Escaping to the summits: Phylogeography and predicted range dynamics of Cerastium dinaricum, an endangered high mountain plant endemic to the western Balkan Peninsula
Graphical abstract
Introduction
The Balkan Peninsula is a hot spot of European biodiversity and endemism (Kryštufek and Reed, 2004, Kier et al., 2009). The underlying processes are complex, with environmental stability through geologic history (Hewitt, 2004, Tzedakis, 2004, Médail and Diadema, 2008) and topographic as well as climatic diversity likely acting as key factors (Kryštufek and Reed, 2004). The mountain range shaping the western Balkan Peninsula are the mostly calcareous Dinaric Mountains (Dinaric Alps, Dinarides). Their topography is highly complex, with summits reaching far up into the alpine zone and deeply incised valleys with thermophilous submediterranean vegetation (Surina et al., 2011).
The Dinaric Mountains have been less affected by Pleistocene glaciations than other southern European mountain systems such as the Alps and the Pyrenees (Bognar et al., 1991, Milivojević et al., 2008). The combination of incomplete glaciation and topographical complexity generated multiple glacial refugia which were facilitating strong genetic differentiation on a small geographical scale (Kryštufek et al., 2007, Médail and Diadema, 2008). Divergence in multiple Pleistocene microrefugia has already been highlighted as a key factor for the evolution of intraspecific diversity within the Iberian macrorefugium (‘refugia-within-refugia hypothesis’; Gómez and Lunt, 2007). The few available studies of animal (Podnar et al., 2004, Kryštufek et al., 2007, Ursenbacher et al., 2008, Previšić et al., 2009) and plant species (Frajman and Oxelman, 2007, Surina et al., 2011) suggest that this pattern also applies to biota of the Balkan Peninsula. So far, no general patterns have emerged, and the area remains largely neglected despite of its importance for understanding and conserving European biodiversity on a broader scale (Hewitt, 2004).
Pleistocene climatic fluctuations and gradual warming after the Last Glacial Maximum have likely shaped both phylogeographic structure and today’s highly fragmented distribution of the Dinaric endemic Cerastium dinaricum Beck & Szyszył. (Caryophyllaceae). This (paleo)tetraploid (Niketić et al., 2013) species shows a highly disjunct distribution in the (sub)alpine zone from Mt. Snežnik in Slovenia in the northwest to the Prokletije Mts. in Montenegro in the southeast (Wraber, 1995, Niketić, 2007; Fig. 1). It inhabits north-facing limestone screes, rocky grounds and rock crevices with cold microclimate in the altitudinal range of 1430–2200(2370) m a.s.l. (Niketić, 2007). Cold-adapted species like C. dinaricum likely had larger, more connected distribution ranges during cold stages and were restricted to small, isolated high-altitude habitats during periods of warmer climate (Stewart et al., 2010). The two disjunct partial distribution areas of C. dinaricum differ in topographical complexity – whereas the southeastern part is highly structured with mountain ranges separated by deep valleys, the northwestern part is more homogeneous and lacks obvious barriers. Partly based on the results derived from Edraianthus serpyllifolius, another endemic high-alpine mountain plant of the southern Dinaric Mountains (Surina et al., 2011), we hypothesize that in the south of its range C. dinaricum most likely responded to Quaternary climatic oscillations with altitudinal range shifts on a small geographical scale, whereas in the North horizontal range expansions during cold periods may also have occurred. This scenario results in stronger genetic differentiation among southern populations as compared to northern ones.
Recent continent-wide plant diversity studies on multiple European mountain summits (Gottfried et al., 2012, Pauli et al., 2012) showed increasing impact of global warming in such environments. The underlying process was termed ‘thermophilization’ and results in a progressive decline of more cold-adapted species and an increase of more warm-adapted species (Gottfried et al., 2012). The effects of the current climate warming are anticipated to have strong deleterious effects for cold-adapted, high-alpine biota of the Dinaric Mountains, as their elevation is substantially lower compared to, e.g., the Alps. Consequently, the possibilities for upward altitudinal migrations of alpine biota are very limited. This seems especially relevant for rare endemics such as C. dinaricum, whose populations only comprise a few individuals at some sites (Wraber, 1995; B. Frajman, D. Kutnjak, personal field observations). Accordingly, the risk of habitat loss by upward displacement is considerable (Rull and Vegas-Vilarrúbia, 2006, Gottfried et al., 2012). Further, C. dinaricum is also a species of high conservation priority in Europe, listed in the Annex II of the EU Habitats directive, and therefore a qualification species for the NATURA 2000 network of protected areas.
