REVIEW Conceptual issues in local adaptation Tadeusz J. Kawecki* and Dieter Ebert��� Division of Ecology and Evolution, Department of Biology, University of Fribourg, Chemin du Musee �� 10, CH-1700 Fribourg, Switzerland *Correspondence: E-mail tadeusz.kawecki@unifr.ch ��� Present address: Zoological Institute, University of Basel, Vesalgasse 1, CH-4051 Basel, Switzerland Abstract Studies of local adaptation provide important insights into the power of natural selection relative to gene flow and other evolutionary forces. They are a paradigm for testing evolutionary hypotheses about traits favoured by particular environmental factors. This paper is an attempt to summarize the conceptual framework for local adaptation studies. We first review theoretical work relevant for local adaptation. Then we discuss reciprocal transplant and common garden experiments designed to detect local adaptation in the pattern of deme �� habitat interaction for fitness. Finally, we review research questions and approaches to studying the processes of local adaptation ��� divergent natural selection, dispersal and gene flow, and other processes affecting adaptive differentiation of local demes. We advocate multifaceted approaches to the study of local adaptation, and stress the need for experiments explicitly addressing hypotheses about the role of particular ecological and genetic factors that promote or hinder local adaptation. Experimental evolution of replicated populations in controlled spatially heterogeneous environments allow direct tests of such hypotheses, and thus would be a valuable way to complement research on natural populations. Keywords Adaptive deme formation, adaptive evolution, coevolution, heterogeneous environ- ments, gene flow, metapopulations, natural selection, population differentiation, reciprocal transplant, review. Ecology Letters (2004) 7: 1225���1241 I N T R O D U C T I O N The forces of natural selection often vary in space, resulting in genotype �� environment interactions for Darwinian fitness. In the absence of other forces and constraints such divergent selection should cause each local population (deme) to evolve traits that provide an advantage under its local environmental conditions (which we refer to as its habitat), regardless of the consequences of these traits for fitness in other habitats. What should result, in the absence of other forces and constraints, is a pattern such that resident genotypes in each deme would have on average a higher relative fitness in their local habitat than genotypes origin- ating from other habitats. This pattern and the process leading to it is local adaptation (Williams 1966). Local adaptation may be hindered by gene flow, confounded by genetic drift, opposed by natural selection due to temporal environmental variability, and constrained by lack of genetic variation or by the genetic architecture of underlying traits. Thus, although divergent natural selection is the driving force, these other forces, in particular gene flow, are integral aspects of the process of local adaptation. Because of those other forces, the pattern of local adaptation is not a necessary outcome of evolution under spatially divergent selection. We reserve the term ��local adaptation�� for patterns and processes observed across local populations of the same species connected, at least potentially, by dispersal and gene flow. This emphasizes the tension between the potentially differentiating effect of natural selection and the homoge- nising effect of gene flow. For convenience, throughout this paper we refer to the local populations as demes, and to the entire spatially structured population (i.e. a set of demes) as metapopulation. However, extinction obliterates locally adapted gene pools, so extinction-colonization dynamics, which is the defining feature of Levins-type metapopulations (Hanski 1999), is unfavourable to local adaptation. Further- more, the concept of local adaptation is not restricted to a patchy environment. The demes may be discrete units in well-delimited habitat patches, or may represent arbitrary sampling units in a continuous species range. Similarly, the spatial variation in the environment may be discrete, with several distinct habitat types, or it may consist of continuous environmental gradients, whereby a ��habitat�� represents the conditions at a given point of the gradient. Ecology Letters, (2004) 7: 1225���1241 doi: 10.1111/j.1461-0248.2004.00684.x ��2004 Blackwell Publishing Ltd/CNRS

The study of local adaptation is obviously within the realm of studying adaptation in general, but there are some specific aspects. Generally, an adaptation is a phenotypic feature which is functionally designed by past natural selection, and which improves Darwinian fitness relative to alternative features (Williams 1966). Thus, studying adapta- tion would require considering the historical aspect, i.e. a comparison between derived, adapted populations and their presumably less adapted ancestors (e.g. Korona 1996 Travisano & Rainey 2000). This is usually not possible. The study of local adaptation offers the more feasible alternative of comparison between local populations, which have evolved under different conditions. In the absence of divergent (i.e. spatially heterogeneous) natural selection, genetic differentiation in fitness-related traits is expected to be obliterated by gene flow. Therefore, local adaptation in a set of demes connected by gene flow must be due to