Polar Biology (2018) 41:2467–2479

https://doi.org/10.1007/s00300-018-2383-5

ORIGINAL PAPER

Range‑wide pattern of genetic variation in Colobanthus quitensis

Justyna Koc1 · Piotr Androsiuk1 · Katarzyna Joanna Chwedorzewska2,3 · Marely Cuba‑Díaz4 · Ryszard Górecki1 ·
Irena Giełwanowska1

Received: 18 May 2017 / Revised: 18 July 2018 / Accepted: 19 July 2018 / Published online: 26 July 2018
© The Author(s) 2018

Abstract
There is only one species representing Magnoliopsida which is considered as native to the Antarctic, i.e., Antarctic pearlwort
(Colobanthus quitensis). Although it was intensively studied toward the morphophysiological adaptation to extreme environ-
mental conditions of that area, there is still a lack of sufficient data on its genetic variability. Nine C. quitensis populations
from Chile and the Maritime Antarctic were sampled to estimate the pattern of genetic variation in relation to the geographic
distribution of analyzed populations and postglacial history of the species. The retrotransposon-based DNA marker system
used in our studies appeared to be effective in revealing genetic polymorphism between individuals and genetic differentia-
tion among populations. Although the level of polymorphism was low (9.57%), the Analysis of Molecular Variance showed
that overall population differentiation was high (FST = 0.6241) and revealed significant differentiation between the Northern
and Southern Group of populations as well as the population from Conguillio Park. The observed genetic subdivision of
C. quitensis populations was confirmed by Bayesian clustering and results of Principal Coordinates Analysis. The South-
ern Group of populations was characterized by generally higher genetic diversity, which was expressed by the values of
the effective number of alleles, expected heterozygosity and by the distribution of private alleles. Our results suggest that
the species may have survived the Last Glacial Maximum in refugia located both on the South American continent and in
geographically isolated islands of the Maritime Antarctic, i.e., they support the concept of the multiregional origin of C.
quitensis in Antarctica.

Keywords Antarctic pearlwort · Genetic diversity · Genetic structure · Antarctica · iPBS

Introduction

Patterns of population genetic structure revealed in the

Electronic supplementary material The online version of this widely distributed plant species are shaped by the interaction
article (https​://doi.org/10.1007/s0030​0-018-2383-5) contains of many factors, including natural processes such as climate
supplementary material, which is available to authorized users. fluctuations, natural barriers, life history (e.g., breeding sys-
tem and life-form) as well as human impacts (Convey et al.
* Piotr Androsiuk
[email protected] 2014). Also, demographic events occurring during range
contractions and expansions are responsible for modifica-
1
Department of Plant Physiology, Genetics tions of the genome-wide patterns of population genetic
and Biotechnology, Faculty of Biology and Biotechnology, diversity (Hewitt 2000; Excoffier et al. 2009). Genetic drift,
University of Warmia and Mazury in Olsztyn, ul. M.
Oczapowskiego 1A, 10‑719 Olsztyn, Poland founder, and bottleneck effects are expected to be especially
2
intense during range expansion, causing gradients or even
Institute of Biochemistry and Biophysics, Polish Academy
of Sciences, ul. Pawińskiego 5A, 02‑106 Warsaw, Poland
abrupt modulations in allele frequencies, genetic diversity
3
and population structure (Klopfstein et al. 2006; Excoffier
Department of Agronomy, Warsaw University of Life
Sciences-SGGW​, Nowoursynowska 159, 02‑766 Warsaw,
and Ray 2008; François et al. 2008). Expansions can affect
Poland the geographic distribution of both neutral and selectively
4
Univ Concepcion, Escuela Ciencias & Tecnol, Lab Biotecnol
important genetic variation and thus complicate the infer-
& Estudios Ambientales, Campus Los Ángeles, Casilla 341, ences drawn from clines in alleles or phenotypic traits
Juan Antonio Coloma 0201, Los Ángeles, Chile

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2468 Polar Biology (2018) 41:2467–2479

