Divergent and narrower climatic niches characterize polyploid species of European primroses in Primula sect. Aleuritia

ORIGINALARTICLE

Divergent and narrower climaticniches characterize polyploid speciesof European primroses in Primula sect.AleuritiaSpyros Theodoridis1,4*, Christophe Randin2,4, Olivier Broennimann3,

Theofania Patsiou2,1,4 and Elena Conti1,4

1Institute of Systematic Botany, University of

Zurich, Zollikerstrasse 107, CH-8008, Zurich,

Switzerland, 2Institute of Botany, University

of Basel, CH-4056, Basel, Switzerland,3Department of Ecology and Evolution,

University of Lausanne, CH-1015, Lausanne,

Switzerland, 4Zurich-Basel Plant Science

Center, CH-8092, Zurich, Switzerland

*Correspondence: Spyros Theodoridis, Institute

of Systematic Botany, University of Zurich,

Zollikerstrasse 107, CH-8008 Zurich,

Switzerland.

E-mail: [email protected]

ABSTRACT

Aim It is hypothesized that the ecological niches of polyploids should be both

distinct and broader than those of diploids – characteristics that might have

allowed the successful colonization of open habitats by polyploids during the

Pleistocene glacial cycles. Here, we test these hypotheses by quantifying and

comparing the ecological niches and niche breadths of a group of European

primroses.

Location Europe.

Methods We gathered georeferenced data of four related species in Primula

sect. Aleuritia at different ploidy levels (diploid, tetraploid, hexaploid and octo-

ploid) and used seven bioclimatic variables to quantify niche overlap between

species by applying a series of univariate and multivariate analyses combined

with modelling techniques. We also employed permutation-based tests to eval-

uate niche similarity between the four species. Niche breadth for each species

was evaluated both in the multivariate environmental space and in geographi-

cal space.

Results The four species differed significantly from each other in mono-

dimensional comparisons of climatological variables and occupied distinct

habitats in the multi-dimensional environmental space. The majority of the

permutation-based tests either indicated that the four species differed signifi-

cantly in their habitat preferences and ecological niches or did not support signif-

icant niche similarity. Furthermore, our results revealed narrower niche breadths

and geographical ranges in species of P. sect. Aleuritia at higher ploidy levels.

Main conclusions The detected ecological differentiation between the four

species of P. sect. Aleuritia at different ploidy levels is consistent with the

hypothesis that polyploids occupy distinct ecological niches that differ from

those of their diploid relative. Contrary to expectations, we find that polyploid

species of P. sect. Aleuritia occupy narrower environmental and geographical

spaces than their diploid relative. These results on the ecological niches of clo-

sely related polyploid and diploid species highlight factors that potentially con-

tribute to the evolution and distribution of polyploid species.

Keywords

Allopolyploidy, Europe, macroecology of polyploidy, niche breadth, niche over-

lap, niche similarity, polyploid speciation, Primulaceae, secondary contact.

INTRODUCTION

Despite intensive studies on speciation for over 150 years

(Darwin, 1859; Mayr, 1947; Levin, 2000), the relationship

between adaptation to different environmental conditions and

species divergence remains poorly understood (Coyne & Orr,

2004). Changes in the ecological attributes of popula-

tions might either precede or follow the onset of reproductive

ª 2013 Blackwell Publishing Ltd http://wileyonlinelibrary.com/journal/jbi 1doi:10.1111/jbi.12085

Journal of Biogeography (J. Biogeogr.) (2013)

isolation (Levin, 2003; Rieseberg & Willis, 2007). In the first

case, divergent natural selection drives adaptation to different

ecological niches, prompting the origin of reproductive barri-

ers between populations or subsets of the same population. In

the second case, however, selection is not the initial mecha-

nism of reproductive isolation and thus speciation (Coyne &

Orr, 2004; Schluter, 2009). Reproductive barriers may also

arise as a result of polyploidization (i.e. genome doubling),

where polyploids are rapidly isolated from their progenitors

via structural chromosomal changes that prompt post-zygotic

(e.g. hybrid inviability/sterility) isolating mechanisms (Grant,

1981). The newly formed polyploids will experience a mating

disadvantage because the rare cytotype will mainly be fertilized

by the majority cytotype, rather than by the fewer, compatible

individuals of the same cytotype: a process called minority-

cytotype exclusion (MCE; Levin, 1975). Therefore, changes in

the ecological and/or reproductive attributes of the polyploids,

including habitat differentiation, pollinator and phenological

switches, and self-fertilization, may be crucial for the establish-

ment of polyploids, for they allow them to avoid MCE and

competition with their progenitors (Petit et al., 1999; Ramsey

& Schemske, 2002). Additionally, it has been proposed that

polyploids should have broader ecological tolerances than their

diploid progenitors, because of their increased genetic and bio-

chemical diversity (Levin, 1983; Otto & Whitton, 2000).

Although the ecological niches of polyploids are expected to be

both distinct from and broader than those of their diploid pro-

genitors, these predictions remain controversial and seem to

be species-specific (see Baack & Stanton, 2005; Sampoux &

Huyghe, 2009; Treier et al., 2009; Ramsey, 2011; Glennon

et al., 2012; McIntyre, 2012; and see te Beest et al., 2012 for a

review).

