Conceived and designed the experiments: RL MF. Performed the experiments: RL. Analyzed the data: RL. Contributed reagents/materials/analysis tools: RL MF. Wrote the paper: RL MF.
Current address: Department of Plant Sciences, University of Oxford, Oxford, United Kingdom
The authors have declared that no competing interests exist.
Local adaptation is of fundamental importance in evolutionary, population, conservation, and global-change biology. The generality of local adaptation in plants and whether and how it is influenced by specific species, population and habitat characteristics have, however, not been quantitatively reviewed. Therefore, we examined published data on the outcomes of reciprocal transplant experiments using two approaches. We conducted a meta-analysis to compare the performance of local and foreign plants at all transplant sites. In addition, we analysed frequencies of pairs of plant origin to examine whether local plants perform better than foreign plants at both compared transplant sites. In both approaches, we also examined the effects of population size, and of the habitat and species characteristics that are predicted to affect local adaptation. We show that, overall, local plants performed significantly better than foreign plants at their site of origin: this was found to be the case in 71.0% of the studied sites. However, local plants performed better than foreign plants at both sites of a pair-wise comparison (strict definition of local adaption) only in 45.3% of the 1032 compared population pairs. Furthermore, we found local adaptation much more common for large plant populations (>1000 flowering individuals) than for small populations (<1000 flowering individuals) for which local adaptation was very rare. The degree of local adaptation was independent of plant life history, spatial or temporal habitat heterogeneity, and geographic scale. Our results suggest that local adaptation is less common in plant populations than generally assumed. Moreover, our findings reinforce the fundamental importance of population size for evolutionary theory. The clear role of population size for the ability to evolve local adaptation raises considerable doubt on the ability of small plant populations to cope with changing environments.
Local adaptation is of fundamental importance in evolutionary, population, conservation, and global-change biology. However, while it is commonly assumed that most plant populations are locally adapted the generality of local adaptation in plants and whether and how it is influenced by specific species, population and habitat characteristics is not clear. Currently, many plant populations are small and isolated and at the same time often facing rapidly changing environments to which they need to adapt to. The ability to adapt may, however, be compromised in small populations because of reduced genetic diversity
In addition to reduced genetic variation and genetic drift, local adaptation can also be constrained by variation in natural selection and gene flow
Plant traits such as mating system, longevity, and clonality have been suggested to affect the evolution of local adaptation mainly due to their effects on the level and distribution of genetic variation. Short-lived and self-compatible species tend to be more strongly differentiated at a smaller scale than long-lived and outcrossing species
We conducted the first quantitative review on local adaptation in plants using 35 published studies on 32 plant species reporting 1032 pairwise comparisons of the performance of plants from local and foreign populations (See
Species | Longevity | Mating system | Clonality | Type of exeriment | Habitat choice | Temporal constancy | Spatia hetero-geneity | Population size | Number of comparisons | Effect size (d) | Variance | Reference |
Annual | SC | Non-Clonal | R | NR | C | HE | S | 16 | 0.036 | 0.013 | Callahan & Pigliucci 2002 | |