(Vasemagi 2006; Keller et al. 2009) or genetic association et al. 2016; Özer et al. 2016). Colobanthus is often described
mapping (Pritchard et al. 2000; Price et al. 2006). Therefore, as a genus showing southern circum-temperate distribution
a proper understanding of how expansion can shape diversity (e.g., West 1991). 26 species are recognized at present in
and population structure is crucial for both inferring from the genus, with the major diversity, occurring in New Zea-
the demographic history of the species but also for studying land—14 species (Sneddon 1999). It exhibits a Gondwanan
the molecular basis and evolution of the locally adaptive distribution, occurring in South America, the sub-Antarctic
traits in natural populations (Nielsen 2005; Wright and Gaut islands, the Antarctic Peninsula, and the Australasian area
2005). including New Zealand, Australia, and Tasmania (West
There are a number of molecular phyleographic studies 1991). The most recent taxonomic studies in Colobanthus
in which maternally inherited organellar DNA markers were are scatter a descriptions of two new species from Australia:
used for determining the patterns of plant population genetic Colobanthus nivicola (Gray 1976) and Colobanthus curti-
structure and inferring processes such as the number and siae (West 1991) and a revision of Colobanthus quitensis
locations of glacial refugia, past migration routes, and colo- (Kunth) Bartl., which is the most wide-ranging species in the
nization dynamics (Comes and Kadereit 1998). The reason genus, occurring from the Antarctic Peninsula (Greene and
for this approach is that the organellar genomes are usually Greene 1963) north along the southern Andes mountains up
characterized by uniparental inheritance and generally does to scattered locations northward to Mexico (Moore 1970;
not undergo recombination, and therefore haplotypes remain Parnikoza et al. 2011). Antarctic pearlwort—C. quitensis.
mostly unchanged when passed to the next generation. Nev- and Antarctic hairgrass—Deschampsia antarctica Desv.
ertheless, the organellar genome reveals only a single gene are the two flowering plant species considered as native to
genealogy and since the genealogical process is highly vari- the Maritime Antarctic. Due to the broad distribution range,
able among genes and is affected by demographic events or both species undergo various selection forces which shape
unexpected loss of lineages (Knowles and Maddison 2002) both their morphological and genetic variability. However,
such analyses may reveal genealogical processes associated information on the genetic variation of these species is lim-
with single genes only, which are not necessarily character- ited and devoted almost exclusively to D. antarctica (e.g.,
istic for the whole species’ history. Chwedorzewska and Bednarek 2008; van de Wouw et al.
On the contrary, nuclear DNA markers which are bi- 2008; Volkov et al. 2010; Chwedorzewska and Bednarek
parentally inherited allow for recombination, integrating 2011; González et al. 2016). As regards C. quitensis, results
many genealogical processes. Currently SSRs (Simple of the genetic variation studies can be found so far in only a
Sequence Repeats) or SNPs (Single Nucleotide Polymor- few papers, which suffer from limited geographic range or
phisms) are the markers of choice for many phyleographic the low number of populations studied (Lee and Postle 1975;
studies (e.g., DeFaveri et al. 2013; Gao et al. 2013; Faivre- Gianoli et al. 2004; Acuña-Rodríguez et al. 2014). More
Rampant et al. 2016; Foote and Morin 2016), however due recently, two more papers concerning C. quitensis genetics
to the high cost and labor intensity involved in their devel- appeared, but they were focused on selected areas of the
opment, they are available generally for model species and species genomics like the sequence of chloroplast genome
those which are economically important. For genetic studies (Kang et al. 2016) or genome size estimated by flow cytom-
on underutilized crops or plants for which genomic data is etry (Cuba-Díaz et al. 2017b).
limited, several PCR (Polimerase Chain Reaction) marker Our previous studies on the genetic variation of C.
systems are available, varying in complexity, reliability, and quitensis (Androsiuk et al. 2015) encompassed the high-
information generating capacity. est number of populations of the species analyzed so far in
Recently, a versatile method of organism genotyping one study, i.e., eight populations from King George Island
based on the use of transposon sequences has been devel- (Southern Shetland Islands). They represented diversified
oped. The iPBS method (inter Primer Binding Sites) is based habitats of the Maritime Antarctic, which vary consider-
on the virtually universal presence of a tRNA complement ably when microclimatic conditions as well as soil mois-
as a reverse transcriptase primer binding site (PBS) in LTR ture and its nutrient content are considered. The applied
(Long Terminal Repeat) retrotransposons (Kalendar et al. DNA markers (iPBS) revealed low genetic variability and
2010). The iPBS technique has been introduced as a power- moderate population differentiation. Moreover, the pat-
ful DNA fingerprinting technology which can be applied tern of population differentiation corresponds well with
without the need of prior sequence knowledge (Kalendar their geographic location. This study demonstrated the
et al. 2010). Moreover, iPBS markers are highly reproducible usefulness of iPBS markers for genetic diversity studies
due to the length of primers and the high stringency achieved in non-model plant species and confirmed our hypothesis
by the annealing temperature, and they have already found that genetic variation revealed by this technique is influ-
application in clone identification, genetic diversity analyses enced by the abiotic stress and thus shaped in the response
and phylogenetic studies (e.g., Smýkal et al. 2011; Mehmood to local environment conditions.

