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Based on Nuclear Genome Markers Utah State University DigitalCommons@USU Ecology Center Publications Ecology Center 9-23-2019 Worldwide Relationships in the Fern Genus Pteridium (Bracken) Based on Nuclear Genome Markers Paul G. Wolf Utah State University Carol A. Rowe Utah State University Sylvia P. Kinosian Utah State University Joshua P. Der California State University, Fullerton Peter J. Lockhart Massey University Lara D. Shepherd Museum of New Zealand Te Papa Tongarewa Follow this and additional works at: https://digitalcommons.usu.edu/eco_pubs See P nextart of page the forEcology additional and E authorsvolutionar y Biology Commons Recommended Citation Wolf, P. G., C. A. Rowe, S. P. Kinosian, J. P. Der, P. J. Lockhart, L. D. Shepherd, P. A. McLenachan, and J. A. Thomson. 2019. Worldwide relationships in the fern genus Pteridium (bracken) based on nuclear genome markers. American Journal of Botany 106(10): 1365–1376. This Article is brought to you for free and open access by the Ecology Center at DigitalCommons@USU. It has been accepted for inclusion in Ecology Center Publications by an authorized administrator of DigitalCommons@USU. For more information, please contact [email protected]. Authors Paul G. Wolf, Carol A. Rowe, Sylvia P. Kinosian, Joshua P. Der, Peter J. Lockhart, Lara D. Shepherd, Patricia A. McLenachan, and John A. Thomson This article is available at DigitalCommons@USU: https://digitalcommons.usu.edu/eco_pubs/91 RESEARCH ARTICLE Worldwide relationships in the fern genus Pteridium (bracken) based on nuclear genome markers Paul G. Wolf1,6,7 , Carol A. Rowe1, Sylvia P. Kinosian1 , Joshua P. Der2 , Peter J. Lockhart3 , Lara D. Shepherd4 , Patricia A. McLenachan3, and John A. Thomson5 Manuscript received 17 March 2019; revision accepted 21 August PREMISE: Spore-bearing plants are capable of dispersing very long distances. However, it is 2019. not known if gene flow can prevent genetic divergence in widely distributed taxa. Here we 1 Department of Biology and Ecology Center, Utah State University, address this issue, and examine systematic relationships at a global geographic scale for Logan, Utah 84322, USA the fern genus Pteridium. 2 Department of Biological Science, California State University, Fullerton, California 92831, USA METHODS: We sampled plants from 100 localities worldwide, and generated nucleotide 3 Institute of Fundamental Sciences, Massey University, Palmerston data from four nuclear genes and two plastid regions. We also examined 2801 single North, New Zealand nucleotide polymorphisms detected by a restriction site-associated DNA approach. 4 Museum of New Zealand Te Papa Tongarewa, PO Box 467, RESULTS: We found evidence for two distinct diploid species and two allotetraploids Wellington 6140, New Zealand between them. The “northern” species (Pteridium aquilinum) has distinct groups at the 5 National Herbarium of New South Wales, Royal Botanic Gardens and Domain Trust, Mrs. Macquaries Road, Sydney, New South Wales continental scale (Europe, Asia, Africa, and North America). The northern European 2000, Australia subspecies pinetorum appears to involve admixture among all of these. A sample from 6 Current address: Department of Biological Sciences, University of the Hawaiian Islands contained elements of both North American and Asian P. aquilinum. Alabama in Huntsville, Huntsville, Alabama 35899, USA The “southern” species, P. esculentum, shows little genetic differentiation between South 7 Author for correspondence (e-mail: [email protected]) American and Australian samples. Components of African genotypes are detected on all Citation: Wolf, P. G., C. A. Rowe, S. P. Kinosian, J. P. Der, P. J. continents. Lockhart, L. D. Shepherd, P. A. McLenachan, and J. A. Thomson. 2019. Worldwide relationships in the fern genus Pteridium (bracken) based CONCLUSIONS: We find evidence of distinct continental-scale genetic differentiation in on nuclear genome markers. American Journal of Botany 106(10): Pteridium. However, on top of this is a clear signal of recent hybridization. Thus, 1365–1376. spore-bearing plants are clearly capable of extensive long-distance gene flow; yet appear doi:10.1002/ajb2.1365 to have differentiated genetically at the continental scale. Either gene flow in the past was at a reduced level, or vicariance is possible even in the face of long-distance gene flow. KEY WORDS allotetraploid; fern; hybrids; introgression; long distance gene flow; spore-bearing plants. Spore-bearing plants are dispersed by microscopic haploid prop- world, often invading grazing land and outcompeting forage species agules that can travel vast distances in wind currents. Thus, many (Holm et al., 1997). Furthermore, Pteridium is toxic to humans and species of ferns, lycophytes, fungi, and