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Heredity (2005) 95, 34 & 2005 Nature Publishing Group All rights reserved 0018-067X/05 $30.00 www.nature.com/hdy NEWS AND COMMENTARY Population genetics ............................................................... Nonrandom dispersal and local adaptation JF Storz ........................................................... Heredity (2005) 95, 34. doi:10.1038/sj.hdy.6800683 Published online 25 May 2005 wo recent studies of wild bird populations provide new insights into mechanisms of microevolutionary change by revealing how variation in tness-related traits may be maintained over very small spatial scales. When a population is distributed across a heterogeneous environment, the prospects for local adaptation depend on the spatial scale of tness variation relative to the spatial scale of dispersal. If the patchiness of environmental conditions is too ��e-grained�� the spatial acuity of natural selection may be severely diminished by the homogenizing effects of gene ow �� (Garca-Ramos and Kirkpatrick, 1997; Lenormand, 2002). For example, habitat variation over a scale of several square kilometers may be sufciently ��oarsegrained��to permit local adaptation in animals with weak dispersal capabilities like snails, but certainly not in more vagile animals like birds. So when nescale patterns of trait differentiation are observed in high gene ow species, some form of ecological or evolutionary explanation is required. These two new studies (Garant et al, 2005; Postma and van Noodwijk, 2005) involved long-term, longitudinal studies of free-ranging great tits (Parus major) in different parts of Europe. The study by Postma and van Noodwijk (2005) documented microgeographic variation in clutch size between subpopulations of great tits that inhabit opposite sides of the tiny (4022 ha) island of Vlieland in the Netherlands. Similarly, the study by Garant et al (2005) documented microgeographic variation in edgling mass between two ecologically distinct sectors of a contiguous woodland in Oxfordshire, England that are separated by less than 4 km. One possible explanation for the ne-scale patterns of differentiation is that the phenotypic variation between different habitats is environmentally induced. Indeed, a role for phenotypic plasticity in causing geographic variation in avian morphology would not be without precedent (James, 1983). Another possible explanation is that the T genetically based trait differences reect the cumulative effects of divergent natural selection toward different trait optima in the different habitats. In both studies, the authors were able to test these alternatives by tracking the natal dispersal and settlement of individually marked birds with known pedigrees: basically, the birds performed their own reciprocal transplant experiments. This allowed the authors to separate out the genetic and environmental components of trait variation. Importantly, the reciprocal transplant experiments also provided the opportunity to assess the tness consequences of genetically based trait variation in each of the different habitats. In both studies, results of pedigree-based analyses revealed that the observed patterns of trait differentiation were not attributable to phenotypic plasticity, nor did they reect habitat-specic differences in selection regimes. So how are these persistent differences in morphology and life history maintained over such small spatial scales? In both cases, nonrandom dispersal appears to be the key. In the case of the great tits on Vlieland (Postma and van Noodwijk, 2005), the microgeographic differentiation in clutch size can be explained by differences in the extent to which local subpopulations are prevented from attaining the islandspecic phenotypic optimum. Small clutches are favored on both the eastern and western sides of the island, but the subpopulation on the western side of the island receives a proportionally greater number of immigrants from outside the island that tend to carry genes for large clutch sizes. Consequently, the subpopulation on the western side of Vlieland receives a continual inux of maladaptive migrant alleles that contribute to an increase in average clutch size that exceeds the island-specic optimum. By contrast, the subpopulation on the eastern side of the island receives proportionally less immigration and the average clutch size remains closer to the island-specic optimum. In the case of the great tits in Oxfordshire (Garant et al, 2005), the microgeographic differentiation in edgling mass can be explained by two factors. One factor is the habitat-specic differences in the expression of genetically based trait variation, and the other, patterns of natal dispersal between habitats that are highly nonrandom with respect to phenotype. Since the evolutionary response to selection on a particular trait is directly proportional to the level of genetic variation in the trait, population differences in trait values could reect differences in heritability (ie the fraction of trait variation that is attributable to genetic differences between individuals) even if the populations are subject to the same selection pressures. This is the case in the woods of Oxfordshire: the heritability of edgling mass is considerably higher in the northern sector of the forest than in the eastern sector, such that the expected response to selection is roughly twice as high in the north. However, it seems likely that any trait variation caused by the habitat-specic differences in heritability would be swamped by gene ow, given that 460% of the breeding birds in a given area are born outside that area. It turns out that habitat-specic differences in the heritability of edgling mass are reinforced by nonrandom dispersal, as larger-than-average birds tend to settle in higher quality habitat in the northern sector of the forest. Thus, levels of genetically based trait variation and patterns of natal dispersal are both strongly inuenced by ne-scale variation in habitat quality. The studies by Garant et al (2005) and Postma and van Noodwijk (2005) are noteworthy because they demonstrate how nonrandom dispersal can promote genetic differentiation in tness-related traits even in the absence of spatial variation in the selection regime. In population genetic models, gene ow is typically viewed as a purely homogenizing force because the rate at which migrant alleles are introduced into a given population is assumed to be independent of their effects on tness. However, in the case of great tits, dispersal between different habitats appears to be highly phenotype dependent. So the alleles that inuence edgling mass and clutch size may be characterized by rates of migration that are nonrandom with respect to their effects on tness in different environments. Both of these studies should change the way we think about mechanisms of microevolutionary change. Geographic patterns of variation in tness-related News and Commentary 4 traits are often assumed to reect the interplay between the diversifying effects of local selection and the homogenizing effects of gene ow (Hendry et al, 2001). In contrast to this conventional view, the patterns of trait differentiation observed in great tits appear to reect the interplay between the diversifying effects of nonrandom dispersal and the homogenizing effects of spatially uniform selection. JF Storz is at the School of Biological Sciences, University of Nebraska, 314 Manter Hall, Lincoln, NE 68588, USA. e-mail: jstorz2@unl.edu Garant D, Kruuk LEB, Wilkin TA, McCleery RH, Sheldon BC (2005). Nature 433: 6065. �� Garca-Ramos G, Kirkpatrick M (1997). Evolution 51: 2128. Hendry AP, Day T, Taylor EB (2001). Evolution 55: 459466. James FC (1983). Science 221: 184186. Lenormand T (2002). Trends Ecol Evol 17: 183189. Postma E, van Noodwijk AJ (2005). Nature 433: 6568. Heredity