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Facilitation: a long-time forgotten interaction due to the predominance of competition
Until the mid-nineties, ecological theories and models have considered only negative interactions (e.g. Grime 1973; Connell 1978; Huston 1979; Tilman 1980, 1982), even though positive interactions (i.e. facilitation) have been reported in experimental studies [Niering et al. 1963 and Turner et al. 1966 in Callaway 2007; Hunter & Aarssen 1988] and ecological theories (Clements 1916). This is because negative interactions (e.g. competition or interference) were thought to be the main biotic filter structuring plant communities (Goldberg & Barton 1992). However, two schools of thoughts regarding the strength of competition along productivity gradients [in plant community ecology] emerged over the time. This divergence in thoughts was known as the “Grime-Tilman debate”. Grime considered that [aboveground] competition decreases from high to low levels of productivity, and interactions vanish under stressful conditions (Grime 1973, 1977). In contrast, Tilman founded his “resource-ratio” theory by arguing that when productivity decreases, competition for limiting resources switches from aboveground to belowground, and thus competition is held constant (Tilman 1980, 1982). Both theories have gained significant attention in the field of plant ecology. Grace (1991) argues that the “Grime-Tilman debate” is due to differences in the definitions of some terms used by each of these authors (e.g. ‘competition’, for Grime, it is the capacity for resource capture and the mechanism by which a plant suppresses the fitness of a neighbour; for Tilman, competitive success is the ability to draw resources to a low level and to tolerate those low levels – to have a low equilibrium resource requirement). Welden & Slauson (1986) tried resolving this ‘debate’ by clarifying the difference between the intensity and the importance of competition (see Box 1 for the definition of ‘competition intensity’ and ‘competition importance’). Competition importance has been proposed to explain Grime’s (1973) theory on competition, whereas intensity explains Tilman’s theory – competition intensity stays constant along the productivity gradient, but switches from aboveground to belowground in unproductive environments – (Welden & Slauson 1986; Grace 1991).
Until recently, negative interaction have been the primary concern of studies in plant community genetics (e.g. Whitlock et al. 2007; Lankau & Strauss 2007; Johnson et al. 2008; Bossdorf et al. 2009; Silvertown et al. 2009; Genung et al. 2011). However, [as already said] facilitation has been found in theoretical and experimental studies (Clements 1916; Hunter & Aarssen 1988). For instance, Clements (1916) argues that plants themselves cause succession to occur by improving site factors (e.g. light capture by leaves, production of detritus, water and nutrient uptake, nitrogen fixation), which allows the establishment of plants of the next succession stage. This means that plants of one stage directly ‘facilitate’ plants of the next succession stage. Though, the little attention given to facilitation and the predominance of competition for a long time in research fields such as ecology is likely because facilitation could go undetected, as it appears weaker than competitive mechanisms (Gross 2008).
Evolution, natural selection and adaptation
In The Origin of Species (1859), Charles Darwin presents evidence of evolution. He argues that all living beings are descendants of an earlier species (shared a common ancestral parent at some point in their history), and explains the existence of evolution by proposing the mechanism of natural selection, which is an important process – but not the only one – by which evolution takes place within a population of organisms. The forces of natural selection act on the apparent characters (phenotype) of an organism; however, only when natural selection acts on heritable characters – selecting the genotype expressing ‘the most appropriate’ phenotype to ‘fit’ its environment – evolution can occur (Whitham et al. 2003), eventually leading to new species or ecotypes (Grassein et al. 2010). As said above, natural selection is not the only mechanism of evolution but one of the processes that leads to it. Since the time when Charles Darwin and Alfred Russel Wallace first came up with The Theory of Evolution, the growing knowledge has led to the ‘evolution’ of this theory giving birth to the Modern Synthesis (or Modern Evolutionary Synthesis) theory [Julien Huxley in Evolution: The Modern Synthesis (1942)]. This theory recognizes several possible mechanisms of evolution other than natural selection, such as genetic drift (or allelic drift), mutations, and migration, which also play a role in the evolution of new species. Also, phenotypic plasticity is believed to be an evolutionary adaptation to environmental variation (Sultan 1995), allowing individuals to change their phenotypes in order to ‘fit’ a new environment.
Evolution implicates two related phenomena: adaptation20 and speciation21. Over the course of time, species struggle to cope with their changing environment, which requires them to modify their phenotypes in ways that permit them to succeed and persist in their environment. These changes in one species can result in the emergence of two or more new species, leading to the multiplication of the number of species.
