Evolutionary theory suggests that quantitative genetic variation within populations can be maintained by spatially varying selection and gene flow (Slatkin 1978
; Barton 1999
; Tufto 2000
; Spichtig & Kawecki 2004
). Although local adaptation is pervasive (Hedrick et al. 1976
; Linhart & Grant 1996
), it is unclear whether gene flow is strong enough to maintain the high levels of genetic variation found in nature. Other processes, such as mutation–selection balance or population bottlenecks, could have a greater effect on levels of genetic variation within populations, obscuring any contribution by gene flow. Evidence from this study shows strong correlation between regional heterogeneity and genetic variance in lodgepole pine (r2
~20%), suggesting that gene flow and heterogeneous selection are making significant contributions to levels of genetic variation within populations.
As this inference is based on correlation, however, there are two possible alternative explanations that should be addressed. First, it is possible that temp
oral heterogeneity is responsible for maintaining diversity within populations (as per Burger & Gimelfarb 2002
). If areas that are more spatially heterogeneous are also more temp
orally heterogeneous, then it would be impossible to evaluate which of these factors is maintaining diversity with the correlation-based approach used here. There is good reason to suspect that temp
oral and spatial heterogeneity in climate would not be well correlated, because other factors such as continentality and oceanic currents can influence temp
oral variations in climate without correlation to spatial influences such as altitude. At the present time, however, there are no long-term climatic records available at a sufficiently fine spatial scale, so this alternative hypothesis cannot be conclusively rejected.
As a second explanation, it is possible that environments within populations are also heterogeneous and that variance within populations is the product of micro-environmental adaptation in their immediate environment. If areas that are regionally heterogeneous also tend to be more heterogeneous at this small scale within populations, then correlations with regional heterogeneity could be an artefact, as described above with respect to temp
oral heterogeneity. Because the datasets we used are interpolated on a coarse 1×1
km scale, they are inappropriate for estimating fine-scale heterogeneity and testing this alternate hypothesis. While local adaptation in Douglas fir (Pseudotsuga menziesii
) has been found over changes in altitude of only a few hundred metres (Campbell 1979
), sampling for the establishment of common gardens in this experiment was conducted over small areas (ca
) and care was taken to avoid sampling over obvious sources of environmental variation within a population. Thus, although it was not possible to conclusively test that variance was not being maintained by micro-environmental adaptation within populations, this seems an unlikely explanation for the correlations found in this study.
While theoretically possible, these alternative explanations are less likely than the suggestion that gene flow and regional heterogeneity maintain diversity within populations. Local adaptation has been demonstrated (Yang et al. 1996
; Rehfeldt et al. 1999
; Wu & Ying 2004
), and gene flow in lodgepole pine is extensive (Perry 1978
), so some effect of gene flow on levels of variance is expected. Assuming that our interpretation is correct, gene flow and regional heterogeneity explain approximately 20% of the variation in diversity within populations of lodgepole pine. In fact, due to the potential for errors in the heterogeneity modelling and estimation of genetic variance, the true correlation may be considerably stronger.
This evidence suggests that gene flow and heterogeneity play an important role in maintaining genetic variance, but how general is this effect? Under what conditions would we expect to see maintenance of variation by environmental heterogeneity and gene flow in other species? First, natural selection must be strong enough to maintain variation in trait means between populations, in spite of gene flow. Second, for the increase in variance to be significant, there must be considerable spatial variation in the optimum trait within the effective range of gene flow. Linear cline models show how the environment must change over a characteristic length defined by the strength of selection and distance of gene flow in order for selection to maintain localized adaptations (Slatkin 1978
; Barton 1999
). Assuming that there is some analogous threshold in more complex heterogeneous environments, there will be some scale of change in environment below which local adaptations are not maintained and genetic variance is unaffected by migration–selection balance. Lodgepole pine is an ideal species in which to detect such an effect, as it has extensive gene flow and inhabits both heterogeneous mountain environments and homogenous plateaus. It remains to be seen whether migration–selection balance plays a significant role in other species, where gene flow is limited and/or environments are more uniform. Unfortunately, the method used here is only applicable when there is substantial variation in the regional heterogeneity; tests based on correlation are powerless to detect an effect when all populations experience equal conditions. It is worth noting that if migration–selection balance plays a significant role in driving levels of diversity, the common statistical assumption of homogeneity of variances across populations may not be warranted when they inhabit environments with different levels of heterogeneity.
Most studies of the impact of gene flow on genetic structure within populations have focused on its maladaptive consequences. Empirical studies have described the impacts of migration load (e.g. Storfer & Sih 1998
), gene swamping (e.g. Raymond & Marquine 1994
) and outbreeding depression (e.g. Price & Waser 1979
), while theoretical studies have noted the limits to local adaptation (e.g. Kirkpatrick & Barton 1997
). Here, we have found evidence suggesting that variance within populations can be maintained by gene flow without homogenizing local adaptations and eliminating diversity between populations. While populations of lodgepole pine are not always perfectly locally adapted (Wu & Ying 2004
), they are able to persist under this genetic load and even maintain ecological dominance. Although genetic load is always maladaptive in environments that do not change over time, genetic variance is necessary for any response to selection (Fisher 1930
); thus, genetic load may be beneficial in times of rapid environmental change. While both mutation and migration can increase variance, migrant alleles from neighbouring populations with slightly different environments are more likely to be adaptive to slight temp
oral variations in environment than random mutations generated de novo
. For example, if two populations inhabit wet and dry environments, respectively, and climatic change causes these habitats to reverse their characteristics, allelic variation maintained by gene flow would be inherently adaptive to the novel change, whereas alleles generated by mutation would often be maladaptive. If migration–selection balance proves to be a widespread and significant factor maintaining variation in quantitative traits, it will be important to consider environmental heterogeneity and gene flow when evaluating conservation and management options, especially when considering adaptation to climatic change. Generally speaking, conserving both heterogeneous landscapes and historical levels of gene flow should maintain diversity within and between populations.