Introduction
Extinction and local extirpation with consequent species
turnover are expected to occur in cold environments because of reduced
habitat suitability for resident species and improved conditions for low
elevation or low latitude migrants (Gottfried et al. 2012, Pauli et al.
2012, Porro et al. 2019). Hence, the distribution of ‘cold-adapted’
species is projected to undergo severe range loss in the next future
(Steinbauer et al. 2020). Arctic species are predicted to experience
range contraction at their southern trailing-range locations while the
distribution range of northern, leading-edge populations may even expand
beyond their historical cold border by migrating poleward (Hickling et
al. 2006). For alpine species, the distribution range of lower-elevation
trailing-edge populations is expected to shrink, unless these peripheral
plants possess full or partial adaptations to expected climate warming
scenarios (Dullinger et al. 2012, Angert et al. 2020). Cold-adapted
alpine species are also predicted to shift their ranges towards colder
locations, i.e., towards higher elevations (Lenoir et al. 2008) or in
micro topographic niches (Körner and Hiltbrunner 2021). Distribution
shifts triggered by climate change are projected using correlational
bioclimate envelope models, which can overestimate species losses
because key aspects such as demographic dynamics, plant plasticity, etc.
are ignored by models (Randin et al. 2009, Niskanen et al. 2017, Casazza
et al. 2021). Phenotypic plasticity, i.e. the responsiveness of plants
to changing environment, consists in the capacity of a genotype to
express different phenotypes under diverse environmental conditions
(Kawecki and Ebert 2004, Garland and Kelly 2006, Leimu and Fischer
2008). If the performance of populations is correlated with
environmental conditions at the provenance site this can be interpreted
as a test of local adaptation, although local adaptation may be marginal
in certain species and environments (Macel et al. 2007, Beierkuhnlein et
al. 2011). Peripheral trailing-edge plant populations often host unique
genetic traits when compared to core populations (Eckert et al. 2008,
Mathiasen et al. 2021). Local adaptation may be particularly
important at range limits where the selective pressure of climatic
conditions on a species’ population is usually stronger than in its
range centre and where genetic recombination may be limited due to
geographic isolation (Choler et al. 2004, Kawecki 2008, Paul et al.
2011). It is less clear whether some of the unique genetic traits of
peripheral populations may be useful to cope with climate change. Abeli
et al. (2018) hypothesized that peripheral plant populations of
cold-adapted species may already be adapted to local warm conditions,
especially in southern refugia. This seems to be supported by long-term
stability of several trailing-edge populations (Abeli et al. 2012,
Mathiasen et al. 2021) and eventually by models in which demographic and
genetic simulations are included (Cotto et al. 2017).
Results of common garden experiments suggest that genotypes from
warmer sites in many cases have an advantage in terms of demographic
traits compared to genotypes from colder sites when exposed to warming
(Peterson et al. 2016, Bontrager and Angert 2019). For example,
individuals of Eucalyptus grandis experiencing natural long-term
exposure to heat waves have higher capacity to express protective
proteins than individuals from populations with lower exposure to
extreme weather events (Maher et al. 2019). Dickman et al. (2019)
recorded adaptation to drought in seeds from peripheral low-elevation
populations of Mimulus laciniatus. On the other hand,
there is increasing empirical evidence that plants can react to climate
warming with mechanisms involving phenotypic plasticity (Schneider
2022). Plasticity allows plants to grow under variable conditions and to
cope with environmental changes by immediate (plastic) responses in the
absence of genetic (evolutionary) variation. There is strong evidence
that phenotypic plasticity is directly conditioned by genotypic
diversity (Eller et al. 2017). However, phenotypic plasticity can also
derive from changes in gene expression controlled by epigenetic
response, which confers plants the ability to respond in the short term
to a rapidly changing environment (Nicotra et al. 2010, Pagliarani and
Gambino 2019, Ashapkin et al. 2020). Furthermore, phenotypic plasticity
can be caused by the intrinsic ability of plants to acclimate to
changing ecological conditions (Valdés et al. 2019). On the other hand,
when environmental conditions exert strong selective pressures on
organisms, like in ecologically/geographically peripheral populations,
useful trait selection and stabilisation may result in loss of
