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Adaptation to climate change through dispersal and inherited timing in an avian migrant

Nature Ecology & Evolution volume 7, pages 1869–1877 (2023)Cite this article

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Abstract

Many organisms fail to adjust their phenology sufficiently to climate change. Studies have concentrated on adaptive responses within localities, but little is known about how latitudinal dispersal enhances evolutionary potential. Rapid adaptation is expected if dispersers from lower latitudes have improved synchrony to northern conditions, thereby gain fitness and introduce genotypes on which selection acts. Here we provide experimental evidence that dispersal in an avian migrant enables rapid evolutionary adaptation. We translocated Dutch female pied flycatchers (Ficedula hypoleuca) and eggs to Sweden, where breeding phenology is ~15 days later. Translocated females bred earlier, and their fitness was 2.5 times higher than local Swedish flycatchers. We show that between-population variation in timing traits is highly heritable, and hence immigration of southern genotypes promotes the necessary evolutionary response. We conclude that studies on adaptation to large-scale environmental change should not just focus on plasticity and evolution based on standing genetic variation but should also include phenotype–habitat matching through dispersal as a viable route to adjust.

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Fig. 1: Translocation experiment of Dutch pied flycatchers to Sweden and their laying date compared to a control group.
Fig. 2: Mean number of recruits per nest of pied flycatcher females in Sweden, measured as locally returning offspring in the 2 years after the translocation treatment of a nest.
Fig. 3: Timing of spring migration and laying date of pied flycatchers in a common garden experiment.

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Data availability

All data used in the analyses are attached in the Source Data and available from DataverseNL (https://doi.org/10.34894/TXG0GC). Source data are provided with this paper.

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Acknowledgements

We are immensely grateful to the many researchers whose input and immense dedication collecting data in the field made this study possible. We particularly thank A. Maurukaite, J. Allain, R. Buhus, R. Engert, L. Jhaveri, H. Roodenrijs, T. Vamos, L. McBride, T. Micallef, E. Zuidema, K. Brouwer, A. Cillard, S. Barrault, J. Bliss, X. Wang and R. Ubels. We also thank S. Martens, who contributed unpublished data from his German study population. Staatsbosbeheer, Natuurmonumenten and Vombverket kindly allowed us to work on their properties. We thank B. Sheldon and P. Edelaar for commenting on an earlier draft. This publication and one of the field seasons was supported by a contribution to K.P.L. from the Meester Prikkebeen Fonds, managed by the Prins Bernhard Cultuurfonds, which oversees more than 450 CultuurFondsen. This study was funded by the Netherlands Organization for Scientific Research (NWO-ALW to C.B. ALWOP.171).

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Authors and Affiliations

  1. Conservation Ecology Group, Groningen Institute for Evolutionary Life Sciences (GELIFES), University of Groningen, Groningen, The Netherlands

    Koosje P. Lamers, Marion Nicolaus & Christiaan Both

  2. Department of Biology, Evolutionary Ecology Lab, Lund University, Lund, Sweden

    Jan-Åke Nilsson

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Contributions

All authors (K.P.L., M.N., J.-Å.N. and C.B.) contributed in conceiving the study and designing the experiments. K.P.L. collected the data in Sweden, and J.-Å.N. contributed vital support. C.B. and M.N. collected data in the Netherlands. K.P.L. analysed the data. K.P.L. and C.B. wrote the first draft. All authors (K.P.L., M.N., J.-Å.N. and C.B.) revised and commented on the manuscript and approved the final version.

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Correspondence to Koosje P. Lamers.

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Extended data

Extended Data Fig. 1 Timing of the Swedish unmanipulated pied flycatcher population compared with the Dutch population and experimental translocation groups.

(A) Mean first egg laying dates of unmanipulated pied flycatcher females in the Dutch and Swedish study sites. Data are shown for the experimental years 2017, 2018 and 2019. The error bars represent ± 2 s.e. and sample sizes and mean values are given in text. (B) Centred first egg laying dates of females of the different translocation treatments breeding in Vomb, Sweden. The bars are stacked in order: Dutch females translocated to Sweden (red), control translocations (blue) and unmanipulated females (grey).

Source data

Extended Data Fig. 2 Mean number of recruits per nest of pied flycatcher females of Dutch origin, measured as locally returning offspring in the two years after the translocation treatment of a nest.

This figure is equivalent to Fig. 2 in the main text: whilst there we examined the fitness of Dutch birds translocated to Sweden in comparison to the new local (Swedish) population, we here display their fitness compared to conspecifics at their location of origin. Data are plotted as four hatching date quantiles per treatment. Point size is scaled to the square root of the sample size of the quantile. The line represents averaged model estimates of a model including hatching date plotted over the range of observed values, with separate intercepts for the treatment groups because the Dutch translocated group had a significantly higher intercept (Extended Data Table 3CD). For each year, hatching date is centred to the median hatching date of unmanipulated females in the Netherlands (and hence the hatching dates differ from Fig. 2). Apart from the two treatment groups that were translocated (either from The Netherlands to Sweden (red dots; n = 20), or within the Netherlands (orange triangles; n = 20)) we also plot the unmanipulated Dutch nests (grey squares; n = 618).

Source data

Extended Data Fig. 3 Mean laying dates of the first egg over the years for pied flycatchers breeding in Vomb, Sweden.

Open symbols represent data we collected of unmanipulated females (2017-2020), while the closed symbols are data of the period 1971-2011 from Källander et al. (2017). The slope of the year-model is represented by the solid line (see Extended Data Table 7).

