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Convergent adaptation and ecological speciation result from unique genomic mechanisms in sympatric extremophile fishes

View ORCID ProfileRyan Greenway, View ORCID ProfileAnthony P. Brown, View ORCID ProfileHenry Camarillo, Cassandra Delich, View ORCID ProfileKerry L. McGowan, Joel Nelson, View ORCID ProfileLenin Arias-Rodriguez, View ORCID ProfileJoanna L. Kelley, View ORCID ProfileMichael Tobler
doi: https://doi.org/10.1101/2021.06.28.450104
Ryan Greenway
1Division of Biology, Kansas State University, Manhattan, KS, USA
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  • For correspondence: ryansgreenway@gmail.com joanna.l.kelley@wsu.edu tobler@ksu.edu
Anthony P. Brown
2School of Biological Sciences, Washington State University, Pullman, WA, USA
3California National Primate Research Center, University of California, Davis, Davis, CA, USA
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Henry Camarillo
1Division of Biology, Kansas State University, Manhattan, KS, USA
4Department of Ecology and Evolutionary Biology, Yale University, New Haven, CT, USA
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Cassandra Delich
1Division of Biology, Kansas State University, Manhattan, KS, USA
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Kerry L. McGowan
2School of Biological Sciences, Washington State University, Pullman, WA, USA
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Joel Nelson
2School of Biological Sciences, Washington State University, Pullman, WA, USA
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Lenin Arias-Rodriguez
5División Académica de Ciencias Biológicas, Universidad Juárez Autónoma de Tabasco, Villahermosa, Tabasco, Mexico
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Joanna L. Kelley
2School of Biological Sciences, Washington State University, Pullman, WA, USA
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  • For correspondence: ryansgreenway@gmail.com joanna.l.kelley@wsu.edu tobler@ksu.edu
Michael Tobler
1Division of Biology, Kansas State University, Manhattan, KS, USA
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  • For correspondence: ryansgreenway@gmail.com joanna.l.kelley@wsu.edu tobler@ksu.edu
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Abstract

Divergent selection along ecological gradients can lead to speciation, and replicated speciation events occur when populations of multiple lineages undergo divergence following colonization of similar environments. In such instances, it remains unclear to what extent reproductive isolation evolves via convergent mechanisms at the genomic level due to biases associated with shared ancestry and variation in selection associated with geographic replicates typically studied in this context. We used a unique system in which three species of poeciliid fishes occur in sympatry in a toxic, hydrogen sulfide (H2S)-rich spring and an adjacent nonsulfidic stream to examine shared patterns of adaptive divergence across multiple levels of biological organization. Despite small spatial scales, we found strong genetic differentiation between populations in sulfidic and nonsulfidic habitats mediated by strong selection against migrants between habitat types. High levels of reproductive isolation were accompanied by convergent patterns of adaptation in morphological and physiological traits, as well as genome-wide patterns of gene expression across all three species. Furthermore, the mitochondrial genomes of each species exhibit shared signatures of selection on key genes involved in H2S toxicity. However, contrary to predictions of speciation theory, analyses of divergence across the nuclear genomes neither revealed evidence for clear genomic islands of speciation nor substantial congruence of outlier regions across population pairs. Instead, heterogenous regions of divergence spread across the genome suggest that selection for polygenic physiological adaptations likely facilitated the rapid evolution of high levels of reproductive isolation. Overall, we demonstrate that substantial convergence across multiple levels of biological organization can be mediated by non-convergent modifications at the genomic level. By disentangling variation in natural selection from lineage-specific evolution in this system of highly divergent, yet sympatric lineages, our results emphasize the outsized role of the genomic substrate upon which selection acts in driving convergent evolution at the phenotypic level.

Significance Statement Divergent lineages that coexist in sympatry and are exposed to the same sources of natural selection provide a unique opportunity to study convergent evolution across levels of organization because confounding factors associated with geographic replications are eliminated. Using three sympatric lineages of livebearing fishes inhabiting toxic and adjacent nontoxic habitats, we show that the convergent evolution of phenotypic adaptation and reproductive isolation can evolve in the absence of substantial convergence at the genomic level. Our results suggest that the nature of selection is less important in producing genomic convergence than the initial genomic substrates that are available for selection to act on.

Competing Interest Statement

The authors have declared no competing interest.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. All rights reserved. No reuse allowed without permission.
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Convergent adaptation and ecological speciation result from unique genomic mechanisms in sympatric extremophile fishes
Ryan Greenway, Anthony P. Brown, Henry Camarillo, Cassandra Delich, Kerry L. McGowan, Joel Nelson, Lenin Arias-Rodriguez, Joanna L. Kelley, Michael Tobler
bioRxiv 2021.06.28.450104; doi: https://doi.org/10.1101/2021.06.28.450104
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Convergent adaptation and ecological speciation result from unique genomic mechanisms in sympatric extremophile fishes
Ryan Greenway, Anthony P. Brown, Henry Camarillo, Cassandra Delich, Kerry L. McGowan, Joel Nelson, Lenin Arias-Rodriguez, Joanna L. Kelley, Michael Tobler
bioRxiv 2021.06.28.450104; doi: https://doi.org/10.1101/2021.06.28.450104

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