Annual | SC | Non-Clonal | R | NR | NC | HO | L | 2 | 0.276 | 0.196 | Nagy 1997 | |
Annual | Clonal | R | NR | C | HO | 35 | 0.004 | 0.037 | Santamaria et al. 2003 | |||
Annual | SC | Non-Clonal | R | NR | NC | HE | L | 12 | −0.157 | 0.118 | Hereford & Moriuchi 2005 | |
Perennial | SI | Clonal | R | RA | NC | HE | L | 2 | 0.220 | 0.706 | Roy 1998 | |
Perennial | SI | Non-Clonal | E | RA | C | HO | L | 4 | −0.247 | 0.202 | Ehlers & Thompson 2004 | |
Annual | SC | Non-Clonal | R | NR | NC | HE | S | 6 | 0.033 | 0.405 | Helenurm 1998 | |
Perennial | SC | Non-Clonal | R | NR | C | HE | L | 18 | −0.207 | 0.058 | Stanton & Galen 1997 | |
Perennial | SC | Non-Clonal | E | NR | NC | HO | S | 4 | 0.049 | 0.203 | Petit & Thompson 1998 | |
Annual | SC | Non-Clonal | R | NR | NC | HO | L | 8 | −0.289 | 0.033 | Schmitt & Gamble 1990 | |
Annual | SC | Non-Clonal | R | NR | C | HO | L | 8 | −0.379 | 0.120 | Donohue et al. 2000 | |
Perennial | SI | Clonal | E | NR | C | HE | S | 12 | 0.033 | 0.322 | Lenssen et al. 2004 | |
Annual | SC | Non-Clonal | R | NR | L | 10 | −1.174 | 0.250 | Jordan 1992 | |||
Perennial | SI | Non-Clonal | E | NR | C | HO | L | 3 | −0.244 | 0.007 | Smith et al. 2005 | |
Perennial | SI | Non-Clonal | R | R | C | HO | S | 68 | −0.017 | 0.127 | Jakobsson & Dinnetz 2005 | |
Annual | SC | Non-Clonal | R | NR | NC | HO | 65 | −0.682 | 0.447 | Volis et al. 2002 | ||
Annual | SC | Non-Clonal | R | NR | NC | HO | L | 14 | −0.618 | 0.146 | Nagy & Rice 1997 | |
Perennial | SC | Non-Clonal | E | RA | C | HO | 10 | 0.640 | 0.244 | Vergeer et al. 2004 | ||
Annual | SC | Non-Clonal | R | NR | C | HE | L | 8 | −0.188 | 0.015 | Verhoeven et al.2004 | |
Annual | SC | Non-Clonal | R | RA | NC | HE | L | 12 | −0.229 | 0.011 | Etterson 2004 | |
Perennial | SI | Non-Clonal | R | RA | C | HO | L | 4 | −0.285 | 0.077 | Kindell et al. 1996 | |
Annual | SC | Non-Clonal | R | NR | C | HO | L | 8 | −0.060 | −0.060 | Bennington & McGraw 1995 | |
Annual | SC | Non-Clonal | R | NR | C | HO | L | 7 | −0.064 | 0.020 | Volis et al. 2002 | |
Annual | SC | Non-Clonal | E | NR | C | HO | S | 4 | 0.179 | 0.187 | Cheplick & White 2002 | |
Perennial | Non-Clonal | R | NR | C | HO | 2 | 0.179 | 0.101 | Boege & Dirzo 2004 | |||
Perennial | SC | Non-Clonal | R | NR | NC | HO | L | 4 | 0.061 | 0.292 | Link et al. 2003 | |
Perennial | Clonal | R | RA | NC | HO | L | 4 | −0.755 | 0.243 | Hämmerli & Reusch 2002 | ||
Perennial | SI | Clonal | R | NR | NC | HO | L | 23 | −0.261 | 0.205 | Knight & Miller 2004 | |
Annual | SC | Non-Clonal | R | NR | C | HO | S | 15 | −0.096 | 0.140 | Rendon &Nunez-Farfan 2000 | |
Perennial | Clonal | R | NR | NC | HO | L | 23 | 0.250 | 0.234 | Thompson et al. 1991 | ||
Perennial | Clonal | R | NR | NC | HO | L | 12 | 0.006 | 0.072 | Platenkamp 1990 | ||
Annual | SI | Clonal | R | NR | C | HO | S | 10 | −0.077 | 0.262 | Genton et al. 2005 | |
Annual | SC | Non-Clonal | E | RA | NC | HO | 71 | 0.087 | 0.226 | Galloway & Fenster 2000 | ||
Perennial | Clonal | R | RA | C | HO | L | 201 | −0.280 | 0.211 | Joshi et al. 2001 | ||
Perennial | SI | Non-Clonal | R | RA | C | HO | L | 156 | −0.272 | 0.220 | Joshi et al. 2001 | |
Perennial | SI | Non-Clonal | R | RA | C | HO | L | 159 | −0.237 | 0.230 | Joshi et al. 2001 |
SC = Self-compatible, SI = Self-incompatible, R = reciprocal transplant experiment, E = experimental test environments, RA = habitats/sites selected randomly, NR = sites selected because of clear habitat differences, NC = environments/habitats not constant in time, C = environments/habitats constant in time, HE = spatially heterogeneous habitats, HO = spatially homogeneous habitats, L = large populations (>1000 individuals), S = small populations (<1000 individuals), number of comparisons refers to local-foreign comparisons (i.e. individual effect sizes) per study and species.