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Polar Biology (2018) 41:2467–2479 2469

In this study, we used the iPBS markers to assess the was dried after collection and stored at − 20 °C until DNA
range-wide genetic variation of C. quitensis in order to infer extraction in presence of silica gel. The DNA from each
about the population history of the vicariants of C. quitensis individual was extracted using Syngen Plant DNA Mini Kit.
in South America and the Maritime Antarctic. We aimed to The quality of DNA was verified on 1% agarose gel and
address the following questions: (1) Do the iPBS markers visualized by staining with 0.5 μg* mL−1 ethidium bromide,
reveal cryptic genetic structure in C. quitensis? (2) Do the while the amount and purity of DNA samples were assessed
levels of genetic diversity in small, isolated marginal popula- spectrophotometrically.
tions differ from those in other populations? Initially, we screened 20 iPBS primers and their combi-
nations for C. quitensis (Kalendar et al. 2010). Six of the
20 iPBS primers which gave polymorphic, clearly identifi-
Materials and methods able and repeatable bands were selected for further anal-
yses. The PCR was performed with the 6 iPBS primers
DNA extraction and genotyping applied individually or in combination with two primers
(Table 2), according to the procedure described in Andro-
The research material consisted of 174 individuals of C. siuk et al. (2015). The amplification products were analyzed
quitensis representing its natural stands (hereinafter referred by gel electrophoresis in 1.5% agarose gels stained with
to as populations) from South America and the Maritime 0.5 μg* mL−1 ethidium bromide.
Antarctic (South Shetland Islands) (Table 1; Fig. 1). C.
quitensis from South America was collected from wet envi-
ronments of both fresh and brackish water, in river deposits Data analysis
flooded by high tides and less frequent on coastal rocks.
In the high mountain ranges, it was found mainly in bogs All amplification products (bands), that could be reliably
flooded by meltwater runoff. It is usually associated with read were treated as single dominant loci and scored either
other herbaceous species. The pPar and pV populations man- present (1) or absent (0) across genotypes (Online Resources
ifest a high degree of deterioration due to human activity: 1). On the basis of the obtained binary matrix of bands the
the presence of pitches for winter sports in pPar and heavy following genetic parameters were estimated: effective num-
grazing in pV. In case of pPA and pL, the ample influence ber of alleles (NB), the percentage of polymorphic bands
of human activity is observed: both populations are close to (P), Shannon’s Information Index (I), and expected het-
roads, especially the pL population is located very nearby to erozygosity (He). Pairwise FST values among all analyzed
the sites with high industrial activity. In the Antarctic sam- C. quitensis populations were also estimated. The above-
ples were taken from coastal zones, from areas with minor mentioned calculations were performed with GenAlEx 6.5
human influence. Each population was represented by 6–30 software (Peakall and Smouse 2006, 2012), except pairwise
individuals. The number of sampled individuals was lim- FST values which were estimated using Arlequin 3.5 soft-
ited by the size of a given population. The plant material ware (Excoffier et al. 2005).

Table 1  The origin of Colobanthus quitensis populations used in the study

Name Sampling site Coordinates (GPS) Altitude (m No. indi-
a.s.l.) viduals

La Parva (pPar) La Parva hill, Santiago, Chile 33°19′S; 70°16′W 3600 30

Conguillio Park (pC) Conguillio National Park, Araucanía, Chile 38°36′S; 71°36′W 2575 29
La Vega (pV) INIA Kampanaike farm, North of Punta Arenas, Chile 52°41′S; 70°56′W 16 10
Laredo Laredo Sector, North of Punta Arenas, Chile 52°58′S; 70°49′W 158 30
(pL)
La Marisma (pPA) St. María Point, South of Punta Arenas, Chile 53°22′S; 70°58′W 1–3 30
Omora Park (pOm) Omora Park, Puerto Williams, Patagonia, Chile 54°56′S; 67°39′W – 7
Elephant Is. Elephant Is., Antarctica 61°06′S; 55°08′W – 8
(pEl)
Arctowski Arctowski Station, 62°09′S; 58°28′W 23 24
(pA) King George Is., Antarctica
Byers Byers Peninsula, Livingston Is., Antarctica 62°40′S; 60°55′W 40 6
(pBy)

Populations are ordered by latitude of origin

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Fig. 1  Map depicting the loca-

tion of the studied sampling
sites of Colobanthus quiten-
sis: a Geographic location of
the populations from South
America, b contour map of
the Drake passage with c the
enlargement area of South Shet-
land Archipelago with Elephant
Island, King George Island
and Livingston Island. pPar La
Parva; pC Conguillio Park; pV
La Vega; pL Laredo; pPA La
Marisma; pOm Omora Park;
pEl Elephant Is.; pA Arctowski;
pBy Byers

