Additivity of allopolyploid climatic niches
The null hypothesis of allopolyploid niche additivity (i.e. the
combination of diploid progenitors’ niches, thereafter the expected
allopolyploid niche) was tested by comparing the observed allopolyploid
niche to the expected niche modeled from combined occurrences of both
its progenitors. The two metrics D and S of niche overlaps between the
observed and expected niches of the allopolyploid species were estimated
as before, with niche similarity test for D. Similarly, observed and
expected niche centroids and breadths were compared using ANOVA and
Tukey tests.
For each allopolyploid species, differences between the observed and the
expected climatic niches were decomposed following the USE framework,
and niche stability S thus corresponds to the fraction of the observed
allopolyploid niche overlapping with the combination of both
progenitors’ niches. The fraction of the observed allopolyploid niche
deviating from the additivity of progenitors (i.e. niche shift) was
decomposed into niche contraction U (i.e. proportion of unoccupied space
as compared to expectations) and niche expansion E (i.e. proportion of
newly occupied space).
Isolation-by-distance and isolation-by-environment in diploid and
allopolyploid species
To what extent demographic vs ecological processes shaped genetic
variation was addressed by signals of genetic isolation-by-distancevs isolation-by-environment within each species (Wang et
al. 2013). Patterns of isolation-by-distance expected under restricted
dispersal of neutral genes were tested by comparing Euclidian geographic
and genetic pairwise distances through Mantel tests with 20,000
permutations in vegan . Genetic distances among individuals were
estimated using Rousset’s a statistics (analogous to
FST/(1-FST)) in SPAGeDi (Hardy &
Vekemans 2002).
Patterns of isolation-by-environment expected when selection favors gene
exchanges among individuals from similar climatic conditions (Wanget al. 2013; Wang & Bradburd 2014) were tested through partial
Mantel tests associating genetic, geographic and climatic distances invegan . Following Legendre & Fortin (2010), correlations of
genetic distances with Euclidian distances from PCs of the common
climatic space while accounting for joint spatial structure were
interpreted as isolation-by-environment. Provided the questioned
performance of such tests (e.g. Legendre et al . 2015),
corresponding patterns were confirmed through multivariate Redundancy
Analysis (RDA) associating individual allelic frequencies to the
geographical coordinates and/or coordinates along PCs of the climatic
space with 20,000 permutations in the R-package adespatial (Drayet al. 2019).
Results
Species phylogeny and genetic additivity of diploids in allopolyploids
Amplicon sequencing of 402 accessions from the eight
diploid-allopolyploid Aegilops species yielded robust allelic
variation at plastid loci (Fig. S2) and at 30 low-copy nuclear genes
(Text S1, Fig. S3). Phylogenies of plastid and nuclear loci among
representative samples resolved species in monophyletic clades and
unambiguously related the different allopolyploids to their respective
maternal x paternal diploid progenitors (Fig. 2A). Consistent with
taxonomy, multi-labeled nuclear species trees accounting for
reticulation related Ae. crassa (DDMM) to ancestors of Ae.
comosa (MM) and other diploids that have hybridized with Ae.
tauschii (DD). Divergent nuclear haplotypes within Ae. crassa(Cr_k2) were related to distinct diploid lineages and included
hexaploids (DDDDMM) of more recent origin (Fig. S3 and S4). Phylogenies
further supported independent origins of multiple lineages within all
allopolyploid species. Nuclear loci indicated an origin of Ae.
geniculata (UUMM) combining ancestors of Ae. umbellulata (UU;
identified as the maternal progenitor by plastid loci) and of Ae.
comosa (MM), with specific samples presenting divergent sequences from
distinct diploid lineages and supporting multiple origins of this
allopolyploid. Multiple origins of Ae. triuncialis (UUCC) were
patent from plastid haplotypes shared with both diploids Ae.
caudata (CC) and Ae. umbellulata (UU) and nuclear loci
congruently supporting such bidirectional hybridization at the origin of
this allopolyploid (Fig. S5). Independent maternal lineages of Ae.
cylindrica (DDCC) were supported by distinct plastid haplotypes ofAe. tauschii (DD) and nuclear loci that identified Ae.
caudata (CC) as the paternal progenitor. Allopolyploids originated at
different times, as indicated by the divergence of their alleles from
corresponding diploids (Fig. S3). Cautious interpretations of molecular
dating show that allopolyploids Ae. crassa andAe. geniculata originated more than 1 Mya, whereas youngerAe. cylindrica and Ae. triuncialis appeared later
(>0.2 Mya) and also went through repeated range
contraction-expansion during the late Pleistocene.