Source data

Extended Data Table 1 Model selection and estimates for the settlement rate of translocated females
Full size table
Extended Data Table 2 Model selection and estimates for the first egg laying dates of females of different translocation treatments breeding in Vomb, Sweden
Full size table
Extended Data Table 3 Model selection and estimates for the number of recruiting offspring of Dutch translocated females, compared to local control females and unmanipulated females
Full size table
Extended Data Table 4 Candidate models for the timing of spring annual cycle activities
Full size table
Extended Data Table 5 Model parameters for the best models for the timing of spring annual cycle activities (spring departure, spring arrival and laying date) of genetically Dutch, half Dutch, and Swedish pied flycatchers
Full size table
Extended Data Table 6 Model selection and estimates for the local recruitment rate in the two years after their birth of pied flycatcher chicks of different genetic categories born in Vomb, Sweden, in the years 2017-2019
Full size table
Extended Data Table 7 Results of mixed effects models of the relationship between laying dates of pied flycatchers and the covariates year and temperature, and with year (factor) as a random effect
Full size table

Supplementary information

Source data

Source Data Fig. 1

Laying dates of translocated females and their release date from the aviary. Same data as for Extended Data Table 2.

Source Data Fig. 2

Number of recruiting offspring after 2 years for females of the three translocation treatments (translocated to Sweden, within Sweden or unmanipulated in Sweden) and their hatching date (centred to the local Swedish population). Same data as for Extended Data Table 3a,b.

Source Data Fig. 3

Data for the timing of spring annual cycle activities (spring departure, spring arrival and laying date in separate files) for ‘nature’ comparisons (comparison between the groups of different genetic origin) and ‘nurture’ comparisons (comparisons between the Netherlands and Sweden for birds of genetically Dutch origin). Dates are in aprildate (1 = 1 April). Age is the number of years a bird is old (hatching in 2019 and spring arrival recorded in 2020 = 1 year old), and sex is female (1) or male (2). Same data as for Extended Data Tables 4 and 5.

Source Data Extended Data Table 1

Settlement rate data for females translocated within the Netherlands (NL_C), within Sweden (SE_C) or from the Netherlands to Sweden (SE_T). Settled = 1 and not settled = 0. The stage at which the female was translocated is included (NB, when nestbuilding; IN, at the start of incubation).

Source Data Extended Data Table 2

Laying dates of translocated females and their release date from the aviary. Same data as for Fig. 1.

Source Data Extended Data Table 3

a,b, Number of recruiting offspring after 2 years for females of the three translocation treatments (translocated to Sweden, within Sweden or unmanipulated in Sweden) and their hatching date (centred to the local Swedish population). Same data as for Fig. 2. c,d, Number of recruiting offspring after 2 years for females of the three translocation treatments (translocated to Sweden, within the Netherlands or unmanipulated in the Netherlands) and their hatching date (centred to the original Dutch population). Same data as for Extended Data Fig. 2.

Source Data Extended Data Table 4

Data for the timing of spring annual cycle activities (spring departure, spring arrival and laying date in separate files) for ‘nature’ comparisons (comparison between the groups of different genetic origin) and ‘nurture’ comparisons (comparisons between the Netherlands and Sweden for birds of genetically Dutch origin). Dates are in aprildate (1 = 1 April). Age is the number of years a bird is old (hatching in 2019 and spring arrival recorded in 2020 = 1 year old), and sex is female (1) or male (2). Same data as for Extended Data Table 5 and Fig. 3.

Source Data Extended Data Table 5

Data for the timing of spring annual cycle activities (spring departure, spring arrival and laying date in separate files) for ‘nature’ comparisons (comparison between the groups of different genetic origin) and ‘nurture’ comparisons (comparisons between the Netherlands and Sweden for birds of genetically Dutch origin). Dates are in aprildate (1 = 1 April). Age is the number of years a bird is old (hatching in 2019 and spring arrival recorded in 2020 = 1 year old), and sex is female (1) or male (2). Same data as for Extended Data Table 4 and Fig. 3.

Source Data Extended Data Table 6

Recruitment rate data for pied flycatchers of different genetic origins born in the Swedish common garden experiment. Birds are of 0%, 50% or 100% Dutch genetic origin and either were caught again at the study site within the two field seasons after the year of hatching (1) or were not caught again (0). The nest box and year combination is included to indicate family, as well as the total number of young hatched in that nest and the hatching date (centred to the median hatching date of the broods of unmanipulated Swedish females).

Source Data Extended Data Table 7

Laying data from pied flycatchers in the Vomb region from the Källander paper37. With added new years from our own field seasons. Temperature data were acquired in the same way as described in Källander et al.37, from the Swedish Meteorological and Hydrological Institute’s Lund weather station. Same data as for Extended Data Fig3.

Source Data Extended Data Fig. 1

a, Laying dates for unmanipulated Swedish and unmanipulated Dutch females in the years of our female translocation experiment. b, Laying dates (centred for each year to unmanipulated females) of females translocated from the Netherlands to Sweden, translocated within Sweden and unmanipulated.

Source Data Extended Data Fig. 2

Number of recruiting offspring after 2 years for females of the three translocation treatments (translocated to Sweden, within the Netherlands or unmanipulated in the Netherlands) and their hatching date (centred to the original Dutch population). Same data as for Extended Data Table 3c,d.

Source Data Extended Data Fig. 3

Laying data from pied flycatchers in the Vomb region from the Källander paper37. With added new years from our own field seasons. Temperature data were acquired in the same way as described in Källander et al.37, from the Swedish Meteorological and Hydrological Institute’s Lund weather station. Same data as for Extended Data Table 7.

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Lamers, K.P., Nilsson, JÅ., Nicolaus, M. et al. Adaptation to climate change through dispersal and inherited timing in an avian migrant. Nat Ecol Evol 7, 1869–1877 (2023). https://doi.org/10.1038/s41559-023-02191-w

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