Leaf anatomy of two reciprocally non-monophyletic mountain plants (Heliosperma spp.): does heritable adaptation to divergent growing sites accompany the onset of speciation?
Leaf anatomy of two reciprocally non-monophyletic mountain plants (Heliosperma spp.): does heritable adaptation to divergent growing sites accompany the onset of speciation?
Clara Bertel 0
Peter Schönswetter 0
Božo Frajman 0
Andreas Holzinger 0
Gilbert Neuner 0
Handling Editor: Peter Nick 0
0 Institute of Botany, University of Innsbruck , Innsbruck , Austria
Evolution is driven by natural selection, favouring individuals adapted in phenotypic traits to the environmental conditions at their growing site. To shed light on ecological and (epi-) genetically based differentiation between Heliosperma pusillum and Heliosperma veselskyi, two reciprocally non-monophyletic, but morphologically and ecologically divergent species from the south-eastern Alps, we studied various leaf anatomical traits and investigated chloroplast ultrastructure in leaves of the two species grown either in their natural habitat or in a common garden. The alpine H. pusillum occurs in open, wet rock habitats, whereas its close relative H. veselskyi is restricted to dry, shady habitats below overhanging rocks in the montane belt. H. pusillum exhibited higher thickness of leaves and palisade layers as adjustments and/or adaptations to higher irradiance and a higher stomatal area index reflecting better water availability. Traits were adjusted plastically, but differed between species grown in a common garden, suggesting that the differentiation between the two species is not solely based on phenotypic plasticity but also has a genetic basis. Our study thus supports the hypothesis that differentiation between the highly interfertile species is likely driven by natural selection.
Adaptation; Alpine plants; Environmentally induced speciation; Leaf anatomy; Leaf ultrastructure
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Adaptation to environmental conditions can become manifest
in various phenotypic traits, as natural selection favours
individuals being able to successfully survive and reproduce in a
particular environment (Coyne and Orr 2004). Habitat
heterogeneity, which is particularly pronounced in mountain areas
(Scherrer and Körner 2011), may trigger the formation of
ecotypes within species. Ecotypes originate from differentiation
of populations that are adapted in various phenotypic traits to a
specific microenvironment (Hufford and Mazer 2003; Lowry
2012). Ecotypic differentiation is most likely driven by a
combination of heritable and non-heritable traits (Pfennig et al.
2010; Bonduriansky et al. 2012). Despite the absence of
intrinsic reproductive barriers, ecological isolation may over time
lead to the formation of new species (Lowry 2012).
An example of a recent ecotypic differentiation is provided
by Heliosperma pusillum and Heliosperma veselskyi
(Caryophyllaceae, Fig. 1). The former has a broad distribution
throughout the southern and central European mountain
ranges and occurs in humid, partly sun-exposed rock crevices
and screes in the upper montane to alpine zone (1700–2300 m
a. s. l.; authors’ personal observations). In contrast, H. veselskyi
is restricted to a few scattered populations below cliff overhangs
in the lower montane belt of the south-eastern Alps and
northernmost Balkan Peninsula (500–1300 m a. s. l.; Neumayer
1923; Frajman and Oxelman 2007). Its growing sites are usually
characterised by low irradiance and limited water availability
(Bertel et al. 2016). Due to morphological divergence, both
entities have been described at the species rank and are still
treated as independent species (e.g. Fischer 2008; Frajman and
Oxelman 2007; Poldini 2002). H. pusillum is glabrous or has
sparsely hairy leaves, whereas H. veselskyi is characterised by a
dense indumentum of long multicellular glandular hairs
(Janka 1858; Neumayer 1923; Frajman and Oxelman 2007;
Fig. 1 H. pusillum (a) grows on
alpine scree sites, whereas
H. veselskyi (b) occurs below cliff
overhangs in the montane belt.
H. veselskyi differs morphologically
from its high elevation relative by
broader leaves, which are covered
by a thick indumentum of
multicellular, glandular hairs.
Despite their ecological and
morphological divergence, both
species are genetically
inseparable (photos modified
from Bertel et al. 2016; (a), R.
Flatscher; (b), M. Sonnleitner)
Fischer 2008). Chloroplast and nuclear low copy DNA
sequence data (Frajman and Oxelman 2007; Frajman et al.
2009) as well as highly resolving restriction associated DNA
markers sampled across the nuclear genome (Trucchi et al.,
unpublished) suggest that the two species are phylogenetically
not distinct and that H. veselskyi is inextricably nested within
H. pusillum. H. veselskyi thus rather represents a habitat
specific ecotype, whose disjunct populations have evolved
postglacially from geographically close populations of
H. pusillum. For the sake of simplicity, we treat H. pusillum
and H. veselskyi as species throughout the text in spite of the
lack of consistent genetic divergence and their highly
debatable taxonomic value.
Significant diffe (...truncated)