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Latitudinal Biogeographic Structuring in the Globally Distributed Moss Ceratodon Purpureus

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Latitudinal Biogeographic Structuring in the Globally Distributed Moss Ceratodon Purpureus University of Wollongong Research Online Faculty of Science, Medicine and Health - Papers: Part B Faculty of Science, Medicine and Health 1-1-2020 Latitudinal biogeographic structuring in the globally distributed moss Ceratodon purpureus Elisabeth Machteld Biersma Peter Convey Rhys Wyber University of Wollongong, [email protected] Sharon A. Robinson University of Wollongong, [email protected] Mark P. Dowton University of Wollongong, [email protected] See next page for additional authors Follow this and additional works at: https://ro.uow.edu.au/smhpapers1 Publication Details Citation Biersma, E. M., Convey, P., Wyber, R., Robinson, S. A., Dowton, M. P., Van De Vijver, B., Linse, K., Griffiths, H., & Jackson, J. A. (2020). Latitudinal biogeographic structuring in the globally distributed moss Ceratodon purpureus. Faculty of Science, Medicine and Health - Papers: Part B. Retrieved from https://ro.uow.edu.au/smhpapers1/1523 Research Online is the open access institutional repository for the University of Wollongong. For further information contact the UOW Library: [email protected] Latitudinal biogeographic structuring in the globally distributed moss Ceratodon purpureus Abstract Biogeographic patterns of globally widespread species are expected to reflect egionalr structure, as well as connectivity caused by occasional long-distance dispersal. We assessed the level and drivers of population structure, connectivity, and timescales of population isolation in one of the most widespread and ruderal plants in the world — the common moss Ceratodon purpureus. We applied phylogenetic, population genetic, and molecular dating analyses to a global (n = 147) sampling data set, using three chloroplast loci and one nuclear locus. The plastid data revealed several distinct and geographically structured lineages, with connectivity patterns associated with worldwide, latitudinal “bands.” These imply that connectivity is strongly influenced by global atmospheric circulation patterns, with dispersal and establishment beyond these latitudinal bands less common. Biogeographic patterns were less clear within the nuclear marker, with gene duplication likely hindering the detection of these. Divergence time analyses indicated that the current matrilineal population structure in C. purpureus has developed over the past six million years, with lineages diverging during the late Miocene, Pliocene, and Quaternary. Several colonization events in the Antarctic were apparent, as well as one old and distinct Antarctic clade, possibly isolated on the continent since the Pliocene. As C. purpureus is considered a model organism, the matrilineal biogeographic structure identified here provides a useful framework for future genetic and developmental studies on bryophytes. Our general findings may also be relevant to understanding global environmental influences on the biogeography of other organisms with microscopic propagules (e.g., spores) dispersed by wind. Keywords purpureus, ceratodon, moss, distributed, globally, biogeographic, structuring, latitudinal Publication Details Biersma, E. Machteld., Convey, P., Wyber, R., Robinson, S. A., Dowton, M. P., Van De Vijver, B., Linse, K., Griffiths, H. & Jackson, J. A. (2020). Latitudinal biogeographic structuring in the globally distributed moss Ceratodon purpureus. Frontiers in Plant Science, Online First 1-14. Authors Elisabeth Machteld Biersma, Peter Convey, Rhys Wyber, Sharon A. Robinson, Mark P. Dowton, Bart Van De Vijver, Katrin Linse, Howard Griffiths, and Jennifer A. Jackson This journal article is available at Research Online: https://ro.uow.edu.au/smhpapers1/1523 ORIGINAL RESEARCH published: 28 August 2020 doi: 10.3389/fpls.2020.502359 Latitudinal Biogeographic Structuring in the Globally Distributed Moss Ceratodon purpureus Elisabeth M. Biersma 1,2,3*, Peter Convey 1, Rhys Wyber 4, Sharon A. Robinson 4, Mark Dowton 5, Bart van de Vijver 6,7, Katrin Linse 1, Howard Griffiths 2 and Jennifer A. Jackson 8 1 Biodiversity, Evolution and Adaptation Team, British Antarctic Survey, Cambridge, United Kingdom, 2 Department of Plant Sciences, University of Cambridge, Cambridge, United Kingdom, 3 Natural History Museum of Denmark, University of Copenhagen, Copenhagen, Denmark, 4 School of Earth, Atmospheric and Life Sciences, University of Wollongong, NSW, Australia, 5 School of Chemistry and Molecular Bioscience, University of Wollongong, Wollongong, NSW, Australia, Edited by: 6 Research Department, Botanic Garden Meise, Meise, Belgium, 7 Ecosystem Management (ECOBE), Department of Biology, Jeffrey Graham Duckett, University of Antwerp, Antwerp, Belgium, 8 Ecosystems Team, British