other such groups are the- other animals; consumption can result in teratogenesis, carcinogen- oretically capable of extensive long-distance dispersal, some of esis, thiamine deficiency, retinal degeneration, and acute poisoning which may lead to establishment. How much intercontinental gene (Alonso-Amelot and Avendano, 2002; Gil da Costa et al., 2012). flow occurs? Is this sufficient to prevent genetic divergence? And Nevertheless, bracken has been used as fuel, thatch, litter, compost, at what scale are we able to detect these processes in spore-bearing food, medicine, and in the production of potash for the glass, soap, plants? Here we address these questions in one of the most widely and bleaching industries (Rymer, 1976; McGlone et al., 2005). distributed genera on the planet: Pteridium (bracken). Pteridium Following a landmark revision by Tryon (1941), Pteridium has Gled. ex Scop. (Dennstaedtiaceae) is a fern genus found in most generally been treated as monospecific, although previously many temperate to tropical regions from almost 70 degrees north (Alaska, more species had been described at regional levels (e.g., Ching, Scandinavia, Siberia) to almost 50 degrees south (Argentina, 1940). In a later review, Page (1976) noted that more systematic Tasmania, New Zealand) and from sea level to above 3000 m (GBIF work is needed at a global scale to understand the number of distinct Secretariat, 2018). Bracken is a noxious weed in many parts of the entities within the genus worldwide, and this is still the case. The American Journal of Botany 106(10): 1365–1376, 2019; http://www.wileyonlinelibrary.com/journal/AJB © 2019 The Authors. American Journal of Botany is published by Wiley Periodicals, Inc. on behalf of the Botanical Society of America. This is an open access article under the terms of the Creative Commons Attribution-NonCommercial License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited and is not used for commercial purposes. • 1365 1366 • American Journal of Botany majority of brackens are diploid (2n = 104: summarized by Page, between them (Thomson, 2008). The genetic basis of these mor- 1976; Marrs and Watt, 2006). Current treatments have converged photypes remains unclear pending detailed comparative nuclear to recognize two diploid species (Thomson, 2012; Zhou et al., 2014; genomic analysis, although simple allelic differences do correlate Wolf et al., 2015; Schwartsburd et al., 2018). Pteridium aquilinum with smaller-scale polymorphisms in other ferns (Thomson, 2008). (L.) Kuhn is predominant in the northern hemisphere whereas P. Many of the main groupings discussed above were identified in esculentum (G. Forst.) Cockayne is predominantly southern hemi- a global scale analysis of molecular variation focused on chloro- sphere in distribution. Additional to the two widespread diploid plast genes (Der et al., 2009). The results again highlighted the di- species, we recognize two allotetraploid taxa resulting from hy- vergence between northern hemisphere (Pteridium aquilinum) and bridization of these two species: (1) P. caudatum (L.) Maxon from southern hemisphere (P. esculentum) clades, a pattern further cor- Central and South America (and parts of North America); and (2) roborated in the work of Zhou and colleagues (Zhou et al., 2014). P. semihastatum (Wall. ex J. Agardh) S.B. Andrews from southeast- At the subspecies level, two results obtained by the latter authors ern Asia and northern Australia. Other allopolyploids and/or intro- are particularly noteworthy. As already noted by Der et al. (2009), gressants may also exist locally where the northern and southern chloroplast sequences from P. aquilinum subsp. japonicum (Nakai) diploid species are, or have been, in contact (Brownsey, 1989; Wolf A. Love and D. Love and P. aquilinum subsp. pinetorum (C.N. Page et al., 2015). and R.R. Mill) J.A. Thomson were not distinguishable, suggesting Studies on any taxon at a worldwide scale face the challenge of their synonymy. In contrast, genomic comparison using AP-PCR sampling populations in such a way as to represent diversity effec- and ISSR sequence data clearly separate these two forms (see Fig. 6 tively, and this is inherently difficult at a global scale. In Pteridium, in Thomson et al., 2005). Secondly, the chloroplast sequence analysis the problem is exacerbated by inconsistencies in morphological vari- presented by Zhou et al. (2014) did not separate the two sub-Saharan ation and what appears to be phenotypic plasticity for many traits forms from each other or from P. aquilinum subsp. aquilinum from (Page, 1976). In P. aquilinum (Boodle, 1903; Bright, 1928; Tryon, western Europe. Additional nuclear genome studies are particularly 1941) and in P. esculentum (O’Brien, 1963; Schwartsburd
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