Niche differentiation and other characteristics frequently

associated with polyploids, including selfing and fixed hetero-

zygosity, have been invoked to explain the successful coloniza-

tion of open habitats by polyploids (Stebbins, 1984;

Brochmann et al., 2004; Rieseberg & Willis, 2007). Uncolon-

ized habitats became available in deglaciated areas during the

Pleistocene glacial cycles. Large-scale climatic oscillations dur-

ing the Pleistocene caused fragmentations, range expansions

and reunions of previously separated populations. Hybridiza-

tion between reconnected populations, accompanied by either

polyploidization or introgression at diploid levels, generated

new races and species, some of which successfully colonized

newly available, ice-free regions. This evolutionary scenario is

known as the ‘secondary contact model’ (Stebbins, 1984).

An ideal system with which to investigate the relationships

between Pleistocene glacial cycles, polyploid speciation, and

changes in ecological preferences is the alpine/arctic Primula

sect. Aleuritia Duby subsect. Aleuritia (Primulaceae; hereafter

P. sect. Aleuritia). Primula sect. Aleuritia includes large varia-

tion of ploidy levels (from diploidy to dodecaploidy) and

breeding systems (from obligatory outcrossing, heterostylous

species, to mainly selfing, homostylous species) and has been

intensively studied from ecological, population genetic, and

phylogenetic perspectives (Bruun, 1932; Hultg�ard, 1990;

Glover & Abbott, 1995; Richards, 2003; Guggisberg et al.,

2006, 2009; de Vos et al., 2012). Speciation via polyploidiza-

tion in P. sect. Aleuritia has been explained within the con-

text of the secondary contact model (Kelso, 1992) and

molecular dating analyses confirmed that this section diversi-

fied during the Pleistocene (J.M. de Vos et al., Institute of

Systematic Botany, Zurich, unpublished data).

One group of four species (Primula farinosa, 2n = 2x = 18;

Primula halleri, 2n = 4x = 36; Primula scotica, 2n = 6x = 54;

Primula scandinavica, 2n = 8x = 72) within P. sect. Aleuritia is

especially suitable for examining the relationship between ploidy

level and ecological preferences, because explicit hypotheses of

evolutionary relationships are available. Phylogenetic analyses

of chloroplast DNA variation (Guggisberg et al., 2006) and

nucleotide polymorphisms in nuclear ribosomal DNA

sequences (Guggisberg et al., 2009) concluded that these four

species are very closely related. More specifically, the analysis of

nucleotide additivity at diagnostic sites of nuclear internal tran-

scribed spacer (ITS) sequences supported the allopolyploid ori-

gin of P. scotica from P. farinosa and P. halleri progenitors

(Guggisberg et al., 2009), corroborating previous hypotheses

based on additivity of chromosome numbers and intermediacy

of various morphological features, including pollen structure

(Hultg�ard, 1990), crossing experiments (Arnold & Richards,

1998), and high levels of intrapopulation allelic variation in

P. scotica revealed by allozyme markers (Glover & Abbott,

1995). Likewise, the analyses of ITS clones (Guggisberg et al.,

2009) suggested an allopolyploid origin of the octoploid P. scan-

dinavica from P. farinosa (diploid) and P. scotica (hexaploid),

supporting hypotheses of previous studies that were based on

high levels of cross-fertility between P. farinosa and P. scandi-

navica (Arnold & Richards, 1998) and the morphological simi-

larities between P. scotica and P. scandinavica (Hultg�ard, 1990,

1993). The tetraploid P. halleri most likely evolved as a poly-

ploid species from the diploid P. farinosa during the glacial

cycles in the Alps (Richards, 2003). The four species are roughly

distributed along a loosely defined latitudinal and elevational

gradient, with P. farinosa having a wide but patchy distribution

throughout Europe, P. halleri occurring in the main mountain

ranges of central eastern Europe, P. scotica restricted to north-

ern Scotland, and P. scandinavica occurring in scattered locali-

ties mainly throughout Norway (Richards, 2003).

Until recently, determining the factors that influence spe-

cies distributions has been hindered by the lack of spatially

explicit environmental data, especially at the continental

scale. However, the current availability of such data, coupled

with the rapid development of species occurrence databases

(e.g. Global Biodiversity Information Facility, GBIF), now

enables us to determine differences between the realized

environmental niches of species or populations and to iden-

tify factors that may limit their dispersal (Peterson et al.,

2011; Wiens, 2011). The realized environmental niche of a

given species is defined as the subset of the abiotic environ-

ment of a species that is actually occupied by the species,

given the accessibility of such environment through dispersal

and the influence of biotic factors (Chase & Leibold, 2003).

Journal of Biogeographyª 2013 Blackwell Publishing Ltd

2

S. Theodoridis et al.

Realized environmental niches are commonly quantified and

compared in either environmental (E)-space using multivari-

ate statistics (e.g. Thuiller et al., 2005; Broennimann et al.,

2012) or in geographical (G)-space using ecological niche

models (ENMs; Warren et al., 2008; Peterson et al., 2011).

The advent of geographic information system (GIS)-based

techniques now allows us to characterize the realized envi-

ronmental niches of related species with both disjunct (i.e.

allopatric) and overlapping (i.e. sympatric) ranges distributed

over large geographical areas and highly heterogeneous envi-

ronments, as in the European P. sect. Aleuritia.

In this study we used environmental factors at the Euro-

pean scale (temperature, precipitation) to define and com-

pare the realized climatic niches of the diploid P. farinosa,

the tetraploid P. halleri, the hexaploid P. scotica and the

octoploid P. scandinavica. We identified individual climatic

variables with low correlation, constructed ENMs for each

species, and used a series of recently developed statistical

approaches to address the following questions.

