Plant reproduction in the alpine landscape Reproductive ecology, genetic diversity and gene flow of the rare monocarpic Campanula thyrsoides in the Swiss Alps INAUGURALDISSERTATION zur Erlangung der Würde eines Doktors der Philosophie vorgelegt der Philosophisch-Naturwissenschaftlichen Fakultät der Universität Basel von HAFDÍS HANNA ÆGISDÓTTIR aus Hafnarfjörður, Island Basel, 2007 Genehmigt von der Philosophisch-Naturwissenschaftlichen Fakultät auf Antrag von Prof. Dr. Jürg Stöcklin Ass. Prof. Marianne Philipp Basel, den 16. Oktober 2007 Prof. Dr. Hans-Peter Hauri Dekan Mig hefur leingi lángað til að verða flökkukona... Það hlýtur að vera gaman að sofa í lýngbrekkum hjá nýbornum ám. Halldór Laxness. Íslandsklukkan. Hið ljósa man, 2. kafli. _____________________________________________________________________ Table of Contents Chapter 1 General introduction 3 Chapter 2 No inbreeding depression in an outcrossing alpine species: 17 The breeding system of Campanula thyrsoides H.H. Ægisdóttir, D. Jespersen, P. Kuss & J. Stöcklin Flora (2007) 202: 218-225 Chapter 3 Pollination-distance effect on reproductive within and between 35 population of a rare monocarpic perennial plant from the Alps H.H. Ægisdóttir, P. Kuss & J. Stöcklin Chapter 4 Development and characterization of microsatellite DNA 57 markers for the Alpine plant species Campanula thyrsoides H.H. Ægisdóttir, B. Koller, P. Kuss & J. Stöcklin Molecular Ecology Notes (2007) 7 (6): 996-997 Chapter 5 High genetic diversity and moderate population differentiation 65 despite natural fragmentation in a rare monocarpic alpine plant H.H. Ægisdóttir, P. Kuss & J. Stöcklin Chapter 6 Spatial differentiation and genetic differentiation in naturally 93 fragmented alpine plant populations P. Kuss, A.R. Plüss, H.H. Ægisdóttir & J. Stöcklin Chapter 7 Evolutionary demography of the long-lived monocarpic 119 perennial Campanula thyrsoides in the Swiss Alps P. Kuss, M.Rees, H.H. Ægisdóttir, S.P. Ellner & J. Stöcklin Chapter 8 The biological flora of Central Europe: Campanula thyrsoides L. 169 P. Kuss, H.H. Ægisdóttir & J. Stöcklin Perspectives in Plant Ecology, Evolution and Systematics (2007) 9 (1): 37-51 Chapter 9 Summary and General discussion 199 Acknowlegement 211 Curriculum vitae 213 _____________________________________________________________________ 1 _____________________________________________________________________ _____________________________________________________________________ 2 GENERAL INTRODUCTION _____________________________________________________________________ Chapter 1 General introduction _____________________________________________________________________ 3 CHAPTER 1 ___________________________________________________________________________________ Alpine ecosystems and fragmentation Habitat fragmentation, i.e. the process of large continuous habitats being subdivided into several smaller spatially isolated remnants, is a serious threat to biodiversity in many terrestrial ecosystems and the root cause of many conservation problems (Young et al. 1996; Frankham et al. 2002). Although discussion on habitat fragmentation, habitat destruction and species extinction has largely been confined to the anthropogenic destruction of formally continuous natural habitats, such as temperate grasslands and tropical rainforests (see e.g. Turner et al. 1996; Debinski & Holt 2000), the fragmentation of other ecosystem types should not be disregarded. Alpine ecosystems are commonly described as naturally strongly fragmented, with many microhabitats, created by the pronounced environmental gradients and the heterogeneous topography of alpine landscapes. These landscape characteristics can greatly affect the life of alpine plants (Körner 2003). We are living in an era of global change, not only in the form of increasing habitat fragmentation and destruction, but also as a result of climatic warming and land use changes, which can have serious consequences for the world’s ecosystems (Saunders et al. 1991; Theurillat & Guisan 2001; Walther et al. 2002; Körner 2003). In the alpine life zone, changes in land use, both in the form of more intense pasturing or, the reverse, abandonment of former, traditionally pastured alpine terrain are considered to be the greatest risk to the loss of alpine biodiversity (Körner 2001, 2003). Moreover, alpine ecosystems have repeatedly been put in the spotlight due to their vulnerability to global warming, with its potential impact on snow cover and permafrost as well as upward migration of species and vegetation shifts, which could lower available surface area and affect the plants’ growing conditions (Grabherr et al. 1994; Theurillat & Guisan 2001). With regard to global warming, knowledge on the genetic variability in alpine plants