Local adaptation: the contribution of genetics and plasticity
Local adaptation is defined as “a process whereby natural selection increases the frequency of traits within a population that enhance the survival or reproductive success of individuals expressing them” (Taylor 1991). In other words, it is an adaptive variation in response to local changes in environmental conditions. Generally, local adaptation is more important for immobile organisms (e.g. plants) than mobile organisms (e.g. animals). This is because, when local conditions become stressful, mobile organisms are often capable to migrate to a more suitable environment, whereas immobile organisms have to increase physiological tolerance or phenotypic plasticity in order to cope with the changes and survive (Bradshaw 1972). Plants can be locally adapted either through genetic variation (e.g. genetic mutation, gene flow, genetic recombination, genetic drift, migration; Kawecki & Ebert 2004) or by phenotypic plasticity22 (Sultan 1995), which is important for short-term responses to environmental change as far as it helps species to persist for a longer period during which evolutionary adaptation may occur (Pratt & Mooney 2013). When no other forces and constraints occur, local adaptation is expressed in improved fitness of each genotype (or deme) in its local habitat than genotypes from other habitats (Kawecki & Ebert 2004). Nevertheless, species performance and distribution is in part determined by their interactions with other species within their community (Brooker & Callaghan 1998).
Detecting local adaptation: reciprocal transplant and common-garden experiments
A way to straightforwardly study local adaptation is throughout reciprocal transplant experiments (Joshi et al. 2001; Kawecki & Ebert 2004; Ågren & Schemske 2012; Bennington et al. 2012). This approach involves assessing the performance of individuals of at least two different genotypes (or phenotypes) by reciprocally raising them in home and away sites. As argued by Kawecki & Ebert (2004), from the viewpoint of local adaptation, a home-site advantage must be evaluated between ‘local’ versus ‘immigrant’ genotypes (or phenotypes) and not between a given genotype at ‘home’ and ‘away’ (which is a reaction norm23 used for assessing plasticity, Pigliucci et al. 2006; Vitasse et al. 2010). When applicable in the field, this approach is highly relevant as it allows assessing the performance of the differing genotypes (or phenotypes) under natural environmental conditions that are difficult or even impossible to artificially reproduce in laboratory. However, an approach of reciprocal transplant with adult individuals is sometimes technically, ethically or legally impossible (Kawecki & Ebert 2004; García-Fernández et al. 2013). In these situations, greenhouse and common-garden24 experiments offer an opportunity to assess the performance of different genotypes (or phenotypes) under controlled environmental conditions, thus excluding confounding effects that cannot be taken into account in the field. Additionally, such experimental approaches are useful as they allow separating the effects of plasticity from those of genetic differences (Clausen et al. 1940; Roach & Wulff 1987; Schmid & Dolt 1994).
What are the relative contributions of genetics and plasticity to the phenotypic differences within F. gautieri? [Chapters 3 and 4]
I used a trait-based approach, a powerful tool allowing visualizing and comparing patterns (Keddy 1992; Garnier & Navas 2012), in a way to understand the morphological differences between F. gautieri phenotypes and the differing effects of these phenotypes on other species of the community. In order to answer my first main question of this thesis, I first adopted an observational approach in order to assess field differences in cushion traits between the phenotypes. In July 2012, I measured maximum leaf length, cushion penetration (an index of cushion compactness and interference), leaf thickness and number of inflorescences on 60 cushions (30 tight and 30 loose) in their natural habitats (42°58’N, 0°45’W, altitude: 1744 m a.s.l., La Pierre Saint-Martin, see Figure 9). In parallel, a shadehouse study was set up in order to experimentally assess the contribution of genetics and plasticity in changing traits among phenotypes and habitats. The shadehouse was located at the INRA station of Cestas-Pierroton, France (44°44’N, 0°46’W; 60 m a.s.l.). Three hundred replicates of each phenotype were grown from April 2011 till September 2013 in contrasting environmental conditions mimicking the two natural habitats (convex topography with shallow, stony and relatively dry soil for the tight cushion vs. concave topography with deep, less stony and wet soil for the loose cushion). The 300 replicates were obtained from 15 mature and discrete cushions (hereafter genotypes) that were collected on site in November 2010, each separated into 20 standardised tillers (leaves: 5-10, roots: 5 cm). Each tiller was transplanted in a separate pot, and all pots were randomly placed on benches. In 2011 and 2012, from April to September, a watering treatment was applied with 10 replicates of each treatment combination (phenotype x watering treatment) by irrigating half of the pots with one litre of tap water (Watered pots) three times a week and the other half once a week only (Dry pots). This was done to assess the potential plastic responses of phenotypes to the occurrence of a weak drought stress. At the beginning and the end of each growing season (April and October respectively), I recorded survival, maximum leaf length, cushion penetration, leaf thickness, cushion surface and leaf density (more details on methods are provided in chapter 3, article published in Oecologia). Additionally, in order to reinforce my results and to evaluate the adaptation of each phenotype to its habitat, I set up a reciprocal transplant experiment at La Pierre Saint-Martin (42°58’N, 0°45’W, altitude: 1615 m a.s.l., see Figure 9). In July 2013, I established two experimental gardens in contrasting topographic positions. The first garden (convex garden hereafter) was set up in a convex topographic position on shallow, stony and relatively dry soil simulating the tight cushion’s natural microhabitat. The second garden (concave garden hereafter) was set up in a concave topographic position on deep, less stony and relatively wet soil simulating the loose cushion’s natural microhabitat (Figure 13). The two gardens were 50 m apart. In each garden, I randomly transplanted 40 mature cushion replicates of each F. gautieri phenotype (50 cm distant from each other), representing 8 different genotypes with 5 replicates each (all transplanted cushions were grown from tillers for 2 years within the shadehouse at Cestas-Pierroton). Before planting out, resident vegetation was manually eliminated to limit competition. The gardens were fenced with metallic nets to prevent herbivory (more details on methods can be found in chapter 4).