1. Do the ecological niches of related diploid and polyploid

species differ significantly?

2. Are the ecological niches of polyploid species broader

than those of closely related diploid species?

MATERIALS AND METHODS

Species distribution and occurrence data

The distributions of the four species of Primula sect. Aleuritia

are shown in Fig. 1 (see Appendix S1 in Supporting Informa-

tion for further details). Starting from the general distribu-

tions, an extensive field survey was performed during the

summer of 2011 and georeferenced localities were recorded

for P. farinosa, P. halleri and P. scandinavica. Further geore-

ferenced occurrence records were obtained from global and

national online databases (GBIF, http://www.gbif.org/;

ANTHOS, http://www.anthos.es/; the Swedish Reporting sys-

tem for Vascular Plants and Fungi, http://artportalen.se/

plants/default.asp; the Scottish Natural Heritage, http://

www.snh.gov.uk; and the Data Center of the Swiss Flora,

CRSF/ZDSF, http://www.crsf.ch/) for all four species. Because

data contained in global databases, such as GBIF, may be

prone to error, the validity of GBIF’s sources was checked

during the field survey. The obtained sampling points were

spatially filtered and occurrences closer than 1-km distance

to each other were removed. The final data set consisted of

1849 occurrence points: 1148 for P. farinosa, 42 for P. halleri,

76 for P. scotica, and 583 for P. scandinavica (Fig. 1).

Climatic variables

We first extracted the 19 bioclimatic variables from the

WorldClim data set at 30-s (c. 1 km) spatial resolution (Hij-

mans et al., 2005) for the extent of Europe considered in this

study (Fig. 1). These variables describe temperature and pre-

cipitation characteristics for global land areas. Temperature

and precipitation are considered as major factors in determin-

ing species boundaries, particularly for large-scale biogeo-

graphical patterns (Wiens, 2011). Furthermore, climatic

variables related to temperature and precipitation play a

60°E50°E

40°E

40°E

30°E

30°E

20°E

20°E

10°E

10°E

0°

0°10°W20°W30°W

60°N

60°N

50°N

50°N

40°N

40°N

0

P. farinosa 2xP. halleri 4xP. scotica 6xP. scandinavica 8x

1000 km

Figure 1 Map of Europe showing the distribution (following Tutin et al., 1972; Richards, 2003; national floras; S. Theodoridis, pers.obs.) of the four related species of Primula sect. Aleuritia and occurrence points used for this study. Ploidy number is indicated next to

each species name. Projection: Lambert azimuthal equal area.

Journal of Biogeographyª 2013 Blackwell Publishing Ltd

3

Macroecology of polyploidy

significant role, directly and indirectly, in plant physiological

limitations and adaptation, especially in arctic and alpine envi-

ronments (K€orner, 2003). We examined the 19 variables for

pairwise correlations based on all locations within the study

area (Europe; Fig. 1). After evaluation, we retained seven vari-

ables that showed a high relative contribution to the ENMs

and were not highly correlated (r � 0.7, Fig. 2).

Niche variation and quantification in E-space

Environmental values were sampled for all the locality points

of each species and interspecific divergence was examined.

Pairwise, interspecific comparisons of environmental vari-

ables and niche models (see below) were performed within

the two triads of diploid–polyploid species for which explicit

evidence of relatedness was available: (1) the diploid P. farin-

osa, the teraploid P. halleri and the hexaploid P. scotica; and

(2) the diploid P. farinosa, the hexaploid P. scotica, and the

octoploid P. scandinavica. We used two different tests to

assess differences between species along each climatic variable

independently: the nonparametric Kruskal–Wallis test and

one-way analysis of variance (ANOVA). Kernel density plots

were used to visualize the distribution of each variable with

the surface of the curve rescaled to 1 for each species. To

quantify niche overlap/divergence between the species and

the niche breadth of each species in multidimensional

E-space we used a principal components analysis (PCA)-

based method recently developed by Broennimann et al.

(2012) and implemented by Petitpierre et al. (2012). Niche

overlap between species in each comparison was expressed

by Schoener’s D similarity index (Schoener, 1970; see Broen-

nimann et al., 2012). See Appendix S1 for a more detailed

description of the niche overlap and niche breadth analyses.

Niche variation and quantification in G-space

Species occurrence data and the seven climatic variables

were used for the construction of ENMs for each species with

Maxent 3.3.3e (Phillips et al., 2006). We used 70% of the

occurrence records for each species to calibrate the model and

30% to test it, as is commonly practised (Phillips et al., 2006).

All other parameters were set to default. The performance of

the models was assessed using the area under the receiver oper-

ating characteristic curve (AUC; Hanley & McNeil, 1982).

Niche breadth and niche overlap (D metric) in G-space were

measured using ENMTools (Warren et al., 2010).