Based on this phylogenetic framework, allopolyploid species (exceptAe. crassa whose ancestral maternal progenitor is elusive) were
consistent with the expected genetic additivity of their diploid
progenitors and presented similar proportions of segregating haplotypes
from each subgenome (Table S2). Patterns of genetic additivity were
further consistent with the relative age of allopolyploid species, with
oldest species such as Ae. geniculata showing 41.9% of
haplotypes from both subgenomes having diverged from diploids, whereas
youngest species such as Ae. cylindrica presented only 3.6% of
derived and mostly (94.3%) conserved haplotypes (Fig. 2B).
Genetic structure within diploid and allopolyploid species
Variation segregating at nuclear loci within species was congruent with
the hypothesis of genetic additivity. Proxies of genetic diversity were
consistently higher in allopolyploids (AR = 2.3–5.9, h = 0.50-0.63 andv = 0.13-0.017) than in their respective progenitor diploids (AR
= 2.78-4.77, h = 0.33-0.50 and v = 0.002-0.007; Table 1).
Allopolyploid species showed not only higher phylogenetic diversity
(v ) than diploids but also the pattern of fixed heterozygosity
(Ho = 0.56-0.66) expected by the strict combination of
divergent diploid loci.
To address phylogeographic processes having shaped genetic variation in
diploids and allopolyploids, the genetic structure across the
distribution range of each species was inferred using STRUCTURE (Fig.
3). Most species presented an optimal number of two or three genetic
clusters and high genetic diversity across Anatolia (Fig. S4). Multiple
spatially-coherent genetic clusters were co-existing within all species
across that region, whereas genetically admixed individuals indicative
of secondary contact between intraspecific lineages were mostly reported
in the Thyracian plain (between the Balkans and Western Anatolia), the
Taurus chain (between Western and Eastern Anatolia) and the Anatolian
Diagonal (separating Eastern Anatolia from the Irano-Turanian region).
In contrast to expectation based on their relative age, all diploid
species presented locally differentiated genetic clusters across their
restricted range, whereas polyploid species showed large areas outside
Anatolia dominated by specific genetic clusters. Such phylogeographic
patterns are consistent with cycles of range contraction-expansion
having shaped coherent hotspots and melting spots of genetic diversity
among wild wheats.
Climatic niches of diploids and allopolyploids
The climatic niche of each Aegilops species was modeled in a
common background based on 20 bioclimatic factors and that summarized
70.69% of the variation along its first two principal components
representative of the Mediterranean-temperate vs.Atlantic-continental climatic gradients (Fig. 4).
Comparative niche modeling addressed the hypothesis that allopolyploids
are the ecological additivity of diploid species. Climatic niches
modeled among the eight species showed specific but consistent D overlap
(Fig. S6 and Table S3) and niche stability S values ranging from 0.39 to
0.93 (Fig. 4). Diploid species presented divergent climatic niche
centroids, with Ae. tauschii and Ae. umbellulata being
more continental than Ae. caudata and Ae. comosa , and
relatively low niche breadths (Table S4). In contrast, all allopolyploid
species, except Ae. crassa , presented relatively broad climatic
niches that were largely coherent with niche additivity of their
progenitors (Fig. 4). The observed niche of allopolyploids presented
higher similarity to the one predicted based on diploids than expected
by chance (Table S3). Alternative insights from bootstraping of observed
niche centroids confirmed this pattern with significant but generally
low differences to the expected niche centroids based on progenitors
(Table S4; Fig. S7). Similarly, independent bioclimatic factors rarely
supported different preferences in allopolyploids as compared to
diploids (Table S4). Alternative approaches were thus largely congruent
and indicate that allopolyploids occupy a combination of climatic ranges
from their diploid progenitors.
Decomposition of the climatic niche of allopolyploids as compared to the
combination of diploid ones confirmed niche conservatism in
allopolyploid wild wheats (Fig. 4). They indeed presented substantial
niche stability (S = 0.72-0.93) and limited evidence of niche
contraction (U = 0.01-0.18). Evidence of niche expansion (E = 0.06-0.19)
indicated that some allopolyploids occupied conditions beyond the
combined range of diploid progenitors toward novel temperate or
continental climates. Corresponding areas were however mostly located
near range margins and were rarely occupied over significant geographic
space (Fig. S8), contrasting with predictions that allopolyploids fill a
new ecological niche. Only Ae. geniculata showed noticeable niche
expansion across aridity gradients of Palestine, suggesting colonization
of novel environments.
The geographical projection of modeled niches was coherent with the
distribution ranges of each species and, as expected under
non-equilibrium, suitable sites were not all occupied (Fig. S9). Large
areas with suitable conditions were available for all species in the
Iberian Peninsula or North Africa, although only allopolyploids densely
occupy such regions. Range filling further assessed how the different
species were distributed across space with tolerable conditions and
showed that diploids effectively occupied only a low fraction of their
suitable areas (0.05 to 0.25) as compared to allopolyploids (0.40 and
0.51; Table 1). Being robust to variable sampling effort (Fig. S10),
such estimates indicate a greater filling of suitable space by
allopolyploids than diploids.