Table 2  The sequence and specification of primers applied in the ver. 2.3.4 software (Pritchard et al. 2000). The model assigns
study individual multilocus genotypes probabilistically to a user-
Primer Sequence Tm (°C) Number of defined number of clusters (K), achieving linkage equilib-
amplified rium within clusters (Pritchard et al. 2000). We conducted
bands 10 replicate runs for each K, ranging from 1 to 9. Each run
iPBS2076 5′-GCT​CCG​ATG​CCA​-3 54a 20b consisted of a burn-in of 500,000 iterations, followed by data
iPBS2085 5′-ATG​CCG​ATA​CCA​-3 50 24 collection over 500,000 iterations. The analysis, with the
iPBS2224 5′-ATC​CTG​GCA​ATG​GAA​ 52 22 implemented admixture model, was conducted without any
CCA​-3 prior information on the original population of each sam-
iPBS2228 5′-CAT​TGG​CTC​TTG​ATA​ 54 20 pled individual. In order to determine the optimal number
CCA​-3′ of clusters (K), an ad hoc statistic ΔK (Evanno et al. 2005)
iPBS2231 5′-ACT​TGG​ATG​CTG​ATA​ 52 27 was used. The ΔK was evaluated in Structure Harvester ver.
CCA​-3′
0.6.94 (Earl and Vonholdt 2012). The second method was a
iPBS2378 5′-GGT​CCT​CAT​CCA​-3′ 53 24
Principal Coordinates Analysis (PCoA), based on the matrix
Total 137
of Euclidean distances between individuals from all ana-
a
Annealing temperature applied in Polymerase Chain Reaction with lyzed populations, performed in PAST software (Hammer
combination of primers iPBS2076 × iPBS2085 et al. 2001).
b
Number of bands scored when primer iPBS2076 was used in combi- Hierarchical Analysis of Molecular Variance (AMOVA;
nation with primer iPBS2085 Excoffier et al. 1992) was carried out using Arlequin 3.5.
For that analysis, the iPBS data were treated as haplotypic,
In order to infer about the geographic pattern of genetic comprising a combination of alleles at one or several loci
variation among C. quitensis populations, two methods (Excoffier et al. 2005). The significance of the fixation indi-
were used. The first approach was a model-based clustering ces was tested using a non-parametric permutation approach
method using the Bayesian analysis with the STRU​CTU​RE (Excoffier et al. 1992).

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The spatial genetic structure was investigated by test- Genetic diversity and differentiation
ing the significance of isolation by distance (IBD) using
a Mantel test with 9999 permutations of the relationship The iPBS markers revealed both the presence of genetic
between the matrix of pairwise FST/(1 − FST) and that of polymorphism between individuals within populations
the logarithm of geographical distance between popula- and genetic variation between populations (Table 4). The
tions (Rousset 1997), using GenAlEx 6.5. number of iPBS bands ranged from 122, for pPar, pC, and
pV populations, to 131 for pPA and pEl populations. The
highest number of polymorphic bands was scored for pPA
population (26.28%) whereas the lowest polymorphism was
Results observed for pV and pBy populations (1.46%). The genetic
variation was assessed with two parameters: Shannon`s
Efficiency of applied PCR primers Information Index and expected heterozygosity, and in both
cases the highest values were observed for pPA population
Our analysis of C. quitensis populations, using six iPBS from La Marisma, whereas the lowest—for pV population
primers/primers combination, yielded 137 clearly distin- (La Vega).
guished bands (Table 2). The highest number, 27 bands, The Bayesian clustering revealed that ΔK, the second-
was revealed by iPBS2231, whereas the lowest number of order rate of change of the likelihood function with respect
bands (20) was scored for iPBS2228 and iPBS2076×2085 to K, has a maximum at K = 3 (Fig. 2). Consequently, we
primers combination. The average number of bands per chose K = 3 as the optimal number of clusters of the upper-
primer was 22.83. Out of all identified loci, 53 (38.68%) most hierarchical level of population structure. The first
were polymorphic. cluster consists of pPA, pOm populations from the south-
Of a total of 137 scored bands, eight (5.84%) were ern edges of the South American continent and pA, pEl,
represented as private bands—i.e., observed only in one pBy populations from the South Shetland Islands, the pPar,
population and absent in the others. Three private bands pV, and pL populations were gathered in the second cluster,
were revealed by each of the following primers: iPBS2085 whereas pC population form solitary, third cluster.
and iPBS2231; whereas primer iPBS2378 revealed two The AMOVA results revealed that most of the described
(Table 3). In this context, pEl (Elephant Island) population genetic variation occurred between populations (59.48%),
appeared as the most abundant in private bands—six of whereas the remaining 40.52% of variation was attributed
them were scored in individuals representing that popula- to the variation among individuals within populations
tion. The remaining two private bands were characteristic (Table 5). With the purpose of investigating how the region
for pPA (La Marisma) population. Moreover, one of the of origin of each population (affiliation to one of the two
bands revealed for pEl population (iPBS2378-12), was clusters revealed by STRU​CTU​RE) influences the partition
characteristic for all individuals representing that sampling of revealed genetic variation of C. quitensis, further analysis
site, and thus may be considered as a potentially diagnostic of variance was performed using the region of origin as an
marker for that population. In the case of the other private
bands, they were scored only for a few (1–5) individuals
Table 4  Population genetic characteristics for analyzed populations
from a given population. of Colobanthus quitensis: effective number of alleles (NB), percentage
of polymorphic bands (P), Shannon’s Information Index (I), expected
heterozygosity (He)