Testing for niche similarity

Niche divergence between species might either be the result

of an effective niche differentiation between two species,

meaning that the species occupy different habitats, or simply

80 130 180 230

hal<sco<farsca<sco<far

BIO5Max Temperature of Warmest Month

−160 −120 −80 −40 0

hal<far<scosca<far<sco

BIO6Min Temperature of Coldest Month

150 190 230 270 310

sco<hal<farsco<far<sca

BIO7Temperature Annual Range

−70 −30 10 50 90 130 170

sco<hal<farsco=sca<far

BIO8Mean Temperature of Wettest Quarter

10 20 30 40 50

far=hal=scofar=sco<sca

BIO15Precipitation Seasonality

100 200 300 400 500 600

far<sco<halfar<sco<sca

BIO18Precipitation of Warmest Quarter

100 200 300 400 500 600

far<hal=scofar<sco=sca

BIO19Precipitation of Coldest Quarter

SpeciesP. farinosa 2xP. haller i 4xP. scotica 6xP. scandinavica 8x

Temperature (°Cx10) Precipitation (mm)

Figure 2 Kernel density plots of the seven climatic variables for the four European species of Primula sect. Aleuritia. Differentiation

among species and the results of Kruskal–Wallis tests are indicated in each plot. A lack of significant difference (at the P = 0.05 level) isindicated by an equal sign, while significant differences are indicated by either higher or lower signs.

Journal of Biogeographyª 2013 Blackwell Publishing Ltd

4

S. Theodoridis et al.

reflect differences in the spatial autocorrelation of the

climatic variables between regions. To check for the effect of

spatial autocorrelation, we applied niche similarity tests in

E-space (Broennimann et al., 2012) and G-space (Warren

et al., 2008, 2010). These tests require the definition of a

background area reflected both in E- and G-space. This area

should ideally include suitable habitats for the species and

the way it is delimited might influence the analysis (Warren

et al., 2008; McCormack et al., 2010). To test for the robust-

ness of our results under different methods of delimiting the

background area, we followed two different approaches: one

that uses the output of the ENM of each species, and these

in combination (common background); and a second

approach that uses a 20-km buffer zone around the occur-

rence points of each species. Overlaying of grids, visualiza-

tion of the models and background delimitation were

conducted in ArcGIS 9.3 (ESRI, Redlands, CA). All statistical

analyses were performed in R 2.14.1 (R Development Core

Team, 2011; see Appendix S1 for a detailed description) using

packages ade4 (Dray & Dufour, 2007) and adehabitat

(Calenge, 2006).

RESULTS

Niche differentiation and quantification in univariate

and multivariate E-space

Primula farinosa, P. halleri and P. scotica differ significantly

(P � 0.05) from each other for five out of the seven indi-

vidual climatic variables while P. farinosa, P. scotica and

P. scandinavica differ for four (Fig. 2, see also Appendix S2).

When compared with the three other species, the habitat of

P. farinosa is characterized by the highest values for the max-

imum temperature of the warmest month (BIO5) and mean

temperature of the wettest quarter (BIO8); and by the lowest

values for the precipitation of the warmest quarter (BIO18)

and the precipitation of the coldest quarter (BIO19). Con-

versely, the habitat of P. halleri is characterized by the lowest

maximum temperatures in the warmest month and highest

precipitation of the warmest quarter. Compared with the

two progenitors, the habitat of P. scotica is characterized by

the highest minimum temperature of the coldest month

(BIO6) and the lowest values for temperature annual range

−8

−6

−4

−2

0

2

4

−2 0 2 4 6PC1 (34.89 %)

PC

2 (3

0.84

%)

−8

−6

−4

−2

0

2

4

−2 0 2 4 6PC1 (34.89 %)

PC

2 (3

0.84

%)

PC1 PC2

0.5

1.0

1.5

2.0

2.5

3.0

3.5

●

●

●

●

● ●

●

●

Nic

he b

read

th SpeciesP. farinosa 2x

P. halleri 4x

P. scotica 6x

P. scandinavica 8x

BIO5

BIO6

BIO7 BIO8

BIO18 BIO19

BIO5

BIO6

BIO7 BIO8

BIO18 BIO19

(a) (b)

(c)

BIO15 BIO15

Figure 3 Niche of the four European species of Primula sect. Aleuritia in climatic space. Panels (a) and (b) represent the niche of thetwo triads of species, i.e. P. farinosa, P. halleri, P. scotica and P. farinosa, P. scotica, P. scandinavica, respectively, along the two-first axes

of the principal components analysis (PCA). Colour shading shows the density of the occurrences of the species by cell. The dashedcoloured contour lines illustrate, respectively, the available (background) environment delimited by 20-km buffer zones around the

occurrence points of each species. The correlation circle at the upper right position shows the contribution of the climatic variables onthe two axes of the PCA. (c) Niche breadth of the four species along the two PCA axes.

Journal of Biogeographyª 2013 Blackwell Publishing Ltd

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Macroecology of polyploidy

(BIO7) and mean temperature of the wettest quarter, with

intermediate values for the maximum temperature of the

warmest month and precipitation of the warmest quarter.

When compared with its two proposed progenitors, the hab-

itat of P. scandinavica is characterized by the lowest values

for the maximum temperature of the warmest month and

minimum temperature of the coldest month; and the highest

values for temperature annual range, precipitation seasonality

(BIO15), and precipitation of the warmest quarter.

Principal components analysis identifies two components

that collectively explain 65.73% of the total variation among

the four species (PC1 = 34.89%, PC2 = 30.84%; Fig. 3a,b).

Most of the variables show an almost equal contribution to

PC1 and PC2, with the exception of BIO6 (minimum tem-

perature of coldest month), which is more strongly associ-

ated with PC1. Principal components analysis clearly

separates the four species in the multidimensional E-space

with respect to the density of their occurrences. For the first

triad of species, the PCA plot indicates that P. halleri occupies

a colder and moister climatic niche than that of P. farinosa.

