ArticlePDF Available

Abstract and Figures

The quantity of DNA in angiosperms exhibits variation attributed to many external influences, such as environmental factors, geographical features, or stress factors, which exert constant selection pressure on organisms. Since invasive species possess adaptive capabilities to acclimate to novel environmental conditions, ragweed (Ambrosia artemisiifolia L.) was chosen as a subject for investigating their influence on genome size variation. Slovakia has diverse climatic conditions, suitable for testing the hypothesis that air temperature and precipitation, the main limiting factors of ragweed occurrence, would also have an impact on its genome size. Our results using flow cytometry confirmed this hypothesis and also found a significant association with geographical features such as latitude, altitude, and longitude. We can conclude that plants growing in colder environments farther from oceanic influences exhibit smaller DNA amounts, while optimal growth conditions result in a greater variability in genome size, reflecting the diminished effect of selection pressure.
This content is subject to copyright. Terms and conditions apply.
Vol:.(1234567890)
Environmental Science and Pollution Research (2024) 31:33960–33974
https://doi.org/10.1007/s11356-024-33410-x
RESEARCH ARTICLE
Environmental impacts onintraspecific variation inAmbrosia
artemisiifolia genome size inSlovakia, Central Europe
MichalHrabovský1 · SilviaKubalová1· KarolMičieta1· JanaŠčevková1
Received: 8 June 2023 / Accepted: 16 April 2024 / Published online: 2 May 2024
© The Author(s) 2024
Abstract
The quantity of DNA in angiosperms exhibits variation attributed to many external influences, such as environmental factors,
geographical features, or stress factors, which exert constant selection pressure on organisms. Since invasive species possess
adaptive capabilities to acclimate to novel environmental conditions, ragweed (Ambrosia artemisiifolia L.) was chosen as
a subject for investigating their influence on genome size variation. Slovakia has diverse climatic conditions, suitable for
testing the hypothesis that air temperature and precipitation, the main limiting factors of ragweed occurrence, would also
have an impact on its genome size. Our results using flow cytometry confirmed this hypothesis and also found a significant
association with geographical features such as latitude, altitude, and longitude. We can conclude that plants growing in
colder environments farther from oceanic influences exhibit smaller DNA amounts, while optimal growth conditions result
in a greater variability in genome size, reflecting the diminished effect of selection pressure.
Keywords Ragweed· Absolute DNA amount· Flow cytometry· Climatic factors· Geographical variables
Introduction
Genome size, a karyological characteristic denoting the
amount of DNA within a cell (Greilhuber etal. 2005),
exhibits significant variation in land plants and is known
to exert a notable influence on their evolutionary trajec-
tory (Gregory and Hebert 1999; Gregory 2005; Knight
etal. 2005; Lysak etal. 2009; Pellicer etal. 2018). Inter-
specific genome size variation is well known due to many
phylogenetic and taxonomic investigations (e.g., Kron etal.
2007; Kolář etal. 2009, 2013; Marhold etal. 2010; Španiel
etal. 2011; Dirkse etal. 2014; Abbasi-Karin etal. 2022).
In contrast, the intraspecific variation among populations
or individuals was revealed for a small number of species
(e.g., Festuca pallens, Šmarda and Bureš 2006; Šmarda
etal. 2008, 2010, Lythrum salicaria, Kubátová etal. 2008;
Phragmites australis, Meyerson etal. 2016; Pyšek etal.
2020, or Euphrasia arctica, Becher etal. 2021). The plant
genome size can be linked for various species or taxonomic
groups with life cycle and life form (Bennett 1972; Albach
and Greilhuber 2004; Hidalgo etal. 2015; Shao etal. 2021;
Carta etal. 2022), growth form (Ohri 2005; Dušková etal.
2010; Trávníček etal. 2019), climatic factors (Bennett
etal. 1982; Bennett 1987; Wakamiya etal. 1993; Caceres
etal. 1998; Carta and Peruzzi 2016), geographical features
(Levin and Funderburg 1979; Rayburn 1990; Bottini etal.
2000; Knight etal. 2005; Meyerson etal. 2016; Bureš etal.
2024), invasiveness (Bennett etal. 1998; Grotkopp etal.
2004; Kubešová etal. 2010; Pyšek etal. 2020), stress fac-
tors or pollution (Madlung and Comai 2004; Vidic etal.
2009; Meyerson etal. 2020), metabolic resources such as
phosphorus and nitrogen (Hessen etal. 2010; Guignard
etal. 2016), or phylogenetic age (Farah etal. 2018; Hoang
etal. 2020). Despite much evidence of adaptive selection,
genetic drift cannot be excluded from the genome size dis-
tribution (Blommaert 2020).
On a broad scale encompassing both geographical and
environmental factors, correlations between genome size
and these variables have been predominantly observed
in native perennial species (e.g., Wakamiya etal. 1993;
Bottini etal. 2000; Mahdavi and Karimzadeh 2010; Enke
etal. 2011; Yotoko etal. 2011; Carta and Peruzzi 2016;
Responsible Editor: Gangrong Shi
* Michal Hrabovský
michal.hrabovsky@uniba.sk
1 Department ofBotany, Faculty ofNatural Sciences,
Comenius University, Révová 39, 81102Bratislava,
Slovakia
Content courtesy of Springer Nature, terms of use apply. Rights reserved.
33961Environmental Science and Pollution Research (2024) 31:33960–33974
Meyerson etal. 2016; Sayadi etal. 2022). On the other
hand, annual plant species can exhibit more rapid evolu-
tionary adaptation (Franks etal. 2007; Osnato 2022) or
undergo faster natural selection (Larios etal. 2014) in
response to environmental changes than perennials. How-
ever, these evolutionary mechanisms may not be effective
in small populations subject to genetic drift (Andrews
2010), whereas gene flow in large populations can poten-
tially counteract selective pressures (Sork 2015). The alien
invasive species often have smaller genomes than their
non-invasive relatives (Bennett etal. 1998; Grotkopp etal.
2004; Kubešová etal. 2010; Pyšek etal. 2020), and in a
changing world, they can adapt better to changing climatic
conditions than their relatives with large genomes (Grime
1998; Knight and Ackerly 2002; Vidic etal. 2009). They
can evolve rapidly in response to selection pressures in
the new environment (Dlugosch and Parker 2008; Zenni
etal. 2017).
For the study of the adaptation processes on the level of
the genome size, the common ragweed (Ambrosia artemisi-
ifolia L.) belonging to the Asteraceae family is a suitable
model organism, due to its following characteristics. It has
a high spread potential in Europe (Lambdon etal. 2008),
where it was introduced from North America and natural-
ized more than 70–150years ago, depending on the region
(Dessaint etal. 2005; Hrabovský etal. 2016; Skálová etal.
2017; Pinke etal. 2019). Climate change, in conjuction
with anthropogenic influences, can facilitate the spread of
invasive thermophilic ragweed to colder regions (Cunze
etal. 2013; Rasmussen etal. 2017; Skálová etal. 2017;
Mang etal. 2018; Lemke etal. 2021; Liu etal. 2021). As an
annual plant, it produces seeds within one growing season,
4 to 6months after germination (Kazinczi etal. 2008). It
is known that the range of its occurrence is limited by air
temperature and precipitation (Gentili etal. 2019); how-
ever, the species has demonstrated the ability to adapt in
mountainous regions recently (Kochjarová etal. 2023). The
large invasive ragweed populations exhibit high levels of
genetic diversity attributable to complete outcrossing (Gen-
ton etal. 2005; Chun etal. 2010; Meyer etal. 2017), while
the related perennial Ambrosia psilostachya shows clonal-
ity and low genetic diversity (Karrer etal. 2023). Some
intraspecific variation in ragweed genome size is docu-
mented as its DNA amount varies from 2.08 to 2.27pg/2C
(Kubešová etal. 2010; Bai etal. 2012; Battlay etal. 2023).
However, this variability has not been linked to environ-
mental factors that are known to affect genome size selec-
tion (Knight and Ackerly 2002; Knight etal. 2005; Bureš
etal. 2024).
The European continent is characterized by diverse eco-
logical conditions and is therefore divided into a number of
different environmental zones (Metzger etal. 2005). The
territory of Slovakia extends into two zones, the lowland
Pannonian and mountain Carpathian, thus providing the
opportunity to investigate the effect of altitude, tempera-
ture, and precipitation gradients on the genome size vari-
ation. Ragweed was only found in the warm Pannonian
flora region until 2000 (Jehlík 1998). After 2000, moun-
tainous areas showed an increase in ragweed occurrence
(Hrabovský and Mičieta 2018; Kochjarová etal. 2023).
We assume, that the genome size of annual alien spe-
cies may exhibit variation within a limited geographical
region, where diverse environmental factors can act upon
naturalized populations over a specific period. This study
endeavors to address the following inquiries: (i) To what
extent does intraspecific variation exist in the DNA content
of naturalized alien species? (ii) Which environmental fac-
tors are associated with genome size variability? (iii) Is there
evidence to suggest that environmental factors contribute
to variability in genome size during or after naturalization,
possibly as a result of climate change?
Materials andmethods
Field sampling
Plant material was collected from 37 naturalized popula-
tions of invasive annual species Ambrosia artemisiifolia
from southern Slovakia in the northernmost regions of the
Pannonian Basin and adjacent Carpathian area, where the
populations have been expanding since the late twentieth
century (Jehlík 1998) (Fig.1). Populations of the rag-
weed were selected accidentally from the Vienna Basin,
Danubian Lowland, Western Carpathians, and the Eastern
Slovak Lowland. The abundance of common ragweed in
the examined area influenced the choice of populations,
as more populations were selected from the west of the
study area, where ragweed is widespread (Hrabovský etal.
2016). The populations can be classified as Carpathian
or Pannonian based on the phytogeographic division of
the area (Futák 1984). Anthropogenic habitats, includ-
ing roadsides, arable land, railways, and ruderal habitats,
were among the diverse habitats sampled. A distal leaf of
at least five individuals was collected from each popula-
tion. Planar-colline levels at the interface of the Pannon-
ian Basin and the Western Carpathians exhibit distinct
variations in elevations, temperatures, and precipitation.
The majority of the examined region exhibits an elevation
range of 110 to 330m a. s. l., with localized exceptions
where altitude may fall below 100m or exceed 800m.
According to WorldClim datasets (Fick and Hijmans
2017), the mean annual temperature in the region fluctu-
ates between 10 and 12.2°C, while the average annual
precipitation totals for the previous decade are reported
to range from 600 to 700mm.
Content courtesy of Springer Nature, terms of use apply. Rights reserved.
33962 Environmental Science and Pollution Research (2024) 31:33960–33974
Genome size estimation
To estimate the 2C value, the methodical recommenda-
tions of Sliwinska etal. (2022) were followed, except for
the direct analysis of fresh material. Fresh leaves from
flowering plants were dried in silica gel. Plant material
was collected during the 1-week period in August–Sep-
tember 2022. Leaf tissues were analyzed sequentially
with an established standard, and the ratios of their G0/1
peak positions were recorded. As the established stand-
ard for the samples, leaves of Bellis perennis were cho-
sen (2C = 3.159pg; Temsch etal. 2022). The nuclei
were isolated using a commercial reagent kit, Cystain PI
OxProtect (Sysmex, United Kingdom), from a sample and
co-chopped standard, and stained with propidium iodide
(PI). The analyses were performed using a Partec CyFlow
Ploidy Analyzer, equipped with a green laser (532nm).
At least 5000 nuclei were analyzed from each sample at
least three times on different days. Samples that exhib-
ited a coefficient of variation (CV) greater than 3% were
excluded from the analysis, and additional samples were
analyzed to ensure that data from at least five individuals
per population were obtained (TableS1).
