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Evolutionary origins of genomic adaptations in an invasive copepod

Nature Ecology & Evolution volume 4, pages 1084–1094 (2020)Cite this article

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Abstract

The ability of populations to expand their geographical ranges, whether as invaders, agricultural strains or climate migrants, is currently one of the most serious global problems. However, fundamental mechanisms remain poorly understood regarding factors that enable certain populations, such as biological invaders, to rapidly transition to novel habitats. According to one hypothesis, environmental fluctuations in the native range could promote successful invasions by imposing balancing selection on key traits and maintaining the genetic variation that enables rapid adaptation in novel habitats. Here we test the genomic predictions of this hypothesis by performing whole-genome sequencing of multiple independent invasive freshwater and native saline populations of the copepod Eurytemora affinis complex. We found that invasive populations have repeatedly responded to selection through the parallel use of the same single-nucleotide polymorphisms and genomic loci, to a much greater degree than expected. These same loci were enriched for signatures of long-term balancing selection in the native ranges, with 15–47% of loci exhibiting significant signatures of balancing selection. The strong association between parallel evolution in the invaded range and balancing selection in the native range supports the hypothesis that fluctuating habitats can promote invasive success and that balancing selection might serve as a widespread and important mechanism that enables rapid adaptation in nature.

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Fig. 1: Population genomic signatures of parallel freshwater invasions.
Fig. 2: Signatures of directional and balancing selection at the NHA cluster in the E. affinis complex genome.
Fig. 3: Loci with signatures of parallel directional selection and association with salinity are enriched for signatures of long-term balancing selection in the native ranges.
Fig. 4: Alternative models of ion uptake from freshwater environments.

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Data availability

Raw sequence data and aligned reads have been deposited in the NCBI Sequence Read Archive under BioProject ID PRJNA610547.

Code availablility

Custom scripts used throughout this analysis are available online at https://github.com/TheDBStern/NEE2020.

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Acknowledgements

This research was funded by National Science Foundation grants OCE-1046372 and OCE-1658517 to C.E.L. and the Michael Guyer Postdoctoral Fellowship to D.B.S. We thank J. Pool, S. Schoville and N. Sharpe for comments on the manuscript. The samples used in this project were collected by M. Bontrager. Computation was performed using the computational resources and assistance of the UW-Madison Center for High Throughput Computing (CHTC) in the Department of Computer Sciences.

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  1. Department of Integrative Biology, University of Wisconsin-Madison, Madison, WI, USA

    David Ben Stern & Carol Eunmi Lee

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C.E.L. contributed to the design of the study and data collection. D.B.S. contributed to the conception and execution of the analyses. Both authors contributed to the writing and approval of the final manuscript.

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Correspondence to Carol Eunmi Lee.

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Extended data

Extended Data Fig. 1 β(2) and NCD2 score density plot for the native, saline Baie de L’Isle Verte population (St. Lawrence drainage, Atlantic clade).

Higher β(2) scores and lower NCD2 scores signify stronger signatures of long-term balancing selection. β(2) scores are higher and NCD2 scores are lower on average for ‘parallel’ candidate SNPs (blue) relative to the rest of the genome (grey).

Extended Data Fig. 2 β(2) and NCD2 score density plot for the native, saline Taylor Bayou (Gulf of Mexico, Gulf clade).

Higher β(2) scores and lower NCD2 scores signify stronger signatures of long-term balancing selection. β(2) scores are higher and NCD2 scores are lower on average for ‘parallel’ candidate SNPs (blue) relative to the rest of the genome (grey).

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Supplementary Box 1, Materials and Methods.

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Stern, D.B., Lee, C.E. Evolutionary origins of genomic adaptations in an invasive copepod. Nat Ecol Evol 4, 1084–1094 (2020). https://doi.org/10.1038/s41559-020-1201-y

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