Population NB P (%) I He

Table 3  Private alleles (bands) per locus and their respective frequen- pPar 1.046 6.57 0.039 0.026
cies revealed in studied Colobanthus quitensis populations pC 1.016 2.92 0.016 0.010
Locus Frequency Population pV 1.002 1.46 0.003 0.001
pL 1.032 6.57 0.031 0.020
iPBS2085-3 0.006 Elephant Island (pEl) pPA 1.175 26.28 0.147 0.099
iPBS2085-10 0.03 La Marisma (pPA) pOm 1.110 13.14 0.083 0.059
iPBS2085-15 0.006 La Marisma (pPA) pEl 1.076 13.87 0.069 0.046
iPBS2231-2 0.025 Elephant Island (pEl) pA 1.093 13.87 0.078 0.053
iPBS2231-3 0.006 Elephant Island (pEl) pBy 1.010 1.46 0.009 0.006
iPBS2231-13 0.012 Elephant Island (pEl) Mean over loci and 1.062 9.57 0.053 0.036
iPBS2378-12 0.05 Elephant Island (pEl) populations
iPBS2378-15 0.018 Elephant Island (pEl)
Populations are ordered by latitude of origin

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2472 Polar Biology (2018) 41:2467–2479

Fig. 2  The uppermost hierarchi-

cal level of genetic structure
of Colobanthus quitensis from
Chile and Maritime Antarctic
using STRU​CTU​RE (Pritchard
et al. 2000). The values of
second-order rate of change of
L (K), ΔK, of data between suc-
cessive K values

Table 5  Partitioning of diversity Region Source of variation df Sum of squares Variance Percentage p
found in Colobanthus quitensis compo- of variation
from all analyzed populations nents
using AMOVA
All ­populationsa Among populations 8 536.356 3.4747 59.48 <0.0001
Within populations 165 390.581 2.3672 40.52 –
Three groups distin- Among groups 2 306.222 1.6852 26.76 0.0017
guished by STRU​ Among populations 6 230.134 2.2448 35.65 <0.0001
CTU​REb within groups
Within populations 165 390.581 2.3671 37.59 –
a
FST = 0.5948 when no genetic structure is considered
b
FST = 0.6241 when gene pool subdivision revealed by STRU​CTU​RE is considered

additional factor. The AMOVA revealed that while the most pPA and pOm point on the high level of genetic variation
genetic variation still occurs between populations (35.65%), found within that populations. Individuals from popula-
and among individuals within populations (37.59%), there is tions La Parva (pPar) and Laredo (pL) form two over-
a significant variation (26.76%) among geographical regions lapping clouds which departed from the others along the
(Table 5). Coordinate 1. The most distinct character is shown by
PCoA indicated that 50.89% of variation was explained Conguillio Park (pC) which individuals departed from the
by the first three components (20.86, 19.75, and 10.28%, others along Coordinate 2. The individuals representing La
respectively). Figure 3 illustrates the projection of the Vega population form the smallest and the densest cloud
analyzed populations on the first two axes. The group- of individuals in the center of Fig. 3.
ing revealed by PCoA pointed on the close relationship A Mantel test showed the highly significant correla-
between three populations from Arctowski (pA), Elephant tion between genetic divergence, denoted by pairwise FST/
Island (pEl), and Byers (pBy) representing the South Shet- (1 − FST), and the logarithm of the geographical distances
land Islands. The individuals representing Populations between populations (R 2 = 0.1299, p < 0.016) (Fig. 4).
La Marisma (pPA) and Omora Park (pOm) from South Pairwise FST/(1 − FST) values plotted against the logarithm
America form two the most dispersed clouds, which over- of geographical distances between populations indicated
lap with each other and also with populations from South that the values increased with the distance between them
Shetlands Islands. The high dispersion of individuals from (IBD).