This study was preceded by verification of intrapopulation
variability in three populations, where 25 2-week-old seed-
lings grown under the same conditions were analyzed from
fresh leaves using the same procedure as above (TableS2,
Fig.S1). We also estimated the genome size of the first rag-
weed individuals introduced to the study area (1949–1956)
and later occuring populations (1957–1984) from herbarium
specimens. According to Viruel etal. (2019), it is difficult
to obtain results from old specimens, but it is possible to
estimate a DNA amount even from 100-year-old speci-
mens (Michalová etal. 2024). A part of a young green leaf
(0.5 × 0.5cm) was macerated for 30min in a Cystain PI
OxProtect nuclei extract solution. Then it was co-chopped
with the standard and stained with PI. The quality of the her-
barium item determines the degree of success. The samples
with a CV greater than 7% were not included in this study.
The conformity of the results with prior estimations,
which were based on the standards calibrated from Oryza
sativa ssp. japonica cv. Nipponbare with an outdated value
of 2C = 0.910pg/2C, could be attained by recalculating the
published data based on the current value of Nipponbare
rice, which is 2C = 0.778pg/2C as stated by Temsch etal.
(2022).
Climatic variables
For each population at each location, the following envi-
ronmental factors were obtained from WorldClim (Fick and
Hijmans 2017) using GIS software (QGIS 3.22.3): mean
annual air temperature (Tmean), mean May–October air tem-
perature relating to the ragweed vegetation season (Tmean
May–October), mean December March air temperature
relating to the dormancy period (Tmean December–March),
annual precipitation totals (P), seasonal May October pre-
cipitation totals (P May–October), and December March
precipitation totals (P December–March). These factors
were extracted for both the historical period of ragweed nat-
uralization in the study area (1970 2000) and the current
period (2020–2021), air temperature in °C, and precipitation
totals in mm. The air temperature and precipitation are the
most notable indicators of continentality in the study area
(Labudová etal. 2013; Vilček etal. 2016). The influence
of continentality on ragweed genome size was presented
through the Tmean and P May–October of the current period.
Data analysis
All data analyses were performed in the statistical soft-
ware R (version 4.2.2). The individuals were experimen-
tally divided into two groups: group 1 with a DNA amount
(2C) smaller than 2.1pg and group 2 with a DNA amount
larger than 2.1pg (Fig.2). Applying the ctree() function
of the “party” package (Hothorn etal. 2006), a non-par-
ametric decision conditional inference tree was created to
find the most important environmental factors affecting the
Fig. 1 The study area with selected populations for measurement.
First-occurrence records were measured from herbarium specimens.
After measurements, the populations with a median genome size
smaller than 2.1pg/2C were labelled as group 1, and the other pop-
ulations with a genome size larger than 2.1pg/2C were labelled as
group 2
Content courtesy of Springer Nature, terms of use apply. Rights reserved.
33963Environmental Science and Pollution Research (2024) 31:33960–33974
ragweed genome size groups distribution in the study area.
As environmental factors, geographical and meteorological
variables such as altitude, latitude, longitude, anthropogenic
habitats, and historical and current abovementioned climatic
variables were tested.
Additionally, a linear mixed-effects model with individu-
als, populations, and measurement dates handled as random
factors was conducted to test the impact of the abovemen-
tioned environmental factors on ragweed genome size dis-
tribution in the study area. The analysis was performed for
all genome size measurements, but also without outliers
(2C < 1.85pg and 2C > 2.4pg), using the “nlme” package
(Pinheiro and Bates 2000) with the lme() function for the
linear mixed-effects model. The effects of the previous fac-
tors on the DNA amount distribution in the studied area
were also assessed using the cca() function of the “vegan”
package (Oksanen 2012) for the constrained correspond-
ence analysis (CCA). The differences in genome size in
different anthropogenic habitats were assessed using the
Kruskal–Wallis test, which was applied following Levene’s
test for homogeneity using the Levene’s test() function of
“cor” package (Guo 2020). Dunn’s test with Bonferroni
correction was performed as a non-parametric post-hoc test
using the Dunn’s test() function of “FSA” package (Ogle
2017).
The distribution of both genome size groups in the
potential ragweed area (M. Hrabovský, unpublished data)
was modelled using species distribution modelling (SDM).
SDM is used to predict the distribution of species in an area
based on environmental predictors (Farashi and Alizadeh-
Noughani 2023). The ideal (presences) and unfavorable
environmental conditions (pseudo-absences) are essential to
determine for the modelling (Wang etal. 2023). For group
1 evaluation, environmental factors associated with group 2
were substituted for pseudo-absences, and vice versa. Mod-
els and predictions were calculated by the sdm() and ensem-
ble() functions of the “sdm” package (Naimi and Araújo
2016) using the support vector machines (SVM) algorithm.
The models were evaluated with cross-validation (tenfold),
and the obtained true skill statistic (TSS) and area under the
relative operating characteristic curve (AUC) values were
higher than 0.7.
Results
DNA amount ofragweed
The mean value of the absolute DNA amount (2C) esti-
mated from 185 individuals was 2.11pg. The range of the
DNA amount (2C) was spanning from 1.819 to 2.516pg.
The exact data for each population are depicted in Table1
and TableS1. The 16 populations belong mostly to group 1
with a smaller genome size, and the 21 populations belong
mostly to group 2 with a larger DNA amount, but some
populations are mixed (Fig.2). The analysis of herbarium
specimens suggests that group 1 with a smaller genome
was introduced to the territory of Slovakia first (Fig.S2).
DNA amount andenvironmental variables
After dividing the populations into groups, 33% of Pannon-
ian populations belong to group 1 and 67% to group 2. On
the contrary, 86% of Carpathian populations are classified
as group 1, whereas only 14% are in group 2. According
to the conditional inference tree (Fig.3), the main factor
affecting the distribution of both groups in the studied area
is latitude and mean annual air temperature in the historical
period (1970 2000). Group 1 occurs mainly in areas with
Fig. 2 Interpopulation variability of Ambrosia artemisiifolia genome
size in the study area. Density plots represent the variability in every
population from Table1. The populations with a smaller genome size
(2C < 2.1 pg) belong to group 1, and the populations with a larger
genome size (2C > 2.1 pg) belong to group 2. Some populations are
mixed (e.g., FE1, OB1)
Content courtesy of Springer Nature, terms of use apply. Rights reserved.
33964 Environmental Science and Pollution Research (2024) 31:33960–33974
a latitude greater than 48.447 N (p < 0.001) and where the
mean annual air temperature was below 9.567°C (p < 0.001)
during the time of ragweed introduction (Fig.S3). This
redistribution of groups was also captured by SDM (Fig.S4).
Results of the linear mixed-effects model (Table2)
indicated that there was a significant (p < 0.001) positive
association between the estimated DNA amounts of group
1 and the current period mean annual air temperature
(beta = 0.017, SE = 0.003, R2 marginal = 0.274), the mean
May–October air temperature (beta = 0.015, SE = 0.003,
R2 marginal = 0.265), and the mean December March air
temperature (beta = 0.021, SE = 0.004, R2 marginal = 0.290),
and a significant negative association with the current period
annual precipitation totals (beta = − 0.0002, SE = 0.0004,
R2 marginal = 0.173), and the seasonal May October
precipitation totals (beta = − 0.0003, SE = 0.0001, R2 mar-
ginal = 0.193). Using historical meteorological data instead
of the current period climate for model calculation results
Table 1 The absolute DNA
amount of naturalized ragweed
populations in the northern
Pannonian Basin
* Mean value of absolute DNA amount averaged per population; Pop, population code; Hab, habitat (AL
arable land, RH ruderal habitats, RS roadsides, RW railways); Group—prevalent genome size group
(1—2C < 2.1 pg, 2—2C > 2.1 pg); Lat, latitude; Long, longitude; Alt, altitude; CV, coefficient of varia-
tionof population
Pop Hab Group Lat Long Alt [m. a. s. l.] 2C* [pg] (min–max) CV [%]
VT1 RH 2 47.75079 18.31760 105.3 2.247 (2.192–2.289) 1.5
VK1 RW 1 48.55485 22.10377 107.3 2.07 (1.859–2.205) 5.7
PA1 RS 2 47.73917 18.31495 108 2.208 (2.154–2.25) 1.4
MH1 AL 2 47.85146 18.68839 111 2.242 (2.159–2.508) 5.9
VM1 AL 2 47.8478 17.78612 112.4 2.228 (2.197–2.291) 1.6
NZ1 RS 2 47.96135 18.18768 115.3 2.162 (2.107–2.203) 1.5
JA1 RS 2 48.12879 18.02957 117.2 2.201 (2.06–2.285) 3.6
OB1 AL 2 47.77706 18.65024 117.4 2.133 (2.016–2.218) 3.7
NV1 AL 1 48.63933 21.685 119.1 2.02 (1.977–2.059) 1.5
GA1 RH 2 48.18709 17.71218 119.3 2.256 (2.197–2.321) 1.8
FE1 AL 1 48.76618 22.08028 119.6 2.069 (1.952–2.243) 6.0
ST1 RW 1 47.8021 18.68476 120.8 1.998 (1.96–2.047) 1.7
GB1 AL 2 47.86129 18.49871 121.5 2.277 (2.249–2.294) 0.7
BA3 RH 2 48.10522 17.10971 133 2.362 (2.151–2.361) 3.8
NR1 RH 2 48.28626 18.09509 136.4 2.155 (2.113–2.228) 1.9
SH1 RS 2 48.08334 18.94056 139.8 2.196 (2.151–2.244) 1.9
VN1 RS 1 48.66862 22.25716 142.8 1.966 (1.819–2.166) 6.7
KP1 AL 2 48.29594 17.44926 151.8 2.202 (2.157–2.26) 1.6
CC1 RS 2 48.23428 18.04753 152 2.158 (2.141–2.176) 0.5
VR1 AL 2 48.23695 18.33368 152.7 2.258 (2.142–2.516) 5.9
KT1 RS 2 48.6582 17.04409 157 2.146 (2.117–2.164) 0.7
BA1 RH 2 48.26141 16.96355 162 2.143 (2.126–2.16) 0.5
PK1 RS 1 48.29365 17.29239 167.5 1.979 (1.931–2.036) 2.1
BO1 RS 1 48.45007 17.50928 170.1 2.017 (1.969–2.048) 1.3
TM1 RS 1 48.34993 18.3644 170.6 2.024 (1.941–2.116) 3.2
BA2 RS 1 48.17538 16.99063 182.4 2.097 (2.029–2.17) 2.2
LC1 RS 2 48.34716 19.65759 187.1 2.234 (2.168–2.332) 3.1
MA1 RS 2 48.44702 17.07451 189.2 2.255 (2.22–2.283) 1.0
KE1 RS 1 48.68977 21.28078 195.9 1.965 (1.881–2.012) 2.4
ZC1 RW 2 48.48316 18.72734 217.8 2.145 (2.115–2.187) 1.3
HR1 RS 1 48.46828 19.95121 239.4 1.959 (1.884–2.082) 3.4
ZH1 RH 1 48.57629 18.83322 240.5 1.971 (1.923–2.052) 2.2
TC1 RS 2 48.35703 18.52149 263.5 2.159 (2.102–2.21) 1.8
SY1 RS 1 48.83974 19.11476 494.6 2.003 (1.956–2.051) 1.9
LI1 RS 1 49.38852 20.63251 775.3 1.911 (1.779–1.95) 2.0
VY1 RS 1 49.15063 20.25393 982 1.88 (1.835–1.91) 1.8
CE1 RS 1 48.90538 19.73179 1206.8 1.877 (1.824–1.926) 2.5
Content courtesy of Springer Nature, terms of use apply. Rights reserved.
33965Environmental Science and Pollution Research (2024) 31:33960–33974
in stronger and statistically significant connections (higher
marginal R2 and t values) between the DNA amount and
the aforementioned environmental parameters. A significant
negative association between geographical variables (alti-
tude, latitude, and longitude) and the absolute DNA amount
was also found by the linear mixed-effects models for group
1 (Table2). The same regression trends (except longitude)
were maintained for group 2, but with a low R2 (Table2). In
addition, a linear-mixed effects model was computed for the
following scenarios: plants were not divided into two groups
(TableS3), outliers were excluded (TableS4), and popula-
tions (TableS5) or measurement dates (TableS6) were used
as random factors. No fundamental differences between the
results of previous models were observed; therefore, a spa-
tio-temporal bias resulting from different habitat selection
or measurement dates can be excludedasthe reason for the
observed trends. CCA analysis yields similar results as the
linear mixed-effects models. The first ordination axis CCA1
corresponds to the altitude and the seasonal May October
precipitation totals, while the second ordination axis CCA2
correlates to longitude (Fig.4).