Here, we examine the phylogeographic structure of C. dinaricum using amplified fragment length polymorphisms (AFLPs), nuclear ribosomal ITS and plastid trnT–ndhJ sequences as well as relative genome size data obtained from almost all known extant populations. Our specific aims were (i) to unravel the species’ response to Quaternary climatic oscillations and to test the refugia-within-refugia hypothesis; as well as (ii) to compare the genetic structure between the topographically less structured northwestern and the more complex southeastern part of the occurrence. Finally, (iii) we search for evolutionary significant units (ESUs) within the species and (iv) model the contraction of its distribution area under increasing global warming. The results will provide a better understanding of the processes, which have shaped the spatial distribution of biodiversity on the western Balkans and will also be relevant for designing specific conservation strategies for this highly threatened species. The gained insights into the range dynamics of this cold-adapted southern European species will additionally contribute to our understanding of influences and risks of global warming in the near future.
Section snippets
Study species and sampling
We visited 14 localities of C. dinaricum known from literature and/or herbaria along its entire distribution range. Presence of the species was confirmed in 10 localities (for details see Table 1 and Fig. 1) and leaf material from four to thirty individuals per population was sampled in silica gel. Cerastium dinaricum was also reported from two localities positioned within the distribution gap between populations 4 and 5 (Fig. 1, see Niketić, 2007, for details), but we were not able to find it
Genome size variation
The estimated DNA ploidy level was the same for all measured samples (the FCM histograms of population 6 were discarded from further analyses due to the high CV of the measurements, but evidently suggested the same ploidy level as measured for the other populations). Average relative genome size ranged from 0.301 in population 1 to 0.327 in population 8 (Table 1), with evident bimodal distribution. One mode corresponds to the northwestern populations (populations 1–4) and the other to the
Discussion
The rare and disjunctly distributed cold-adapted mountain plant Cerastium dinaricum, which is endemic to the Dinaric Mountains, the backbone of the western Balkan Peninsula, exhibits a deep phylogeographic split strongly supported by nuclear data (AFLPs and relative genome size; Fig. 2, Fig. 3) splitting the northwestern populations 1–4 (NW group) from the southeastern populations 5–10 (SE group). The groups are separated by a distribution gap of about 100 km (Fig. 1). The northern border of the
Acknowledgments
The study was financed by the European Commission in the SEE-ERA.NET PLUS framework (project ‘BalkBioDiv’ to PS) and the Ministry of Education, Science and Technological Development of the Republic of Serbia (Grant 173030). The sampling permission for C. dinaricum on Snežnik was granted by the Slovenian Environment Agency ARSO (35603-6/2010-4). Thanks to Ivana Rešetnik, Sandro Bogdanović and Antun Alegro for help with sampling and to Marianne Magauer, Daniela Pirkebner and Manuela Winkler for
References (72)
- et al.
Reticulate phylogenetics and phytogeographical structure of Heliosperma (Sileneae, Caryophyllaceae) inferred from chloroplast and nuclear DNA sequences
Mol. Phylogenet. Evol.
(2007) The use of ‘altitude’ in ecological research
Trends Ecol. Evol.
(2007)- et al.
Pleistocene glacial relief of the central part of Mt. Prokletije (Albanian Alps)
Quatern. Int.
(2008) - et al.
Mitochondrial phylogeography of the Dalmatian wall lizard, Podarcis melisellensis (Lacertidae)
Org., Div. Evol.
(2004) - et al.
Inferring the history of the polyploid Silene aegaea (Caryophyllaceae) using plastid and homoeologous nuclear DNA sequences
Mol. Phylogenet. Evol.
(2001) - et al.
Molecular phylogeography of the nose-horned viper (Vipera ammodytes, Linnaeus (1758)): evidence for high genetic diversity and multiple refugia in the Balkan peninsula
Mol. Phylogenet. Evol.
(2008) - et al.
Pleistocene distribution range shifts were accompanied by breeding system divergence within Hornungia alpina (Brassicaceae) in the Alps
Mol. Phylogenet. Evol.
(2010) - et al.
Validation of species-climate impact models under climate change
Glob. Change Biol.
(2005) - Biomatters Ltd., 2010. Geneious v5.5. Biomatters Ltd., New Zealand,...
- et al.
Glaciation traces on the Northern Velebit
Geografski Glasnik
(1991)