However, in the strict sense (sensu Kawecki and Ebert
The effect size measures the difference in fitness of foreign and local plants (“a” or “b”) at one site (“A” or “B”). A positive effect size indicates that local plants perform better than foreign plants at their site of origin. A) The case where local plants perform better than foreign plants at both compared sites, i.e. where the reaction norms for fitness cross and both effect sizes are positive ( = POS-POS). B, C) Plants of one origin (“A”) perform better at both compared sites. In this case of non-crossing reaction norms for fitness one effect size is positive and one is negative ( = POS-NEG). The resulting mean effect size can be positive (B) or negative (C). D) Foreign plants perform better than local plants at both sites indicating maladaptation (effect sizes negative = NEG-NEG).
Our meta-analysis revealed that, overall, local plants clearly outperformed foreign plants (Effect size Hedges'
The reaction norms for fitness crossed (i.e. the respective local plants outperformed foreign ones in both compared environments;
Local plants performed better than foreign plants in a given environment only in large plant populations as indicated by a significant positive overall effect size, whereas in small populations there was no significant difference in plant performance between plant origins (
A) The better performance of local plants compared to foreign plants is significantly greater for large (N = 24) than for small (N = 8) populations. The bars denote bias-corrected 95% confidence limits. B) The frequencies of cases where reaction norms for fitness cross (POS-POS, see
Local adaptation was independent of the plant or habitat characteristics considered in our study (
A) Effects of plant characteristics and B) of population characteristics on the effect size (Hedges'
The strength or direction of the effect size were not significantly associated with geographic distance between the compared sites of plant origin (Pair-wise comparisons of plant origins pooled by traits:
For the graph we pooled the data for each pair of plant origins by the traits reported for this pair. For the statistical tests reported in the text we also used data pooled by study and species to avoid pseudoreplication.
Our meta-analysis reveals that on average, local plants perform better than foreign plants at their site of origin. Overall, this was found in 71.0% of the transplant sites. However, the pair-wise comparisons of the performances of local and foreign plants at both of the two sites between which plants had been reciprocally transplanted revealed that local plants performed better at both compared sites in only 45.3% of the cases. Only the latter finding gives accurate evidence of divergent selection and thus local adaptation in the strict sense suggested by Kawecki and Ebert
A major finding of our study is that large plant populations are generally locally adapted whereas this is unusual for small populations. This is both indicated by the higher overall effect size for large populations and by the much higher frequency of POS-POS cases for pairs of large compared to pairs of small populations (
Using precise estimates of population sizes would have allowed us to analyze the effects of population size on adaptation in a more detailed way and, for example, to examine potential threshold population sizes for adaptation. Unfortunately, due to temporal and demographic variation it is difficult to accurately estimate population sizes in the field. Therefore, for our study the authors could only provide the very coarse “small” or “large” estimates of population size. However, although these estimates are coarse there is no reason to believe that they would have biased our results. On the contrary, more precise estimates might even have resulted in a closer relationship between population size and local adaptation.
Small populations can have a low evolutionary potential and fail to adapt locally for various reasons. Firstly, larger populations can accumulate higher levels of heritable variability and beneficial mutations and might therefore respond to selection better than small populations do
Plant responses to environmental variation may depend on plant life history. However, our study did not confirm any prediction on the roles of species longevity, mating system and clonality for local adaptation (
Local plants performed better than foreign plants regardless of whether plant origins had been selected randomly by the experimenters or based on clear differences in the compared environments and regardless of whether plants were transplanted reciprocally in the field or to deliberately designed test environments. This matters from a methodological point of view, as it excludes the possibility that the studies used in our meta-analysis could have been biased towards pronounced local adaptation due to selection of study systems. In addition, it suggests that local adaptation is not necessarily driven by obvious environmental differences between habitats. Of course these considerations only hold to the degree to which the experimenters were able to identify the environmental factors relevant for adaptation.
We detected no effects of the spatial or of the temporal heterogeneity of the compared habitats on local adaptation. Thus, our study suggests that effects of temporal and spatial heterogeneity on the evolution of local adaptation are either less important than previously thought, or that they cancel each other. Nevertheless, it must be kept in mind that the authors could only provide quite coarse estimates of spatial and temporal heterogeneity. Therefore, these considerations only hold to the degree that seemingly homogeneous habitats do not actually provide heterogeneous conditions for the organism under study, as found in some studies
It has been suggested that the likelihood of detecting local adaptation increases with greater geographic distance between compared sites, because genetic isolation and environmental differences usually increase with increasing distance
While, as just discussed, the mean level of local adaptation was independent of the distance between the sites, variation in the strength of local adaptation was greater at smaller than at larger geographic scale. This indicates that environmental conditions are always very likely to differ between geographically distant populations, whereas the conditions between populations that are geographically less distant apart can either be similar or very different.