DNA amount andhabitats
Based on Kruskal–Wallis test, the genome size seems to
vary with selected types of anthropogenic biotopes such
as roadsides, arable land, railways, or ruderal habitats
(χ2 = 26.6, p < 0.001). A post-hoc test shows no differences
between arable land and ruderal habitats (adjusted p = 1) and
roadsides and railways (adjusted p = 1). However, these cou-
ples (Fig.5) differ significantly from one another (adjusted
p < 0.001).
Discussion
Intraspecific variation ofAmbrosia artemisiifolia
genome size
It is a controversial subject, whether there is any diversity in
genome size below the level of a species (Greilhuber 1998).
Despite the doubts, intraspecific variability of genome size
was confirmed in Asteraceae family (Suda etal. 2007; Slovák
etal. 2009; Dirkse etal. 2014) and in other flowering plants
(e.g., Poaceae, Šmarda and Bureš 2006; Šmarda etal. 2008;
Ranunculaceae, Cires etal. 2010; Amaryllidaceae, Ducho-
slav etal. 2013; Anacardiaceae, Aliyu 2014; Caprifoliaceae,
Frajman etal. 2015; Caryophyllaceae, Terlević etal. 2022).
Ragweed’s intraspecific variability has not yet been inves-
tigated. The known genome size values of the ragweed
were determined by examining specimens collected from
both its native North American area–2.08pg/2C (Bai etal.
2012) and non-native Europe–2.12pg/2C (Kubešová etal.
2010) or 2.18 to 2.27pg/2C (Battlay etal. 2023). We esti-
mated approximately the same genome size value averaged
from 185 ragweed individuals (2.11 ± 0.3pg/2C) as it was
Fig. 3 The conditional infer-
ence showing the main factors
(latitude and mean annual air
temperature in the historical
period) affecting the distribu-
tion of ragweed genome size in
the study area; yellow—group
1 (2C < 2.1pg), red—group 2
(2C > 2.1pg)
Content courtesy of Springer Nature, terms of use apply. Rights reserved.
33966 Environmental Science and Pollution Research (2024) 31:33960–33974
Table 2 Linear mixed-effects model coefficients and statistics for two different DNA amount groups of ragweed, and meteorological and geographical variables as fixed effects, and an indi-
vidual plant (i.e., results from repeated measurements of the same plant) as a random effects
* p < 0.05, **p < 0.01, ***p < 0.001
NS, non-significant; Tmean, mean air temperature; P, total precipitation; black square, historical period (1970–2000), white square, current period (2020–2021); SE, standard error, R2c, condi-
tional R2 for random and fixed effects, R2m, marginal R2 for fixed effects
Group 1 (2C < 2.1pg) Group 2 (2C > 2.1pg)
Variables (fixed effects) DNA amount
(intercept)
beta SE t
(p value) df = 76 R2c R2mDNA amount
(intercept)
beta SE t
(p value) df = 108 R2c R2m
Tmean 1.808 0.0198 0.003 6.06*** 0.991 0.323 1.897 0.0305 0.0135 2.25* 0.990 0.044
1.810 0.017 0.003 5.38*** 0.991 0.274 1.891 0.0279 0.012 2.3* 0.990 0.046
Tmean May–October 1.715 0.017 0.0029 5.78*** 0.991 0.310 1.694 0.0305 0.0127 2.4* 0.990 0.050
1.726 0.015 0.003 5.55*** 0.991 0.265 1.693 0.028 0.0113 2.5* 0.990 0.054
Tmean December–March 1.977 0.024 0.004 6.46*** 0.991 0.350 2.172 0.0217 0.0126 1.72 NS 0.990 0.026
1.965 0.021 0.004 5.62*** 0.991 0.290 2.161 0.0205 0.0112 1.82 NS 0.990 0.029
P2.153 − 0.0003 0.00004 − 6.01*** 0.991 0.318 2.284 − 0.0001 0.0001 − 1.49 NS 0.990 0.029
2.109 − 0.0002 0.00004 − 4.01*** 0.991 0.173 2.313 − 0.0001 0.0001 − 1.65 NS 0.990 0.024
P May–October 2.141 − 0.0008 0.00006 − 6.46*** 0.991 0.350 2.254 − 0.0001 0.0001 − 1.2 NS 0.990 0.013
2.111 − 0.0003 0.0001 − 4.23*** 0.991 0.193 2.258 − 0.0001 0.0001 − 1.1 NS 0.990 0.011
P December–March 2.429 − 0.008 0.0002 − 3.73*** 0.991 0.154 2.323 − 0.0008 0.0004 − 2.02* 0.990 0.036
2.034 − 0.0004 0.0002 − 1.91NS 0.991 0.046 2.363 − 0.001 0.0004 − 2.69** 0.990 0.062
Altitude 2.018 − 0.0001 0.00002 − 5.97*** 0.991 0.317 2.267 − 0.0004 0.0002 − 2.66** 0.990 0.059
Latitude 6.71 − 0.097 0.02 − 5.37*** 0.991 0.271 5.40 − 0.066 0.024 − 2.77** 0.990 0.066
Longitude 2.283 − 0.015 0.006 − 3.25*** 0.991 0.118 2.158 0.002 0.006 − 0.4 NS 0.990 0.001
Content courtesy of Springer Nature, terms of use apply. Rights reserved.
33967Environmental Science and Pollution Research (2024) 31:33960–33974
Fig. 4 Results of the constrained correspondence analysis (CCA).
CCA1 axis corresponds to the altitude and the seasonal May Octo-
ber precipitation totals, CCA2 axis to longitude; points repre-
sent 37 studied ragweed populations. The acute angle between the
arrows indicates a strong association between variables. The arrow
length represents the strength of the correlation, which can be posi-
tive or negative according to the arrow direction. The permutation
test (n = 999) confirmed the significance of the analysis (F = 1197,
p < 0.001)
Fig. 5 Differences in DNA amount at different biotope types. The
smaller genome size (2C < 2.1 pg) is more frequent along roadsides
and railways than in arable land and ruderal habitats
Fig. 6 Flower cytometry histogramwith the double peak showing the
differences in the ragweed genome size betweenthe selected sam-
ples of both genome size groups. The samples wereco-chopped for
the analysis. The ratio between peaks of group 1 (sample VN105) and
group 2 (sample KP103) is 0.81
in North America or Europe. A noticeable disparity in the
peak distance was observed between the sample with smaller
genome size (2C < 2.1pg) and the larger genome size sample
(2C > 2.1pg) (Fig.6). Intraspecific genome size variability
can be generally caused by a number of genomic mechanisms,
such as transposable elements, tandem repeats, or recombina-
tion rate, often driven by environmental changes (Tiley and
Burleigh 2015; Wang etal. 2021). Aneuploidy, as a possible
source of variation, has not been observed in both native pop-
ulations (Jones 1936; Bolkhovskikh etal. 1969; Bassett and
Crompton 1975) and naturalized individuals within the study
area (Májovský etal. 1974; Feráková and Javorčíko1974).
It is less likely that all plants in populations with smaller or
larger genome sizes would be aneuploids. The observed vari-
ability can be clarified when the measured values are divided
into two groups. It is likely that these groups represent dif-
ferent races that originated in North America. There are two
genetic groups of ragweed in Europe (Gladieux etal. 2011),
but it is not certain whether they correlate with the groups we
have discovered. The first ragweed populations were brought
to Slovakia from Canada (Hrabovský etal. 2016). We now
estimated that their genome size was smaller. It might seem
Content courtesy of Springer Nature, terms of use apply. Rights reserved.
33968 Environmental Science and Pollution Research (2024) 31:33960–33974
that the sizes of larger genomes are more difficult to estimate
from herbarium specimens (Viruel etal. 2019) and there-
fore were not found. However, we also found sample with a
larger genome from 1971. Such plants could have occurred
earlier in the study area. The problem is the absence of a suf-
ficient amount of ragweed herbarium collections that would
help determine the exact period of introduction of the second
ragweed group with a larger genome size to Slovakia. Rag-
weed was brought to most European countries from the USA
(Makra etal. 2015). Therefore, only the group with a larger
genome size has been detected in Europe so far (Kubešo
etal. 2010; Battlay etal. 2023). Most likely, this group
migrated into Slovakia from Hungary and mixed with already
imported populations with smaller genome size.
The importance ofclimatic factors forragweed
genome size selection
Latitude is the most evident factor that correlates with the
genome size of many plant species. In the northern hemi-
sphere, the genome size increases from the equator to the
temperate zone and decreases again towards the pole (Yu
etal. 2018; Bureš etal. 2024). Monoploid genome size in
Ambrosia species increases from subtropical regions to the
temperate zone (Sliwinska etal. 2009; Zonneveld 2019),
but in temperate Ambrosia artemisiifolia, it is again smaller
(Kubešová etal. 2010; Pustahija etal. 2013; Zonneveld
2019). We observed two ragweed genome size groups that
correlate with latitude. This might be related to the shorter
life cycle of ragweed, which grows in northern latitudes
(Scalone etal. 2016). It can be assumed that the different
ecological preferences of the groups, which are dispersed
throughout the region, are the reason for the observed cor-
relations between ragweed genome size and other environ-
mental factors. However, our analyses showed that there
are associations between genome size and environmental
factors within each group. These associations have com-
parable regression trends but different R2 values. Plants
of group 1 growing in more northern latitudes seem to be
under higher selection pressure than plants of group 2. A
similar case was observed in perennial Phragmites austra-
lis, where different genome size groups are known, but their
monoploid genome size had opposing correlation trends
(Meyerson etal. 2024). Relationships between variability
in the genome size and various environmental factors due
to natural selection are also known in annual plants such as
Eragrostis (Hutang etal. 2023) or wild Zea mays (Rayburn
and Auger 1990; Bilinski etal. 2018). The negative cor-
relation between genome size, latitude, and seasonal pre-
cipitation and a positive association with the annual mean
temperature, as we observed in ragweed, are known in sun-
flowers (Qiu etal. 2019). This may be explained by their
genetic relatedness (Urbatsch etal. 2000).
The phenotypic variability of the ragweed is contingent
upon factors such as temperature, latitude, and longitude
(Dickerson and Sweet 1971; Leiblein-Wild and Tackenberg
2014). Our investigation has augmented the current under-
standing of this subject matter by highlighting the correla-
tion between genome size and the aforementioned factors.
In the studied area, the latitude, longitude, and elevation
are in a close relationship with temperature-precipitation
regime (Čimo etal. 2020). This regime exhibits a marked
shift from west to east, owing to the alternating maritime
transition zone and continentality (Vilček etal. 2016). The
influence of continentality on ragweed genome size distribu-
tion in studied area, manifested by increasing temperature
and decreasing precipitation, is reflected in our results. Thus,
indications of selection of group 1 with smaller genome can
be observed in areas with unfavorable climatic conditions
due to continentality or elevation, while in areas charac-
terized by optimal conditions, genetic drift could account
for the observed variability, and hence the selection is less
evident. Furthermore, the average genome size values are
significantly lower in regions with unfavorable climatic con-
ditions for ragweed survival. This is in line with the large
genome constraint hypothesis (Knight etal. 2005), according
to which extreme environmental conditions constrain species
with large genomes. Genome size reduction helps invasive
plants adapt better to a new environment (Lavergne etal.
2010). The reason for the selection of a smaller genome in
mountain regions could be attributed to an adaptive strategy
to cope with a shorter vegetation period, given that plants
with reduced genome sizes have comparatively shorter life
cycle (Bennett 1972; Leitch and Bennett 2007). Ragweed
populations that have evolved to a shorter life cycle as a
result of environmental conditions are known (Hodgins and
Rieseberg 2011; Scalone etal. 2016; Gentili etal. 2018).