ongoing (or very recent) natural selection related to differences in environmental conditions experienced by different demes. In contrast, traits that are unconditionally adaptive will tend to become fixed within the species. Once a trait has become genetically fixed, it may continue to be expressed even if an environmental change causes it to lose its advantage or become detrimental (Stearns 1994). Therefore, in local adaptation studies it is often possible to identify the selective forces at work, while in classical adaptation studies this may not be possible anymore (Williams 1993). This has made local adaptation studies a paradigm for testing hypotheses about adaptations thought to be favoured by specific environmental factors (Reznick & Ghalambor 2001). Examples include life history evolution in response to predation (e.g. Reznick & Endler 1982), geographic variation in diapause strategies (e.g. Bradford & Roff 1995), reproductive phenology on alternative host species (e.g. Filchak et al. 2000), or types of cues used in spatial learning depending on the stability of the environ- ment (e.g. Girvan & Braithwaite 1998). Several other aspects of local adaptation make its study particularly interesting in the general context of adaptive evolution in natural populations. First, gene flow hinders local adaptation. Therefore, the existence of a pattern of local adaptation despite gene flow certifies to the strength of natural selection imposed by particular environmental factors. Second, it is sometimes possible to infer the age of a deme from geological or historical data this allows one to estimate the rate of adaptive evolutionary change (e.g. Stearns 1983 Gomi & Takeda 1996). Third, local adaptation has been recognized as an important mechanism maintain- ing genetic variation (reviewed by Felsenstein 1976 Hedrick et al. 1976 Hedrick 1986). Finally, a number of scenarios for allopatric and sympatric speciation (reviewed by Schluter 2001 Turelli et al. 2001 Via 2001) assign local adaptation a crucial role in initiating the divergence of incipient species. This paper is an attempt to review conceptual issues relevant for local adaptation studies. It is not intended as a summary of the existing local adaptation literature we use selected examples to illustrate specific points. In the next section, we briefly review population genetic theory relevant to local adaptation. Then we discuss reciprocal transplant and common garden experiments designed to detect the pattern of local adaptation in the pattern of deme �� habitat interaction for fitness. Finally, we review the research questions and approaches to study the processes of local adaptation. We conclude with a call for studies directly addressing the predictions of the theory as to how much local adaptation should be expected under what circum- stances. T H E O R Y O F L O C A L A D A P T A T I ON Models of adaptive divergence A large body of theoretical literature is concerned with the interplay between spatially divergent selection and gene flow, and its effect on adaptive evolution. Although much of that work has been motivated by other questions (e.g. maintenance of genetic polymorphism, evolution of spe- cialization, dispersal, or phenotypic plasticity) and often even does not mention local adaptation, it has yielded important predictions concerning local adaptation, provi- ding theoretical underpinning of local adaptation studies. In this section, we briefly review the predictions of those studies relevant for local adaptation. Genotype �� environment interaction for fitness is an obvious pre-requisite for local adaptation. Of several forms such an interaction can take, the most important for local adaptation is antagonistic pleiotropy, whereby the alleles have opposite effects on fitness in different habitats. Such antagonistic pleiotropy implies that no single genotype is superior in all habitats, leading to trade-offs in adaptation to different habitats. Beginning with Levene (1953) a number of authors (reviewed in Felsenstein 1976 Hedrick et al. 1976 Hedrick 1986) have shown that spatial heterogeneity facilitates maintenance of polymorphism that shows such antagonistic pleiotropy, provided that density-dependence (population regulation) operates within demes (Christiansen 1975 Pimm 1979 Karlin & Campbell 1981). Density- dependence operating independently in different demes favours rare alleles that improve fitness in a habitat, in which most individuals perform poorly. This is a form of frequency-dependent selection, which helps to maintain polymorphism, even when the average fitness of the heterozygote is below that of both homozygotes (under- dominance). In the less likely case of population regulation operating at the level of the global (meta-)population (known as ��hard selection��), a single locus polymorphism will 1226 T. J. Kawecki and D. Ebert ��2004 Blackwell Publishing Ltd/CNRS

