Evolution driven by differential dispersal within a wild bird population

Abstract

Evolutionary theory predicts that local population divergence will depend on the balance between the diversifying effect of selection and the homogenizing effect of gene flow1,2,3. However, spatial variation in the expression of genetic variation will also generate differential evolutionary responses. Furthermore, if dispersal is non-random it may actually reinforce, rather than counteract, evolutionary differentiation. Here we document the evolution of differences in body mass within a population of great tits, Parus major, inhabiting a single continuous woodland, over a 36-year period. We show that genetic variance for nestling body mass is spatially variable, that this generates different potential responses to selection, and that this diversifying effect is reinforced by non-random dispersal. Matching the patterns of variation, selection and evolution with population ecological data, we argue that the small-scale differentiation is driven by density-related differences in habitat quality affecting settlement decisions. Our data show that when gene flow is not homogeneous, evolutionary differentiation can be rapid and can occur over surprisingly small spatial scales. Our findings have important implications for questions of the scale of adaptation and speciation, and challenge the usual treatment of dispersal as a force opposing evolutionary differentiation.

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Figure 1: Distribution of standardized directional selection differentials for great tits for each year from 1965 to 2000 in Wytham13.
Figure 2: Within-population differences in great tit fledging mass trends from 1965 to 2000.
Figure 3: Temporal trends in fledging mass of great tit nestlings born within the eastern and northern parts of Wytham from 1965 to 2000.
Figure 4: Mean adult mass of great tits immigrating to the eastern and northern parts of Wytham.
Figure 5: Mean polygon area (m2) of breeding pairs of great tits in north (grey line, open circles) and east (black line, filled circles) areas over the study period (values are means ± 95% confidence intervals).

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Acknowledgements

We are grateful to A. Charmantier, A. G. Gosler, J. L. Quinn and C. M. Perrins for comments on the manuscript and to the many people who collected data during the long-term tit study in Wytham. D.G. was financially supported by a Natural Sciences and Engineering Research Council of Canada (NSERC) Postdoctoral Research Fellowship, and by a Biotechnology and Biological Sciences Research Council (BBSRC) grant to B.C.S. and L.E.B.K, who are both Royal Society University Research Fellows; T.A.W. was funded by a studentship from the BBSRC.Authors' contributions D.G. conducted analyses and discovered the original pattern, and drafted the manuscript together with B.C.S., who also provided overall guidance, and L.E.B.K., who also advised over quantitative genetic analyses. T.A.W. conducted spatial analyses. R.H.McC. maintained the long-term database.

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Correspondence to Dany Garant.

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Supplementary information

Supplementary Information Figure 1

Illustrates the detailed patterns of dispersal in Wytham woodland and shows the average annual contribution of residents and immigrants to each of the breeding area of the wood. (DOC 146 kb)

Supplementary Information Methods

This file contains further details on the difference between the statistical analyses performed using a cross-sectional (yearly average of individuals) approach versus a linear mixed modelling method (information for each individual included). (DOC 19 kb)

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Garant, D., Kruuk, L., Wilkin, T. et al. Evolution driven by differential dispersal within a wild bird population. Nature 433, 60–65 (2005). https://doi.org/10.1038/nature03051

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