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Imprinting sets the stage for speciation

Abstract

Sexual imprinting—a phenomenon in which offspring learn parental traits and later use them as a model for their own mate preferences—can generate reproductive barriers between species1. When the target of imprinting is a mating trait that differs among young lineages, imprinted preferences may contribute to behavioural isolation and facilitate speciation1,2. However, in most models of speciation by sexual selection, divergent natural selection is also required; the latter acts to generate and maintain variation in the sexually selected trait or traits, and in the mating preferences that act upon them3. Here we demonstrate that imprinting, in addition to mediating female mate preferences, can shape biases in male–male aggression. These biases can act similarly to natural selection to maintain variation in traits and mate preferences, which facilitates reproductive isolation driven entirely by sexual selection. Using a cross-fostering study, we show that both male and female strawberry poison frogs (Oophaga pumilio) imprint on coloration, which is a mating trait that has diverged recently and rapidly in this species4. Cross-fostered females prefer to court mates of the same colour as their foster mother, and cross-fostered males are more aggressive towards rivals that share the colour of their foster mother. We also use a simple population-genetics model to demonstrate that when both male aggression biases and female mate preferences are formed through parental imprinting, sexual selection alone can (1) stabilize a sympatric polymorphism and (2) strengthen the trait–preference association that leads to behavioural reproductive isolation. Our study provides evidence of imprinting in an amphibian and suggests that this rarely considered combination of rival and sexual imprinting can reduce gene flow between individuals that bear divergent mating traits, which sets the stage for speciation by sexual selection.

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Fig. 1: Map of the Bocas del Toro archipelago, showing the diversity of colour and pattern among populations of O. pumilio.
Fig. 2: O. pumilio rearing experiment.
Fig. 3: Polymorphism stability and associations between trait and preference.

Data availability

The datasets generated during and/or analysed during the current study have been deposited in Figshare (https://doi.org/10.6084/m9.figshare.9628406).

Code availability

Code files for statistical analysis (R) and mathematical models (Mathematica) have been deposited in Figshare (https://doi.org/10.6084/m9.figshare.9628406).

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Acknowledgements

We thank A. Benge, A. Devar, D. Gonzalez, R. Cossio, M. Dugas, T. Stetzinger, J. Yeager and G. Zawacki for help with the rearing experiments, and V. Prémel, J. P. Lawrence, S. A. Echeverri and I. J. Wang for providing photographs for the O. pumilio colour morphs. The Smithsonian Tropical Research Institute (STRI) provided logistical support for this project, and we are particularly grateful to G. Jacome and P. Gondola of the Bocas del Toro Field Station. This research was supported by the Smithsonian Institution, the University of California President’s Office, Tulane University’s Newcomb College Institute and the National Science Foundation (award numbers OISE-0701165 and DEB-1146370 to C.L.R.-Z. and DEB-1255777 to M.R.S.). The Panamanian National Authority for the Environment (ANAM) provided research and export permission for this study. This work complied with IACUC protocols (STRI no. 2007-17-12-15-07 and Tulane no. 0382).

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Contributions

C.L.R.-Z. designed the rearing experiment and collected data, and Y.Y. carried out statistical analyses, for the breeding experiment. Y.Y. and M.R.S. performed the theoretical research. Y.Y. drafted the manuscript, and M.R.S. and C.L.R.-Z. contributed to writing and revision.

Corresponding author

Correspondence to Yusan Yang.

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The authors declare no competing interests.

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Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Peer review information Nature thanks Peter Dijkstra, Leithen M’Gonigle and Machteld Nicolette Verzijden for their contribution to the peer review of this work.

Extended data figures and tables

Extended Data Fig. 1 Effects of starting frequency.

Simulations of 2,000 generations demonstrate the effects of the starting frequencies of alleles on the maintenance of polymorphism. Each panel represents a combination of a particular starting frequency for T1 (t1, labelled on top), association between mating trait and behaviour (phenogenotypic linkage disequilibrium (LD) between the trait genotype and the behavioural phenotype, labelled on the right) (Supplementary Information), and types of imprinting (maternal or paternal, labelled on the right). Within each panel, we ran every combination of α and β from 0.01 to 100, with a step size of 100.1. Axes are on logarithmic scales.

Extended Data Fig. 2 Frequency of the trait-1 phenotype at stable polymorphic equilibrium.

In this extended model, the value of α and β varies with the phenotype on which the individual imprinted (Supplementary Information). Frequency of the trait-1 phenotype includes T11 and T12 individuals (x1x2x4x5). Each panel represents a particular combination of α1 and β1 from the set {0.01, 1, 100}, labelled on the top and the right. Within each panel, we ran every combination of α2 and β2 from 0.01 to 100, with a step size of 100.2. Axes are on logarithmic scales. The white area in each panel is the parameter space in which no stable polymorphism can be found. The frequency of the trait-1 phenotype at polymorphic equilibrium for a given combination of αk and βk is slightly different between the models of maternal and paternal imprinting (<0.1, not shown).

Extended Data Fig. 3 Dcor at stable polymorphic equilibrium.

In this extended model, the value of α and β varies with the phenotype that the individual imprinted on (Supplementary Information). Trait–behaviour linkage disequilibrium between the trait genotype and the behavioural phenotype (Dcor, calculated as D/√(p1p2t1t2)) at the stable polymorphic equilibrium. Each panel represents a particular combination of α1 and β1 from the set {0.01, 1, 100}, labelled on the top and the right. Within each panel, we ran combinations of α2 and β2 from 0.01 to 100, with a step size of 100.2. Axes are on logarithmic scales. The figure presents results from maternal imprinting models. Overall, the paternal imprinting models produced higher Dcor at polymorphic equilibrium than did the maternal imprinting models, but the differences were very small (<0.1, not shown).

Extended Data Table 1 Proportions of association time for the three groups of rearing treatment
Extended Data Table 2 Proportions of approaches for the three groups of rearing treatment

Supplementary information

Supplementary Information

This file contains Supplementary section S1 (rearing experiment), Supplementary section S2 (population genetic models) and associated references.

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Yang, Y., Servedio, M.R. & Richards-Zawacki, C.L. Imprinting sets the stage for speciation. Nature 574, 99–102 (2019). https://doi.org/10.1038/s41586-019-1599-z

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