Even outside mountainous areas, the temperature and pre-
cipitation can limit the life cycle of the ragweed (Dicker-
son 1968; Bassett and Crompton 1975). Although ragweed
thrives in warm environments, its geographic range is
restricted by low winter temperatures and limited precipita-
tion during the growing season (Shrestha etal. 1999; Gentili
etal. 2019). The positive correlation between the ragweed
DNA amount with winter and summer temperatures indi-
cates the influences of warm summer months as well as a
cold winter period for the adaptive DNA amount variation.
The precipitation regime, on the other hand, appears to be
an effective selective factor for genome size only during the
growing season (May–October).
Climatic change andadaptation reflected
ingenome size
The results of our study do not provide definitive evidence
as to whether the emergence of genome size variability
Content courtesy of Springer Nature, terms of use apply. Rights reserved.
33969Environmental Science and Pollution Research (2024) 31:33960–33974
occurred during the naturalization period (1970 2000) or
whether it is an ongoing selective process that extends to the
present. The observed differences in meteorological vari-
ables (i.e., an increase in mean temperature of 0.78–1.40°C
and an increase in precipitation of 42.6–80.9mm) between
historical and current periods at the study sites did not have
a significant impact on the statistical results. This is because
the correlation between historical and current period mean
temperature and precipitation is strong (ρ = 0.99, p < 0.001).
This fails to provide definitive evidence as to whether the
genome size variation is more strongly associated with his-
torical environmental factors or the current climate. How-
ever, climate change often produces new selection pressure
(Hoffmann and Sgrò 2011), and the evolutionary response
to such change can be rapid (Whitney and Gabler 2008).
Stressful conditions andragweed genome size
Anthropogenic biotopes such as roadsides, arable land, rail-
ways, or ruderal habitats are often exposed to mixtures of
various factors (e.g., traffic emissions, alkalinization of soils,
pesticides) with a stressful effect on the plant (Klumpp etal.
2006). We found that the genome size of ragweed growing
along the road and rail network is lower than that in arable
land and ruderal habitats. The observed difference between
ragweed genome size in different anthropogenic habitats
can be caused by the aforementioned relationships between
genome size and environmental factors, since ragweed tends
to grow primarily along roads and railways in the mountains,
which are associated with colder climates, while it grows in
every anthropogenic habitat in warmer and drier lowland
areas (Hrabovský and Mičieta 2018). However, along roads
and railways, unlike ruderal habitats and fields, there is fre-
quent mowing, and only individuals with a shorter life cycle
can produce seeds under disturbation pressure.
In conclusion, climate could be one of the factors in shap-
ing the distribution of two Ambrosia artemisiifolia genome
size groups in the study area. It is worth noting that due
to the localized nature of our research, the identified rela-
tionships may lack generalizability to other European or
non-European regions. In the future, it will be interesting
to monitor the genome size of more ragweed populations in
mountain regions where naturalization processes are cur-
rently underway.
Supplementary Information The online version contains supplemen-
tary material available at https:// doi. org/ 10. 1007/ s11356- 024- 33410-x.
Acknowledgements We are grateful to reviewers for their inspirational
ideas and recommendations.
Author contribution Michal Hrabovský: conceptualization, data
curation, formal analysis, software, writing—original draft, review,
and editing; Silvia Kubalová: writing—review and editing; Karol
Mičieta: conceptualization, validation; Jana Ščevková: supervision,
writing—review and editing. All authors read and approved the final
manuscript.
Funding Open access funding provided by The Ministry of Educa-
tion, Science, Research and Sport of the Slovak Republic in coop-
eration with Centre for Scientific and Technical Information of the
Slovak Republic. The study was supported by the Operation Program
of Integrated Infrastructure for the project, Advancing University
Capacity and Competence in Research, Development, and Inno-
vation, ITMS2014 + :313021X329, co-financed by the European
Regional Development Fund and by the Operation Program of Inte-
grated Infrastructure for the project, UpScale of Comenius University
Capacities and Competence in Research, Development, and Innovation,
ITMS2014 + : 313021BUZ3, co-financed by the European Regional
Development Fund. This study was supported by Grant Agency VEGA
(Bratislava), Grant No. 1/0180/22.
Data availability All data generated or analyzed during this study are
included in this published article.
Declarations
Ethics approval and consent to participate Not applicable.
Consent to participate Not applicable.
Consent for publication Not applicable.
Competing interests The authors declare no competing interests.
Open Access This article is licensed under a Creative Commons Attri-
bution 4.0 International License, which permits use, sharing, adapta-
tion, distribution and reproduction in any medium or format, as long
as you give appropriate credit to the original author(s) and the source,
provide a link to the Creative Commons licence, and indicate if changes
were made. The images or other third party material in this article are
included in the article’s Creative Commons licence, unless indicated
otherwise in a credit line to the material. If material is not included in
the article’s Creative Commons licence and your intended use is not
permitted by statutory regulation or exceeds the permitted use, you will
need to obtain permission directly from the copyright holder. To view a
copy of this licence, visit http://creativecommons.org/licenses/by/4.0/.
References
Abbasi-Karin S, Karimzadeh G, Mohammadi-Bazargani M (2022)
Interspecific chromosomal and genome size variations in in
vitro propagated willow herb (Epilobium spp.) Medicinal
Plant. Cytologia 87:129–135. https:// doi. org/ 10. 1508/ cytol
ogia. 87. 129
Albach DC, Greilhuber J (2004) Genome size variation and evolution
in Veronica. Ann Bot 94:897–911. https:// doi. org/ 10. 1093/ aob/
mch219
Aliyu OM (2014) Analysis of absolute nuclear DNA content reveals a
small genome and intra-specific variation in cashew (Anacardium
occidentale L.). Anacardiaceae Silvae Genetica 63:285–292.
https:// doi. org/ 10. 1515/ sg- 2014- 0036
Andrews CA (2010) Natural selection, genetic drift, and gene flow do
not act in isolation in natural populations. Nat Educ Knowl 3:5
Bai C, Alverson WS, Follansbee A, Waller DM (2012) New reports
of nuclear DNA content for 407 vascular plant taxa from the
Content courtesy of Springer Nature, terms of use apply. Rights reserved.
33970 Environmental Science and Pollution Research (2024) 31:33960–33974
United States. Ann Bot 110:1623–1629. https:// doi. org/ 10. 1093/
aob/ mcs222
Bassett IJ, Crompton CW (1975) The biology of Canadian weeds.: 11.
Ambrosia artemisiifolia L. and A. psilostachya DC. Can J Plant
Sci 55:463–476. https:// doi. org/ 10. 4141/ cjps75- 072
Battlay P, Wilson J, Bieker VC, Lee C, Prapas D, Petersen B, Craig
S, van Boheemen L, Scalone R, de Silva NP, Sharma A (2023)
Large haploblocks underlie rapid adaptation in the invasive weed
Ambrosia artemisiifolia. Nat Commun 14:1717. https:// doi. org/
10. 1038/ s41467- 023- 37303-4
Becher H, Powell RF, Brown MR, Metherell C, Pellicer J, Leitch IJ,
Twyford AD (2021) The nature of intraspecific and interspecific
genome size variation in taxonomically complex eyebrights. Ann
Bot 128:639–651. https:// doi. org/ 10. 1093/ aob/ mcab1 02
Bennett MD (1972) Nuclear DNA content and minimum generation
time in herbaceous plants. Proc R Soc Lond B 181:109–135.
https:// doi. org/ 10. 1098/ rspb. 1972. 0042
Bennett MD (1987) Variation in genomic form in plants and its eco-
logical implications. New Phytol 106:177–200. https:// doi. org/
10. 1111/j. 1469- 8137. 1987. tb046 89.x
Bennett MD, Smith JB, Lewis Smith RI (1982) DNA amounts of angio-
sperms from the Antartic and South Georgia. Environ Exp Bot
22:307–318. https:// doi. org/ 10. 1016/ 0098- 8472(82) 90023-5
Bennett MD, Leitch IJ, Hanson L (1998) DNA amounts in two samples
of angiosperm weeds. Ann Bot 82:121–134. https:// doi. org/ 10.
1006/ anbo. 1998. 0785
Bilinski P, Albert PS, Berg JJ, Birchler JA, Grote MN, Lorant A, Quez-
ada J, Swarts K, Yang J, Ross-Ibarra J (2018) Parallel altitudinal
clines reveal trends in adaptive evolution of genome size in Zea
mays. PLoS Genet 14:e1007162. https:// doi. org/ 10. 1371/ journ
al. pgen. 10071 62
Blommaert J (2020) Genome size evolution: towards new model
systems for old questions. Proc R Soc Lond B 287:20201441.
https:// doi. org/ 10. 1098/ rspb. 2020. 1441
Bolkhovskikh ZV, Grif VG, Zakhar’eva OI, Matveeva TS (1969) Chro-
mosome numbers of flowering plants. Nauka, Leningrad
Bottini MCJ, Greizerstein EJ, Aulicino MB, Poggio L (2000) Relation-
ships among genome size, environmental conditions and geo-
graphical distribution in natural populations of NW Patagonian
species of Berberis L. (Berberidaceae). Ann Bot 86:565–573.
https:// doi. org/ 10. 1006/ anbo. 2000. 1218
Bureš P, Elliott TL, Veselý P, Šmarda P, Forest F, Leitch IJ, Lughadha
EN, Gomez MS, Pironon S, Brown MJ, Šmerda J (2024) Zedek
F (2024) The global distribution of angiosperm genome size is
shaped by climate. New Phytol. https:// doi. org/ 10. 1111/ nph.
19544
Caceres ME, De Pace C, Scarascia Mugnozza GT, Kotsonis P, Cec-
carelli M, Cionini PG (1998) Genome size variations within
Dasypyrum villosum: correlations with chromosomal traits, envi-
ronmental factors and plant phenotypic characteristics and behav-
iour in reproduction. Theor Appl Genet 96:559–567. https:// doi.
org/ 10. 1007/ s0012 20050 774
Carta A, Peruzzi L (2016) Testing the large genome constraint hypoth-
esis: plant traits, habitat and climate seasonality in Liliaceae.
New Phytol 210:709–716. https:// doi. org/ 10. 1111/ nph. 13769
Carta A, Mattana E, Dickie J, Vandelook F (2022) Correlated evolu-
tion of seed mass and genome size varies among life forms in
flowering plants. Seed Sci Res 32:46–52. https:// doi. org/ 10. 1017/
S0960 25852 20000 71
Chun YJ, Fumanal B, Laitung B, Bretagnolle F (2010) Gene flow and
population admixture as the primary post-invasion processes
in common ragweed (Ambrosia artemisiifolia) populations in
France. New Phytol 185:1100–1107. https:// doi. org/ 10. 1111/j.
1469- 8137. 2009. 03129.x
Čimo J, Šinka K, Novotná B, Tárník A, Aydin E, Toková L, Kišš V,
Kotuš T (2020) Change in temperature conditions of slovakia to
the reference period 1961–2010 and their expected changes to
time horizons years 2035, 2050, 2075 and 2100 under the condi-
tions of changing climate. J Ecol Eng 21:232–240. https:// doi.
org/ 10. 12911/ 22998 993/ 125585
Cires E, Cuesta C, Revilla MA, Fernández Prieto JA (2010) Intraspe-
cific genome size variation and morphological differentiation of
Ranunculus parnassifolius (Ranunculaceae), an Alpine–Pyre-
nean–Cantabrian polyploid group. Biol J Linn Soc 101:251–271.
https:// doi. org/ 10. 1111/j. 1095- 8312. 2010. 01517.x
Cunze S, Leiblein MC, Tackenberg O (2013) Range expansion of
Ambrosia artemisiifolia in Europe is promoted by climate
change. Int Sch Res Not: 610126. https:// doi. org/ 10. 1155/ 2013/
610126
Dessaint F, Chauvel B, Bretagnolle F (2005) L’ambroisie: chronique
de l’extension d’un “polluant biologique” en France. Med Sci
(paris) 21:207–209. https:// doi. org/ 10. 1051/ medsci/ 20052 12207
Dickerson CT, Sweet RD (1971) Common ragweed ecotypes. Weed Sci
19:64–66. https:// doi. org/ 10. 1017/ S0043 17450 00482 81
Dickerson CT (1968) Studies on the germination, growth, development
and control of common ragweed (Ambrosia artemisiifolia L.).
PhD thesis, Cornell University
Dirkse GM, Duistermaat H, Zonneveld BJM (2014) Morphology and
genome weight of Symphyotrichum species (Asteraceae) along
rivers in The Netherlands. New J Bot 4:134–142. https:// doi. org/
10. 1179/ 20423 49714Y. 00000 00049
Dlugosch KM, Parker IM (2008) Founding events in species invasions:
genetic variation, adaptive evolution, and the role of multiple
introductions. Mol Ecol 17:431–449. https:// doi. org/ 10. 1111/j.
1365- 294X. 2007. 03538.x
Duchoslav M, Šafářová L, Jandová M (2013) Role of adaptive and
non-adaptive mechanisms forming complex patterns of genome
size variation in six cytotypes of polyploid Allium oleraceum
(Amaryllidaceae) on a continental scale. Ann Bot 111:419–431.
https:// doi. org/ 10. 1093/ aob/ mcs297
Dušková E, Kolář F, Sklenář P, Rauchová J, Kubešová M, Fér T, Suda
J, Marhold K (2010) Genome size correlates with growth form,
habitat and phylogeny in the Andean genus Lasiocephalus
(Asteraceae). Preslia 82:127–148
Enke N, Fuchs J, Gemeinholzer B (2011) Shrinking genomes? Evi-
dence from genome size variation in Crepis (Compositae). Plant
Biol 13:185–193. https:// doi. org/ 10. 1111/j. 1438- 8677. 2010.
00341.x
Farah AH, Lee SY, Gao Z, Yao TL, Madon M, Mohamed R (2018)
Genome size, molecular phylogeny, and evolutionary history
of the tribe Aquilarieae (Thymelaeaceae), the Natural source of
agarwood. Front Plant Sci 29:712. https:// doi. org/ 10. 3389/ fpls.
2018. 00712
Farashi A, Alizadeh-Noughani M (2023) Basic introduction to species
distribution modelling. Ecosystem and species habitat modeling
for conservation and restoration. Springer Nature, Singapore, pp
21–40
Feráková V, Javorčíková D (1974) Floristische Angaben von der Stadt
Bratislava und ihrer Umgebung I. Acta Fac Rerum Nat Univ
Comen Bot 22:115–122
Fick SE, Hijmans RJ (2017) WorldClim 2: new 1-km spatial resolution
climate surfaces for global land areas. Int J Climatol 37:4302–
4315. https:// doi. org/ 10. 1002/ joc. 5086
Frajman B, Rešetnik I, Weiss-Schneeweiss H, Ehrendorfer F, Schön-
swetter P (2015) Cytotype diversity and genome size variation in
Knautia (Caprifoliaceae, Dipsacoideae). BMC Evol Biol 15:140.
https:// doi. org/ 10. 1186/ s12862- 015- 0425-y
Franks SJ, Sim S, Weis AE (2007) Rapid evolution of flowering time
by an annual plant in response to a climate fluctuation. Proc Natl
Content courtesy of Springer Nature, terms of use apply. Rights reserved.
33971Environmental Science and Pollution Research (2024) 31:33960–33974
Acad Sci USA 104:1278–1282. https:// doi. org/ 10. 1073/ pnas.
06083 79104
Futák J (1984) Fytogeografické členenie Slovenska. In: Bertová L (ed)
Flóra Slovenska IV/1. Veda, Bratislava, p 418–420
Gentili R, Ambrosini R, Montagnani C, Caronni S, Citterio S (2018)
Effect of soil pH on the growth, reproductive investment and
pollen allergenicity of Ambrosia artemisiifolia L. Front Plant Sci
9:1335. https:// doi. org/ 10. 3389/ fpls. 2018. 01335
Gentili R, Asero R, Caronni S, Guarino M, Montagnani C, Mistrello G,
Citterio S (2019) Ambrosia artemisiifolia L. temperature-respon-
sive traits influencing the prevalence and severity of pollinosis: a
study in controlled conditions. BMC Plant Biol 19:155. https://
doi. org/ 10. 1186/ s12870- 019- 1762-6
Genton B, Shykoff JA, Giraud T (2005) High genetic diversity in
French invasive populations of common ragweed, Ambrosia
artemisiifolia, as a result of multiple sources of introduction.
Mol Ecol 14:4275–4285. https:// doi. org/ 10. 1111/j. 1365- 294X.
2005. 02750.x
Gladieux P, Giraud T, Kiss L, Genton BJ, Jonot O, Shykoff JA (2011)
Distinct invasion sources of common ragweed (Ambrosia
artemisiifolia) in Eastern and Western Europe. Biol Invasions
13:933–944. https:// doi. org/ 10. 1007/ s10530- 010- 9880-y
Gregory TR (2005) The C-value enigma in plants and animals: a review
of parallels and an appeal for partnership. Ann Bot 95:133–146.
https:// doi. org/ 10. 1093/ aob/ mci009
Gregory TR, Hebert PDN (1999) The modulation of DNA content:
proximate causes and ultimate consequences. Genome Res
9:317–324. https:// doi. org/ 10. 1101/ gr.9. 4. 317
Greilhuber J (1998) Intraspecific variation in genome size: a critical
reassessment. Ann Bot 82:27–35. https:// doi. org/ 10. 1006/ anbo.
1998. 0725
Greilhuber J, Doležel J, Lysak MA, Bennett MD (2005) The origin,
evolution and proposed stabilization of the terms ‘Genome
size’ and ‘C-value’ to describe nuclear DNA contents. Ann Bot
95:255–260. https:// doi. org/ 10. 1093/ aob/ mci019
Grime JP (1998) Plant classification for ecological purposes: is there
a role for genome size? Ann Bot 82(suppl A):117–120. https://
doi. org/ 10. 1006/ anbo. 1998. 0723
Grotkopp E, Rejmánek M, Sanderson MJ, Rost TL (2004) Evolution
of genome size in pines (Pinus) and its life-history correlates:
supertree analyses. Evolution 58:1705–1729. https:// doi. org/ 10.
1111/j. 0014- 3820. 2004. tb004 56.x
Guignard MS, Nichols RA, Knell RJ, Macdonald A, Romila C-A,
Trimmer M, Leitch IJ, Leitch AR (2016) Genome size and ploidy
influence angiosperm species’ biomass under nitrogen and phos-
phorus limitation. New Phytol 210:1195–1206. https:// doi. org/
10. 1111/ nph. 13881
Guo G (2020) A block bootstrap for quasi-likelihood in sparse func-
tional data. Statistics 54:909–925. https:// doi. org/ 10. 1080/ 02331
888. 2020. 18239 79
Hessen DO, Jeyasingh PD, Neiman M, Weider LJ (2010) Genome
streamlining and the elemental costs of growth. Trends Ecol Evol
25:75–80. https:// doi. org/ 10. 1016/j. tree. 2009. 08. 004
Hidalgo O, Garcia S, Garnatje T, Mumbrú M, Patterson A, Vigo J,
Vallés J (2015) Genome size in aquatic and wetland plants: fitting
with the large genome constraint hypothesis with a few relevant
exceptions. Plant Syst Evol 301:1927–1936. https:// doi. org/ 10.
1007/ s00606- 015- 1205-2
Hoang PTN, Fiebig A, Novák P, Macas J, Cao HX, Stepanenko A, Chen
G, Borisjuk N, Scholz U, Schubert I (2020) Chromosome-scale
genome assembly for the duckweed Spirodela intermedia, inte-
grating cytogenetic maps, PacBio and Oxford Nanopore libraries.
Sci Rep 10:19230. https:// doi. org/ 10. 1038/ s41598- 020- 75728-9
Hodgins KA, Rieseberg L (2011) Genetic differentiation in life-his-
tory traits of introduced and native common ragweed (Ambrosia
artemisiifolia) populations. J Evol Biol 24:2731–2749. https://
doi. org/ 10. 1111/j. 1420- 9101. 2011. 02404.x
Hoffmann AA, Sgrò CM (2011) Climate change and evolutionary adap-
tation. Nature 470:479–485. https:// doi. org/ 10. 1038/ natur e09670
Hothorn T, Hornik K, Zeileis A (2006) Unbiased recursive partition-
ing: a conditional inference Framework. J Comput Graph Stat
15:651–674. https:// doi. org/ 10. 1198/ 10618 6006X 133933
Hrabovský M, Mičieta K (2018) New findings of the common ragweed
(Ambrosia artemisiifolia) in Slovakia in the year 2017. Acta Bot
Univ Comen 53:25–27
Hrabovský M, Ščevková J, Mičieta K, Lafférsová J, Dušička J (2016)
The expansion and aerobiology of Ambrosia artemisiifolia L. in
Slovakia. Ann Agric Environ Med 23:64–70. https:// doi. org/ 10.
5604/ 12321 966. 11968 54
Hutang GR, Tong Y, Zhu XG, Gao LZ (2023) Genome size varia-
tion and polyploidy prevalence in the genus Eragrostis are
associated with the global dispersal in arid area. Front Plant Sci
14:1066925. https:// doi. org/ 10. 3389/ fpls. 2023. 10669 25
Jehlík V (1998) Cizí expanzivní plevele České republiky a Slovenské
republiky. Academia, Praha
Jones KL (1936) Studies on Ambrosia, I. The inheritance of floral types
in the ragweed. Ambrosia Elatior l Am Midl Nat 17:673–699.
https:// doi. org/ 10. 2307/ 24200 93
Karrer G, Hall RM, Le Corre V, Kropf M (2023) Genetic structur-
ing and invasion status of the perennial Ambrosia psilostachya
(Asteraceae) in Europe. Sci Rep 13:3736. https:// doi. org/ 10.
1038/ s41598- 023- 30377-6
Kazinczi G, Béres I, Novák R, Bíró K, Pathy Z (2008) Common rag-
weed (Ambrosia artemisiifolia): a review with special regards
to the results in Hungary. Taxonomy, origin and distribution,
morphology, live cycle and reproduction strategy. Herbologia
9:55–91
Klumpp A, Ansel W, Klumpp G, Calatayud V, Garrec JP, He S, Peñue-
las J, Ribas À, Ro-Poulsen H, Rasmussen S, Sanz MJ, Vergne
P (2006) Tradescantia micronucleus test indicates genotoxic
potential of traffic emissions in European cities. Environ Pol-
lut 139:515–522. https:// doi. org/ 10. 1016/j. envpol. 2005. 05. 021
Knight CA, Ackerly DD (2002) Variation in nuclear DNA content
across environmental gradients: a quantile regression analysis.
Ecol Lett 5:66–76. https:// doi. org/ 10. 1046/j. 1461- 0248. 2002.
00283.x
Knight CA, Molinari NA, Petrov DA (2005) The large genome con-
straint hypothesis: evolution, ecology and phenotype. Ann Bot
95:177–190. https:// doi. org/ 10. 1093/ aob/ mci011
Kochjarová J, Blanár D, Jarolímek I, Slezák M (2023) Wildlife sup-
plementary feeding facilitates spread of alien plants in for-
ested mountainous areas: a case study from the Western Car-
pathians. Biologia 78:1381–1389. https:// doi. org/ 10. 1007/
s11756- 023- 01339-0
Kolář F, Štech M, Trávníček P, Rauchová J, Urfus T, Vít P, Kubešová
M, Suda J (2009) Towards resolving the Knautia arvensis agg.
(Dipsacaceae) puzzle: primary and secondary contact zones and
ploidy segregation at landscape and microgeographic scales. Ann
Bot 103:963–974. https:// doi. org/ 10. 1093/ aob/ mcp016
Kolář F, Lučanová M, Vít P, Urfus T, Chrtek J, Fér T, Ehrendorfer
F, Suda J (2013) Diversity and endemism in deglaciated areas:
ploidy, relative genome size and niche differentiation in the
Galium pusillum complex (Rubiaceae) in Northern and Central
Europe. Ann Bot 111:1095–1108. https:// doi. org/ 10. 1093/ aob/
mct074
Kron P, Suda J, Husband BC (2007) Applications of flow cytometry
to evolutionary and population biology. Annu Rev Ecol Syst
38:847–876. https:// doi. org/ 10. 1146/ annur ev. ecols ys. 38. 091206.
095504
Content courtesy of Springer Nature, terms of use apply. Rights reserved.
33972 Environmental Science and Pollution Research (2024) 31:33960–33974
Kubátová B, Trávníček P, Bastlová D, Čurn V, Jarolímová V, Suda J
(2008) DNA ploidy-level variation in native and invasive popula-
tions of Lythrum salicaria at a large geographical scale. J Bio-
geogr 35:167–176. https:// doi. org/ 10. 1111/j. 1365- 2699. 2007.
01781.x
Kubešová M, Moravcová L, Suda J, Jarošík V, Pyšek P (2010) Natural-
ized plants have smaller genomes than their non-invading rela-
tives: a flow cytometric analysis of the Czech alien flora. Preslia
82:81–96
Labudová L, Šťastný P, Trizna M (2013) The north atlantic oscillation
and winter precipitation totals in Slovakia. Morav Geogr Rep
21:38–49. https:// doi. org/ 10. 2478/ mgr- 2013- 0019
Lambdon PW, Pyšek P, Başnou C, Hejda M, Arianoutsou M, Essel F,
Jarošík V, Pergl J, Winter M, Anastasiu P, Andriopoulos P, Bazos
I, Brundu G, Celesti-Grapow L, Chassot P, Delipetrou P, Josefs-
son M, Kark S, Klotz S, Kokkoris Y, Kühn I, Marchante H, Per-
glová I, Pino J, Vilà M, Zikos A, Roy D, Hulme PE (2008) Alien
flora of Europe: species diversity, temporal trends, geographical
patterns and research needs. Preslia 80:101–149
Larios E, Búrquez A, Becerra JX, Lawrence Venable D (2014) Natu-
ral selection on seed size through the life cycle of a desert
annual plant. Ecology 95:3213–3220. https:// doi. org/ 10. 1890/
13- 1965.1
Lavergne S, Muenke NJ, Molofsky J (2010) Genome size reduction can
trigger rapid phenotypic evolution in invasive plants. Ann Bot
105:109–116. https:// doi. org/ 10. 1093/ aob/ mcp271
Leiblein-Wild MC, Tackenberg O (2014) Phenotypic variation of
38 European Ambrosia artemisiifolia populations measured in
a common garden experiment. Biol Invasions 16:2003–2015.
https:// doi. org/ 10. 1007/ s10530- 014- 0644-y
Leitch IJ, Bennett MD (2007) Genome size and its uses: the impact
of flow cytometry, in: Doležel J, Greilhuber J, Suda, J. (Eds.),
Flow cytometry with plant cells: analysis of genes, chromosomes
and genomes. Wiley-VCH, Weinheim, Germany, pp. 153–176.
https:// doi. org/ 10. 1002/ 97835 27610 921. ch7
Lemke A, Buchholz S, Kowarik I, Starfinger U, von der Lippe M
(2021) Interaction of traffic intensity and habitat features shape
invasion dynamics of an invasive alien species (Ambrosia arte-
misiifolia) in a regional road network. NeoBiota 64:155–175.
https:// doi. org/ 10. 3897/ neobi ota. 64. 58775
Levin DA, Funderburg SW (1979) Genome size in angiosperms: tem-
perate versus tropical species. Am Nat 114:784–795. https:// doi.
org/ 10. 1086/ 283528
Liu X-L, Li H-Q, Wang J-H, Sun X-P, Fu Y-Y, Xing L-G (2021) The
current and future potential geographical distribution of common
ragweed, Ambrosia artemisiifolia in China. Pak J Bot 53:167–
172. https:// doi. org/ 10. 30848/ PJB20 21- 1(18)
Lysak MA, Koch MA, Beaulieu JM, Meister A, Leitch IJ (2009) The
dynamic ups and downs of genome size evolution in Brassi-
caceae. Mol Biol Evol 26:85–98. https:// doi. org/ 10. 1093/ mol-
bev/ msn223
Madlung A, Comai L (2004) The Effect of Stress on Genome Regula-
tion and Structure. Ann Bot 94:481–495. https:// doi. org/ 10. 1093/
aob/ mch172
Mahdavi S, Karimzadeh G (2010) Karyological and nuclear DNA con-
tent variation in some Iranian endemic Thymus species (Lami-
aceae). J Agr Sci Tech 12:447–458
Májovský J etal (1974) Index of chromosome numbers of Slovakian
flora (Part 3). Acta Fac Rerum Nat Univ Comen Bot 22:1–20
Makra L, Matyasovszky I, Hufnagel L, Tusnády G (2015) The history
of ragweed in the world. Appl Ecol Environ Res 13:489–512.
https:// doi. org/ 10. 15666/ aeer/ 1302_ 489512
Mang T, Essl F, Moser D, Dullinger S (2018) Climate warming drives
invasion of Ambrosia artemisiifolia in central Europe. Preslia
90:59–81. https:// doi. org/ 10. 23855/ presl ia. 2018. 059
Marhold K, Kudoh H, Pak J-H, Watanabe K, Španiel S, Lihová J (2010)
Cytotype diversity and genome size variation in eastern Asian
polyploid Cardamine (Brassicaceae) species. Ann Bot 105:249–
264. https:// doi. org/ 10. 1093/ aob/ mcp282
Metzger MJ, Bunce RGH, Jongman RHG, Mücher CA, Watkins JW
(2005) A climatic stratification of the environment of Europe.
Glob Ecol Biogeogr 14:549–563. https:// doi. org/ 10. 1111/j. 1466-
822x. 2005. 00190.x
Meyer L, Causse R, Pernin F, Scalone R, Bailly G, Chauvel B, Délye C,
Le Corre V (2017) New gSSR and EST-SSR markers reveal high
genetic diversity in the invasive plant Ambrosia artemisiifolia
L. and can be transferred to other invasive Ambrosia species.
PLoS ONE 12:e0176197. https:// doi. org/ 10. 1371/ journ al. pone.
01761 97
Meyerson LA, Cronin JT, Bhattarai GP, Brix H, Lambertini C,
Lučanová M, Rinehart S, Suda J, Pyšek P (2016) Do ploidy
level and nuclear genome size and latitude of origin modify the
expression of Phragmites australis traits and interactions with
herbivores? Biol Invasions 18:2531–2549. https:// doi. org/ 10.
1007/ s10530- 016- 1200-8
Meyerson LA, Pyšek P, Lučanová M, Wigginton S, Tran C-T, Cronin
JT (2020) Plant genome size influences stress tolerance of
invasive and native plants via plasticity. Ecosphere 11:e03145.
https:// doi. org/ 10. 1002/ ecs2. 3145
Meyerson LA, Cronin JT, Lučanová M, Lambertini C, Brix H,
Packer JG, Čuda J, Wild J, Pergl J (2024) Pyšek P (2024)
Some like it hot: small genomes may be more prevalent under
climate extremes. Biol Invasions. https:// doi. org/ 10. 1007/
s10530- 024- 03253-1
Michalová M, Hrabovský M, Kubalová S (2024) Miháliková T (2024)
Modelling the Symphyotrichum lanceolatum invasion in Slova-
kia. Central Europe Model Earth Syst Environ. https:// doi. org/
10. 1007/ s40808- 023- 01945-6
Naimi B, Araújo MB (2016) Sdm: a reproducible and extensible R plat-
form for species distribution modelling. Ecography 39:368–375.
https:// doi. org/ 10. 1111/ ecog. 01881
Ogle D (2017) Package ‘FSA.’ Cran Repos 1:1–206
Ohri D (2005) Climate and Growth Form: The consequences for
genome size in plants. Plant Biol 7:449–458. https:// doi. org/ 10.
1055/s- 2005- 865878
Oksanen J (2012) Constrained ordination: tutorial with R and vegan.
R-Packace Vegan 1(10):1–9
Osnato M (2022) The floral transition and adaptation to a changing
environment: from model species to cereal crops. Plant Cell
34:e2. https:// doi. org/ 10. 1093/ plcell/ koac3 04
Pellicer J, Hidalgo O, Dodsworth S, Leitch IJ (2018) Genome size
diversity and its impact on the evolution of land plants. Genes
9:88. https:// doi. org/ 10. 3390/ genes 90200 88
Pinheiro JC, Bates DM (2000) Mixed-effects models in S and S-PLUS.
Springer, New York. https:// doi. org/ 10. 1007/ b98882
Pinke G, Kolejanisz T, Vér A, Nagy K, Milics G, Schlögl G, Bede-
Fazekas Á, Botta-Dukát Z, Czúcz B (2019) Drivers of Ambrosia
artemisiifolia abundance in arable fields along the Austrian-
Hungarian border. Preslia 91:369–389. https:// doi. org/ 10. 23855/
presl ia. 2019. 369
Pustahija F, Brown SC, Bogunić F, Bašić N, Muratović E, Ollier S,
Hidalgo O, Bourge M, Stevanović V, Siljak-Yakovlev S (2013)
Small genomes dominate in plants growing on serpentine soils
in West Balkans, an exhaustive study of 8 habitats covering
308 taxa. Plant Soil 373:427–453. https:// doi. org/ 10. 1007/
s11104- 013- 1794-x
Pyšek P, Čuda J, Šmilauer P, Skálová H, Chumová Z, Lambertini C,
Lučanová M, Ryšavá H, Trávníček P, Šemberová K, Meyerson
LA (2020) Competition among native and invasive Phrag-
mites australis populations: an experimental test of the effects
Content courtesy of Springer Nature, terms of use apply. Rights reserved.
33973Environmental Science and Pollution Research (2024) 31:33960–33974
of invasion status, genome size, and ploidy level. Ecol Evol
10:1106–1118. https:// doi. org/ 10. 1002/ ece3. 5907
Qiu F, Baack EJ, Whitney KD, Bock DG, Tetreault HM, Rieseberg
L, Ungerer MC (2019) Phylogenetic trends and environmental
correlates of nuclear genome size variation in Helianthus sun-
flowers. New Phytol 221:1609–1618. https:// doi. org/ 10. 1111/
nph. 15465
Rasmussen K, Thyrring J, Muscarella R, Borchsenius F (2017) Cli-
mate-change-induced range shifts of three allergenic ragweeds
(Ambrosia L.) in Europe and their potential impact on human
health. PeerJ 5:e3104. https:// doi. org/ 10. 7717/ peerj. 3104
Rayburn AL (1990) Genome size variation in Southwestern United
States Indian maize adapted to various altitudes. Evol Trends
Plants 4:53–57
Rayburn AL, Auger J (1990) Genome size variation in Zea mays ssp.
mays adapted to different altitudes. Theor Appl Genet 79:470–
474. https:// doi. org/ 10. 1007/ BF002 26155
Sayadi V, Karimzadeh G, Naghavi MR, Monfared SJ (2022) Interspe-
cific genome size variation of Iranian endemic Allium species
(Amaryllidaceae). Cytologia 87:335–338. https:// doi. org/ 10.
1508/ cytol ogia. 87. 335
Scalone R, Lemke A, Štefanić E, Kolseth A-K, Rašić S, Andersson L
(2016) Phenological variation in Ambrosia artemisiifolia L. facili-
tates near future establishment at northern latitudes. PLOS ONE
11:e0166510. https:// doi. org/ 10. 1371/ journ al. pone. 01665 10
Shao C, Li Y, Luo A, Wang Z, Xi Z, Liu J, Xu X (2021) Relationship
between functional traits and genome size variation of angiosperms
with different life forms. Biodivers Sci 29:575–585. https:// doi. org/
10. 17520/ biods. 20204 50
Shrestha A, Roman ES, Gordon Thomas A, Swanton CJ (1999) Modeling
germination and shoot-radicle elongation of Ambrosia artemisiifolia.
Weed Sci 47:557–562. https:// doi. org/ 10. 1017/ S0043 17450 00922 62
Skálová H, Guo W-Y, Wild J, Pyšek P (2017) Ambrosia artemisiifolia in
the Czech Republic: history of invasion, current distribution and
prediction of future spread. Preslia 89:1–16. https:// doi. org/ 10.
23855/ presl ia. 2017. 001
Sliwinska E, Pisarczyk I, Pawlik A, Galbraith DW (2009) Measuring
genome size of desert plants using dry seeds. Botany-Botanique
87:127–135. https:// doi. org/ 10. 1139/ B08- 120
Sliwinska E, Loureiro J, Leitch IJ, Šmarda P, Bainard J, Bureš P, Chumova
Z, Horova L, Koutecký P, Lučanová M, Trávníček P (2022) Appli-
cation-based guidelines for best practices in plant flow cytometry.
Cytometry A 101:749–781. https:// doi. org/ 10. 1002/ cyto.a. 24499
Slovák M, Vít P, Urfus T, Suda J (2009) Complex pattern of genome size
variation in a polymorphic member of the Asteraceae. J Biogeogr
36:372–384. https:// doi. org/ 10. 1111/j. 1365- 2699. 2008. 02005.x
Šmarda P, Bureš P (2006) Intraspecific DNA content variability in Fes-
tuca pallens on different geographical scales and ploidy levels. Ann
Bot 98:665–678. https:// doi. org/ 10. 1093/ aob/ mcl150
Šmarda P, Bureš P, Horová L, Rotreklová O (2008) Intrapopulation
genome size dynamics in Festuca pallens. Ann Bot 102:599–607.
https:// doi. org/ 10. 1093/ aob/ mcn133
Šmarda P, Horová L, Bureš P, Hralová I, Marková M (2010) Stabiliz-
ing selection on genome size in a population of Festuca pallens
under conditions of intensive intraspecific competition. New Phytol
187:1195–1204. https:// doi. org/ 10. 1111/j. 1469- 8137. 2010. 03335.x
Sork VL (2015) Gene flow and natural selection shape spatial patterns of
genes in tree populations: implications for evolutionary processes and
applications. Evol Appl 9:291–310. https:// doi. org/ 10. 1111/ e va. 12316
Španiel S, Marhold K, Passalacqua NG, Zozomová-Lihová J (2011) Intri-
cate variation patterns in the diploid-polyploid complex of Alyssum
montanum-A. repens (Brassicaceae) in the Apennine peninsula:
evidence for long-term persistence and diversification. Am J Bot
98:1887–1904. https:// doi. org/ 10. 3732/ ajb. 11001 47
Suda J, Weiss-Schneeweiss H, Tribsch A, Schneeweiss GM, Trávníček P,
Schönswetter P (2007) Complex distribution patterns of di-, tetra-,
and hexaploid cytotypes in the European high mountain plant Sene-
cio carniolicus (Asteraceae). Am J Bot 94:1391–1401. https:// doi.
org/ 10. 3732/ ajb. 94.8. 1391
Temsch EM, Koutecký P, Urfus T, Šmarda P, Doležel J (2022) Refer-
ence standards for flow cytometric estimation of absolute nuclear
DNA content in plants. Cytometry 101:710–724. https:// doi. org/
10. 1002/ cyto.a. 24495
Terlević A, Bogdanović S, Frajman B, Rešetnik I (2022) Genome size
variation in Dianthus sylvestris Wulfen sensu lato (Caryophyl-
laceae). Plants 11:1481. https:// doi. org/ 10. 3390/ plant s1111 1481
Tiley GP, Burleigh JG (2015) The relationship of recombination rate,
genome structure, and patterns of molecular evolution across
angiosperms. BMC Evol Biol 15:194. https:// doi. org/ 10. 1186/
s12862- 015- 0473-3
Trávníček P, Čertner M, Ponert J, Chumová Z, Jersáková J, Suda J (2019)
Diversity in genome size and GC content shows adaptive potential
in orchids and is closely linked to partial endoreplication, plant life-
history traits and climatic conditions. New Phytol 224:1642–1656.
https:// doi. org/ 10. 1111/ nph. 15996
Urbatsch LE, Baldwin BG, Donoghue MJ (2000) Phylogeny of the cone-
flowers and relatives (Heliantheae: Asteraceae) based on nuclear
rDNA internal transcribed spacer (ITS) sequences and chlorplast
DNA restriction site data. Sys Bot 25:539–565. https:// doi. org/ 10.
2307/ 26666 95
Vidic T, Greilhuber J, Vilhar B, Dermastia M (2009) Selective signifi-
cance of genome size in a plant community with heavy metal pol-
lution. Ecol Appl 19:1515–1521. https:// doi. org/ 10. 1890/ 08- 1798.1
Vilček J, Škvarenina J, Vido J, Nalevanková P, Kandrík R, Škvareninová J
(2016) Minimal change of thermal continentality in Slovakia within
the period 1961–2013. Earth Syst Dyn 7:735–744. https:// doi. org/
10. 5194/ esd-7- 735- 2016
Viruel J, Conejero M, Hidalgo O, Pokorny L, Powell RF, Forest F, Kantar
MB, Soto Gomez M, Graham SW, Gravendeel B, Wilkin P, Leitch
IJ (2019) A target capture-based method to estimate ploidy from
herbarium specimens. Front Plant Sci 10:937. https:// doi. org/ 10.
3389/ fpls. 2019. 00937
Wakamiya I, Newton RJ, Spencer Johnston J, James Price H (1993)
Genome size and environmental factors in the genus Pinus. Am
J Bot 80:1235–1241. https:// doi. org/ 10. 1002/j. 1537- 2197. 1993.
tb153 60.x
Wang D, Zheng Z, Li Y, Hu H, Wang Z, Du X, Zhang S, Zhu M, Dong
L, Ren G, Yang Y (2021) Which factors contribute most to genome
size variation within angiosperms? Ecol Evol 11:2660–2668.
https:// doi. org/ 10. 1002/ ece3. 7222
Wang X, Xu Q, Liu J (2023) Determining representative pseudo-absences
for invasive plant distribution modeling based on geographic simi-
larity. Front Ecol Evol 11:1193602. https:// doi. org/ 10. 3389/ fevo.
2023. 11936 02
Whitney KD, Gabler CA (2008) Rapid evolution in introduced species,
‘invasive traits’ and recipient communities: challenges for predict-
ing invasive potential. Divers Distrib 14:569–580. https:// doi. org/
10. 1111/j. 1472- 4642. 2008. 00473.x
Yotoko KSC, Dornelas MC, Togni PD, Fonseca TC, Salzano FM, Bon-
atto SL, Freitas LB (2011) Does variation in genome sizes reflect
adaptive or neutral processes? New Clues from Passiflora Plos
ONE 6:e18212. https:// doi. org/ 10. 1371/ journ al. pone. 00182 12
Yu J, Li D, Lou Y, Guo S (2018) Nuclear DNA content variation of
herbaceous angiosperm species on 10 global latitudinal tran-
sects. J Torrey Bot Soc 145:340–352. https:// doi. org/ 10. 3159/
TORREY- D- 16- 00062.1
Zenni RD, Dickie IA, Wingfield MJ, Hirsch H, Crous CJ, Meyerson LA,
Burgess TI, Zimmermann TG, Klock MM, Siemann E, Erfmeier
A, Aragon R, Montti L, Le Roux JJ (2017) Evolutionary dynamics
of tree invasions: complementing the unified framework for bio-
logical invasions. AoB Plants 9:plw085. https:// doi. org/ 10. 1093/
aobpla/ plw085
Content courtesy of Springer Nature, terms of use apply. Rights reserved.
33974 Environmental Science and Pollution Research (2024) 31:33960–33974
Zonneveld BJ (2019) The DNA weights per nucleus (genome size) of more
than 2350 species of the Flora of The Netherlands, of which 1370
are new to science, including the pattern of their DNA peaks. Forum
Geobotanicum 8:24–78. https:// doi. org/ 10. 3264/ FG. 2019. 1022
Publisher's Note Springer Nature remains neutral with regard to
jurisdictional claims in published maps and institutional affiliations.
Content courtesy of Springer Nature, terms of use apply. Rights reserved.
1.
2.
3.
4.
5.
6.
Terms and Conditions
Springer Nature journal content, brought to you courtesy of Springer Nature Customer Service Center GmbH (“Springer Nature”).
Springer Nature supports a reasonable amount of sharing of research papers by authors, subscribers and authorised users (“Users”), for small-
scale personal, non-commercial use provided that all copyright, trade and service marks and other proprietary notices are maintained. By
accessing, sharing, receiving or otherwise using the Springer Nature journal content you agree to these terms of use (“Terms”). For these
purposes, Springer Nature considers academic use (by researchers and students) to be non-commercial.
These Terms are supplementary and will apply in addition to any applicable website terms and conditions, a relevant site licence or a personal
subscription. These Terms will prevail over any conflict or ambiguity with regards to the relevant terms, a site licence or a personal subscription
(to the extent of the conflict or ambiguity only). For Creative Commons-licensed articles, the terms of the Creative Commons license used will
apply.
We collect and use personal data to provide access to the Springer Nature journal content. We may also use these personal data internally within
ResearchGate and Springer Nature and as agreed share it, in an anonymised way, for purposes of tracking, analysis and reporting. We will not
otherwise disclose your personal data outside the ResearchGate or the Springer Nature group of companies unless we have your permission as
detailed in the Privacy Policy.
While Users may use the Springer Nature journal content for small scale, personal non-commercial use, it is important to note that Users may
not:
use such content for the purpose of providing other users with access on a regular or large scale basis or as a means to circumvent access
control;
use such content where to do so would be considered a criminal or statutory offence in any jurisdiction, or gives rise to civil liability, or is
otherwise unlawful;
falsely or misleadingly imply or suggest endorsement, approval , sponsorship, or association unless explicitly agreed to by Springer Nature in
writing;
use bots or other automated methods to access the content or redirect messages
override any security feature or exclusionary protocol; or
share the content in order to create substitute for Springer Nature products or services or a systematic database of Springer Nature journal
content.
In line with the restriction against commercial use, Springer Nature does not permit the creation of a product or service that creates revenue,
royalties, rent or income from our content or its inclusion as part of a paid for service or for other commercial gain. Springer Nature journal
content cannot be used for inter-library loans and librarians may not upload Springer Nature journal content on a large scale into their, or any
other, institutional repository.
These terms of use are reviewed regularly and may be amended at any time. Springer Nature is not obligated to publish any information or
content on this website and may remove it or features or functionality at our sole discretion, at any time with or without notice. Springer Nature
may revoke this licence to you at any time and remove access to any copies of the Springer Nature journal content which have been saved.
To the fullest extent permitted by law, Springer Nature makes no warranties, representations or guarantees to Users, either express or implied
with respect to the Springer nature journal content and all parties disclaim and waive any implied warranties or warranties imposed by law,
including merchantability or fitness for any particular purpose.
Please note that these rights do not automatically extend to content, data or other material published by Springer Nature that may be licensed
from third parties.
If you would like to use or distribute our Springer Nature journal content to a wider audience or on a regular basis or in any other manner not
expressly permitted by these Terms, please contact Springer Nature at
onlineservice@springernature.com
Article
Full-text available
Solidago canadensis is an invasive species from North America that is spreading to higher and higher altitudes in Europe. We tracked its spread into the Slovak High Tatras National Park, where it is beginning to occur in high mountain valleys. We determined the absolute DNA amount of these individuals, which is 2C = 1.848-1.885 pg. In comparison, another invasive species, Solidago gigantea, from the same genus has a higher DNA amount of 2C = 3.238 pg, which makes it easy to distinguish these species from each other not only on the basis of morphological characters, but also by flow cytometry using propidium iodide staining. During our research, we recorded other non-native species in the High Tatras (e.g., Reynoutria japonica, Galinsoga parviflora, Erigeron annuus, Ambrosia artemisiifolia, Symphyotrichum × salignum, Symphyotrichum × versicolor), which tend to spread from lowlands to higher altitudes.
Article
Full-text available
In the paper, we provide information on the occurrence of the newly introduced, escaped species Galanthus elwesii in Slovakia and summarize the known karyological knowledge about snowdrops in Slovakia with an emphasis on their genome size and chromosome number.
Article
Full-text available
Changing climates can influence species range shifts and biological invasions, but the mechanisms are not fully known. Using the model species Phragmites australis (Cav.) Trin. ex Steud. (Poaceae), we conducted a global analysis of climate and plant native and introduced cytotypes to determine whether this relationship influences population distributions, hypothesizing that smaller genomes are more common in regions of greater environmental stress. First, we identified 598 Phragmites australis field-collected native and introduced genome size variants using flow cytometry. We then evaluated whether temperature and precipitation were associated with P. australis monoploid genome size (Cx-value) distributions using Cx-value and Worldclim data. After accounting for potential spatial autocorrelation among source populations, we found climate significantly influenced Cx-value prevalence on continents. The relationships of Cx-value to temperature and precipitation varied according to whether plants were native or introduced in North America and Europe, and Cx-values were strongly influenced by precipitation during the dry season. Smaller plant monoploid genome size was associated with more stressful abiotic conditions; under extreme high temperatures and under drought, plants had smaller Cx-values. This may influence genome dominance, biological invasions, and range expansions and contractions as climate change selects for genome sizes that maximize fitness.
Article
Full-text available
Symphyotrichum lanceolatum (Willd.) G. L. Nesom is an alien invasive species in Europe, where it presents a potential threat to natural habitats. Its rapid expansion in recent decades raises questions and concerns about the causes and consequences of its spread in Slovakia. We investigated natural and anthropogenic habitats along with topographic and environmental factors, including changing climatic conditions such as air temperature and precipitation totals to adjust prediction models of the species distribution. Using 19 various algorithms, the models for the past, present, and future were calculated based on 395 octoploid populations selected by flow cytometry. The models revealed the potential species distribution along rivers and in human settlements and its increasing during the period 1970–2060 from 23.6 to 53.85% of the territory as a result of climatic change. A conditional inference tree indicates that the expansion can be limited by a mean annual air temperature below 8 °C and a pH of soil less than 5.5. Therefore, there is a high probability of the further spread of S. lanceolatum across Slovakia.
Article
Full-text available
Angiosperms, which inhabit diverse environments across all continents, exhibit significant variation in genome sizes, making them an excellent model system for examining hypotheses about the global distribution of genome size. These include the previously proposed large genome constraint, mutational hazard, polyploidy‐mediated, and climate‐mediated hypotheses. We compiled the largest genome size dataset to date, encompassing 16 017 (> 5% of known) angiosperm species, and analyzed genome size distribution using a comprehensive geographic distribution dataset for all angiosperms. We observed that angiosperms with large range sizes generally had small genomes, supporting the large genome constraint hypothesis. Climate was shown to exert a strong influence on genome size distribution along the global latitudinal gradient, while the frequency of polyploidy and the type of growth form had negligible effects. In contrast to the unimodal patterns along the global latitudinal gradient shown by plant size traits and polyploid proportions, the increase in angiosperm genome size from the equator to 40–50°N/S is probably mediated by different (mostly climatic) mechanisms than the decrease in genome sizes observed from 40 to 50°N northward. Our analysis suggests that the global distribution of genome sizes in angiosperms is mainly shaped by climatically mediated purifying selection, genetic drift, relaxed selection, and environmental filtering.
Article
Full-text available
Introduction The use of pseudo-absence data constrained by environmental conditions can facilitate potential distribution predictions of invasive species. However, pseudo-absence data generated by existing methods are usually not representative because the relationship between the presence and pseudo-absence points is either simplistic or neglected. This could under or overestimate the potential distribution of invasive species. Methods To address this deficiency, this study proposes a new method for obtaining pseudo-absence data based on geographic similarities. First, the reliability of pseudo-absences was quantified based on the geographic similarity to the occurrence of species. Subsequently, a representative pseudo-absence reliability threshold interval was determined. Finally, different pseudo-absence acquisition methods were assessed by combining virtual species with a real invasive species. Results The analysis demonstrated that the geographic similarity method can improve model accuracy and achieve a more realistic distribution compared with the traditional method of sampling for pseudo-absence data. Discussion This result indicates that the pseudo-absence data obtained using the geographic similarity approach were more representative. Our study provides valuable insights into improving invasive plant distribution predictions by considering the geographical relationships between species occurrences and the surrounding environments.
Article
Full-text available
Adaptation is the central feature and leading explanation for the evolutionary diversification of life. Adaptation is also notoriously difficult to study in nature, owing to its complexity and logistically prohibitive timescale. Here, we leverage extensive contemporary and historical collections of Ambrosia artemisiifolia—an aggressively invasive weed and primary cause of pollen-induced hayfever—to track the phenotypic and genetic causes of recent local adaptation across its native and invasive ranges in North America and Europe, respectively. Large haploblocks—indicative of chromosomal inversions—contain a disproportionate share (26%) of genomic regions conferring parallel adaptation to local climates between ranges, are associated with rapidly adapting traits, and exhibit dramatic frequency shifts over space and time. These results highlight the importance of large-effect standing variants in rapid adaptation, which have been critical to A. artemisiifolia’s global spread across vast climatic gradients.
Article
Full-text available
Background Biologists have long debated the drivers of the genome size evolution and variation ever since Darwin. Assumptions for the adaptive or maladaptive consequences of the associations between genome sizes and environmental factors have been proposed, but the significance of these hypotheses remains controversial. Eragrostis is a large genus in the grass family and is often used as crop or forage during the dry seasons. The wide range and complex ploidy levels make Eragrostis an excellent model for investigating how the genome size variation and evolution is associated with environmental factors and how these changes can ben interpreted. Methods We reconstructed the Eragrostis phylogeny and estimated genome sizes through flow cytometric analyses. Phylogenetic comparative analyses were performed to explore how genome size variation and evolution is related to their climatic niches and geographical ranges. The genome size evolution and environmental factors were examined using different models to study the phylogenetic signal, mode and tempo throughout evolutionary history. Results Our results support the monophyly of Eragrostis. The genome sizes in Eragrostis ranged from ~0.66 pg to ~3.80 pg. We found that a moderate phylogenetic conservatism existed in terms of the genome sizes but was absent from environmental factors. In addition, phylogeny-based associations revealed close correlations between genome sizes and precipitation-related variables, indicating that the genome size variation mainly caused by polyploidization may have evolved as an adaptation to various environments in the genus Eragrostis. Conclusion This is the first study to take a global perspective on the genome size variation and evolution in the genus Eragrostis. Our results suggest that the adaptation and conservatism are manifested in the genome size variation, allowing the arid species of Eragrostis to spread the xeric area throughout the world.
Article
Full-text available
The perennial western ragweed (Ambrosia psilostachya DC.) arrived from North America to Europe in the late nineteenth century and behaves invasive in its non-native range. Due to its efficient vegetative propagation via root suckers, A. psilostachya got naturalized in major parts of Europe forming extensive populations in Mediterranean coastal areas. The invasion history, the spreading process, the relationships among the populations as well as population structuring is not yet explored. This paper aims to give first insights into the population genetics of A. psilostachya in its non-native European range based on 60 sampled populations and 15 Simple Sequence Repeats (SSR). By AMOVA analysis we detected 10.4% of genetic variation occurring among (pre-defined) regions. These regions represent important harbors for trading goods from America to Europe that might have served as source for founder populations. Bayesian Clustering revealed that spatial distribution of genetic variation of populations is best explained by six groups, mainly corresponding to regions around important harbors. As northern populations show high degrees of clonality and lowest levels of within-population genetic diversity (mean Ho = 0.40 ± 0.09), they could preserve the initial genetic variation levels by long-lived clonal genets. In Mediterranean populations A. psilostachya expanded to millions of shoots. Some of those were obviously spread by sea current along the coast to new sites, where they initiated populations characterized by a lower genetic diversity. For the future, the invasion history in Europe might get clearer after consideration of North American source populations of western ragweed.
Article
Full-text available
The genus Allium L. is in Amaryllidaceae family with approximately 900 species distributed worldwide. The key aim of this study was to examine variations among eight Iranian endemic Allium species based on genome size. The results showed that among eight Allium species examined, seven were diploid (A. sativum, A. stipitatum, A. fistolosum, A. umbellicatum, A. lenkoranicum, A. stamineum, and A. rubellum; 2n=2x=16). Interestingly, the chromosome number 2n=3x=24 was evidenced in A. atroviolaceum. Strong interspecific diversity was identified in the studied Allium genome size. The overall average genome sizes of examined species were 34.17 pg, varying from 22.24 pg in A. fistolosum to 43.80 pg in A. stipitatum. The positive and significant correlations between genome size and total chromosome volume (TCV), altitude, and latitudes indicate that the species with larger genome sizes were situated in higher sea levels and low latitudes areas. These results may provide suitable information for Allium evolutionary, genetics, and breeding studies.
Article
Full-text available
The genus Epilobium, belonging to the family Onagraceae, is an endemic Iranian medicinal plant that has illustrated a vast variety of pharmacologically important metabolites. The cytological characteristics of eight species collected from different regions of Iran were assessed for the first time. All species analyzed were diploid, six species (E. hirsutum, E. parviflorum, E. roseum, E. algidum, E. anatolicum, and E. confusum) had 2n=2x= 36 chromosomes, except for two species (E. frigidum, E. lanceolatum) had 2n=2x=38 chromosomes with unequal in size. The mean chromosome length of all species was 0.53 µm, ranging from 0.46 to 0.64 µm. Propidium iodide (PI) and Solanum lycopersicum cv. Stupicke (2C DNA= 1.96 pg) as an internal standard were used for flow cytometric survey of genome size and the levels of ploidy. The mean genome size (2Cx DNA) of all species was 0.86 pg, varied from 0.74 to 0.90 pg, confirming inter-specific variation and revealing considerable variation in genome size within each species. Valuable information on cytogenetics can be used in some research fields, including polygenetic analysis, taxonomic relationships, evolutionary characteristics, ecology, plant growth, and development of plant breeding.
Article
Ecological relationships between supplementary feeding and baiting in situ and vegetation patterns were studied in the mostly forest landscape of the Western Carpathians. We aimed to test the role of wildlife management practices in alien plants spreading. Altogether 82 localities with diverse hunting facilities stretched throughout several mountain areas and hills from northern to southern Slovakia were examined. Presence of vascular plant species was recorded for each locality. In addition, we sampled 33 phytosociological relevés to cover main vegetation types using methods of Zürich-Montpelière approach. Altogether 208 taxa of vascular plants consisting of 144 native and 64 alien ones were found. Among aliens, 44 archaeophytes and 20 neophytes were recognized, including 8 invasive species (Amaranthus retroflexus, Ambrosia artemisiifolia, Bidens frondosa, Conyza canadensis, Echinochloa crus-galli, Galinsoga urticifolia, Helianthus tuberosus, and Stenactis annua). Different habitat conditions as well as intensity and frequency of disturbances result in high community heterogeneity. Six plant communities and one group of stands with weak phytosociological relations were identified. A canonical correspondence analysis (CCA) was applied to explain the effect of hunting facilities, artificial feeds and elevation on species compositional pattern of vascular plants and neophyte species, while variation in percentage of aliens and neophytes was modeled using general linear model (GLM). The CCA revealed the significant role of bait site, elevation, coarse fodder (hay), grain feed and fleshy feed for species composition assemblages. The proportion of aliens decreased at higher elevations and increased with the occurrence of bait sites and with the use of grain feed and corn silage. The neophyte frequency was negatively associated with elevation and coarse fodder (hay), but positively associated with the presence of high shooting stand and crushed corn. Based on results concerning risk of alien and/or invasive plant species spreading, wildlife supplementary feeding, baiting and whatever fodder and crop decoy applications (except hay of local provenience) seem to be undesirable. Especially in natural ecosystems and strictly protected areas, consistent and controlled abidance of regulation has to be enforced.