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Fig. 3  Plot of Coordinate 1 versus Coordinate 2 obtained by Principal (filled square); pL Laredo (open circle); pPA La Marisma (filled cir-
Coordinates Analysis (PCoA) based on Euclidean distances between cle); pOm Omora Park (asterisk); pEl Elephant Is.(times); pA Arc-
all individuals from nine Colobanthus quitensis populations. pPar towski (open triangle); pBy Byers (open diamond)
La Parva (plus sign); pC Conguillio Park (open square); pV La Vega

Fig. 4  Analysis of isolation 12.000

by distance. The pairwise FST/
(1 − FST) values are plotted
against the logarithm of the 10.000
geographical distances (km)
between studied populations of 8.000
Colobnathus quitensis
FST/(1-FST)

6.000

R² = 0,1299
4.000 p<0.016

2.000

0.000
0.000 0.500 1.000 1.500 2.000 2.500 3.000 3.500 4.000
log km

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Discussion consist of 4-5 times higher number of individuals, i.e., pC

and pL. Similarly, uneven distribution of polymorphism
Genetic diversity and differentiation of Colobanthus can be found in our previous studies on C. quitensis from
quitensis King George Island, where the level of revealed polymor-
phism was on average 14.25% (Androsiuk et al. 2015).
Colobanthus quitensis geographic range spreads over In the studies of other authors, the average level of poly-
thousands of kilometers from Mexico (17°N) to the Ant- morphism for iPBS markers was much higher and reached
arctic Peninsula (68°S) and from sea level to 4200 m a.s.l. 85.7% for guava accessions (Mehmood et al. 2013), 86.3%
(Moore 1970). Our studies covered the area of Chile and for grape varieties (Guo et al. 2014) or even 97.4% for
the Maritime Antarctic from 33°S to 62°S and spread over Myrica rubra (Chen and Liu 2014). So far the lowest level
3 300 km, which is the distance between the most distant of polymorphism of iPBS markers (4.88%) was reported
pPar and pBy populations. In Chile, C. quitensis can be by Baránek et al. (2012), but their analyses aimed at
found along the Andes, usually in bogs at high altitudes genetic identification of clones of the apricot cultivar.
in the north, but close to sea level in the south (Moore The AMOVA revealed that the genetic variation was
1970; Hoffmann et al. 1998). In the Antarctic, the sites of almost equally partitioned between populations (35.65%)
C. quitensis occurrence are disjunct, situated mainly on and among individuals within studied populations (37.59%);
the Antarctic islands and the Antarctic Peninsula coastal remaining 26.76% was observed between geographical
ice-free areas, often separated from one another by natu- regions with a high fixation index (FST) pointing at a low
ral barriers (open sea, glacial, or mountains) limiting the historical gene flow between them. Previously high genetic
exchange of gene pool (Lewis-Smith 2003). variability between populations (71%) was revealed by
Colobanthus. quitensis became an interesting subject AMOVA in Acuña-Rodríguez et al. (2014), who describe
of morphophysiological investigations aiming to iden- the results of the genetic study of C. quitensis from popula-
tify ecotypic variation (Gianoli et al. 2004), to analyze tions separated by the Drake Passage; the remaining 29%
its reproduction performance (Giełwanowska et al. 2011; of revealed genetic variation was portioned between indi-
Sanhueza et al. 2017) or identify the characteristic endo- viduals. The results obtained by van de Wouw et al. (2008)
phytic fungal communities (Santiago et al. 2012, 2017). for another flowering plant from the Antarctic region, D.
Moreover, as the only representative of Magnoliopsida antarctica, reveal the opposite situation: 74.6% of detected
that grows in the extreme environmental conditions of the genetic variation was portioned among studied regions and
Antarctic, C. quitensis was extensively studied in terms of only 15.1% among populations. It needs to be emphasized
the morphological, physiological, and biochemical basis of that the study area covered an extremely large geographic
adaptation to extremely cold climate, ample thermal oscil- range which included the Indian Ocean, South Georgia,
lations, short vegetation season, high UV-B radiation, and the Falklands, and Antarctic Zone. However, when only
salinity (Bravo et al. 2007; Bascunan-Godoy et al. 2012; the regions within the Antarctic Zone were considered, the
Navarrete-Gallegos et al. 2012; Cuba-Díaz et al. 2017a). In situation changed significantly: 45.6% of the variation was
contrast, the genetic diversity of this species is still poorly found among populations within Antarctic sites and 33.9%
studied and deserves more attention. among Antarctic sites, the rest of variation was portioned
Our data on the genetic variation of C. quitensis showed among individuals within populations. High values of the
that on average 9.57% of the bands revealed by iPBS prim- fixation index also indicated low historical gene flow (van
ers were polymorphic. However, the uneven distribution de Wouw et al. 2008).
of the revealed polymorphism between the analyzed pop- The results of model-based clustering analysis showed
ulation needs to be emphasized here—the value of this that there was a clear gene pool subdivision within the
parameter ranged from 26.28% in pPA to 1.46% in pV nine populations of C. quitensis. According to STRU​
and pBy. The level of polymorphism seems to be associ- CTU​RE, pPA, pOm, pBy, pA, and pEl populations form
ated here with a sample size for individual populations: one cluster (hereinafter called the Southern Group), C.
the highest polymorphism was found in pPA population, quitensis from pL, pV, and pPar form another one (fur-
which was represented by 30 individuals, whereas the low- ther called the Norther Group), whereas population pC
est number of polymorphic loci was characteristic for C. departed from the others and form solitary third clus-
quitensis stands represented by 10 and 6 individuals, pV ter PCoA revealed a similar pattern of population sub-
and pBy respectively. However, our data show also that division, where an individual character of population
even populations represented by a relatively low num- pC was also observed. The unique character of pC
ber of individuals, e.g., pEl (6 plants) or pOm (7 plants), population was previously revealed by Cuba-Díaz et al.
can reveal higher polymorphism than populations which (2017b). The authors, using flow cytometry, estimated
the genome size of three C. quitensis populations and

