Transgenerational selection driven by divergent ecological impacts of hybridizing lineages

Abstract

Dynamic interactions between ecological conditions and the phenotypic composition of populations likely play an important role in evolution, but the direction and strength of these feedbacks remain difficult to characterize. We investigated these dynamics across two generations of threespine sticklebacks from two evolutionary lineages undergoing secondary contact and hybridization. Independently manipulating the density and lineage of adults in experimental mesocosms led to contrasting ecosystem conditions with strong effects on total survival in a subsequent generation of juveniles. Ecosystem modifications by adults also varied the strength of selection on competing hybrid and non-hybrid juveniles. This variation in selection indicated (1) a negative eco-evolutionary feedback driven by lineage-specific resource depletion and dependence and (2) a large performance advantage of hybrid juveniles in depleted environments. This work illustrates the importance of interactions between phenotype, population density and the environment in shaping selection and evolutionary trajectories, especially in the context of range expansion with secondary contact and hybridization.

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Fig. 1: Location and phenotypic divergence of two major evolutionary lineages of threespine sticklebacks in Switzerland.
Fig. 2: Effects of adult fish on experimental ecosystems, including prey availability, habitat structure and GPP.
Fig. 3: Juvenile survival and condition.
Fig. 4: Determinants of selection on juveniles.
Fig. 5: Stable isotope signatures of juvenile fish and potential prey.

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Acknowledgements

We thank M. Lürig, G. Antoniazza, E. Birnstiel, L. Catalano, K. Müller, A. Taverna, E. Schäffer, F. Brunner, D. Hohmann and D. Steiner for major contributions to fish breeding and care, as well as experimental set-up, maintenance and sampling. We thank K. Lucek, S. Mwaiko and C. Schmid for assistance with microsatellite genotyping, and D. Marques and M. McGee for input on the study system and experimental design. S. Robert, P. Kathriner and B. Kienholz provided laboratory facilities and infrastructure support. We thank M. Rheinhof for access to sampling sites on Lake Constance.

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B.M., J.M.A.-R., O.S. and R.J.B. designed the core experiment. R.J.B. and J.M.A.-R. carried out the experiment. M.C.L. designed and carried out the isotopic analysis, and D.W.S. provided supplementary data on feeding efficiency. R.J.B. analysed the data and wrote the manuscript with substantial contributions and revisions from all authors.

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Correspondence to Rebecca J. Best.

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Best, R.J., Anaya-Rojas, J.M., Leal, M.C. et al. Transgenerational selection driven by divergent ecological impacts of hybridizing lineages. Nat Ecol Evol 1, 1757–1765 (2017). https://doi.org/10.1038/s41559-017-0308-2

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