To date, studies on local adaptation in plants are only available for herbaceous plants in temperate regions. While among these studies local genotypes performed on average better than foreign genotypes at their site of origin, selection favoured locally adapted plants only in less than half of the pair-wise site comparisons. This suggests that local adaptation is less widespread than commonly believed. In contrast to a wealth of hypotheses brought up during recent decades, local adaptation appeared to be independent of the considered plant life-history traits, the degree of spatial and temporal habitat heterogeneity, and of the geographic distance between study populations. In contrast to all other tested factors potentially affecting local adaptation studied in our meta-analysis population size had a very large and clear effect. The much lower likelihood of local adaptation in small populations reinforces the fundamental interest of population size for evolutionary theory. In addition, the clear role of population size for the evolution of local adaptation raises considerable doubt on the ability of small plant populations to cope with changing environments.
The standard method to examine local adaptation in plants is the reciprocal transplant experiment, where plants from different populations are either transplanted between these field populations or to corresponding test environments. The latter refers to experiments where for instance plants from a dry and from a wet meadow are planted both to dry and wet experimental environments. To search for such studies we conducted key word searches in the Web of Science (ISI) database using combinations of the key word “plant” with “local adaptation”, “reciprocal transplant*”, “adaptation” and “adaptive evolution”. The search resulted in a list of 211 articles. Moreover, we screened the reference lists of these articles to identify further potentially relevant articles. The criterion for including published studies in our meta-analysis was that they reported mean values, variance and sample sizes of performance of local plants and foreign plants at one or several sites. Because early studies on local adaptation
The reported fitness-relevant measures included measures of plant reproductive success (such as the number of fruits, flowers, or seeds, fruit set, or seed set), plant size (such as biomass, leaf size, plant height, or number of ramets), survival rates, and germination rates. We extracted altogether 1032 pairwise comparisons of the performance of local plants and foreign plants at a given site. For each performance measure we calculated the effect size, Hedge's
To test for the importance of different sources of variation we classified our data according to characteristics of populations, habitats, studies, and plant life-history. This data was to a large extent obtained directly from the authors. As population characteristic we tested the effect of population size. Information on population size had been provided only in very few articles. Thus, we inquired this information directly from the authors. Since population size had not been considered explicitly in most of the studies, the authors could not provide count data on population sizes but were able to state with certainty whether populations in their experiments were smaller or larger than 1000 flowering individuals. Although a finer classification would have been desirable, we consider this coarse classification nevertheless appropriate, because genetic problems in terms of reduced genetic variation and increased inbreeding of small population have been predicted for population sizes lower than 100–1000
We avoided non-independent pair-wise comparisons, which would correspond to pseudo-replication, by pooling data by species and by measure of plant performance (reproduction, growth, survival, germination) when testing for effects of population size, life-history traits, type of study and habitat heterogeneity and homogeneity on the strength of the effect. Data was pooled by pair-wise site comparison to test for the effect of geographic distance on the strength of the effect (see below). When effect sizes for several measures of plant performance were obtained per study we pooled the data by calculating mean effect sizes and their pooled variances. Of course, it would be best to analyse whole life-cycle estimates of fitness rather than the single or few components provided by the published studies. At least, to some degree the pooling of data by study and species takes aspects of total fitness into account, because fitness components with opposing trends cancel out each other in pooling.
To test whether the effect sizes differed depending on the different plant, habitat or study characteristics we examined between-group heterogeneity using the chi-square test statistic,
To examine the association of geographic distance and effect size we used random-effects continuous-model meta-analysis
We used Meta Win 2.0
We analysed the frequencies of cases where the measures of plant performance were higher for local plants at both sites (“POS-POS”- case of crossing reaction norms, where both effects sizes are positive,
List of studies included in the meta-analysis
(0.04 MB DOC)
We thank the authors of the articles used for the meta-analysis for readily providing additional data, Jana Raabova, Marianna Riipi, Dani Prati, and Frank Schurr for discussion and Dieter Ebert, Bernhard Schmid, Jessica Gurevitch for detailed comments on earlier drafts and Angus Buckling and the anonymous referees for valuable comments.