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found that mountainous populations from pC present a Phytogeography

smaller genome size (0.84 pg), almost half of that found
in the other studied pA and pPA populations originating Postglacial migration and gene flow associated with this
from lower altitudes (1.95 pg), which may suggest that process had major consequences for the population genet-
pA and pPA are tetraploids. This variation in genome ics of both animal and plant species. On the one hand, spe-
size could be attributed to ecographic, adaptive variation cies repeatedly encountered founder events and experienced
to site-specific local environmental conditions, and inter- more or less drastic bottlenecks (Newton et al. 1999; Hewitt
preted as a sign of incipient speciation (Murray 2005). 2000). This could be observed both during retreat and re-
The hypothesis on adaptive character of the genetic vari- immigration, which may lead to a reduction in the number
ation pattern revealed here can be supported by the results of genotypes with increasing distance from glacial refugium
of our previous study on C. quitensis with application of (Hewitt 1996). On the other hand, the merging and expand-
iPBS markers, which proved to be a very helpful tool in ing population from different glacial refugia, which had
assessment of genome rearrangements, associated with evolved genetically isolated, could increase genetic variation
activation of transposable elements arising in a response in zones of secondary contact (Taberlet et al. 1998).
to various abiotic stress characteristic for a given popula- In case of the Antarctic flora, it is difficult to draw con-
tion site (Androsiuk et al. 2015). Undoubtedly, C. quiten- clusions about its evolutionary history since data on con-
sis populations analyzed in the present study also repre- temporary species distributions are not sufficient and this
sent a very wide range of environmental conditions and question requires an approach combining knowledge of
therefore undergo various selecting forces which indepen- Antarctic plant species distribution with studies concerning
dently shape their genetic variation. their genetic diversity and rates of evolution. Unfortunately,
The presence of genetic structure within the analyzed in case of the C. quitensis studies which can provide insights
C. quitensis population was accompanied by an interest- into previous population fragmentation and bottlenecks,
ing geographic pattern of genetic diversity distribution. historical patterns of dispersal and gene flow, relatedness
Although low values of the effective number of alleles between the Antarctic and South American populations are
and expected heterozygosity were found among the popu- still at a very early stage (Gianoli et al. 2004; Acuña-Rod-
lations studied, populations from the Southern Group had ríguez et al. 2014).
generally higher genetic diversity (on average NB = 1.0939 Currently available data for C. quitensis point at two pos-
and He = 0.053) when compared to those from the North- sible scenarios describing its history and dispersal in the
ern Group and population pC all together (on average Antarctic. According to one of them, C. quitensis is, most
NB = 1.024 and He = 0.014) (data not shown). Moreover, likely, a recent postglacial immigrant in the Antarctic and its
the Southern Group was characterized by a higher number presence in this region is estimated on Holocene, which was
of bands scored for each population (on average 127.4 proved by identification of pollen grains and macro-remains
bands per population for the Southern Group and 122.25 of the species in peat deposits dated on 6000 years BP on
for the Northern Group + pC population), among which King George Island, South Shetlands Islands (Birkenmajer
eight private bands can be found which were absent in et al. 1985). In this context, the Antarctic pearlwort is not
C. quitensis from pC population as well as in popula- an exception—the recent origin for much of the flowering
tions from the Northern Group. Six of the revealed private plants is supported by species richness patterns with the
bands were scored in pEl, one of the three populations highest number of species occurring in localities closest
representing a geographically isolated area of the South to neighboring continents and areas where there are more
Shetland Islands. Population pEl was also characterized favorable climatic conditions for establishment. It is cer-
by a higher than average value of H e. The unique char- tainly clear that Antarctica experiences a continuous, but at
acter of pEl was not an exception since another popula- the low level, the input of propagules from the other South-
tion (pA) from this remote geographic area has He which ern Hemisphere continents (Marshall 1996). Some species
was higher than the average value of that parameter for may have potentially overcome natural colonization barriers
the whole Northern Group of C. quitensis populations. of the Antarctic, those transported in a natural manner like
Only C. quitensis from pBy represents a very low level anemochory (Lewis-Smith 1984, 1991, 1993, 2014; Barga-
of genetic diversity, which can be attributed to a limited gli et al. 1996; Marshall 1996; Muñoz et al. 2004), hydro-
number of individuals available for that site. Significantly chory (Coulson et al. 2002), zoochory (Barnes et al. 2004),
higher levels of allelic richness and higher expected het- or marine debris (Barnes et al. 2004; Lewis et al. 2005),
erozygosity for the Maritime Antarctic populations of but recent evidence of this kind of transportation is rather
C. quitensis in comparison to the population from Punta limited (Hughes et al. 2006).
Arenas (South America) was also observed by Acuña- According to the second scenario, C. quitensis could have
Rodríguez et al. (2014). survived in highly isolated refugia south of Drake Passage