Conversely, P. scotica’s distinct climatic niche is characterized

mainly by higher minimum temperatures and a more

balanced temperature annual range (Fig. 3a). For the triad of

species that includes P. scandinavica, the PCA plot indicates

that this species occupies a colder climatic niche than that of

the proposed progenitors (Fig. 3b). These results are in

accordance with univariate analyses obtained with the Krus-

kal–Wallis and ANOVA tests.

The distribution of the niche breadth values for each spe-

cies along the two PCA axes is illustrated in Fig. 3c. Primula

scandinavica demonstrates a wider climatic niche along PC1,

followed by P. farinosa, P. halleri and P. scotica with a much

narrower climatic niche. Niche breadth along PC2 is equal

between P. farinosa and P. halleri, but narrower for P. scan-

dinavica and P. scotica. Niche overlap is higher between

P. farinosa and P. scandinavica (0.463) and between P. farin-

osa and P. halleri (D = 0.394), but the niches of P. farinosa

versus P. scotica, P. halleri versus P. scotica, and P. scotica

versus P. scandinavica overlap only slightly (D = 0.044,

D = 0.002 and D = 0.048, respectively).

60°N

50°N

40°N

0 1000 km

(a)60°N

50°N

40°N

0

(b)

1000 km

60°N

50°N

40°N

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(c)

1000 km

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(d)

1000 km

0.00

0.02

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0.10

0.12

Nic

he b

read

th

SpeciesP. farinosa 2xP. halleri 4xP. scotica 6xP. scandinavica 8x

(e)

Figure 4 Predicted distributions in Europe for (a) Primula farinosa, (b) P. halleri, (c) P. scotica, and (d) P. scandinavica, and (e) theirniche breadth in geographical space.

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S. Theodoridis et al.

ENMS

Models inferred from occurrence records accurately predict

the observed distribution of all four species (Fig. 4). Addition-

ally, high AUC values (> 0.9 for all models) and low test omis-

sion rates indicate excellent model performance for the four

species. The predicted distribution of P. farinosa is much

broader than those of the three other species and an overlap of

predicted suitable areas between P. farinosa and P. halleri, and

between P. farinosa and P. scandinavica, is observed mainly in

the mountain ranges of central-eastern Europe (Fig. 4; see

Appendix S1 for a detailed description of the results).

Niche breadth was greater for P. farinosa, followed by

P. scandinavica, P. halleri and P. scotica (Fig. 4e). Niche over-

lap was much higher between P. farinosa and P. halleri (0.4);

and between P. farinosa and P. scandinavica (0.218). Niche

overlap was notably lower between P. farinosa and P. scotica;

between P. halleri and P. scotica; and between P. scotica and

P. scandinavica (0.047, 0.021 and 0.011, respectively). These

niche breadth and overlap values are in accordance with

those obtained from the analysis in the E-space (see Fig. 3).

Niche similarity tests

Observed niche overlap values in the multivariate niche space

consistently fall within the 95% confidence limits of the null

distributions under all three different backgrounds and all

comparisons, except one (Table 1; see also Appendix S3).

These results suggest that the ecological differences between

species are not more or less similar than expected due to cli-

matic differentiation, implying that these differences reflect

the environmental heterogeneity between the habitats avail-

able (i.e. background) to the species and they are not neces-

sarily the result of habitat selection.

Results of background similarity tests in G-space are more

complex, but significant niche differentiation is detected in

all three pairwise comparisons P. farinosa–P. scotica, P. farin-

osa–P. scandinavica, and P. scotica–P. scandinavica (observed

overlap lower than 95% of the null distribution; Table 1).

Most of the comparisons between P. farinosa and P. halleri

(four out of six) support a significant niche similarity

between the two species (see Appendix S1 for a detailed

description of the Results).

DISCUSSION

Niche differentiation

The divergence of habitat preferences between diploid and

polyploid species of P. sect. Aleuritia (Table 1; Figs 2 & 3a,b)

mirrors the results of some previous studies, while con-

tradicting the findings of others (for a review, see te Beest

et al., 2012). Using methods similar to those employed in

our analyses, McIntyre (2012) and Glennon et al. (2012)

demonstrated that different cytotypes of Claytonia perfoliata

(Portulacaceae) and Houstonia longifolia (Rubiaceae), respec-

tively, occupy distinct realized environmental niches, while

Allen (2001) provided qualitative evidence that the ecological

niche of the allopolyploid Erythronium quinaultense (Lilia-

ceae) diverged from those of its parents. Conversely, the

niches of distinct cytotypes of Houstonia purpurea did not

differ significantly (Glennon et al., 2012), probably as a

result of either incomplete reproductive isolation between

them or the effects of MCE. Likewise, transplant experiments

provided scarce evidence for ecological differentiation

between spatially segregated diploid and tetraploid popula-

tions of Ranunculus adoneus (Ranunculaceae; Baack & Stan-

ton, 2005). A similar pattern was observed between different

Table 1 Results of niche similarity tests in environmental and geographical space for the four European species of Primula sect.

Aleuritia used in the study. Backgrounds are defined by applying 20-km buffer zones around the occurrence points of each species(20-km buffer), by each species’ ecological niche model set to a baseline threshold that maximizes the sum of sensitivity and specificity

of the test data (ENM), and by combining each species’ predicted background in a common background for the four species of P. sect.Aleuritia (ENM common). Significant results are indicated by ‘less’ for significant divergence or ‘more’ for significant similarity between

the two species under comparison.