not be maintained (protected) by selection alone unless there is overdominance for fitness averaged over the habitats (Dempster 1955 Christiansen 1975 Karlin & Campbell 1981). Population genetics theory often contrasts ��hard�� with ��soft�� selection. The latter assumes an extreme form of population regulation, such that the reproductive output of each local population is fixed, no matter how well or poorly the population is adapted (Christiansen 1975). In reality, population regulation is likely to fall somewhere between the ��hard�� and ��soft�� extremes, and models with intermediate population regulation show that the more ��soft��-like is population regulation, the more favourable are the conditions for maintenance of protected polymorphism (Pimm 1979 Christiansen 1985 Wilson & Turelli 1986 Holsinger & Pacala 1990). Maintenance of polymorphism in continuously varying environments has been studied by models of clinal variation (e.g. Slatkin 1973, 1978 Barton 1999). Protected polymorphism in a heterogeneous environment may be maintained even if dispersal results in complete mixing of the gene pool. However, in such a case demes will not differentiate genetically, i.e. there will be no local adaptation. Thus, restricted gene flow is a pre-requisite for local adaptation. Restricted gene flow (due to low passive dispersal or active habitat choice) also makes the conditions for maintenance of polymorphism more favourable (e.g. Maynard Smith 1966). The conditions for maintenance of polymorphism are more favourable for loci with large effects such loci also show greater differentiation of allele frequencies under divergent selection (Hedrick et al. 1976). Furthermore, alleles with strong effects are less likely to be lost by drift (Crow & Kimura 1970). Therefore, loci with large effects on fitness should disproportionally contribute to local adaptation (Macnair 1991). This is indeed the case in the classic examples of local adaptation of plants to sites contaminated with heavy metals (reviewed in Macnair 1987, 1991). Nonetheless, many fitness-related characters likely to play a role in local adaptation show polygenic variation. In contrast to single-locus models, the theory of poly- genic traits under divergent selection remains relatively unexplored. Most theory relevant for local adaptation concentrates on the evolution of ecological specialization, assuming a trade-off in fitness across habitats mediated by a quantitative trait or traits (reviewed in Futuyma & Moreno 1988 Jaenike 1990 Fry 1996). Models developed under this heading usually take an ESS approach (Maynard Smith 1982), assuming continuous variation in the focal trait, and aiming to identify an evolutionarily stable state, i.e. a phenotypic composition of the population, which makes it impossible for genotypes with other phenotypes to invade when rare. Three extremes define the range of possible evolutionarily stable states: (i) a single generalist phenotype showing a similar degree of adaptation to all habitats (ii) a single specialist phenotype optimally adapted to one habitat (usually the habitat that is most frequently encountered or of highest quality) and poorly adapted to other habitats and (iii) a set of specialist phenotypes each maximizing fitness in one habitat type. Local adaptation requires an outcome close to (iii). Because it also requires limited gene flow, we limit our attention to models that consider limited dispersal. The evolution of divergent specialized phenotypes in such models results from selection at equilibrium being effect- ively disruptive (Day 2000). Of course, in a sexual population the evolution of such divergent specialized phenotypes will be prevented by recombination (unless there is very strong assortative mating). Instead, in a sexual population such disruptive selection will tend to maintain polymorphism at a greater number of loci, and thus promote differentiation between demes living in different habitats (Spichtig & Kawecki 2004). The evolutionarily stable state predicted by the ESS models is often a discontinuous function of parameters (Brown & Pavlovic 1992 Kisdi 2002). Spichtig & Kawecki (2004) observe similar sharp transitions in their sexual polygenic model, where a small increase in dispersal rate can result in large differences in the number of polymorphic loci and the amount of equilibrium genetic variance. Popula- tion differentiation corresponding to local adaptation is promoted by low dispersal and strong selection (Brown & Pavlovic 1992 Day 2000 Kisdi 2002 Spichtig & Kawecki 2004). However, if selection is very strong (i.e. fitness falls off very quickly as the phenotype deviates from the local optimum), intermediate genotypes have low fitness in all habitats. This makes it difficult for a population initially adapted to one habitat to invade other habitats and evolve into a set of locally adapted demes, promoting the stability of an ��asymmetric�� equilibrium with a single phenotype specialized on one habitat (Day 2000 Kawecki 2000, 2003 Ronce & Kirkpatrick 2001 Kisdi 2002). At such an equilibrium the population has a source-sink structure, characterized by asymmetric gene flow (Holt & Gaines 1992 Dias 1996), which makes it difficult for alleles improving adaptation in a sink habitat to spread (Holt & Gaines 1992 Kawecki 1995 Holt 1996). Therefore, the conditions for local adaptation mediated by polygenic traits are most favourable when selection in habitat 1 against genotypes well adapted to habitat 2 and vice versa is strong, but selection against intermediate (recombinant) genotypes is moderate. If selection against intermediate genotypes is weak, intermediate generalist phenotypes are likely to be favoured, leading to loss of genetic variance and little differentiation (Spichtig & Kawecki 2004). If it is too strong, the population is likely to be trapped in a source-sink situation with little differentiation among demes (in a single- locus model this case corresponds to loss of polymorphism Local adaptation 1227 ��2004 Blackwell Publishing Ltd/CNRS