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.
References
Anderson, R.P. (2017). When and how should biotic interactions be
considered in models of species niches and distributions? J.
Biogeogr. , 44, 8–17.
Archer, F.I., Adams, P.E. & Schneiders, B.B. (2017). strataG: An r
package for manipulating, summarizing and analysing population genetic
data. Mol. Ecol. Resour. , 17, 5–11.
Arnold, B.J., Lahner, B., DaCosta, J.M., Weisman, C.M., Hollister, J.D.,
Salt, D.E., et al. (2016). Borrowed alleles and convergence in
serpentine adaptation. Proc. Natl. Acad. Sci. U. S. A. , 113,
8320–8325.
Baniaga, A.E., Marx, H.E., Arrigo, N. & Barker, M.S. (2019). Polyploid
plants have faster rates of multivariate niche differentiation than
their diploid relatives. Ecol. Lett. ,
https://doi.org/10.1111/ele.13402.
Barve, N., Barve, V., Jiménez-Valverde, A., Lira-Noriega, A., Maher,
S.P., Peterson, A.T., et al. (2011). The crucial role of the
accessible area in ecological niche modeling and species distribution
modeling. Ecol. Model. , 222, 1810–1819.
te Beest, M., Le Roux, J.J., Richardson, D.M., Brysting, A.K., Suda, J.,
Kubesova, M., et al. (2012). The more the better? The role of
polyploidy in facilitating plant invasions. Ann. Bot. , 109,
19–45.
Bernhardt, N., Brassac, J., Kilian, B. & Blattner, F.R. (2017). Dated
tribe-wide whole chloroplast genome phylogeny indicates recurrent
hybridizations within Triticeae. BMC Evol. Biol. , 17, 141.
Blaine Marchant, D., Soltis, D.E. & Soltis, P.S. (2016). Patterns of
abiotic niche shifts in allopolyploids relative to their progenitors.New Phytol. , 212, 708–718.
Brochmann, C., Brysting, A.K., Alsos, I.G., Borgen, L., Grundt, H.H.,
Scheen, A.-C., et al. (2004). Polyploidy in arctic plants.Biol. J. Linn. Soc. , 82, 521–536.
Broennimann, O., Fitzpatrick, M.C., Pearman, P.B., Petitpierre, B.,
Pellissier, L., Yoccoz, N.G., et al. (2012). Measuring ecological
niche overlap from occurrence and spatial environmental data.Glob. Ecol. Biogeogr. , 21, 481–497.
Burton, O.J., Phillips, B.L. & Travis, J.M.J. (2010). Trade-offs and
the evolution of life-histories during range expansion. Ecol.
Lett. , 13, 1210–1220.
Castric, V. & Bernatchez, L. (2003). The rise and fall of isolation by
distance in the anadromous brook charr (Salvelinus fontinalisMitchill). Genetics , 163, 983–996.
Di Cola, V., Broennimann, O., Petitpierre, B., Breiner, F.T., D’Amen,
M., Randin, C., et al. (2017). ecospat: an R package to support
spatial analyses and modeling of species niches and distributions.Ecography , 40, 774–787.
Doyle, J.J. & Egan, A.N. (2010). Dating the origins of polyploidy
events. New Phytol. , 186, 73–85.
Drake, J.M. (2015). Range bagging: a new method for ecological niche
modelling from presence-only data. J. Roy. Soc. Interface , 12,
20150086.
Dray, S., Bauman, D., Blanchet, G., Borcard, D., Clappe, S. & Guenard,
G. (2019). adespatial: Multivariate Multiscale Spatial Analysis. R
package version 0.3-7. https://CRAN.R-project.org/package=adespatial.
R. .
Drummond, A.J., Suchard, M.A., Xie, D. & Rambaut, A. (2012). Bayesian
phylogenetics with BEAUti and the BEAST 1.7. Mol. Biol. Evol. ,
29, 1969–1973.
Duong, T. (2019). ks: Kernel Smoothing. R package version 1.11.4.https://CRAN.R-project.org/package=ks.
Earl, D.A. & vonHoldt, B.M. (2012). STRUCTURE HARVESTER: a website and
program for visualizing STRUCTURE output and implementing the Evanno
method. Conserv. Genet. Resour. , 4, 359–361.
Evanno, G., Regnaut, S. & Goudet, J. (2005). Detecting the number of
clusters of individuals using the software structure: a simulation
study. Mol. Ecol. , 14, 2611–2620.
Excoffier, L., Foll, M. & Petit, R.J. (2009). Genetic consequences of
range expansions. Annu. Rev. Ecol. Evol. Syst. , 40, 481–501.
Feldman, M. & Levy, A.A. (2015). Origin and evolution of wheat and
related Triticeae species. In: Alien introgression in wheat (eds.
Molnár-Láng, M., Ceoloni, C. & Doležel, J.). Springer, Cham, pp.
21–76.
Fowler, N.L. & Levin, D.A. (1984). Ecological constraints on the
establishment of a novel polyploid in competition with its diploid
progenitor. Am. Nat. , 124, 703–711.
Funk, D.J., Egan, S.P. & Nosil, P. (2011). Isolation by adaptation inNeochlamisus leaf beetles: host-related selection promotes
neutral genomic divergence. Mol. Ecol. , 20, 4671–4682.
Glennon, K.L., Ritchie, M.E. & Segraves, K.A. (2014). Evidence for
shared broad-scale climatic niches of diploid and polyploid plants.Ecol. Lett. , 17, 574–582.
Guisan, A., Petitpierre, B., Broennimann, O., Daehler, C. & Kueffer, C.
(2014) Unifying niche shift studies: insights from biological invasions.Trends Ecol. Evol. , 29, 260-269.
Hardy, O.J. & Vekemans, X. (2002). SPAGeDi: a versatile computer
program to analyse spatial genetic structure at the individual or
population levels. Mol. Ecol. Notes , 2, 618–620.
Hegazy, A.K. & Lovett Doust, J. (2016). Plant ecology in the
Middle East . Oxford University Press, Oxford, United Kingdom.
Hewitt G. (2000). The genetic legacy of the Quaternary ice ages.Nature , 405, 907-913.
Huson, D.H. & Bryant, D. (2006). Application of phylogenetic networks
in evolutionary studies. Mol. Biol. Evol. , 23, 254–267.
Huynh, S., Marcussen, T., Felber, F. & Parisod, C. (2019).
Hybridization preceded radiation in diploid wheats. Mol. Phyl.
Evol. , 139, 106554.
Jakobsson, M. & Rosenberg, N.A. (2007). CLUMPP: a cluster matching and
permutation program for dealing with label switching and multimodality
in analysis of population structure. Bioinformatics , 23,
1801–1806.
Karger, D.N., Conrad, O., Böhner, J., Kawohl, T., Kreft, H., Soria-Auza,
R.W., et al. (2017). Climatologies at high resolution for the
earth’s land surface areas. Sci. Data , 4, 170122.
Kilian, B., Mammen, K., Millet, E., Sharma, R., Graner, A., Salamini,
F., et al. (2011). Aegilops. In: Wild Crop Relatives:
Genomic and Breeding Resources (ed. Kole, C.). Springer Berlin,
Heidelberg, pp. 1–76.
Legendre, P. & Fortin, M.-J. (2010). Comparison of the Mantel test and
alternative approaches for detecting complex multivariate relationships
in the spatial analysis of genetic data. Mol. Ecol. Resour. , 10,
831–844.
Legendre, P., Fortin, M.-J. & Borcard, D. (2015). Should the Mantel
test be used in spatial analysis? Meth. Ecol. Evol. , 6,
1239–1247.
Levin, D.A. (1975). Minority cytotype exclusion in local plant
populations. Taxon , 24, 35–43.
Levin, D.A. (2002). The role of chromosomal change in plant
evolution . Oxford University Press, New York.
Levy, A.A. & Feldman, M. (2004). Genetic and epigenetic reprogramming
of the wheat genome upon allopolyploidization. Biol. J. Linn.
Soc. , 82, 607–613.
Li, C., Sun, X., Conover, J.L., Zhang, Z., Wang, J., Wang, X., et
al. (2019). Cytonuclear coevolution following homoploid hybrid
speciation in Aegilops tauschii . Mol. Biol. Evol. , 36,
341–349.
Lyons, K.G., Shapiro, A.M. & Schwartz, M.W. (2010). Distribution and
ecotypic variation of the invasive annual barb goatgrass (Aegilops
triuncialis ) on serpentine soil. Invasive Plant Sci. Manag. , 3,
376–389.
Maherali, H., Walden, A. E. & Husband, B. C. (2009). Genome duplication
and the evolution of physiological responses to water stress. New
Phytol ., 184, 721–731.
Martin, S. L., & Husband, B. C. (2009). Influence of phylogeny and
ploidy on species ranges of North American angiosperms. J. Ecol. ,
97, 913–922.
Meimberg, H., Rice, K.J., Milan, N.F., Njoku, C.C. & McKay, J.K.
(2009). Multiple origins promote the ecological amplitude of
allopolyploid Aegilops (Poaceae). Am. J. Bot. , 96,
1262–1273.
Middleton, C.P., Senerchia, N., Stein, N., Akhunov, E.D., Keller, B.,
Wicker, T., et al. (2014). Sequencing of chloroplast genomes from
wheat, barley, rye and their relatives provides a detailed insight into
the evolution of the Triticeae tribe. PLoS ONE , 9, e85761.
Mohammadin, S., Peterse, K., van de Kerke, S. J., Chatrou, L. W.,
Dönmez, A. A., Mummenhoff, K., et al. (2017). Anatolian origins
and diversification of Aethionema , the sister lineage of the core
Brassicaceae. Am. J. Bot. , 104, 1042–1054.
Mráz, P., Garcia-Jacas, N., Gex-Fabry, E., Susanna, A., Barres, L. &
Müller-Schärer, H. (2012). Allopolyploid origin of highly invasiveCentaurea stoebe s.l. (Asteraceae). Mol. Phylogenet.
Evol. , 62, 612–623.
Nei, M. (1978). Estimation of average heterozygosity and genetic
distance from a small number of individuals. Genetics , 89,
583–590.
Oksanen, J., Blanchet, F.G., Friendly, M., Kindt, R., Legendre, P.,
McGlinn, D., et al. (2019). vegan: Community Ecology
Package. R package version 2.4-4.https://CRAN.R-project.org/package=vegan.
Olson, D.M., Dinerstein, E., Wikramanayake, E.D., Burgess, N.D., Powell,
G.V.N., Underwood, E.C., et al. (2001). Terrestrial ecoregions of
the world: a new map of life on Earth. BioScience , 51, 933–938.
Pannell, J.R. & Fields, P.D. (2014). Evolution in subdivided plant
populations: concepts, recent advances and future directions. New
Phytol. , 201, 417–432.
Parisod, C. & Broennimann, O. (2016). Towards unified hypotheses of the
impact of polyploidy on ecological niches. New Phytol. , 212,
540–542.
Parisod, C., Holderegger, R. & Brochmann, C. (2010). Evolutionary
consequences of autopolyploidy: Research review. New Phytol. ,
186, 5–17.
Petit, R.J., Duminil, J., Fineschi, S., Hampe, A., Salvini, D., &
Vendramin, G. G. (2005). Comparative organization of chloroplast,
mitochondrial and nuclear diversity in plant populations. Mol.
Ecol. , 14, 689–701.
Pritchard, J.K., Stephens, M. & Donnelly, P. (2000). Inference of
population structure using multilocus genotype data. Genetics ,
155, 945–959.
Rambaut, A., Drummond, A.J., Xie, D., Baele, G. & Suchard, M.A. (2018).
Posterior summarization in Bayesian phylogenetics using Tracer 1.7.Syst. Biol. , 67, 901–904.
Ramsey, J. & Ramsey, T.S. (2014). Ecological studies of polyploidy in
the 100 years following its discovery. Philos. Trans. R. Soc. B
Biol. Sci. , 369, 20130352–20130352.
Rice, A., Šmarda, P., Novosolov, M., Drori, M., Glick, L., Sabath, N.,et al. (2019). The global biogeography of polyploid plants.Nat. Ecol. Evol. , 3, 265–273.
Rosche, C., Hensen, I., Mráz, P., Durka, W., Hartmann, M., & Lachmuth,
S. (2017). Invasion success in polyploids: the role of inbreeding in the
contrasting colonization abilities of diploid versus tetraploid
populations of Centaurea stoebe s.l. J. Ecol. , 105,
425–435.
Salamini, F., Ozkan, H., Brandolini, A., Schäfer-Pregl, R. Martin, W.
(2002). Genetics and geography of wild cereal domestication in the near
east. Nat. Rev. Genet. , 3, 429-441.
Schoener, T.W. (1968). The Anolis lizards of Bimini: resource
partitioning in a complex fauna. Ecology , 49, 704–726.
Senerchia, N., Felber, F., North, B., Sarr, A., Guadagnuolo, R. &
Parisod, C. (2016). Differential introgression and reorganization of
retrotransposons in hybrid zones between wild wheats. Mol. Ecol. ,
25, 2518–2528.
Senerchia, N., Felber, F. & Parisod, C. (2014). Contrasting
evolutionary trajectories of multiple retrotransposons following
independent allopolyploidy in wild wheats. New Phytol. , 202,
975–985.
van Slageren, M.W.S.J.M. (1994). Wild wheats: a monograph ofAegilops L. and Amblyopyrum (Jaub. & Spach) Eig (Poaceae):
a revision of all taxa closely related to wheat, excluding wild Triticum
species, with notes on other genera in the tribe Triticcae, especially
Triticum . Wageningen Agricultural University papers, Wageningen.
Soltis, D.E., Visger, C.J., Marchant, D.B. & Soltis, P.S. (2016).
Polyploidy: pitfalls and paths to a paradigm. Am. J. Bot. , 103,
1146–1166.
Soltis, P.S. & Soltis, D.E. (2000). The role of genetic and genomic
attributes in the success of polyploids. Proc. Natl. Acad. Sci. U.
S. A. , 97, 7051–7057.
Stebbins, G. L. (1985). Polyploidy, hybridization, and the invasion of
new habitats. Ann. Miss. Bot. Gard. , 72, 824–832.
Stebbins, G.L. (1971). Chromosomal evolution in higher plants .
University Park Press, London.
Stewart, J.R., Lister, A.M., Barnes, I. & Dalén, L. (2010). Refugia
revisited: individualistic responses of species in space and time.Proc. R. Soc. B Biol. Sci. , 277, 661–671.
Svenning, J. & Skov, F. (2004). Limited filling of the potential range
in European tree species. Ecology Letters , 7, 565-573.
Theodoridis, S., Randin, C., Broennimann, O., Patsiou, T. & Conti, E.
(2013). Divergent and narrower climatic niches characterize polyploid
species of European primroses in Primula sect. Aleuritia .J. Biogeogr. , 40, 1278–1289.
Thompson, K. A., Husband, B. C. & Maherali, H. (2014). Climatic niche
differences between diploid and tetraploid cytotypes of Chamerion
angustifolium (Onagraceae). Am. J. Bot., 101, 1868–1875.
Trabucco, A. & Zomer, R.J. (2010). Global soil water balance geospatial
database. CGIAR Consort. Spat. Inf. Publ. Online Available
CGIAR-CSI GeoPortal Httpwwwcgiar-Csiorg .
Treier, U.A., Broennimann, O., Normand, S., Guisan, A., Schaffner, U.,
Steinger, T., et al. (2009). Shift in cytotype frequency and
niche space in the invasive plant Centaurea maculosa .Ecology , 90, 1366–1377.
Wang, I.J. & Bradburd, G.S. (2014). Isolation by environment.Mol. Ecol. , 23, 5649–5662.
Wang, I.J., Glor, R.E. & Losos, J.B. (2013). Quantifying the roles of
ecology and geography in spatial genetic divergence. Ecol. Lett. ,
16, 175–182.
Warren, D.L., Glor, R.E. & Turelli, M. (2008). Environmental niche
equivalency versus conservatism: quantitative approaches to niche
evolution. Evolution , 62, 2868–2883.
Wisz, M.S., Pottier, J., Kissling, W.D., Pellissier, L., Lenoir, J.,
Damgaard, C.F., et al. (2013). The role of biotic interactions in
shaping distributions and realised assemblages of species: implications
for species distribution modelling. Biol. Rev. , 88, 15–30.
Wood, T.E., Takebayashi, N., Barker, M.S., Mayrose, I., Greenspoon, P.B.
& Rieseberg, L.H. (2009). The frequency of polyploid speciation in
vascular plants. Proc. Natl. Acad. Sci. U. S. A. , 106,
13875–13879.
Zohary, M. (1973). Geobotanical foundations of the Middle East .
Gustav Fisher Verlag, Stuttgart, Swets & Zeitlinger, Amsterdam.