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Polyploid Plants Have Faster Rates of Multivariate Niche Differentiation Than Their Diploid Relatives 3 4 Authors and Affiliations 5 Anthony E

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Polyploid Plants Have Faster Rates of Multivariate Niche Differentiation Than Their Diploid Relatives 3 4 Authors and Affiliations 5 Anthony E 1 Title 2 Polyploid plants have faster rates of multivariate niche differentiation than their diploid relatives 3 4 Authors and affiliations 5 Anthony E. Baniaga¹*, Hannah E. Marx1,2, Nils Arrigo1,3, Michael S. Barker¹ 6 7 ¹Department of Ecology & Evolutionary Biology, University of Arizona, Tucson, AZ, USA 8 2Department of Ecology & Evolutionary Biology, University of Michigan, Ann Arbor, MI, USA 9 3Department of Ecology & Evolution, University of Lausanne, Switzerland 10 11 [email protected] 12 [email protected] 13 [email protected] 14 [email protected] 15 16 Short running title Climatic niche evolution of polyploid plants 17 18 Keywords 19 climatic niche, niche breadth, polyploid, speciation, sympatric speciation 20 21 Type of article Letter 22 23 Number of words in Abstract: 146, Main Text: 4881, Text boxes: 0. 24 Number of References: 155; Number of Figures: 2; Number of Tables: 2; Number of Text 25 Boxes: 0. 26 27 Statement of Authorship: AB and MSB conceived of project, AB and NA generated the 28 dataset, AB and HM performed analyses, AB and MSB co-wrote the manuscript. Author Manuscript 29 This is the author manuscript accepted for publication and has undergone full peer review but has not been through the copyediting, typesetting, pagination and proofreading process, which may lead to differences between this version and the Version of Record. Please cite this article as doi: 10.1111/ELE.13402 This article is protected by copyright. All rights reserved 30 Data Accessibility Statement: Upon acceptance all necessary R scripts, data, and files 31 supporting the results will be archived on FigShare with the data DOI included at the end of the 32 article. 33 34 *author for correspondence 35 Anthony E. Baniaga 36 The University of Arizona 37 Department of Ecology & Evolutionary Biology 38 P.O. Box 210088 39 Tucson, AZ 85721 40 Phone: 520–626–0946 Fax: 520–621–9190 Email: [email protected] 41 42 43 44 45 46 47 Abstract 48 Polyploid speciation entails substantial and rapid postzygotic reproductive isolation of nascent 49 species that are initially sympatric with one or both parents. Despite strong postzygotic isolation, 50 ecological niche differentiation has long been thought to be important for polyploid success. 51 Using biogeographic data from across vascular plants, we tested whether the climatic niches of 52 polyploid species are more differentiated than their diploid relatives and if the climatic niches of 53 polyploid species differentiated faster than those of related diploids. We found that polyploids 54 are often more climatically differentiated from their diploid parents than the diploids are from 55 each other. Consistent with this pattern, we estimated that polyploid species generally have 56 higher rates of multivariate niche differentiation than their diploid relatives. In contrast to recent 57 analyses, our results confirm that ecological niche differentiation is an important component of Author Manuscript 58 polyploid speciation and that niche differentiation is often significantly faster in polyploids. 59 60 This article is protected by copyright. All rights reserved 61 62 63 64 65 66 67 68 69 70 Introduction 71 Among vascular plants, polyploidy or whole genome duplication (WGD) is associated with an 72 estimated 15–30% of speciation events (Wood et al. 2009). These WGD events are also common 73 throughout the evolutionary history of vascular plants (Landis et al. 2018), such as the ancestry 74 of seed plants (Jiao et al. 2011; Li et al. 2015), angiosperms (Amborella Genome Project), core 75 eudicots (Tuskan et al. 2006; Jaillon et al. 2007; Jiao et al. 2012; Vekemans et al. 2012), as well 76 as taxonomically rich clades like the Asteraceae (Barker et al. 2008; Barker et al. 2016a; Huang 77 et al. 2016; Badouin et al. 2017) and Poaceae (Paterson et al. 2004; Paterson et al. 2009; Estep et 78 al. 2014; McKain et al. 2016). However, most nascent polyploid lineages have lower estimated 79 net diversification rates than their diploid relatives (Mayrose et al. 2011). This may be due to the 80 multiple ecological and evolutionary obstacles that newly formed polyploid species face such as 81 small populations sizes and competition with their diploid relatives (Otto & Whitton 2000; 82 Comai 2005; Arrigo & Barker 2012; Barker et al. 2016b). 83 84 Competition significantly influences the ecological niches of species (Connell 1961; MacArthur 85 1972), and the niches of closely related species tend to be more similar to each other than to 86 those of more distantly related ones (Harvey & Pagel 1991; Wiens 2004; Pyron et al. 2015). 