RUNNING HEAD : Niche Expansion Via Generalist Clones

Range and niche expansion are commonly associated with transitions to asexuality, polyploidy, and hybridity (allopolyploidy) in plants. The ability of asexual polyploids to colonize novel habitats may be due to widespread generalist clones, multiple ecologically specialized clones, or may be a neutral byproduct of multiple, independent origins of asexual polyploids throughout the range. We have quantified niche size and divergence for hawthorns of the Pacific Northwest using data from herbarium vouchers with known cytotypes. We find that all polyploid niches diverge from that of the diploid range, and allopolyploids have the broadest niches. Allotetraploids have the largest niche and the widest geographic distribution. We then assessed the genetic mechanism of range expansion by surveying the ecological and geographic distribution of genotypes within each cytotype from sites in which fine-scale habitat assessments were completed. We find no isolation by either geographic or ecological distance in allopolyploids, suggesting high dispersal and colonization ability. In contrast, autotriploids and diploids show patterns of isolation by geographic distance. We also compared the geographic and ecological distributions of clonal genotypes with those of randomly drawn sites of the most widespread cytotype. We found that most clones are geographically widespread and occur in a variety of habitats. We interpret these findings to suggest that patterns of range and niche expansion in Pacific Northwest Hawthorns may stem from these widespread, ecologically generalist clones of hybrid origin. This article is protected by copyright. All rights reserved. A cc ep te d A rt ic le Introduction: Polyploidization is a common evolutionary transition, particularly in plants (Ramsey and Schemske 1998; Otto and Whitton 2000; Comai 2005). In plants, however, polyploidization is also often associated with hybridity (allopolyploidization) and the transition to asexual reproduction (i.e. through gametophytic apomixis; the formation and parthenogenetic development of unreduced female gametes; reviewed in Hörandl 2006 and De Storme and Mason 2014). The evolutionary potential of these asexual allopolyploid taxa has long been debated (i.e. Stebbins 1940; Comai 2005; Otto 2007; Mayrose et al. 2011), but one common consequence is the expansion of range and niche in asexual polyploid taxa relative to their sexual, diploid progenitors (Geographic Parthenogenesis; Vandel 1928; Bierzychudek 1985; Lowry and Lester 2006; Hijmans et al. 2007). Asexuality, polyploidization, and hybridization may each contribute to niche expansion, either independently, or in concert. Asexuality allows for single individuals to colonize new geographic areas without mate limitation (Baker’s Law, Baker 1955; Pannell and Barrett 1998) or risk of inbreeding depression (Bierzychudek 1985; Hörandl 2006). Polyploidization may allow for better adaptive potential, as the probability of a mutation (including beneficial mutations) increases with increasing gene copy number (see Otto and Whitton 2000 for details). Hybridization may also increase adaptive potential, as hybrid individuals may be able to access one or both parental genomes (Shimizu-Inatsugi et al. 2017) and in some cases, have been shown to have novel patterns This article is protected by copyright. All rights reserved. A cc ep te d A rt ic le of gene expression relative to their progenitors (Paun et al. 2011). These potential benefits are amplified in allopolyploid apomicts, which do not undergo recombination via sexual reproduction and are fixed heterozygotes. An increase in adaptive potential paired with a lack of mate limitation can increase colonization ability and niche breadth, and thus allow for the colonization of geographically and ecologically novel environments. However, we lack a comprehensive understanding of the genetic mechanisms by which range and niche expansion are achieved in asexual polyploids. Two main hypotheses regarding the distribution of clonal genotypes have been proposed. The ‘General-Purpose Genotypes’ hypothesis posits that a given clonal genotype, having access to multiple alleles at each locus, may have greater plasticity, and hence would be able to live in a greater variety of habitats than their sexual, diploid relatives (Baker 1965; Lynch 1984). Evidence for this hypothesis is mixed. Many studies have found that asexual polyploids possess less variance in fitness components across environmental gradients (Hancock and Bringhurst 1981; Bierzychudek 1989, Michaels and Bazzaz 1989; Oplaat and Verhoeven 2015, although see Bretagnolle and Thompson 2001), or have more adaptively plastic gene expression across environments (ShimizuInatsugi et al. 2017). However, of the few studies that have genotyped range-wide samples of cytotypes, widespread clonal genotypes are often very rare or non-existent (Ellstrand and Roose 1987; van Dijk 2003; Cosendai et al. 2013). Alternatively, the ‘Frozen Niche’ hypothesis posits that a given asexual polyploid taxon comprises several, genetically diverse, ecologically specialized clonal lineages, and collectively these clones increase niche breadth (Vrijenhoek 1984; Vrijenhoek and Parker 2009). While, most clones do tend to be geographically restricted to one or two sites (Ellstrand and Roose This article is protected by copyright. All rights reserved. A cc ep te d A rt ic le 1987), or even to particular habitats within sites (Paun et al. 2006), few studies have distinguished whether these clones are truly ecologically specialized (i.e. locally adapted), or simply just of recent origin and/or with limited dispersal ability. The few studies which have been able to quantify the extent of local adaptation among populations of higher cytotypes (either through quantifying fitness (i.e. Ramsey (2011)), or quantified the spread of alleles across ecological gradients (i.e. Parisod and Christin (2008)), have been done in autopolyploids. Thus, we also lack an understanding of how hybridization may contribute to differences in the genetic mechanism by which niche expansion is accomplished in polyploid taxa. Apparent niche expansion may also simply be a byproduct of the demographic history by which asexual polyploid taxa evolved (i.e. van Dijk and Bakx-Schotman 1997; Thompson and Whitton 2006). If an asexual allopolyploid lineage originates multiple times, each time in a separate geographic area or habitat, the combined range and/or niche of these independent allopolyploid lineages could appear larger than the diploid progenitor ranges. For example, Meimberg et al. (2009) have found that range and niche expansion in Aegilops is associated with the number of origins of a given asexual cytotype. Here we aim to compare the ecological distributions of cytotypes of hawthorns (Crataegus L., Rosaceae) of the Pacific Northwest, moderately long-lived woody perennials that exhibit geographic parthenogenesis (Lo et al. 2013; Coughlan 2014). Using range wide data, we first confirm the result that while diploids occupy a relatively limited geographic range, polyploids are considerably more widely distributed. We then test whether the polyploids have undergone niche differentiation and/or niche expansion, This article is protected by copyright. All rights reserved. A cc ep te d A rt ic le and whether this phenomenon differs among alloand autopolyploids. We then use the geographic and ecological distribution of genotypes to test whether niche expansion in allotetraploids is associated with (a) widespread, ecologically generalist clones, consistent with the general purpose genotypes hypothesis, (b) geographically restricted, ecologically specialized clones, consistent with the frozen niche hypothesis, or (c) highly spatially structured populations, consistent with multiple origins. Materials and Methods: