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Phenotypic plasticity versus local adaptation to explain
drought-resistance under elevated temperature at
seedling stage in native and invasive populations of a
shrub (Ulex europeaus, L.)
Mathias Christina, Celine Gire, Mark Bakker, Alan Leckie, Jianming Xue, W
Clinton, Zaira Negrin-Perez, José Ramon Arevalo Sierra, Arevalo Sierra,
Jean-Christophe Domec, et al.
To cite this version:
Mathias Christina, Celine Gire, Mark Bakker, Alan Leckie, Jianming Xue, et al.. Phenotypic plasticity versus local adaptation to explain drought-resistance under elevated temperature at seedling stage in native and invasive populations of a shrub (Ulex europeaus, L.). 2020. �hal-02863202�
Christina et al., preprint 2020
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Phenotypic plasticity versus local adaptation to explain drought-resistance under
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elevated temperature at seedling stage in native and invasive populations of a shrub
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(Ulex europeaus, L.)
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Mathias Christina a,b, Céline Gire a,c, Mark R. Bakker a,c, Alan Leckied, Jianming Xued, Peter
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W. Clintond, Zaira Negrin-Pereze, José Ramon Arevalo Sierrae, Jean-Christophe Domec a,c,
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Maya Gonzalez a,c
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a INRA, UMR 1391 ISPA, CS20032, 33882 Villenave d’Ornon cedex, France.
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b CIRAD, UPR 115 AIDA, 97490 Saint-Clotilde, La Reunion.
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c Bordeaux Sciences Agro, UMR 1391 ISPA, Gradignan F-33883, France.
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d SCION Institute, 8011 Christchurch, New Zealand.
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e Department of Botany, Ecology and Plant Physiology, University of La Laguna, 38206 La
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Laguna.
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* Corresponding author: mathias.christina@cirad.fr
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Christina et al., preprint 2020
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Abstract
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1. The assumption that climatic requirements of invasive species are conserved between
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their native and non-native environment is a key ecological issue in the evaluation of
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risk of invasion. We conducted a growth chamber experiment to compare climatic
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requirements between native and introduced populations of common gorse (Ulex
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europeaus, L.) seedlings, an invasive evergreen shrub.
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2. Seeds were sampled from 20 populations from 5 areas from both native (France,
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Spain) and non-native areas (New Zealand, Canary and Reunion islands). The
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seedlings were grown over 36 days in two temperature treatments (ambient, at 24 °C
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and elevated, at 30 °C in average) combined with two water treatments (irrigated or
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watering withheld). Temperature treatments were defined after assessing the niche
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temperature of the species in the different countries, and the elevated temperature was
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defined as the highest temperature at the niche margin.
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3. Invasive populations were more drought resistant and performant at high temperature
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than native ones. Under elevated temperature and drought, native populations showed
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a greater mortality rate (53%) than invasive populations (16%) after 36-days of growth.
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Invasive seedlings also showed a higher aerial and roots development than native ones
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under this constrain climate. The difference between populations in mortality could be
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explained by difference in phenotypic plasticity at the population level (e.g. specific root
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length - SRL) and local adaptation to the environment of origin (average temperature).
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The difference in growth in height and root area was also correlated with phenotypic
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plasticity (SRL and above to belowground ratio, respectively) and the climate of origin
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(precipitation of the warmest quarter and temperature of the driest quarter,
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respectively).
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4. Assessing the importance of phenotypic divergences and plasticity of invasive species
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at the margins of their climatic distribution range is a key step to highlight where
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management efforts should be concentrated once the species is naturalized in order to
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limit and prevent its spread.
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Keywords: invasion ecology; alien plants; drought; climatic niche; establishment; growth
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chamber; species invasion;
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1. Introduction
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Biological invasion is a major economical and environmental ecosystem threat that is currently
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enhanced by global change (Vitousek et al. 1996; Andersen et al. 2004), and the invasion of
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islands by plant species is a serious threat to endemic species (Caujapé-Castells et al. 2010).
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For the efficient allocation of management resources, we need to understand which factors
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limit or prevent their establishment and spread, to therefore characterize the species’
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ecological niche.
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The assumption that climatic requirements of invasive species are conserved between their
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native and invaded environment is a key issue in the assessment of invasive risk (Pearman et
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al., 2008). However, this assumption is not well supported. For example, evidence of climatic
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niche shifts has been shown for specific invasive plants (Gallagher et al., 2010; Broennimann
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et al., 2007; Hernandez-Lambraño et al., 2016) but a review concluded that ~85% of terrestrial
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invasive plants would not be able to shift their climatic niche (Petitpierre et al. 2012).
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Nevertheless, Webber et al (2012) disagreed with this statement and suggested that niche
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conservation for invasive species would be the exception rather than the rule. Assessing the
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climatic niche in native and invasive environments of invasive plants is a key step to limit their
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establishment as anticipation appears as the most efficient management strategy (Leung et al.
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2002). Moreover, detecting climatic niche shifts due to evolutionary changes in invasive plants
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(Lavergne and Molofsky 2007) is crucial under rapid climate change.
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Invasive species often present rapid evolution (Buswell et al., 2011) and a high genetic
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plasticity thus improving species adaptation to new ecosystems (Lavergne and Molofsky,
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2007). For those introduced species that spread across a wide distributional range, phenotypic
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plasticity has often been proposed as an important contributor to invasion success (Davidson
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et al. 2011). In particular, the phenotypic plasticity could improve survival rates during the initial
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establishment in a new environment (Ghalambor et al. 2007). It is crucial to assess the
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importance of phenotypic plasticity in response to climate, in particular how this would enable
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an invasive plant species to colonize a wide range of habitats and elevations (Alexander et al.
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2011) and could allow such a species to occupy ecosystems outside its native climatic niche
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(Sexton et al., 2002). Additionally, rapid evolution of invasive species could promote local
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adaptation and facilitate range expansion of invasive plants (Colautti and Barret, 2013).
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Nevertheless, there still debate on the relative importance of local adaptation of invasive
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species in comparison to native ones (Oduor et al., 2016) as process of local adaptation was
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not necessary the rule for all species (Li et al., 2015; Wallendael et al., 2018).
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A new plant species introduced outside its native range has to cross several barriers before
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becoming an invader (Richardson et al. 2000; Blackburn et al. 2011). An initial stage is the
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establishment (survival) of young introduced individuals, which is strongly influenced by abiotic
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conditions. Many studies pointed out that seedling establishment is restricted by climatic
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conditions such as temperature, water availability or light (Danner and Knapp 2003, Kellman
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2004, Hou et al. 2014, Leiblein-Wild et al. 2014, Nguyen et al. 2016), particularly for
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elevation ecosystems (Arévalo et al., 2010, Tecco et al. 2016). Yet, few have dealt with the
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influence of abiotic factors on seedling establishment at the margin of its climatic niche (e.g.
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Kellman 2004, Laube et al. 2015). In addition to the increase in mean annual temperatures,
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extreme temperature frequencies are predicted to become more frequent under future climate
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Christina et al., preprint 2020
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scenarios (Katz and Brown 1992; Wagner 1996; IPCC 2014). These extreme events are likely116
to cause dramatic change to ecological communities (Diez et al. 2012). Therefore, a better
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understanding of the effect of extreme temperature changes on plant invasion is needed.
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In this study, we tested the tolerance of an invasive shrub (common gorse, Ulex europaeus)
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to two imposed abiotic factors (temperature and water availability) at the margin of its observed
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climatic niche. Gorse is a particularly interesting model species as it is among the 30 most
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invasive plant species worldwide (IUCN) at latitudes ranging from 54°S to 60°N and at altitudes
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ranging from sea level to 3,550 m asl. (Hornoy et al., 2013). Its world-scale distribution
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suggests a potentially broad niche with respect to climatic variables (particularly temperature)
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with a compensatory phenomenon with soil water content and atmospheric humidity (e.g.
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gorse is only present at high altitude for lower latitudes). Recent modeling studies suggested
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that the climatic niche of introduced populations changed in comparison to native populations
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in North America, South America and North Europe (Christina et al., 2019, Hernandez-
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Lambraño et al., 2016).
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The main objective of this study was to assess gorse seedling tolerance to abiotic factors
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(temperature and water availability) at the margin of its observed climatic niche. The
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hypotheses were that:
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i) Invasive gorse seedlings were more performant to elevated temperature and low
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soil humidity than native ones,
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ii) The difference of performance among gorse populations could be explained by
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phenotypic divergence in terms of individual traits,
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iii) The difference of performance among gorse populations results from both
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difference in phenotypic plasticity and local adaptation to the climate of origin.
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2. Materials and Methods
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2.1. Assessing the temperature niche of Ulex europaeus in studied countries
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Ulex europaeus, L. (gorse) native populations from France and Spain and invasive populations
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from Canary, Reunion Islands and New Zealand were used in this study (Table 1). Prior to the
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experiment, the climatic niche of gorse was assessed in each country. Localization of gorse
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populations was performed in a previous study using various internet network, field
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reconnaissance and literature search (Christina et al., 2019). In total, 2627, 1068, 5, 1005 and
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457 gorse populations were located in France, Spain, Canary, Reunion islands and New
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Zealand, respectively. These data were then transformed to a 5 arc min (~10 km) grid of gorse
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presence and matched with WordClim bioclimatic variables (5 arc min, worldclim.org, version
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1.4, Hijmans et al., 2005). We used the WorldClim bioclimatic variables to define two
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temperature ranges, one ambient temperature corresponding to an average temperature
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where gorse was present and one elevated temperature corresponding to a temperature at the
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margin of the temperature tolerance of gorse. Climatic data were presented using a beanplot
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(Kampstra, 2008) based on a normal density function (Fig. 1).
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Fig. 1. WorldClim climatic data where Ulex europaeus is present in the different studied countries
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(maximum temperature of the warmest month, mean temperature or driest quarter and annual mean
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temperature) from 1960 to 1990. Data are presented using a beanplot with median (black line), normal
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density (purple background) and populations (green lines). The red dashed lines represent the values
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used to define the elevated and ambient temperature in the growth chamber experiment. The black
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dashed lines represent the median values of all five countries.
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2.2. Studied populations
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Seeds were sampled from 20 populations from five countries and altitude ranging from sea
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level to 2000 m asl. Names and location of populations are presented in supplementary
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information (Table 1). Eleven populations were considered as natives (seven from France and
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four from Spain) and nine populations sampled in non-native ecosystems (five from Reunion
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Island, three from New Zealand and one from Canary Island). In each population, 50 pods on
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20 different individuals were sampled during the reproductive period. Only mature brown pods
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were collected. The seeds were stored in the pods at 4ºC until required. The seeds were
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carefully examined to exclude any seeds that had been attacked by insects.
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Table 1.Gorse (Ulex europaeus) source population information. Climatic data at each location
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were obtained from WorldClim: mean annual temperature (TMEAN), temperature of the driest
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quarter (TDRYQUARTER), annual precipitation (PPTANNUAL) and precipitation of the warmest quarter
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(PPTWARMQUARTER).