87 Considering the abrupt origins of polyploid species, interspecific competition likely plays an 88 important role in whether polyploid species establish and persist. This is because newly formed Author Manuscript 89 polyploid species are initially imbued with substantial postzygotic isolation from their 90 progenitors, while also sympatric and competing with either one or both parental species 91 (Ramsey & Schemske 1998, 2002). Mathematical models indicate that polyploid establishment This article is protected by copyright. All rights reserved 92 is promoted by high selfing rates, high rates of polyploid formation, local propagule dispersal, 93 and ecological niche differentiation (Levin 1975; Fowler & Levin 1984; Felber 1991; Rodriguez 94 1996; Husband 2000; Baack 2005; Rausch & Morgan 2005; Fowler & Levin 2016). The 95 importance of ecological niche differentiation is also supported by species coexistence theory 96 (Tilman 1982, 1985; Chesson 2000, 2004) which suggests that coexistence of related species, 97 such as polyploid and progenitor species, is possible if they have different resource needs or 98 utilization strategies. 99 100 Some polyploid species are long known to have different geographical distributions, novel 101 ecological niches, and wider niche breadths than their progenitors (Hagerup 1932; Tischler 1937; 102 Wulff 1937; Love & Love 1943; Clausen et al. 1945; Stebbins 1950; Stebbins 1971; Levin 103 1975). However, previous analyses have found mixed support for the importance of ecological 104 niche differentiation to polyploid establishment (Stebbins 1971; Felber-Girard et al. 1996; Petit 105 & Thompson 1999; Martin & Husband 2009; Glennon et al. 2014; Marchant et al. 2016). This is 106 surprising given that polyploids may adapt faster than diploids (Orr & Otto 1994; Otto & 107 Whitton 2000; Otto 2007; Selmecki et al. 2015). 108 109 To better understand the role of ecological niche differentiation during polyploid speciation, we 110 evaluated the rates of climatic niche differentiation of polyploids and their diploid relatives. We 111 explored two aspects of climatic niche differentiation in polyploid species. First, we analyzed the 112 amount of climatic niche overlap between allopolyploid species and their diploid progenitors in 113 25 genera of plants. We then examined whether polyploid species, in which we did not know 114 whether they were allo- or autopolyploid, evolved multivariate climatic niche traits (mean and 115 breadth) at faster rates than their diploid relatives in 33 genera of plants. We hypothesized that if 116 climatic niche differentiation is not important for polyploid establishment, then the rates of 117 climatic niche differentiation of polyploid species would not be significantly different than those 118 of diploid species. Conversely, if climatic niche differentiation is important for polyploid 119 establishment, we expected polyploid species to have faster rates of climatic niche differentiation Author Manuscript 120 than related diploids. Our results provide insight into the importance of ecological divergence for 121 polyploid species establishment, and highlight the role of ecological divergence in speciation 122 processes generally. This article is protected by copyright. All rights reserved 123 124 Materials & Methods 125 Climatic niche overlap between allopolyploid species and their diploid progenitors 126 Data on allopolyploids and their known diploid parents were collected from the literature. We 127 used the Taxonomic Name Resolution Service v4.0 (Boyle et al. 2013) to verify taxonomy and 128 filter non-valid species. This filtering left 52 trios comprised of two diploid parents and an 129 allopolyploid, which included 131 unique taxa from 16 families and 25 genera. In this dataset 130 eighteen diploid species were parents of at least two or more allopolyploid species. 131 132 For each species we downloaded all available georeferenced locations from the union of the 133 Global Biodiversity Information Facility (GBIF.org), the Consortium of California Herbaria 134 2016, and SEINet Portal Network 2016. Georeferenced data were cleaned by removing duplicate 135 records using the R dismo package duplicated function, and any record in which latitude or 136 longitude was not precise to two decimal points was excluded. Occurrences were then manually 137 examined for erroneous records. Refinements were based on literature data in cases of unclear 138 species ranges. 139 140 We used Ecospat to quantify the multivariate climatic niche overlap among the taxa of a trio 141 (Broennimann et al. 2012). We chose to employ Ecospat for two key reasons. First, it applies a 142 kernel density function to occurrence points to mitigate potential biases in geographic 143 representation related to sampling effort. Second, it reduces the dimensionality of climate data 144 into two dimensional space, and projects this onto a gridded
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