Antarctic Survey, Cambridge, United Kingdom Natural History Museum, United Kingdom fl Reviewed by: Biogeographic patterns of globally widespread species are expected to re ect regional Alexander Zizka, structure, as well as connectivity caused by occasional long-distance dispersal. We German Centre for Integrative assessed the level and drivers of population structure, connectivity, and timescales of Biodiversity Research (iDiv), Germany — Santiago Mart´ın-Bravo, population isolation in one of the most widespread and ruderal plants in the world the Universidad Pablo de Olavide, Spain common moss Ceratodon purpureus. We applied phylogenetic, population genetic, and *Correspondence: molecular dating analyses to a global (n = 147) sampling data set, using three chloroplast Elisabeth M. Biersma loci and one nuclear locus. The plastid data revealed several distinct and geographically [email protected] structured lineages, with connectivity patterns associated with worldwide, latitudinal Specialty section: “bands.” These imply that connectivity is strongly influenced by global atmospheric This article was submitted to circulation patterns, with dispersal and establishment beyond these latitudinal bands Plant Systematics and Evolution, less common. Biogeographic patterns were less clear within the nuclear marker, with a section of the journal gene duplication likely hindering the detection of these. Divergence time analyses Frontiers in Plant Science indicated that the current matrilineal population structure in C. purpureus has Received: 02 October 2019 Accepted: 13 August 2020 developed over the past six million years, with lineages diverging during the late Published: 28 August 2020 Miocene, Pliocene, and Quaternary. Several colonization events in the Antarctic were Citation: apparent, as well as one old and distinct Antarctic clade, possibly isolated on the continent Biersma EM, Convey P, Wyber R, since the Pliocene. As C. purpureus is considered a model organism, the matrilineal Robinson SA, Dowton M, van de Vijver B, Linse K, Griffiths H and biogeographic structure identified here provides a useful framework for future genetic and Jackson JA (2020) Latitudinal developmental studies on bryophytes. Our general findings may also be relevant to Biogeographic Structuring in the fl Globally Distributed Moss understanding global environmental in uences on the biogeography of other organisms Ceratodon purpureus. with microscopic propagules (e.g., spores) dispersed by wind. Front. Plant Sci. 11:502359. doi: 10.3389/fpls.2020.502359 Keywords: phylogeography, model organism, moss, spore, wind, bryophyte, global, Antarctica Frontiers in Plant Science | www.frontiersin.org 1 August 2020 | Volume 11 | Article 502359 Biersma et al. Global Biogeography Ceratodon purpureus INTRODUCTION including some Northern Hemisphere specimens, and several more distantly related distinct lineages from equatorial Bryophytes tend to show extensive distributions, often spanning regions, suggesting that migration between Australasian and multiple continents and/or both hemispheres (Schofield and Holarctic regions was more common than among equatorial Crum, 1972). In particular, the often extremely prolific spore regions. Overall, the study found that, while markers differed production (Longton, 1997) combined with small spore size in implied population structure, the overall global population (generally ~10–20 mm diameter in mosses; Frahm, 2007) give structure in C. purpureus was sparse, and provided evidence that many bryophytes strong potential for long distance dispersal. migration is ongoing. Mounting evidence from experimental (e.g. Sundberg, 2013) and Here, we aim to gain a better understanding of the biogeography phylogeographic studies (e.g. McDaniel and Shaw, 2005; of C. purpureus and assess the level of connectivity between its Huttunen et al., 2008; Pokorny et al., 2011; Stenøien et al., globally widespread populations. Building on the previous 2011; Karlin et al., 2012; Piñeiro et al., 2012; Szövényi et al., biogeographic analysis of McDaniel and Shaw (2005),we 2012; Lewis et al., 2014a; Pisa et al., 2014; Kyrkjeeide et al., 2016; considerably increased the global sampling (n = 147 samples; 257 Biersma et al., 2017) has demonstrated the occurrence of long- newly obtained sequences), focusing primarily on three chloroplast distance dispersal in mosses with disjunct or widespread ranges, markers, the rps4 gene and trnL-F and atpB-rbcL spacers and, to a and suggests that the majority of bryophyte distribution patterns lesser degree, one nuclear marker, the Internal Transcribed Spacer are underlain by relatively frequent short distance, and less (ITS). We tested for global latitudinal and longitudinal population frequent long distance, dispersal events (Heinrichs et al., 2009; structure, providing an overall assessment of biogeographic patterns Patiño
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