has become particularly important since high genetic diversity is considered essential for plants to keep pace with the changing environment (Booy et al. 2000; Theurillat & Guisan 2001; Till-Bottraud & Gaudeul 2002). This thesis comprehensively studies the effects of natural fragmentation and patchiness on the life of isolated plant populations in the fragmented alpine landscape. The focus is specifically on its effects on plant reproduction, such as mating system _____________________________________________________________________ 4 GENERAL INTRODUCTION _____________________________________________________________________ and inbreeding depression, as well as on the genetic variability and gene flow within and among alpine plant populations. Plant reproduction in the alpine landscape Although, many alpine plant species are long-lived and rely on clonal growth for reproduction (Billings & Mooney 1968; Bliss 1971; Körner 2001), the importance of sexual reproduction, should not be understated, above all in the case of plants living in ever-changing and fragmented environments. Unlike clonal growth, sexual reproduction can by risky, especially for species that are unable to self-pollinate, but it is nevertheless important for alpine plants in order to retain genetic diversity and to develop ecotypic differentiation of traits (Körner 2001). Sexual reproduction in alpine plants is dominated by outcrossing although the majority of alpine plants are also able to self-pollinate (Körner 2001, 2003). That is not surprising bearing in mind that according to Baker’s law, self-compatibility should be favoured in plant species living in isolated populations in a fragmented landscape in order to ensure sexual reproduction if pollination fails (Baker 1955, 1967). Despite self-compatibility being frequent among plants, including alpine plants, many monoecious and hermaphroditic plant species have mechanisms that promote outcrossing and prevent self-fertilization, such as dichogamy or self- incompatibility system (Richards 1997; Byers & Waller 1999). Dichogamy promotes outcrossing by seperating pollen shedding and stigma receptivity in time. It doesn’t however guarantee, outcrossing since multiflowered plants might be self-pollinated with pollen from other flowers on the same plants (geitonogamy). Self-incompatibility (SI) in plants is, conversely, controlled by a SI locus, named the S-locus. The S-locus has many different alleles and pollen is rejected when it carries the same alleles as the plant being pollinated. Plants self-incompatibility systems can be either gametophytic (GSI) or sporophytic (SSI). In GSI systems, the pollen grain must match either of the alleles present in the diploid maternal tissue to be accepted, making semi- compatibility (mating between half-siblings) possible. In contrast, the pollen grains in the less common SSI must match both of the alleles present in the given female parent to be accepted, making semi-compatibility impossible (Richards 1997). _____________________________________________________________________ 5 CHAPTER 1 ___________________________________________________________________________________ Inbreeding- and outbreeding depression Outcrossing in plants is often maintained by inbreeding depression, defined as the reduction of fitness due to selfing or mating between close relatives. The genetic causes of inbreeding depression are usually considered to be due to partial dominance, overdominance, or by combination of both. Partial dominance, which is sufficient to explain most inbreeding depression in higher plants, is the result of expression of deleterious recessive alleles at homozygous loci. The less common overdominance could lead to inbreeding depression, in which heterozygotes have a higher fitness than both types of homozygotes (Charlesworth & Charlesworth 1987; Dudash & Fenster 2000; Keller & Waller 2002). Inbreeding depression is expected to be more pronounced in historically large and outcrossing populations than in mainly selfing populations or in populations that have experienced repeated bottlenecks. The reason for this is that the latter mentioned populations (selfing, repeated bottlenecks) have been purged of their genetic load due to selection (Charlesworth & Charlesworth 1987; Barrett & Charlesworth 1991). The risk of inbreeding depression is not the only risk that plant populations might be faced with. If plants get pollinated with pollen from distant populations, their offspring might suffer from an outbreeding depression. Two mechanisms are thought to cause outbreeding depression. Firstly crosses with distant pollen might make offspring less adapted to local environments than their parents due to disruption of adaptation to local biotic and abiotic conditions, and