Niche overlapBackground used

D 20-km buffer ENM ENM common

Environmental space

P. farinosa–P. halleri 0.393 n.s., n.s. n.s., n.s. n.s., n.s.

P. farinosa–P. scotica 0.044 n.s., n.s. n.s., n.s. n.s., n.s.

P. farinosa–P. scandinavica 0.463 n.s., n.s. n.s., n.s. n.s., n.s.

P. halleri–P. scotica 0.002 n.s., n.s. n.s., more(*) n.s., n.s.

P. scotica–P. scandinavica 0.048 n.s., n.s. n.s., n.s. n.s., n.s.

Geographical space

P. farinosa–P.halleri 0.4 n.s., more (**) more (**), more (**) less (**), more (**)

P. farinosa–P. scotica 0.047 less(**), less(**) less (**), less (**) less (**), less (**)

P. farinosa–P. scandinavica 0.218 less(**), less(**) less(**), less(**) less(**), less(**)

P. halleri–P.scotica 0.021 less (**), n.s. less (*), more (*) less (**), less (**)

P. scotica–P. scandinavica 0.011 less(**), less(**) less(**), less(**) less (**), less (**)

**P � 0.01; *P � 0.05; non-significant (n.s.) P > 0.05.

Journal of Biogeographyª 2013 Blackwell Publishing Ltd

7

Macroecology of polyploidy

cytotypes of Myosotis lamottiana (Boraginaceae; Stepankova,

2001) and Aster amellus (Asteraceae; Mand�akov�a &

M€unzbergov�a, 2006). Sampoux & Huyghe (2009) revealed a

rather limited realized niche differentiation among ploidy

levels in Festuca subg. Festuca (Poaceae) using multivariate

approaches, but pointed out the major role of climatic fac-

tors for taxa with large-scale geographical distributions. The

conflicting results of the aforementioned studies underscore

that ecological differentiation is not a necessary prerequisite

for polyploid establishment, but rather an idiosyncratic qual-

ity of specific polyploid speciation events.

While our results supported significant niche differentiation

in most of the pairwise comparisons, the niches of P. farinosa

and P. halleri were more similar than expected by chance in

G-space (Table 1), a result that might be explained by the

partly sympatric ranges of these two species at a broad spatial

scale. The use of environmental predictors at higher resolu-

tion (see Randin et al., 2009; Lassueur et al., 2006) might be

necessary to identify significant ecological divergence in

G-space. Furthermore, ENMs may not completely serve as a

substitute for experimental approaches, such as transplant

experiments, which can be a powerful tool to investigate the

role of competition and dispersal limitation in determining

species distribution (Wright et al., 2006; Holt, 2009).

In contrast to niche similarity tests in G-space, those in

E-space did not support either significant differentiation or

significant similarity in most of the pairwise comparisons

(Table 1). This discrepancy can be attributed to differences

in the definition of null distributions for the tests between

the two approaches. Simulated niche overlap values in

E-space are generated by random shifts of the entire shape of

the species’ niche over the species’ background area (repre-

sented by the dashed coloured contour lines in Fig. 3a,b),

therefore preserving niche breadth. In contrast, simulated

models in G-space are generated by selecting random points

from the background area of the species, potentially leading

to predicted distributions and niche breadth values larger

than observed, particularly in highly heterogeneous land-

scapes, such as mountain ranges. Even though the tests in

E-space do not allow us to formally draw conclusions about

significant differentiation or similarity, the niches are clearly

distinct (see Fig. 3) and indicate that polyploids are adapted

to different environments.

Pairwise comparisons of uncorrelated climatic variables

indicated that the tetraploid P. halleri and the octoploid

P. scandinavica are characterized by higher tolerance to

colder conditions than their diploid relative, P. farinosa

(Fig. 2). It is believed that polyploidization might enhance

tolerance to environmental stresses (including cold), thus

enabling polyploids to colonize new habitats (Otto & Whit-

ton, 2000; Brochmann et al., 2004). However, the results of

experimental studies are controversial. Liu et al. (2011) dem-

onstrated an increased tolerance to cold, but decreased heat

tolerance of tetraploid versus diploid individuals of Den-

dranthema nankingense (Asteraceae), while reduced cold tol-

erance of tetraploids versus diploids was demonstrated in

Centaurea stoebe (Asteraceae; Broennimann et al., 2007), in

tetraploid Festuca pratensis var. apenni (Poaceae; Tyler et al.,

1978) and in Lolium perenne (Poaceae; Sugiyama, 1998). In

terms of precipitation, all three polyploid primrose species

occupy habitats with higher precipitation levels both in the

warmest and in the coldest quarter of the year than their

diploid progenitor P. farinosa (Figs 2 & 3a,b). Our results

are in contrast with previous investigations showing that

polyploids generally occupy regions with drier climate (e.g.

Treier et al., 2009).

Differently from P. farinosa and P. halleri, the hexaploid

P. scotica occupies sites that are the least exposed to extreme

minimum temperatures and characterized by intermediate

maximum temperatures and the smallest temperature fluctu-

ations during the year (Fig. 2). These results imply that

P. scotica is adapted to a milder, more equable climate, as

that typical of coastal conditions in northern Scotland, than

those preferred by its progenitors, P. farinosa and P. halleri.

Our findings are in accordance with those of Bullard et al.

(1987), which underscored the importance of mild winters

in maintaining population size in this species. In contrast,

the octoploid P. scandinavica prefers sites that are more

exposed to extreme minimum and lower maximum tempera-

tures and characterized by large annual temperature fluctua-

tions compared with its likely progenitors (i.e. P. farinosa

and P. scotica; Fig. 2). These results highlight the adaptation

of P. scandinavica to more severe climatic conditions.

The findings from interspecific comparisons of climatic

variables help to illuminate the origins of the polyploid spe-

cies of P. sect. Aleuritia within the context of Pleistocene

climatic fluctuations. According to previous studies, P. halleri

evolved as a polyploid homostyle from diploid, heterostylous

populations of P. farinosa during glacial cycles in the Alps

(Richards, 2003; Guggisberg et al., 2009). Where the ranges of

the two species overlap, P. halleri occupies sites at notably

higher elevations than those of P. farinosa (S. Theodoridis,

pers. obs.). The increased cold tolerance of P. halleri, espe-

cially its ability to withstand extremely low winter tempera-

tures (Fig. 2), might have allowed it to colonize higher sites,

such as those freed by glacial retreat during Pleistocene inter-

glacials in the Alps, the Carpathian and the Bulgarian ranges,

where its diploid, more cold-sensitive progenitors could not

expand. Moreover, the ability of P. halleri to self (de Vos

et al., 2012) may have played a crucial role in its initial estab-

lishment, by allowing it both to avoid MCE in sympatry and

to cope with the reduced availability of pollinators at higher

elevations. However, the proposed correlation between poly-

ploidy and elevation is not clearly supported, especially in the

flora of the Alps (Stebbins, 1971; te Beest et al., 2012).

Hybridization between the diploid P. farinosa and the tet-

raploid P. halleri, promoted by cycles of habitat fragmenta-

tion and reconnection during the Pleistocene glaciations,

probably gave rise to P. scotica (Hultg�ard, 1990; Guggisberg

et al., 2009). However, the current range of P. scotica does

not overlap with those of the proposed progenitors. It has

been suggested that edaphic conditions (i.e. preference for

Journal of Biogeographyª 2013 Blackwell Publishing Ltd

8

S. Theodoridis et al.

base-rich soils), rather than climatic factors, impose direct

limits to the distribution of P. scotica (Ritchie, 1955). Owing

to the greater availability of such habitats during full- and

late-glacial periods, Ritchie (1955) suggested that P. scotica

occupied a greater area at those times than it does today, but

that subsequent climatic changes, prompting changes in veg-

etation such as the development of the post-glacial tree

cover, resulted in a gradual reduction of the area of base-rich

habitats. Moreover, fossil seeds attributed to P. scotica from

Pleistocene deposits of southern England suggest that the

species once occurred there (Hultg�ard, 1990). Similarly, fos-

sils seeds attributed to P. halleri were recovered from the

same area in southern England (Dovaston, 1956), even

though the tetraploid species presently does not occur in the

British islands, implying a past co-occurrence of the three

species in the same region (southern England). The distinct

niche of P. scotica (Figs 3a & 4), its fixed-heterozygosity

(Glover & Abbott, 1995) and self-compatible reproductive

system (Richards, 2003) might have increased the ability of

the hexaploid species to colonize deglaciated regions and

persist in ice-free glacial refugia from where its lower-ploidy

progenitors were excluded (e.g. higher latitudes).

Based on the secondary contact hypothesis, Hultg�ard (1993)

proposed a periglacial origin of the octoploid P. scandinavica

in Fennoscandia (e.g. unglaciated lowlands of north-western

Europe) from previously isolated populations of the diploid

P. farinosa and the hexaploid P. scotica, with subsequent

migration into Scandinavia. Similarly to P. scotica, P. scandi-

navica is a weak competitor and requires open, base-rich and

disturbed habitats (Olsson et al., 2004), and thus probably had

a wider distribution during late glacial and early post-glacial

periods (Hultg�ard, 1993). Furthermore, Nordal (1987), focus-

ing on the endemic element of the Scandinavian arctic–alpine

flora, proposed that P. scandinavica might not be older than

about 15,000 years, while Paus (1988), based on pollen analy-

sis, demonstrated a northward spread for this species in south-

western Norway since the last deglaciation, approximately

16,000 years ago. The early unglaciated mountains of south-

western Norway probably served as suitable post-glacial colo-

nization areas for P. scandinavica, from where it continued its

expansion to the north.

Changes of breeding system between diploid and polyploid

relatives may also play an important role in elucidating the ori-

gin of polyploids during the Pleistocene climatic oscillations.

In our case study, the diploid P. farinosa is heterostylous, thus

obligately outcrossing, while the polyploid P. halleri, P. scotica

and P. scandinavica are homostylous, thus mainly selfing (de

Vos et al., 2012; Piper et al., 1984). The polyploid species

occur either at the elevational (P. halleri) or latitudinal (P. sco-

tica, P. scandinavica) margins of the diploid P. farinosa

(Fig. 1), suggesting that the mostly autogamous polyploids

might have been more successful at colonizing newly available,

alpine–arctic areas during Pleistocene interglacials, for they are

not dependent on pollinator services that are less reliable in

the fluctuating, extreme weather conditions typical of glacial

margins (Totland, 1994; Bergman et al., 1996). Indeed, the

ability of autogamous, homostylous primroses to outcompete

their allogamous, distylous relatives where pollinators or mates

are scarce has been demonstrated in arctic primulas (Carlson

et al., 2008).

