN) relaxed clock dated tree produced using the root calibration scheme (normal prior, mean 20 Ma, sd 3) based on values in Villarreal A et al. 2015. (b). UCLN dated tree produced using a 2-calibration scheme, based on the root calibration and a crown age for A. punctatus–agrestis (mean 6 Ma, sd 1) based on values in Villarreal A et al. 2015. (c). UCLN dated tree produced using a 3-calibration scheme, based on the root calibration, a crown age for A. punctatus–agrestis and the age of Ascension Island as a proxy for A. cristatus (normal prior, mean 1 Ma, sd 0.25).

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Dawes, T.N., Villarreal A., J.C., Szövényi, P. et al. Extremely low genetic diversity in the European clade of the model bryophyte Anthoceros agrestis. Plant Syst Evol 306, 49 (2020). https://doi.org/10.1007/s00606-020-01676-6

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