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Early neurogenomic response associated with variation in guppy female mate preference

Abstract

Understanding the evolution of mate choice requires dissecting the mechanisms of female preference, particularly how these differ among social contexts and preference phenotypes. Here, we studied the female neurogenomic response after only 10 min of mate exposure in both a sensory component (optic tectum) and a decision-making component (telencephalon) of the brain. By comparing the transcriptional response between females with and without preferences for colourful males, we identified unique neurogenomic elements associated with the female preference phenotype that are not present in females without preference. A network analysis revealed different properties for this response at the sensory-processing and the decision-making levels, and we show that this response is highly centralized in the telencephalon. Furthermore, we identified an additional set of genes that vary in expression across social contexts, beyond mate evaluation. We show that transcription factors among these loci are predicted to regulate the transcriptional response of the genes we found to be associated with female preference.

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Fig. 1: Experimental set-up used to find neurogenomic pathways associated with mate preferences.
Fig. 2: Hierarchical gene-expression clustering of Preference DE genes.
Fig. 3: Optic tectum and telencephalon co-expression networks’ module overview.
Fig. 4: Differential transcriptional signature of Social DE genes in females exposed to attractive males.

Data availability

Normalized counts for all groups of differentially expressed genes as well as all expressed genes are available in Supplementary Data 1 and 2. RNA reads have been deposited at the NCBI Sequencing Read Archive, BioProject ID PRJNA413692. Additional data may be requested from the authors.

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Acknowledgements

This work was funded by a Marie Sklodowska-Curie Fellowship (654699) and a National Science Foundation Postdoctoral Fellowship in Biology (1523669) to N.I.B., by grant agreements 260233 and 680951 from the European Research Council to J.E.M., a Swedish Research Council grant (2016-03435) to N.K. and a Knut and Alice Wallenberg grant (102 2013.0072) to N.K. We gratefully acknowledge support from a Royal Society Wolfson Merit Award to J.E.M. We thank P. Almeida, I. Darolti, J. Morris, V. Oostra, A. Wright and T. Price for valuable discussions and help with manuscript preparation. We thank the Oxford Genomics Centre at the Wellcome Centre for Human Genetics (funded by a Wellcome Trust grant (reference 203141/Z/16/Z)) for the generation and initial processing of the sequencing data, and the UCL Legion High Performance Computing Facility (Legion@UCL).

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N.I.B., A.C.-L., N.K. and J.E.M. conceived of the study and designed the experiments. A.K. and N.K. created the brain size selection lines. A.K. and S.D.B. performed laboratory work for fish housekeeping. A.C.-L. and S.D.B. selected fish for the experiments. A.C.-L. performed the behavioural tests and dissected the brain regions. N.I.B. performed all laboratory RNA work and analysed the data. All authors contributed to writing the manuscript.

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Correspondence to Natasha I. Bloch.

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Supplementary Data 1

Optic tectum normalized count data for differentially expressed genes

Supplementary Data 2

Telencephalon normalized count data for differentially expressed genes

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Bloch, N.I., Corral-López, A., Buechel, S.D. et al. Early neurogenomic response associated with variation in guppy female mate preference. Nat Ecol Evol 2, 1772–1781 (2018). https://doi.org/10.1038/s41559-018-0682-4

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