Do the differing phenotypes have contrasting effects on the subordinate species? Are these effects heritable? [Chapters 3 and 4]
I set up three experiments to evaluate the competitive and/or facilitative ability (effect and response) of both F. gautieri phenotypes: in their natural environment (in the field), in the shadehouse and in the reciprocal transplant gardens. I used adult tight and loose cushions of F. gautieri to assess their competitive/facilitative effects, and three target individuals, Agrostis capillaris and the two phenotypes of F. gautieri to also assess their competitive/facilitative response.
In the field, a cushion removal experiment was set up (Al Hayek et al. 2014). In June 2011, 5 sites distant of at least 100 m were selected in a northern slope. In each site, we selected 6 discrete cushions of each F. gautieri phenotype that include one discrete individual of A. capillaris. For half of the cushions (3 tight and 3 loose in each site), we removed the aboveground parts of F. gautieri cushions within a circular area of 15 cm in diameter centred on the A. capillaris individual. Then, we transplanted one individual (tiller) of each F. gautieri phenotype at 5 cm from A. capillaris (this was done within removed and control cushions; Figure 14). In July 2012, we recorded survival, height, leaf number and biomass of all target individuals.
Differences in cushion effects between F. gautieri phenotypes
A field cushion-removal experiment was conducted to quantify the potential variation in cushion facilitative and/ or competitive effects on subordinate species across phenotypes and habitats (Online Resource 1). Three target species with contrasting drought-tolerance abilities and habitat distributions were used to encompass a large and representative panel of possible responses to neighbours (Brooker et al. 2008). We chose two drought-intolerant target species, i.e. the loose fescue phenotype itself and A. capillaris (its most frequent subordinate species), and a drought-tolerant target, the tight fescue phenotype itself. Both fescue phenotypes were chosen as targets to also assess responses to neighbours, since both the effect of a neighbour on a tar- get individual and the response of a target individual to the effect of a neighbour are important components of species competitive/facilitative abilities (Goldberg 1990; Liancourt et al. 2009; Le Bagousse-Pinguet et al. 2013). We used naturally occurring individuals for A. capillaris and trans- plants for the two F. gautieri phenotypes. In June 2011, we selected five sites in a northern slope with a distance of at least 100 m between sites. In each site, six cushions of each phenotype that included one discrete individual of A. capillaris were selected. For half of the cushions (three tight and three loose at each site), we removed by hand the aboveground parts of F. gautieri cushions within a circular area of 15 cm in diameter centred on the target individual of A. capillaris. Then, one individual of each F. gautieri phenotype was transplanted at 5 cm from the A. capillaris individual, both within removed and control cushions of both phenotypes. Transplanted individuals of both F. gautieri phenotypes were randomly collected at the site in at least ten cushions of each phenotype. Each transplanted individual had from five to ten leaves. All target individuals were tagged with metal rings. Thus, there were five replicates of each combination of the three treatments (cushion phenotype, removal and target species). In late July 2012, we recorded survival, measured height and leaf number of all target individuals. All target individuals were harvested for aboveground biomass measurements. Harvested target individuals were dried for 2 days at 70 °C and weighed. Survival was expressed in percentages (0, 33, 66 or 100 %) per treatment combination (cushion phenotype and removal) and per site, and growth data were averaged per treatment combination and per site before statistical analyses.
Table of contents :
CHAPTER ONE: LITERATURE OVERVIEW
1- Bridging ‘community ecology’ to ‘evolutionary biology’: the emergence of ‘community genetics’
2- Community assembly: from genes to communities
3- Evolution, natural selection and adaptation
4- Thesis objectives
CHAPTER TWO: STUDY SITES, MODEL SPECIES AND EXPERIMENTAL DESIGNS
1- The study site in the Pyrenees, the model species (Festuca gautieri subsp. scoparia Hackel & Kerner), and the experimental designs
2- The study site in the Mount-Lebanon, the model species (Onobrychis cornuta (L.) Desv.) and the experimental design
CHAPTER THREE: Phenotypic differentiation within a foundation grass species correlates with species richness in a subalpine community
CHAPTER FOUR: Disentangling the heritable and plastic components of the competitive and facilitative effects of two contrasting phenotypes of a foundation species
CHAPTER FIVE: Differential effects of contrasting phenotypes of a foundation legume shrub drive plant-plant interactions in a Mediterranean mountain
CHAPTER SIX: SYNTHESIS
1- Determinism of the observed phenotypic variation: the contribution of genetic variation and phenotypic plasticity
2- Consequences of the phenotypic variation within foundation species on the subordinate species
3- Perspectives for future studies
REFERENCES