Niche breadth

The increased genetic and biochemical diversity of polyploids

generated the expectation that their ecological tolerances and

geographical ranges should be broader than those of their dip-

loid relatives (Levin, 1983; Otto & Whitton, 2000). However,

evidence for the presumed broader ecological tolerances of

polyploids remains controversial. Martin & Husband (2009),

focusing on 144 North American angiosperm genera and using

two diploid representatives and one polyploid for each genus,

found no significant differences of ecological breadth between

diploids and polyploids. In contrast, McIntyre (2012) showed

that, within the Claytonia perfoliata species complex, polyploid

cytotypes exhibit broader ecological niches when compared

with diploids. Moreover, polyploid species within the genus

Clarkia demonstrate significantly larger range sizes than their

diploid relatives (Lowry & Lester, 2006). In contrast, our

results revealed narrower niche breadths and distributional

ranges in species of P. sect. Aleuritia at higher ploidy levels.

Primula farinosa has been proposed as the ‘ancestor’ of

most extant European taxa (Bruun, 1932; Hultg�ard, 1990;

Guggisberg et al., 2006). The presumably older age of this

species and its higher levels of intraspecific genetic polymor-

phisms (Guggisberg et al., 2006, 2009) may have allowed it

to spread and adapt to a variety of habitats before the origin

of the polyploid species. Once the diploid species was estab-

lished in the suitable habitats, the effect of the minority cyto-

type reproductive disadvantage might have led to a spatial

segregation of the different cytotypes (Baack, 2005), with the

polyploids occupying the fewer available habitats. Further-

more, the mostly selfing reproductive strategy of the homo-

stylous, polyploid P. halleri, P. scotica and P. scandinavica

might result in higher levels of inbreeding and genetic drift

(Lloyd, 1980; Hamrick & Godt, 1996), thus diminishing the

potential of such species to occupy a variety of habitats. In

contrast, particularly in a heterogeneous environment, out-

crossed plants would be more likely to have at least some

members with genetic combinations that are adaptive for a

diversity of niches. This would be the case for heterostylous

species, such as P. farinosa, which are obligate outcrossers, thus

explaining the broader niche and range of fitness. Therefore,

the longer persistence of P. farinosa, coupled with differences

in breeding systems and likely adaptive potential between dip-

loid and polyploid relatives, provides plausible explanations

for its broader ecological niche and distributional range, as

compared to those of P. halleri, P. scotica and P. scandinavica.

CONCLUSIONS

Our results reveal ecological differentiation between the four

species of P. sect. Aleuritia at different ploidy levels and are

Journal of Biogeographyª 2013 Blackwell Publishing Ltd

9

Macroecology of polyploidy

consistent with the hypothesis that polyploids occupy distinct

ecological niches that differ from those of their diploid pro-

genitors, a hypothesized prerequisite for their establishment

in nature (Brochmann et al., 2004). Taken together, our

findings suggest that the ability of polyploids to colonize

marginal habitats freed up by glacial retreat might have

allowed their survival and establishment, providing support

for the role of Pleistocene glaciations in the origin of polyp-

loids (Stebbins, 1984). Furthermore, our study provides one

of the few explicit, quantitative tests of the hypothesis that

the ecological niche of polyploids is broader than that of

diploid relatives, a prediction derived from the genetic and

biochemical characteristics of polyploids. Contrary to expecta-

tions, we found that polyploid species of P. sect. Aleuritia

occupy a narrower E- and G-space than their diploid relative.

Further data on the ages of the species under comparisons,

their genetic diversity and realized mating system should be

considered to fully explain this result. Our findings on the eco-

logical niches of closely related polyploid and diploid species

provide a starting point for future studies that explore the role

of biogeography in polyploid evolution and distribution.

ACKNOWLEDGEMENTS

We thank Per Tor€ang, Camille Madec, Mihai Puscas, Borja

Jim�enez-Alfaro Gonz�alez, Nikolai Nikolov, Todor Karakiev,

Michal Hajek, John Richards, Jurriaan de Vos and Robert

Crawford for providing valuable information on species

localities and help during field surveys; Dan Warren for

providing Perl scripts for data analysis; and the editor and

anonymous referees for significantly improving the manu-

script. This project was financially supported by the Pro-

Doc Research Module in Plant Sciences and Policy by the

Swiss National Science Foundation (grant no. 132471 to

Elena Conti and Christoph Randin) and is affiliated to the

Zurich-Basel Plant Science Center ProDoc PhD Program in

Plant Sciences & Policy, the Claraz Foundation, the Institute

of Systematic Botany of the University of Zurich and was

officially endorsed by DIVERSITAS-bioGENESIS.

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SUPPORTING INFORMATION

Additional Supporting Information may be found in the

online version of this article:

Appendix S1 Detailed description of the methods and

results.

Appendix S2 Results of the statistical tests applied for each

species pair and each climatic variable.

Appendix S3 Histograms of background similarity tests in

environmental and geographical space.

BIOSKETCH

Spyros Theodoridis is a PhD student at the Institute of

Systematic Botany of the University of Zurich in Switzerland.

He is interested in broad-scale ecological and biogeographical

patterns of alpine and arctic plant species in relation to cli-

mate oscillations.

Author contributions: E.C., S.T., C.R. and O.B. conceived

the ideas; S.T. and T.P. collected the data; O.B., S.T. and

C.R. developed the R scripts; S.T. analysed the data; S.T.,

E.C. and C.R. led the writing; and all authors discussed the

ideas and commented on the manuscript.

Editor: Richard Pearson

Journal of Biogeographyª 2013 Blackwell Publishing Ltd

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