plasticity (Anstett et al. 2021; Usui et al. 2023). Whatever the
mechanisms involved, phenotypic plasticity plays an important role in
explaining adaptation of cold-climate plants to warming climate. For
example, high level of phenotypic variation buffers the alpine cliff
plant Heterotheca brandegeei from the negative impacts of warming
and drought in southern North America (Winkler et al. 2019). For
arctic-alpine plant species it is more problematic to define where core
areas and marginal areas are located within their highly fragmented
distribution ranges. Therefore, it is conceptually difficult to evaluate
the geographic location of trailing-edge vs. leading-edge populations of
arctic-alpine species. In fact, arctic-alpine species underwent multiple
re-colonization events during the climatic vicissitudes that occurred
during the Pleistocene. So, arctic-alpine species with similar
present-day distributions may have had different glacial refugia and
their distribution range may thus have differed strongly during the
Pleistocene (Brochmann and Brysting 2008). This has profound implication
on the putative genetic differentiation among populations. Marginal
populations of many plant and animal species often show lower genetic
diversity and high differentiation of molecular markers compared to
conspecific core populations (Van Rossum et al. 2004, Tsumura et al.
2007, Eckert et al. 2008). Based on their complex colonization history,
populations of arctic-alpine species may reflect differing pathways of
genetic differentiation, possibly untethered by latitude. Furthermore,
populations located at the southern margin of the present-day
distribution area do not represent the warmest sites within the species’
range (Abeli et al. 2015). This may constitute a mismatch between
geographic and ecological marginality (Soule 1973). It is generally
assumed that the distribution range of southern populations of
arctic-alpine species will shrink unless these peripheral plants possess
full or partial adaptations to expected climate warming scenarios (Abeli
et al. 2018, Dullinger et al. 2012). The distribution range of northern
populations may even expand beyond their historical cold border.
However, northward expansion will be precluded if warming negatively
impacts growth of plants from northern populations at cooler
temperatures compared to plants from southern populations (DeMarche et
al. 2018). Interestingly, a recent study predicted stronger decline of
arctic-alpine species at the northern range margins than at southern
locations. (Niskanen et al. 2019).
In this study, we used the Alpine catchfly [Viscaria
alpina (L.) G. Don] for assessing the potential of northern and
southern populations of an arctic-alpine species to cope with a warming
climate. V. alpina represents an excellent model to examine
multi-faceted responses of different populations to global warming. In
fact, V. alpina has a broad distribution range that consists in a
vast high-latitude area extending from North America to eastern Eurasia
and a set of smaller mid-latitude mountain areas prevalently located in
southern Europe, from the Pyrenées and the Cantabrian mountains to the
Alps and the Northern Apennines (Nagy 2013). V. alpina exhibits
relatively high genetic diversity among populations whose locations
differ strongly in terms of climatic, altitudinal and edaphic features
(Haraldsen and Wesenberg 1993). Most important, both the southern and
the northern populations of V. alpina span a wide thermal range
with differences of up to 7-9 °C in average mean annual temperature
(Nagy 2013). To assess the ability of V. alpina to cope with a
warmer climate, we selected four European populations, two from
a northern area and two from a southern area. In both areas one of the
two populations stemmed from a colder site and the other from a warmer
site with mean annual temperature difference of about 5 °C between the
two sites. We cultivated plants originated from seeds collected
from the four populations at warm temperature and assessed their
responses in terms of morphological and ecophysiological traits based on
phenotypic short-term response to high temperature. Furthermore, we
cultivated a further set of plants under more extreme thermal conditions
that simulated a short-term heat spell mimicking heat wave conditions.
Indeed, the frequency of heat waves is increasing in recent years which
results in compound effects of heat and drought (Mukherjee and Mishra
2021) besides the single effects of higher temperature. Experiments were
conducted on seedlings, as this early life stage is highly sensitive to
variation in climate and represents a major bottleneck to species
recruitment, playing a key role in the distribution and dynamics of
plant populations (Vázquez-Ramírez and Venn 2021).