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Origine Pays Population Latitude Longitude Elevation (m) TMEAN (°C) TDRYQUARTER (°C) PPTANNUAL (mm) PPTWARMQUARTER (mm) Number of individuals Nat iv e S p a in COM 43.283 -5.017 793 10.3 16.4 845 163 8 MdR 43.283 -5.000 910 10.3 16.4 845 163 8 CA 42.983 -4.233 1114 10 16 893 169 15 LdE 43.267 -4.983 1146 10.3 16.4 845 163 6 Fr a n c e AND 44.733 -1.100 10 12.7 19.1 1020 195 22 BPM 48.683 -1.933 10 11.4 10.3 745 174 5 CAUD 44.567 -0.983 22 12.7 19.1 1020 195 5 MAD 44.750 -0.400 86 12.7 19.1 1020 195 9 FSP 43.367 -1.533 98 13.8 17.6 1346 287 12 BVE 48.117 -3.333 200 10.7 15.6 1007 187 16 SAR 43.333 -1.583 206 12.2 18.2 1304 261 7 In v a s iv e Canary LAG 28.510 -16.322 680 15.6 19.2 488 16 12 N e w -Zea lan d WAI -44.667 170.967 340 11.2 7.2 590 160 6 RV -41.150 173.567 400 11.7 16 1681 331 17 Inw -41.567 172.933 890 10 14.3 1559 326 14 R e u n ion RPP -21.137 55.613 1100 17.5 15.2 1613 700 6 RCA -21.276 55.584 1290 17 14.7 1615 686 13 RSI -21.225 55.582 1620 16.8 14.5 1644 704 6 RMB -21.062 55.374 1850 16.9 14.6 1671 726 7 RMM -21.069 55.379 1990 16.9 14.6 1671 726 18
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2.3. Seed germination
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All equipment was sterilized in an autoclave and sterile water was used. To further minimize
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the risk of infestation by fungi and bacteria, seed samples were washed in 2.5% sodium
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hypochlorite (NaOCl) for 10 min and then rinsed during 5 min. Seeds were then scarified using
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sulfuric acid (Sixtus et al. 2003). Two volumes of acid to one volume of seeds were used.
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Seeds were placed in sulfuric acid for 3h and then washed in sterile water. After rinsing the
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seeds were placed in petri dishes at 15°C until germination (~2 weeks). Petri dishes were
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regularly humidified.
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After germination, seeds were planted at 2 cm depth in individual pots (10 cm depth) and grown
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in a greenhouse. The soil used in pots was a typical acid sandy soil representative of southern
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France soil where native gorse grows (Dry morrland: 5.9 - 12.7 mg C g-1, 0.40 - 0.67 mg N g
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1, 0.026 - 0.030 mg PTOT g-1, 0.13 - 0.19 mg OxAl g-1, 0.08 - 0.15 mg OxFe g-1). At the end of
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the growing period, 220 homogeneous seedlings were chosen for the experiment and
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assigned to the four treatments (76 from seven populations in France; 40 from five populations
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in Spain; 12 from one population in Canary Islands; 52 from six populations in Reunion Island
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and 40 from five populations in New Zealand). In each country, seedlings were chosen in
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different populations to take into account phenotypic variability within studied areas. These
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seedlings were pooled by country and population belonging (native vs. invasive) in the
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following analyses. In the rest of the paper we will use the term “native population” or “invasive
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population” for these pools of individuals.
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2.4. Temperature and watering treatment definitions
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For each treatment, we defined a maximum daily temperature using the WorldClim maximum
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daily temperature of the warmest month, and an average daily temperature using the
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WorldClim daily mean temperature of the driest quarter (Fig. 1) as the interaction between two
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environmental variables, temperature and watering was tested. We used two phytotrons
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(growth chambers) in this study to separate elevated and ambient temperature treatments. In
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each phytotron the daily period was separated in four periods : night period with PAR=0 (TNIGHT,
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12h), morning and afternoon periods with mean temperature (TMEAN, PAR≈100 µmol m-2 s-1,
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each one 3h) and a high temperature period at midday (TMAX, PAR≈100 µmol m-2 s-1, 6h). The
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night temperature was set to have the same temperature diurnal range between the two
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treatments. In conclusion, the two treatments were defined as follows :
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- Phytotron ambient : TMAX = 24°C, TMEAN = 17°C, TNIGHT = 10°C
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- Phytotron elevated : TMAX = 30°C, TMEAN = 23°C, TNIGHT = 16°C
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In each phytotron, relative humidity was adjusted to have similar non-limiting (low enough)
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vapour pressure deficit (VPD) during the daytime. Consequently, relative humidity in the
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phytotron with elevated temperature was set to 74% during the night and 70% during the day,
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corresponding to VPDNIGHT = 0.41, VPDMEAN = 0.7 and VPDMAX = 1.01 kPa periods. In the
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phytotron with ambient temperature, relative humidity was set to 74% during the night and 60%
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during the day, corresponding to VPDNIGHT = 0.29, VPDMEAN = 0.67 and VPDMAX = 0.98 kPa
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periods.
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Finally, in each phytotron two treatments of watering were defined: a watered treatment where
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pots were watered with 20 mL of water three times a week to maintain soil saturated (wet
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treatment); and a drought treatment where pots were not watered over the 36-days period of
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the experiment (dry treatment).
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2.5. Seedling growth and acclimation
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As described above, four treatments were applied using two phytotrons (ambient temperature,
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wet and dry in phytotron #1, elevated temperature, wet and dry in phytotron #2). In this
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experimental design, due to a limited number of available phytotron, the temperature treatment
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was nested to a “phytotron treatment”. Nevertheless, as other climatic factors (PAR, VPD)
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were controlled and similar between phytotrons, we assumed that this design was adequate
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to test the temperature effect. At the beginning, both phytotrons started with the ambient
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temperature setting and all seedlings were watered. During the first 10 days, temperature of
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the phytotron #2 increased gradually to reach the elevated temperature treatment. At the end
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of this temperature/watering acclimation period, and thus at the beginning of the experiment,
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seedlings heights were similar (p value = 0.59) among all native and invasive populations (Fig.
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S1), and were around 19 mm. Watering treatments started after this acclimation period and
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were maintained over 36 days.
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2.6. Measurements
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At the end of the 36-days period, various plant traits were measured at the individual level
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(Table 2). Based on Violle et al. (2007) we defined two types of traits: performance and
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functional traits. Performance traits were measurements of individual fitness (vegetative
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biomass; plant survival) extended to traits linked to the plant growth (height, leaf area, roots
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length and areas). Functional traits were defined as traits which impacts fitness indirectly via
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its effects on growth. Plant height was defined as the height up the apex. Considering plant
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organs, stem, leaves/spines and roots were separated manually for each individual. Then,
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fresh roots and leaves were scanned (400 dpi). Leaf area was calculated using the ImageJ
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software (Schneider et al. 2012) while total root length, area and average roots diameter were
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calculated using the Winrhizo software (Arsenault et al. 1995). Stem, roots and leaves were
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then dried at 65°C for three days and weighed to obtain the dry weights. Contrary to plant
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traits, mortality rate was calculated at the population level.
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Table 2. Plant traits definition measured in this study. All traits were measured at the individual
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levels.
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Performance trait Functional traits
Description Unit Code Description Unit Code
Height mm H Above to belowground ratio ABRATIO
Leaf area cm² LA Leaf to aboveground ratio LARATIO
Total dry mass g TDM Specific leaf area cm² g-1 SLA
Leaves dry mass g LDM Root diameter mm RD
Roots dry mass g RDM Specific root length m g-1 SRL
Root length m RL Specific root area cm² g-1 SRA
Root area cm² RA
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2.7. Data analyses
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The effects of temperature (T24, T30), watering treatment (wet, dry), population belonging
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(native or invasive) and their interaction on H, LA, TDM, LDM, RDM, RL, RA, ABRATIO,LARATIO, RD,
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SLA, SRL and SRA were tested using a linear mixed-effect model of variance (lmer function
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from lme4 R package). All traits were log-transformed prior to analysis to satisfy assumption
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of normality. The main general linear model included the following fixed effects: origin (Inv/Nat),
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growth temperature (T), watering treatment (W) and their interaction. Random, nested effects
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were used in calculating fixed effects F ratios: population (P) was used as the error terms to
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test the effect of Inv/Nat, TxP was used as the error terms to test the effects of T and T x
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Inv/Nat, WxP was used as the error terms to test the effect of W and W x Inv/Nat and finally P
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x T:W was used to test the effect of the interaction TxW and the interaction between Inv/Nat x
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T x W:303
𝑇𝑟𝑎𝑖𝑡 ~ 𝐼𝑛𝑣𝑁𝑎𝑡 ∗ 𝑇 ∗ 𝑊 + (1|𝑃) + (𝑇|𝑃) + (𝑊|𝑃) + (𝑇: 𝑊|𝑃)304
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Post-hoc analyses were then performed to compare invasive and native gorse. The
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comparison of mortality rate of invasive and native populations was performed using a non
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parametric dunn test (dunn.test function from dunn.test package). Comparison of
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transformed traits of native and invasive seedlings were performed using the t.test function.
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Correlation between individual performance traits and functional traits was assessed using a
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spearman correlation coefficient (cor.test function).
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Based on one index from Vallardes et al., 2006, we assessed the phenotypic plasticity of
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functional traits at the population level:
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𝑃𝐼 − 𝑡𝑟𝑎𝑖𝑡 = 𝜎(𝑀𝑒(𝑡𝑟𝑎𝑖𝑡)) 𝑀𝑒(𝑡𝑟𝑎𝑖𝑡)
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Where 𝑀𝑒(𝑡𝑟𝑎𝑖𝑡) is the median trait of gorse seedlings in each treatment, 𝜎(𝑀𝑒(𝑡𝑟𝑎𝑖𝑡)) the
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standard deviation of the median trait across treatments and 𝑀𝑒(𝑡𝑟𝑎𝑖𝑡) the average of the
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median trait across treatments. Comparison of phenotypic plasticity index between native and
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invasive populations was then performed using t.test. Correlation between average
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performance trait at the population level and plasticity index, on one hand, and average climatic
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factor of origin (TMEAN, TDRYQUARTER, PPTANNUAL and PPTWARMQUARTER), on the other hand, was
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tested using spearman correlation coefficient (cor.test function). Finally, for visual purpose,
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polynomial smooth regressions were added in the figures using the loess R function. All
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statistical analyses were performed using R.3.6.1 (R Development Core Team 2019).
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3. Results
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3.1. Gorse niche temperature
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Gorse niche temperature differed considering the countries of origin (Fig. 1). In terms of annual
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mean temperature, the warmest areas occupied by gorse were found in invasive areas in
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Canary and Reunion Island, but invasive populations from New Zealand occupied areas with
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similar temperature to native populations (France and Spain). During dry seasons warmest
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areas occupied by gorse could be found in both native (Spain and France) and invasive
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(Canary Island) areas. Additionally, the maximum daily temperatures were observed in native
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areas in Spain.345
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3.2. Gorse performance347
Mortality rate at the population levels and performance traits of gorse seedlings were
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influenced by air temperature, watering levels and population belonging (native vs invasive,
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Table 3). Under ambient (T24) temperature or watered treatments mortality rate was almost
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null while it reached 36% in average under T30 x dry treatments (Fig. 2). Within this treatment,
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mortality rate of native populations (53%) was higher than invasive populations (16%) in
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average. The populations with the lowest mortality rates were found in Canary (0%) and
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Reunion island (5%, Table S1) while mortality rate was similar among native populations
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(53%).
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Considering performance traits, all traits were significantly influenced by watering level
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(Table 3) and H and LA were additionally influenced by temperature. Moreover, TDM and LDM
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were influenced by the native vs invasive origin of the populations, as well as RL and RA by the
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interaction between watering level and origin (Table 3). Among the T30 x wet treatment invasive
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seedlings showed a higher H and LA by 17 and 24%, respectively, than native seedlings
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(Fig. 2). Similarly, among the T30 x dry treatment, invasive seedlings had a higher TDM, RDM, RL
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and RA than native seedlings by 41, 39, 30 and 42% in average. In this treatment, the seedlings
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with the highest plant height and biomass were found in Canary (Table S1).
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Table 3. Effect of air temperature (T, ambient vs elevated), watering levels (W, wet vs dry),
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population belonging (native or invasive, Inv/Nat) and their interaction on gorse traits measured
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in the growth chamber experiment and described in Table 2. Variance (F) analyses were
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performed using a linear mixed-effect model. P values were abbreviated as (.), *, **, *** when
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lower than 0.1, 0.05, 0.01,0.001, respectively.
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Inv/Nat T W T x W Inv/Nat x T Inv/Nat x W Inv/Nat x T x W Performance traits H F=3.9 (.) F=60.5 *** F=11.7 ** F=9.4 ** F=3.2 (.) F=1.6 F=0.2 LA F=3.6 (.) F=14.6 ** F=57.6 *** F=3.7 (.) F=2.4 F=0.7 F=1.0 TDM F=9.6 ** F=0.5 F=22.5 *** F<0.1 F<0.1 F=0.1 F=0.3 LDM F=8.0 * F=1. 0 F=16.5 *** F<0.1 F<0.1 F=0.4 F=0.7 RDM F=3.8 (.) F=0.2 F=8.6 ** F=0.3 F=0.6 F=3.0 (.) F=0.4 RL F=0.3 F=2.8 F=9.1 ** F=0.3 F<0.1 F=8.1 ** F=0.2 RA F=2.1 F=0.4 F=60.4 *** F<0.1 F=0.4 F=6.9 * F=0.2 Functional traits ABRATIO F=1.2 F<0.1 F=8.0 ** F=0.8 F=0.2 F=5.3 * F<0.1 LARATIO F=0.6 F=3.9 (.) F=2.4 F<0.1 F=0.6 F=3.1 F=1.5 SLA F=4.9 * F=72.6 *** F=30.4 *** F=9.8 ** F=9.5 ** F=0.4 F<0.1 RD F=1.0 F=24.5 *** F=187.3 *** F=6.6 * F=4.9 * F=1.0 F<0.1 SRL F=1.5 F=4.4 (.) F<0.1 F=0.1 F=0.5 F=5.3 * F=0.2 SRA F=2.4 F=0.1 F=98.3 *** F=1.5 F<0.1 F=2.8 F=0.2388
389
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392
393
394
395
396
397
398
399
400
401
402
403
404
405
406
407
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Christina et al., preprint 2020
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409
Fig. 2. Change in seedlings mortality rate within populations and plant performance traits:
410
height, total dry, leaves and roots dry mass (DM), leaf area, root length and area, depending
411
on growth chamber treatment. T24 and T30 corresponded to the ambient and elevated
412
temperature treatments, respectively. Wet and Dry corresponded to the watering treatment.
413
Significant difference between native (blue) and invasive (red) populations are indicated by ns,
414
(.), * and ** for p value > 0.1, <0.1, <0.05 and <0.01, respectively.
415
416
417
418
419
420
421
422
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Christina et al., preprint 2020
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3.3. Growth functional traits
424
Across all treatments significant spearman correlation were found between mortality rate or
425
plant performance traits and functional traits (Table 4). Populations with the highest mortality
426
rate were population with the lowest RD and SRA. Nevertheless, the only difference between
427
native and invasive populations were found in the T30 x wet treatments (Fig. 3). In this
428
treatment root diameter was higher in invasive seedlings than native ones by 5% and SRA
429
was lower in invasive seedlings than native one by 5%.
430
Considering light competition traits such as height or leaf area, significant correlation were
431
found between H and ABRATIO and SLA, and between LA and ABRATIO, SLA, RD and SRA (Table
432
3). Except for SRA and RD, no difference at the individual’s levels between native and invasive
433
seedlings were found for these functional traits in the T30 treatments. Nevertheless, ABRATIO
434
was higher in invasive seedlings than native ones in the T24 x wet treatments. On the other
435
hand, SLA was lower in invasive seedlings than native ones in the T24 treatments.
436
Total dry mass was only correlated with root diameter (Table 3) which was higher in the
437
invasive seedlings than native ones in the T30 x wet treatments. While we found no correlation
438
between root dry mass and functional traits, the seedlings with the highest root area were
439
seedlings with the highest SLA, RD and SRA.
440
441
442
443
Table 4. Spearman correlation between seedlings performance traits and functional traits at
444
the individual level across all treatments. P values were abbreviated as (.), *, **, *** when lower
445
than 0.1, 0.05, 0.01,0.001, respectively. the number of individuals (n) used in the correlation
446
are indicated.
447
Mortality rate H LA TDM RDM RA
Functional traits All treatments n
ABRATIO -0.14 0.27 * 0.35 ** 0.16 -0.19 0 74 LARATIO 0.04 -0.1 0.12 0.1 0.13 -0.01 74 SLA -0.14 0.48 *** 0.59 *** 0.09 0.03 0.34 ** 73 RD -0.48 *** 0.15 0.42 *** 0.33 ** 0.18 0.46 *** 74 SRL -0.03 -0.05 -0.02 -0.17 -0.21(.) 0.2 (.) 74 SRA -0.42 *** 0.1 0.38 ** 0.16 0.01 0.61 *** 74
448
449
450
Christina et al., preprint 2020
14
451
Fig. 3. Change in seedlings functional traits: above to belowground ratio (ABRATIO), leaf to
452
aboveground ratio (LARATIO), specific leaf area (SLA), root diameter (RD), specific root length
453
(SRL) and specific root area (SRA) depending on growth chamber treatment. T24 and T30
454
corresponded to the ambient and elevated temperature treatments, respectively. Wet and Dry
455
corresponded to the watering treatment. Significant difference between native (blue) and
456
invasive (red) populations are indicated by ns, (.), * and ** for p value > 0.1, <0.1, <0.05 and
457
<0.01, respectively.458
459
460
461
462
463
464
465
466
467
468
469
Christina et al., preprint 2020
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3.4. Phenotypic plasticity and local adaptation
470
While no difference has been found in terms of functional traits plasticity between native and
471
invasive populations (Fig. 4), plasticity index (PI) was variable depending on population and
472
function traits. PI coefficient of variation range from 24 to 53% with the lowest variations
473
observed in RD and the highest variations in SRL. Some of these PI were correlated with
474
average performance traits at the population (Table 5). Within the T30 x wet treatment average
475
population height was correlated with PI - SRL (ρSPEAR = 0.6 *) and increased from around 25
476
mm to 45 mm (Fig. 5). Within the T30 x dry treatment, mortality rate was also significantly
477
correlated with PI – SRL (ρSPEAR = - 0.52 *) and mortality was only observed in population with
478
PI – SRL < 0.2. Finally, root area was correlated with PI – ABRATIO and increase from 10 cm²
479
to 20 cm² with increasing ABRATIO. Average seedlings performance at the population levels
480
were also correlated in some case with the climate of origin of the populations (Worldclim
481
index). In particular, mortality rate was correlated with the average daily temperature (ρSPEAR =
482
-0.45 *, Table 5). While populations located in environment with TMEAN < 14°C showed a highly
483
variable mortality, populations located in environments with TMEAN > 14°C showed almost no
484
mortality and were exclusively invasive populations (Fig. 5.). Under well-watered conditions
485
(T30 x wet), average seedlings height per populations was correlated with PPTWARMQUARTER
486
(ρSPEAR = 0.45 *, Table 5). Finally, roots area was also correlated with TDRYQUARTER (ρSPEAR =
-487
0.56 *). On the contrarty, seedlings biomass were not correlated with either plasticity index or
488
climate of origin (Table 5). For its part, leaf area showed a tendency to increase with
489
PI – ABRATIO and PI – LARATIO but the p value was only < than 0.1.
490
491
492
493
494
Fig 4. Functional traits plasticity index at the population levels depending of native or invasive
495
origin. Difference between origin of populations were tested using t.test and indicated as “ns”
496
and (.) when non-significant and p < 0.1, respectively. Functional traits description are given in
497
Table 2.
Christina et al., preprint 2020
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499
500
Table 5. Spearman correlation between average performance traits at the population level,
501
functional traits plasticity indices and environment of origin. P values were abbreviated as (.),
502
*, **, *** when lower than 0.1, 0.05, 0.01,0.001, respectively. The number of poluations (n)
503
used in the correlation are indicated.
504
505
Mortality rate H LA TDM RDM RA
Treatment T30 x Dry T30 x Wet T30 x Dry n Plasticity index PI – ABRATIO -0.11 -0.02 0.47 (.) 0.35 0.28 0.55 * 15 PI – LARATIO -0.24 0.05 0.48 (.) 0.19 0.09 0.19 15 PI – SLA -0.16 0.06 -0.16 -0.19 -0.19 0.01 14 PI – RD 0 0.01 -0.43 -0.23 -0.14 -0.35 15 PI – SRL -0.52 * 0.60 * -0.1 -0.32 -0.35 -0.21 15 PI – SRA 0.23 0 -0.24 -0.19 -0.15 -0.31 15 Climate of origin TMEAN -0.45 * 0.17 0.32 0.25 0.28 0.09 20 TDRYQUARTER 0.24 -0.41 (.) -0.26 -0.30 -0.34 -0.56 * 20 PPTANNUAL -0.23 0.44 (.) 0.19 0.11 0.2 0.15 20 PPTWARMQUARTER -0.31 0.45 * 0.22 0.16 0.27 0.2 20
506
507
508
509
510
511
512
513
Christina et al., preprint 2020
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514
Fig. 5. Change in mortality rate, average seedling height and average root area at the population level
515
with phenotypic plasticity index at the population level (specific root length, PI – SRL, and above to
516
belowground ratio, PI – ABRATIO) and the average climatic data of the environment of origin (average
517
daily temperature – TMEAN, precipitation of the warmest quarter – PPTWARMQUARTER and average daily
518
temperature of the driest quarter – TDRYQUARTER). The treatment were the traits were average are
519
indicated (T24 x Wet or T30 x Dry). The spearman correlation coefficient are given (ρSPEAR) and
520
significant correlation (p < 0.05) are indicated by *. A polynomial smooth regression on all populations
521
was added for visual purpose. As an indication, native and invasive populations are indicated by blue
522
and red points, respectively.
523
524
525
526
527
528
529
Christina et al., preprint 2020
18
4. Discussion
530
531
4.1. Establishment and temperature barrier at the climatic niche margin
532
Assessing whether the environmental niche of a species may change between different
533
geographical areas or time periods is extremely important for predicting the spread of invasive
534
species in the context of ongoing climate change (Alexander and Edwards 2010; Guisan et al.
535
2014; Gonzalez-Moreno et al. 2015). During the invasion process, an introduced population
536
can fail to establish because individuals in the population do not survive or cannot reproduce.
537
Such failure could result from factors associated with the species (e.g. reproductive rate or
538
specialist species), the location (e.g. presence of enemies or absence of mutualists),
539
stochastic features of the individual introduction event (especially propagule pressure) or, often
540
their interaction. Despite having different responses to extreme temperatures, the tolerance to
541
temperature stress might be critical for germination and survival of seedlings of invasive plants.
542
While rising global temperatures might facilitate the survival and reproduction of invasive
543
species in regions where they could not have existed before (Walther et al. 2009), extreme
544
temperatures events can reduce invasive plant competitiveness if conditions become
545
unsuitable (Hellmann et al. 2008).
546
The results described in this study suggest that the temperature tolerance at the thermal niche
547
margin may change between native and invasive populations, depending on their adaptation
548
to different climatic habitats and interaction with other abiotic factors (such as water
549
availability). As an example, the mortality rate of gorse under combined elevated temperature
550
and drought was higher for native seedlings that invasive seedlings (except for seedlings from
551
New Zealand, Table S1, featuring a climate similar to that in the native areas). A similar pattern
552
was observed in a greenhouse experiment with Ulmus pumila seedlings (Hirsch et al., 2016),
553
where mortality rate of seedlings from native populations from China was greater than of those
554
from non-native populations from Argentina and the U.S.A under various watering and
555
temperature treatments. Change in gorse seedlings thermal and drought tolerance between
556
invasive and native populations may be factors explaining the climatic niche shift observed at
557
the global scale by Christina et al. (2019) and the niche expansion of this species in South
558
America (Hernandez-Lambraño et al., 2016).
559
560
4.2. Phenotypic divergence and seedling performance
561
Among the most influential hypotheses about plant invasion, the Evolution of Increased
562
Competitive Ability hypothesis (EICA) states that, in the absence of enemies, exotic plants
563
evolve in the allocation of resources, from defense to reproduction or to growth (Blossey and
564
Notzold 1995). This increase in vegetative growth and/or reproductive effort, for some species,
565
would result in a better competitive ability of the invasive species in the introduced ranges (Zou
566
et al., 2007; Ordonez et al., 2010; Heberling et al., 2016). In terms of vegetative growth, our
567
study showed a greater height growth rate for invasive gorse populations than native
568
populations in the early phases of the invasive process (seedlings establishment) under
569
optimal conditions (warm and wet). This observation is in accordance with previous studies
570
showing an increase in vegetative growth (Hornoy et al., 2011) and reproductive effort (Udo et
571
al., 2017) in introduced Ulex europaeus populations compared to native ones.
572
The better performance of gorse seedlings from invasive populations in extreme environments
573
may result from phenotypic divergence with native populations. For example, while in our study
574
root biomass of seedlings from native populations decreased due to drought, invasive
575
Christina et al., preprint 2020
19
seedlings succeeded into maintaining their root biomass under drought, which could explain576
the greater drought resistance of invasive compared to native populations. Accordingly,
577
seedlings populations with the lowest mortality were populations with the highest RD and SRA.
578
In another study, Song et al. (2010) focused on the impact of extreme high temperatures on
579
Wedelia seedlings. They found that invasive Wedelia (Sphagneticola sp. Asteraceae) suffered
580
less inhibition in terms of growth rates due to high temperature than the native Wedelia, which
581
was consistent with the change of photosystem II activity and efficiency, as well as net
582
photosynthetic rate between native and invasive seedlings. Similarly, focusing on cellular
583
photosynthetic metabolism, Duarte et al. (2016) showed that Sphagneticola maritima (native
584
in Western Europe marshes) and S. patens (American species invasive in Western Europe)
585
have a different thermal tolerance. Accordingly, many studies support that rising temperatures
586
may increase the risk of invasion (Bradley et al. 2010; Verlinden and Nijs 2010; Wang et al.
587
2011), which seems to be in contradiction with a meta-analysis showing that native and
non-588
native plants largely respond similarly to climate manipulations (Sorte et al. 2013).
589
Nevertheless, this meta-analysis reports very few plant studies in which extreme temperatures
590
were manipulated.
591
592
4.3. Phenotypic plasticity during seedling stage
593
Invasive species often present phenotypic plasticity that improves species adaptation to new
594
ecosystems (Lavergne and Molofsky, 2007) which could therefore be an important contributor
595
to invasion success (Davidson et al. 2011). The phenotypic plasticity could improve survival
596
rates during the initial establishment in a new environment (Ghalambor et al. 2007). In the
597
current study, we have found no difference in phenotypic plasticity at the population level
598
between native and invasive populations, contrary to previous studies on mature gorse where
599
invasive gorses were more plastic in response to shading (Atlan et al., 2015). Nevertheless,
600
this study highlighted how populations with highest phenotypic plasticity were more
drought-601
tolerant (i.e. lower mortality). Similarly, populations with highest phenotypic plasticity in SRL or
602
ABRATIO were also population with the highest growth rate in height under optimal conditions
603
(warm and wet) and root development under dry conditions, which is crucial in terms of light,
604
water and nutrients acquisition strategies for young seedlings. Such plasticity could lead to an
605
increase in competitive ability in invasive areas.
606
It is crucial to assess the importance of phenotypic plasticity in response to climate as this
607
allows evaluating whether invasive plants could reach and colonize ecosystems outside of
608
their native climatic niche or not (Sexton et al., 2002). Many recent studies have revealed
609
phenotypic plasticity between native and invasive plants on various mechanisms such as
610
sexual and vegetative reproductions (Xu et al., 2010), fitness-related traits (photosynthetic
611
capacity, survival and growth, Molina-Montenegro et al., 2016, Martinez and Fridley, 2018),
612
and in response to abiotic factors (e.g. water availability Nguyen et al. 2016). The role played
613
by the species’ ability to cope with changing conditions will be probably most important at the
614
margins of the distribution range of the species, where management efforts should be
615
concentrated once the species is naturalized in order to prevent its spread.
616
617
618
619
620
621
Christina et al., preprint 2020
20
4.4. Local adaptation to climate
622
It has been often suggested that rapid evolution of local adaptation to novel environments may
623
enable invasive plant species to thrive across a broad range of habitats in their introduced
624
ranges (Colautti and Barrett, 2013; Buswell et al., 2011; Li et al., 2014). Unlike native plants
625
with a much longer residence time, invasive plant species typically have a relatively short
626
residence time in their introduced ranges, typically decades or just a few centuries (Pysek &
627
Jarosık 2005; Hulme 2009; Colautti & Lau 2015). Nonetheless, a meta-analysis comparing
628
native and invasive species in the same environments concluded that invasive species were
629
as adapted as the native ones (Oduor et al., 2016).
630
Considering gorse, Christina et al. (2020) highlighted how a niche shift occurred in introduced
631
areas in comparison to climatic niche of native gorse. Our results here confirmed the local
632
adaptation of invasive populations to warmer environments, which could explain their higher
633
tolerance to warm and dry environments and therefore there niche expansion in Australia,
634
North America or South Africa (Christina et al., 2020). The evolution of phenotypic traits in
635
invasive gorse populations was demonstrated in common garden experiments (Hornoy et al.,
636
2011). This evolution was facilitated by the hexaploid karyotype of the species, and by its high
637
genetic polymorphism in both native and invasive populations (Hornoy et al., 2013).
638
Considering that in the majority of introduced regions, invasion occurred since XXXs, an
639
explanation to the rapid evolution of local adaptation could result from the release of natural
640
enemies (EICA Hypothesis; Blossey and Notzold 1995; Joshi and Vrieling 2005). Indeed, the
641
specific weevil Exapion ulicis, that can eat up to 80% of the seeds in the native region, was not
642
introduced in the invaded regions as the same time as the plant (even if it was further
643
introduced in most regions for biological control). The release from this predator may have
644
relaxed the genetic constraints resulting by the complex strategies of seed predation
645
avoidance (Atlan et al., 2010), facilitated the rapid adaptation to new climate and contributed
646
to the niche expansion in introduced regions.
647
648
5. Conclusion
649
The study assessed the influence of the interaction between extreme temperature (at the niche
650
margin) and drought on establishment success (seedling survival and growth) of the invasive
651
gorse. Our results highlighted some seedlings phenotypic divergences in terms of above and
652
belowground development between native and invasive gorse, which could explain the
653
observed greater drought resistance of invasive populations at extreme temperature.
654
Population performances and survival were correlated to both local adaptation to climate as
655
well as phenotypic plasticity, even if no evidence of a higher phenotypic plasticity in invasive
656
populations than native ones has been observed. A better understanding of the phenotypic
657
divergences and plasticity between native and invasive gorse populations at the margins of
658
their climatic distribution range is a key step to highlight where management efforts should be
659
concentrated once the species is naturalized in order to prevent its spread, especially in higher
660
elevations.661
662
663
664
665
666
667
Christina et al., preprint 2020
21
Acknowledgements
668
This study was financially supported by the MARIS ANR project (Agence Nationale de la
669
Recherche, grant ANR-14-CE03-0007-01) and INRA institute (Institut National de la
670
Recherche Agronomique). We are grateful to the UMR SAVE (in particular D. Thierry, P. Rey,
671
J. Jollivet and J. Roudet) for their support with the growth chambers. We thank N. Udo (UMR
672
ECOBIO), A. Atlan (UR ESO), M. Tareyre-Renouard (UMR ECOBIO), S. Niollet and N.
673
Gallegos (UMR ISPA) for the support in collecting seeds and F. Delerue for his advice. We are
674
grateful to the Parque Nacional de los Picos de Europa (Spain) and Cabildo de Tenerife
675
(Canary Island) for their authorization to collect gorse seeds. We thank the landowners with
676
whom we have had access to their land to study and collect gorse seeds
677
678
679
680
Authors’ contributions681
CM, GM, DJC and BM conceived the ideas and designed methodology. LA, XJ, CPW, NPZ ,
682
SJRA and GC collected the seeds in the different countries and advised on the methodology.
683
CM, GM, BM and GC collected the data and CM and GM analysed them. CM and GM led the
684
writing of the manuscript. All authors contributed critically to the drafts and gave final approval
685
for publication.686
687
Data accessibility688
The data used in this study will be made freely available in the CIRAD or INRA data verse
689
during the revision process.
690
691
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