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- Materials and Methods
- Supporting Information
Local adaptation is thought to be a major contributor to the evolution of reproductive isolation (RI) between parapatric populations (Rundle & Nosil, 2005; Schemske, 2010). Although gene flow usually turns the odds against the formation of new species (Felsenstein, 1981), ecological contributions to RI in parapatry are not uncommon, having a long history in natural and experimental settings. For instance, adjacent populations of grasses on soils containing high or low concentrations of toxic heavy metals have evolved into morphologically and physiologically differentiated populations that persist despite gene flow (McNeilly & Antonovics, 1968; Antonovics & Bradshaw, 1970; Antonovics, 2006). Similarly, Anthoxanthum odoratum populations exposed to different environmental conditions have evolved both morphological differences and RI since the inception of the Park Grass Experiment in 1856 (Davies & Snaydon, 1976; Silvertown et al., 2005). These empirical results echo those from theory, where the predicted conditions for parapatric speciation seem to be common in nature (e.g. isolation by distance between populations, and patchy and linear habitats along rivers and coasts; Gavrilets et al., 2000). However, studies of RI often fail to identify the agents of divergent natural selection or quantify the relative contributions of multiple reproductive barriers to gene flow during the lifetime of organisms (c.f. studies reviewed in Lowry et al., 2008a). As a consequence, our knowledge of which barriers trigger the speciation process, and the relative importance of extrinsic vs intrinsic barriers to gene flow remains limited in most studies of ecotype and species formation in plants.
Local adaptation creates barriers to gene flow in parapatry through various mechanisms (Schluter, 2001; Rundle & Nosil, 2005; Hendry et al., 2007). When locally adapted populations exchange migrants, theory predicts that they will fare poorly in the environment of the sister population. This creates greater opportunities for interbreeding within rather than between populations, in turn limiting gene flow (Nagy & Rice, 1997; Hendry, 2004; Nosil, 2004; Thibert-Plante & Hendry, 2009). Local adaptation can also cause ecologically dependent reductions in F1 hybrid fitness, a phenomenon known as extrinsic postzygotic RI (Schluter, 2000; Rundle & Whitlock, 2001; Rundle & Nosil, 2005). Generally, ecologically dependent reductions in hybrid fitness occur because hybrids express intermediate parental phenotypic values for locally adapted traits (Barton & Hewitt, 1985; Schluter, 2000; Rundle & Nosil, 2005), thus rendering them unfit in parental habitats. The extent to which hybrids are ecologically disadvantaged depends on the form of inheritance for the traits under divergent natural selection (e.g. dominance vs additivity; Arnold, 1997; Barton, 2001; Berner et al., 2011). However, reductions in F1 hybrid fitness could also result from their failure to cope with stressful conditions, including those experienced in the field (Coyne & Orr, 2004). This form of hybrid failure is also extrinsic but not specific to the environment of the parents that produced the hybrid offspring. These mechanisms of postzygotic RI only manifest under field or stressful conditions but dissipate under controlled or benign conditions, such as those found in glasshouses (Hoffmann & Merilä, 1999; Bordenstein & Drapeau, 2001).
The mechanisms creating divergent natural selection are often difficult to identify and quantify. However, some habitat differences are known to contribute to local adaptation in plants (Kruckeberg, 1986; O'Dell & Rajakaruna, 2011). Edaphic and climatic differences usually cause strong divergent selection between populations, possibly because of drought (Stebbins, 1952; Bray, 2002), toxicity (Brady et al., 2005), temperature (Keller & Seehausen, 2012) or a combination of them. These effects are common across many plant taxa (Kruckeberg, 1951; Wu et al., 1975; Emms & Arnold, 1997; Nagy & Rice, 1997; Vekemans & Lefèbvre, 1997; Berglund et al., 2004; Kay, 2006; Martin et al., 2006; Sambatti & Rice, 2007; Lowry et al., 2008a) and suggest that environmental stress could create strong extrinsic prezygotic and varying degrees of postzygotic extrinsic RI, thus playing an important role during the early stages of ecotype and species formation (Lowry, 2012).
Plant and animal interactions can also contribute to the evolution of RI between plant populations. The most famous examples involve systems where pollinators discriminate floral differences between ecotypes or species (Emms & Arnold, 1997; Bradshaw & Schemske, 2003; Kephart & Theiss, 2004; DellíOlivo et al., 2011). A less studied biotic cause of RI is the contributions of herbivores and parasites to reductions in gene flow between populations (Sork et al., 1993; Combes, 1996; Fritz et al., 1999; Elias et al., 2012). For instance, hybrids between populations of willows show differential responses to aphids and mites (Fritz et al., 1994; Czesak et al., 2004), similar to the adult hybrids of Oenanthe conioides and O. aquatica that are preferentially grazed by waterfowls and snails in the environment of O. conioides (Westberg et al., 2010). Further exploration is required to conclude whether this kind of interaction between plants and invertebrates is important for the progress towards speciation and the origins of RI in plants.
Populations of the groundsel Senecio lautus that inhabit the sandy dunes (Dune populations) and rocky headlands (Headland populations) along the Australian coast are an excellent system to study the origin and maintenance of ecotypes and the early stages of speciation. Often found adjacent to each other along the coast, Dune and Headland populations show marked morphological differentiation (Thompson, 2005; Supporting Information Fig. S1 for typical ecotype morphologies), which has evolved repeatedly and independently multiple times, and in the face of gene flow (Roda et al., 2013a). Dune and Headland populations retain their morphologies in glasshouse conditions (see Abbott, 1976 for a similar case in European Senecio), and reportedly exhibit weak intrinsic reproductive barriers (Ali, 1964, 1968). Previous transplant experiments in S. lautus suggest that some populations are adapted to their local environment (Radford et al., 2004). However, little is known about what causes differentiation in the system and whether local adaptation is driving the evolution of RI in parapatric populations. We chose one of these parapatric pairs to investigate the evolution of reproductive isolating barriers in response to adaptation to contrasting coastal environments. Through field observations and common garden experiments in the field and the glasshouse we estimated various components of RI between these two parapatric populations, and identified possible ecological mechanisms causing divergent natural selection. We discuss how these results inform us about the relative contributions of extrinsic and intrinsic reproductive barriers during the early stages of speciation with gene flow.