Isolation-by-distance and isolation-by-environment
Associating genetic variation with spatial and ecological gradients, we assessed to what extent phylogeographic patterns of diploid and polyploid species were driven by neutral vs adaptive processes. Consistent with genetic variation shaped by neutral gene flow among individuals, both Mantel tests and RDA consistently showed significant pattern of isolation-by-distance within all diploid species, exceptAe. tauschii (Table 1). All allopolyploid species, exceptAe. cylindrica , contrastingly presented non-significant (Mantel test) or weak (RDA) patterns of isolation by distance, as expected when closely-related individuals expanded across wide geographical space.
Taking the spatial component of both genetic and climatic variation into account with partial Mantel tests and RDA, significant patterns of isolation-by-environment were observed within all diploid species. Allopolyploids, except Ae. triuncialis , contrastingly presented non-significant isolation-by-environment, suggesting a limited impact of climatic drivers in shaping genetic variation in such species. Overall, the distribution of genetic variation within species is consistent with locally adapted diploid progenitors and allopolyploid species having successfully expanded across large distribution ranges during environmental changes.

Discussion

Comparative phylogeography of diploid and allopolyploid wild wheats
Hybridization of diploid wild wheat species produced differential combinations of divergent genomes in allopolyploid species, offering a fruitful comparative system. Plastid and nuclear loci from across species ranges generally offered insights coherent with taxonomy (reviewed in Feldman & Levy 2015) and highlighted multiple origins of allopolyploid species through recurrent hybridization with the same maternal progenitor species (Ae. geniculata , Ae. cylindrica ) or bidirectional hybridization with both progenitor species (Ae. triuncialis ). Phylogenetic insights further supported origins of allopolyploid wild wheats at different times during the late Quaternary, with Ae. crassa and Ae. geniculata being older than Ae. triuncialis and Ae. cylindrica . A conservative interpretation of molecular dating (Doyle & Egan 2010) is that all diploid species and their allopolyploid derivatives went through multiple cycles of range expansion-contraction following Pleistocene climatic oscillations (Hewitt 2000).
Historical changes in distribution ranges have shaped genetic variation within both diploids and allopolyploids, and promoted long-term maintenance of phylogenetic diversity across the Anatolian region connecting the Mediterranean and the Irano-Turanian flora (Zohary 1973; Hegazy & Lovett Doust 2016). Diploid wild wheats are restricted to areas where populations likely survived the ice age (Stewart et al. 2010) and, there, show locally differentiated genetic clusters. As allopolyploids also present most of their genetic clusters there, Anatolia appears as an evolutionary cradle having fostered polyploid speciation (Mohammadin et al . 2017). However, in contrast to diploids, allopolyploid species have expended far beyond Anatolia with genetically homogeneous lineages currently occupying large areas towards the west and/or the east. Such a pattern typically left by range expansion (Excoffier et al. 2009) indicates that allopolyploids have efficiently colonized new territories during the late Pleistocene. Only the ancient Ae. crassa seemingly declined throughout its prior range despite additional rounds of polyploidy and represents an exception among otherwise successful allopolyploid species having established across the whole Mediterranean area. Such comparative phylogeography supports a critical impact of historical demography in shaping variation in diploid and allopolyploid wild wheats under climate changes.
Impact of climatic constraints on the distribution of diploids and allopolyploids
According to neutral expectations, allopolyploid wild wheats combined genetic variation from both their diploid progenitors as fixed heterozygosity across loci. When accounting for existing environments matching the combined tolerances of diploids (i.e. non-convex nichesensu Drake 2015), allopolyploids filled climatic conditions more similar to the combined ranges of their progenitors than could be expected by chance. Although other environmental factors such as biotic interactions may underlie niche novelties not captured here (Wiszet al. 2013; Anderson 2017), the observed pattern supports conservative niche evolution in allopolyploids and contrasts with the significant niche differentiation predicted under their competitive exclusion by diploids (Fowler & Levin 1984).
Diploid wild wheats typically presented patterns of genetic isolation-by-environment suggestive of divergent gene pools adapted to local climatic conditions (Funk et al. 2011), whereas allopolyploids presented weak spatial or environmental patterns rather coherent with their expansion over large areas (Castric & Bernatchez 2003). More generally, divergent evolution of climatic tolerance in allopolyploids was supported here by only few occurrences showing niche novelties at range margins and rarely coincided with noticeable expansion. Only Ae. geniculata significantly spread into locally semi-arid environments of Palestine, where local hybridization withAe. triuncialis (Senerchia et al. 2016) may have promoted adaptive introgression, as shown in other species (Arnold et al.2016). In contrast to repetitive elements showing large genomic changes in allopolyploid wheats (e.g. Levy & Feldman 2004; Senerchia et al. 2014), the here used low-copy loci emphasized long-term neutral divergence and thus established ecotypes. While our data ideally link genetic and environmental changes at a biogeographic scale, further studies should address the interplay between spatial expansion and adaptive radiation at finer scales (Pannell & Fields 2014).
Drivers of allopolyploid expansion
Following range dynamics of the late Pleistocene, allopolyploid wild wheats have spread beyond their sites of origin and, despite their younger age, currently occupy wider geographical space than their diploid progenitors. Genetic and ecological patterns congruently emphasize processes having conserved the additivity of progenitors. The combination of genetic variation from diploid species being differentially adapted to climatic conditions accordingly supported the expansion of allopolyploids (except the contracting Ae. crassa ) across a large range of conditions. Unlike novelties lessening competition from diploid progenitors, conservative evolution of allopolyploids was seemingly favored under historical demographic fluctuations and here supported consistent occupancy of suitable space, whereas diploid species remained restricted to a small fraction of their suitable range.
Being selfing ruderals with diaspores promoting dispersal, all wild wheat species were offered similar opportunities to expand with climate changes and the rise of agriculture (Salamini et al. 2002). The two times higher filling of potential range exhibited by allopolyploids is therefore consistent with an intrinsic advantage conferred by such a genetic system. Fixed heterozygosity in allopolyploids is likely key as it masks recessive alleles and thus reduces expression of the genetic load to support successful expansion of populations through recurrent founder events (Soltis & Soltis 2000; Brochmann et al. 2004). Successful invasion of new territories by allopolyploid species such asCentaurea stoebe (Treier et al. 2009; Mráz et al. 2012) has accordingly been associated with reduced inbreeding depression (Rosche et al. 2017). Wild wheats here suggest that allopolyploidy supports climate-enforced range shifts and calls for additional knowledge on inbreeding depression across distribution ranges of diploid-polyploid systems to understand drivers of their range dynamics. More generally, to what extent niche divergence commonly described in allopolyploids deviates from the here supported genetic and ecological conservatism and may significantly reduce competition from progenitors remains largely unknown. Furthermore, autopolyploids may similarly benefit from increased heterozygosity under climate changes (Parisod et al. 2010), although studies in Chamerion angustifolium rather indicated adaptive evolution of eco-physiological traits and niche divergence (Maherali et al. 2009; Thompson et al. 2014). It is not our intention to here offer comparisons along the continuum of polyploid systems or to explore macro-evolutionary patterns, although we notice that the developed framework can promote generalization with larger sets of species (e.g. Baniaga et al . 2019; Burton et al. 2010; Rice et al. 2019). Fostering integration of historical and ecological constraints, it will shed light on the possible advantages of species resulting from pervasive polyploidy.

Acknowledgments

This work was funded by the Swiss National Science Foundation (31003A-153388). Data analyzed in this paper were generated at the Genetic Diversity Centre, ETH Zurich. We thank J.-C. Walser and T. Marcussen for their help with this multilocus dataset as well as E. Allan, S. Grünig and three anonymous reviewers for their valuable comments on the manuscript.

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