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Mito-nuclear selection induces a trade-off between species ecological dominance and evolutionary lifespan

Nature Ecology & Evolution volume 6, pages 1992–2002 (2022)Cite this article

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Abstract

Mitochondrial and nuclear genomes must be co-adapted to ensure proper cellular respiration and energy production. Mito-nuclear incompatibility reduces individual fitness and induces hybrid infertility, which can drive reproductive barriers and speciation. Here, we develop a birth–death model for evolution in spatially extended populations under selection for mito-nuclear co-adaptation. Mating is constrained by physical and genetic proximity, and offspring inherit nuclear genomes from both parents, with recombination. The model predicts macroscopic patterns including a community’s species diversity, species abundance distribution, speciation and extinction rates, as well as intraspecific and interspecific genetic variation. We explore how these long-term outcomes depend upon the parameters of reproduction: individual fitness governed by mito-nuclear compatibility, constraints on mating compatibility and ecological carrying capacity. We find that strong selection for mito-nuclear compatibility reduces the equilibrium number of species after a radiation, increasing species’ abundances and simultaneously increasing both speciation and extinction rates. The negative correlation between species diversity and diversification rates in our model agrees with the broad empirical pattern of lower diversity and higher speciation/extinction rates in temperate regions, compared to the tropics. We conclude that these empirical patterns may be caused in part by latitudinal variation in metabolic demands and corresponding variation in selection for mito-nuclear function.

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Fig. 1: Model of selection for mito-nuclear compatibility.
Fig. 2: Diversification events and species richness.
Fig. 3: Species abundances distributions at time T = 1,000 and species lifespans.
Fig. 4: Long-term evolutionary fates of species that were extant at time T = 1,000.
Fig. 5: Genetic diversity within and between species.
Fig. 6: From selection at the individual level to ecological and macro-evolutionary patterns.

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Data availability

There are no empirical data associated with this study.

Code availability

All simulations were coded in Fortran. All code for simulations and Python scripts for data analysis are available in the GitHub repository at https://github.com/deborapr/mito-nuclear-speciation.

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Acknowledgements

This work was partly supported by the São Paulo Research Foundation (FAPESP), grant nos. 2018/11187-8 (D.P.), 2019/24449-3 (D.P.), 2019/20271-5 (M.A.M.A.) and 2016/01343-7 (ICTP-SAIFR). M.A.M.A. was supported by Conselho Nacional de Pesquisas Científicas, grant no. 301082/2019-7. J.B.P. and D.P. acknowledge support from the David & Lucille Packard Foundation and Simons Foundation (Math+X grant to the University of Pennsylvania).

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Authors and Affiliations

  1. Instituto de Física ‘Gleb Wataghin’, Universidade Estadual de Campinas, Campinas, Brazil

    Débora Princepe & Marcus A. M. de Aguiar

  2. Department of Biology, University of Pennsylvania, Philadelphia, PA, USA

    Débora Princepe & Joshua B. Plotkin

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D.P. performed the simulations and wrote the manuscript draft. D.P., M.A.M.A. and J.B.P. conceived and designed the study, analysed the data and contributed to interpretation of the data and the manuscript revisions.

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Correspondence to Débora Princepe.

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Princepe, D., de Aguiar, M.A.M. & Plotkin, J.B. Mito-nuclear selection induces a trade-off between species ecological dominance and evolutionary lifespan. Nat Ecol Evol 6, 1992–2002 (2022). https://doi.org/10.1038/s41559-022-01901-0

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