Sexual size dimorphism in mammals is associated with changes in the size of gene families related to brain development

Benjamin Padilla Morales; Alin Patricia Acuna Alonzo; Albus Kilili; Atahualpa Castillo Morales; Karina Díaz-Barba; Kathryn Maher; Laurie Fabian; Evangelos Mourkas; Tamás Székely; Martin Alejandro Serrano-Meneses; Diego Cortez; Sergio Ancona; Araxi Urrutia

doi:10.1038/s41467-024-50386-x

Sexual size dimorphism in mammals is associated with changes in the size of gene families related to brain development

Benjamin Padilla Morales
, Alin Patricia Acuna Alonzo
, Albus Kilili
, Atahualpa Castillo Morales
, Karina Díaz-Barba
, Kathryn Maher
, Laurie Fabian
, Evangelos Mourkas
, Tamás Székely
, Martin Alejandro Serrano-Meneses
, Diego Cortez
, Sergio Ancona
, Araxi Urrutia

Cardiff University
Universidad Nacional Autónoma de México
Uppsala University
University of Sheffield
Universidad de las Américas Puebla
Instituto de Ecología, UNAM

Research output: Contribution to journal › Article › peer-review

3 Citations (SciVal)

Abstract

In mammals, sexual size dimorphism often reflects the intensity of sexual selection, yet its connection to genomic evolution remains unexplored. Gene family size evolution can reflect shifts in the relative importance of different molecular functions. Here, we investigate the associate between brain development gene repertoire to sexual size dimorphism using 124 mammalian species. We reveal significant changes in gene family size associations with sexual size dimorphism. High levels of dimorphism correlate with an expansion of gene families enriched in olfactory sensory perception and a contraction of gene families associated with brain development functions, many of which exhibited particularly high expression in the human adult brain. These findings suggest a relationship between intense sexual selection and alterations in gene family size. These insights illustrate the complex interplay between sexual dimorphism, gene family size evolution, and their roles in mammalian brain development and function, offering a valuable understanding of mammalian genome evolution.

Original language	English
Article number	6257
Journal	Nature Communications
Volume	15
Issue number	1
Early online date	24 Jul 2024
DOIs	https://doi.org/10.1038/s41467-024-50386-x
Publication status	Published - 31 Dec 2024

Data Availability Statement

All source data and datasets are provided with this paper. Supplementary Data 1 contains the gene family expansion/contraction analysis for sexual size dimorphism along with their corresponding statistical significance per gene family. Supplementary Data 2 provides the average gene expression levels in different tissues for adults and prenatal stages. Supplementary Data 3 includes the BrainSpan data (https://www.brainspan.org/static/download.html) used for the brain tissue-specific gene expression analysis. It includes Gene stable ID to Entrez Gene ID to GO category with gene expression and foldchange results with p-values. Supplementary Data 4 lists the species used in the analysis with phenotypical data and sources. Supplementary Data 5 presents the accession names of the CDS sequences for each species used for orthology mapping analysis, also including the download links from the Refseq FTP repository (https://ftp.ncbi.nlm.nih.gov/genomes/all/). Supplementary Data 6 contains the output from gene family expansion/contraction analysis, including zero variance gene families for sexual size dimorphism. Supplementary Data 7 lists the species with brain size used in the research, along with references. Lastly, Supplementary Table 1 provides a list of terms, abbreviations, and descriptions of brain structures used for sex-biased gene expression in temporal brain analysis. Supplementary files are available on the Figshare repository (https://doi.org/10.6084/m9.figshare.22770731). Source data are provided with this paper.

Acknowledgements

We thank professors Laurence Hurst, Jason Wolf, and Dr. Nick Longrich for their valuable advice.

Funding

This study was supported by a University of Bath Ph.D. fee scholarship to B.P.-M.; TRNC Department of Higher Education and Foreign Affairs State Scholarship for Doctoral Studies, The Korner Travelling Fellowship Fund 2020 and Santander Mobility Award 2020 to H.K.; CONACyT PhD scholarships to A.P.A.-A. and A.C.-M.; a NERC GW4+ studentship (NE/L002434/1) to K.H.M., a travel grant SEP-UNAM-FUNAM Programa de Capacitación en Métodos de investigación, the Korner Travelling Fellowship Fund and TELMEX foundation fellowship to K.D.-B.; a Frontiers in Science CONACyT grant (No. FC-2016 /1682) and a Royal Society Newton Advanced Fellowship (no. NA160564) to T.S., D.C. and A.O.U.; a Frontiers in Science CONACyT (FC-2020/682142) to S.A., D.C., T.S. and A.O.U.; a NERC grant (NE/P004121/1) and PAPPIT-DGAPA-UNAM grant (IA204020) to A.O.U.

Funders	Funder number
TELMEX foundation
University of Bath
Consejo Nacional de Ciencia y Tecnologia
Royal Society Newton	FC-2020/682142, NA160564, NE/P004121/1
Frontiers in Science CONACyT	FC-2016 /1682
PAPPIT-DGAPA-UNAM	IA204020
Natural Environment Research Council	NE/L002434/1

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Padilla Morales, B., Acuna Alonzo, A. P., Kilili, A., Castillo Morales, A., Díaz-Barba, K., Maher, K., Fabian, L., Mourkas, E., Székely, T., Serrano-Meneses, M. A., Cortez, D., Ancona, S., & Urrutia, A. (2024). Sexual size dimorphism in mammals is associated with changes in the size of gene families related to brain development. Nature Communications, 15(1), Article 6257. https://doi.org/10.1038/s41467-024-50386-x

Padilla Morales, B, Acuna Alonzo, AP, Kilili, A, Castillo Morales, A, Díaz-Barba, K, Maher, K, Fabian, L, Mourkas, E, Székely, T, Serrano-Meneses, MA, Cortez, D, Ancona, S & Urrutia, A 2024, 'Sexual size dimorphism in mammals is associated with changes in the size of gene families related to brain development', Nature Communications, vol. 15, no. 1, 6257. https://doi.org/10.1038/s41467-024-50386-x

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Sexual size dimorphism in mammals is associated with changes in the size of gene families related to brain development

Abstract

Data Availability Statement

Acknowledgements

Funding

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