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2476 Polar Biology (2018) 41:2467–2479

and inhabited this region from a Mid-Early Cenozoic or even Glacial Maximum (Pecl et al. 2017) have been observed even
Late Cretaceous (Convey and Stevens 2007; Parnikoza et al. in remote Antarctic terrestrial ecosystems (Pertierra et al.
2007, 2011). Moreover, although during Last Glacial Maxi- 2017b). Expansion of the distribution ranges of two native
mum (LGM) in Pleistocene, all low altitude, coastal regions Antarctic flowering plant species has been the most stud-
in the Maritime Antarctic are believed to have been oblit- ied example of a biological response to the recent environ-
erated by expanding glaciers and ice sheets (Larter and Van- mental change in maritime the Antarctic (e.g., Gerighausen
neste 1995) and only re-exposed as ice has retreated over, et al. 2003; Znój et al. 2017; Wódkiewicz et al. 2018). Thus,
at most, the last 10,000 years (Maslen and Convey 2006; with the growing risk of homogenization of Antarctic biota
Pugh and Convey 2008), there are palaeolimnological data (Terauds et al. 2012) the distribution, population size and
for coastal continental Antarctic according to which some diversity of Antarctic native plants became an important
oases have hosted terrestrial life for up to 150,000 years ecological bioindicators of environmental changes.
(Hodgson et al. 2001; Squier et al. 2005), and hence that at
least some of them have a considerably longer continuous Acknowledgements This research was partly supported by the Pol-
ish Ministry of Scientific Research and Higher Education Grant
history of exposure extending beyond the LGM (Peat et al. NN303796240. Samples were also collected on Henryk Arctowski Pol-
2007). Recently even, when propagules from lower latitudes ish Antarctic Station. We would like to thank Editor and three anony-
cross geographical barrier isolating the Antarctic the most mous Reviewers for constructive advice that has improved our paper.
important obstacle are harsh abiotic conditions, diminish-
ing the probability of their establishment. There are a lot of Compliance with ethical standards
species which have ecophysiological features required for
survival in the polar environment including those from the Conflicts of interest Authors declare no conflicts of interest.
Colobanthus genus like e.g., C. lycopodioides, C. subulatus
Open Access This article is distributed under the terms of the Crea-
and, C. lechleri, that partly cover C. quitensis range and tive Commons Attribution 4.0 International License (http://creat​iveco​
tolerate similar edaphic conditions. That support partly fact mmons​.org/licen​ses/by/4.0/), which permits unrestricted use, distribu-
that only records of successful introduction and establish- tion, and reproduction in any medium, provided you give appropriate
ment of species in Maritime Antarctic form lower latitudes credit to the original author(s) and the source, provide a link to the
Creative Commons license, and indicate if changes were made.
(e.g., Chwedorzewska et al. 2015; Pertierra et al. 2017a) are
via human vectors (Lityńska-Zając et al. 2012).
Our molecular data which revealed the presence of evi-
dent genetic structure within analyzed C. quitensis popu-
lations seems to support the concept of the multiregional
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