Abstract
The establishment and success of polyploids are thought to often be facilitated by ecological niche differentiation from diploids. Unfortunately, most studies compared diploids and polyploids, ignoring variation in ploidy level in polyploids. To fill this gap, we performed a large-scale study of 11,163 samples from 1,283 populations of the polyploid perennial geophyte Allium oleraceum with reported mixed-ploidy populations, revealed distribution ranges of cytotypes, assessed their niches and explored the pattern of niche change with increasing ploidy level. Altogether, six ploidy levels (3x−8x) were identified. The most common were pentaploids (53.6%) followed by hexaploids (22.7%) and tetraploids (21.6%). Higher cytotype diversity was found at lower latitudes than at higher latitudes (>52° N), where only tetraploids and pentaploids occurred. We detected 17.4% of mixed-ploidy populations, usually as a combination of two, rarely of three, cytotypes. The majority of mixed-ploidy populations were found in zones of sympatry of the participating cytotypes, suggesting they have arisen through migration (secondary contact zone). Using coarse-grained variables (climate, soil), we found evidence of both niche expansion and innovation in tetraploids related to triploids, whereas higher ploidy levels showed almost zero niche expansion, but a trend of increased niche unfilling of tetraploids. Niche unfilling in higher ploidy levels was caused by a contraction of niche envelopes toward lower continentality of the climate and resulted in a gradual decrease of niche breadth and a gradual shift in niche optima. Field-recorded data indicated wide habitat breadth of tetraploids and pentaploids, but also a pattern of increasing synanthropy in higher ploidy levels. Wide niche breadth of tetra- and pentaploids might be related to their multiple origins from different environmental conditions, higher “age”, and retained sexuality, which likely preserve their adaptive potential. In contrast, other cytotypes with narrower niches are mostly asexual, probably originating from a limited range of contrasting environments. Persistence of local ploidy mixtures could be enabled by the perenniality of A. oleraceum and its prevalence of vegetative reproduction, facilitating the establishment and decreasing exclusion of minority cytotype due to its reproductive costs. Vegetative reproduction might also significantly accelerate colonization of new areas, including recolonization of previously glaciated areas.
Highlights
Polyploidy is a widespread phenomenon among flowering plants (e.g., Wendel, 2000; Van de Peer et al, 2017)
We addressed the following questions: (1) What is the diversity of A. oleraceum cytotypes and the pattern of their geographic distribution over the species range? Is there a different cytotype composition in the contact zones with presumed progenitors in comparison to northern, previously glaciated regions without such contacts? (2) Is the current cytotype distribution a consequence of niche divergence? Is there a different pattern of niche shift with increasing ploidy level? (3) How frequent are mixed-ploidy populations, which cytotypes participate in their composition, and what processes stand behind their existence?
We found a great diversity of ploidy levels in A. oleraceum, ranging from triploids to octoploids
Summary
Polyploidy is a widespread phenomenon among flowering plants (e.g., Wendel, 2000; Van de Peer et al, 2017). It has been evidenced repeatedly that polyploids (prevalently tetraploids) have a broader niche or may differ in their niche optima from their diploid progenitors (Soltis and Soltis, 1995, 2000; Levin, 2002; Weiss-Schneeweiss et al, 2013; Ramsey and Ramsey, 2014; Baniaga et al, 2020) They are reported to have a stronger colonization ability (Treier et al, 2009), including invasion potential (Pandit et al, 2006, 2011), and increased ability to cope with environmental extremes better, especially at higher latitudes and elevations, and in arid or artificially disturbed habitats (Grant, 1981; Stebbins, 1984; Brochmann et al, 2004; Wu et al, 2010; Ramsey, 2011; Manzaneda et al, 2012; te Beest et al, 2012; Muñoz-Pajares et al, 2018; Rice et al, 2019; Castro et al, 2020; Decanter et al, 2020)
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