Invasion and rapid adaptation of guppies (Poecilia reticulata) across the Hawaiian Archipelago

William C. Rosenthal, Peter B. McIntyre, Peter J. Lisi, Robert B. Prather, Kristine N. Moody, Michael J. Blum, James Derek Hogan, Sean D. Schoville

Research output: Contribution to journalArticlepeer-review

7 Scopus citations

Abstract

How much does natural selection, as opposed to genetic drift, admixture, and gene flow, contribute to the evolution of invasive species following introduction to a new environment? Here we assess how evolution can shape biological invasions by examining population genomic variation in non-native guppies (Poecilia reticulata) introduced to the Hawaiian Islands approximately a century ago. By examining 18 invasive populations from four Hawaiian islands and four populations from the native range in northern South America, we reconstructed the history of introductions and evaluated population structure as well as the extent of ongoing gene flow across watersheds and among islands. Patterns of differentiation indicate that guppies have developed significant population structure, with little natural or human-mediated gene flow having occurred among populations following introduction. Demographic modeling and admixture graph analyses together suggest that guppies were initially introduced to O‘ahu and Maui and then translocated to Hawai‘i and Kaua‘i. We detected evidence for only one introduction event from the native range, implying that any adaptive evolution in introduced populations likely utilized the genetic variation present in the founding population. Environmental association tests accounting for population structure identified loci exhibiting signatures of adaptive variation related to predators and landscape characteristics but not nutrient regimes. When paired with high estimates of effective population sizes and detectable population structure, the presence of environment-associated loci supports the role of natural selection in shaping contemporary evolution of Hawaiian guppy populations. Our findings indicate that local adaptation may engender invasion success, particularly in species with life histories that facilitate rapid evolution. Finally, evidence of low gene flow between populations suggests that removal could be an effective approach to control invasive guppies across the Hawaiian archipelago.

Original languageEnglish
Pages (from-to)1747-1761
Number of pages15
JournalEvolutionary Applications
Volume14
Issue number7
DOIs
StatePublished - Jul 2021

Funding

The authors thank the Cornell Museum of Vertebrates for providing the tissue samples from Venezuela. This research was supported by the University of Wisconsin—Madison's Holstrom Environmental Research Fellowship, the Zoology Undergraduate Summer Research Award, and the Chase‐Noland Research Fellowship. Additional funding was provided by the Department of Defense Strategic Environmental Research and Development Program (SERDP) through projects RC‐1646 and RC‐2447 and by a Packard Fellowship in Science & Engineering. This manuscript has been authored in part by UT‐Battelle, LLC, under contract DE‐AC05‐00OR22725 with the US Department of Energy (DOE). The US government retains and the publisher, by accepting the article for publication, acknowledges that the US government retains a nonexclusive, paid‐up, irrevocable, worldwide license to publish or reproduce the published form of this manuscript, or allow other to do so, for US government purposes. DOE will provide public access to these results of federally sponsored research in accordance with the DOE Public Access Plan ( http://energy.gov/downloads/doe‐public‐access‐plan ).

FundersFunder number
Department of Defense Strategic Environmental Research and Development Program
University of Wisconsin—Madison's Holstrom Environmental Research Fellowship
U.S. Department of Energy
Strategic Environmental Research and Development ProgramRC‐2447, RC‐1646

    Keywords

    • Hawai‘i
    • biological adaptation
    • introduced species
    • molecular evolution
    • population genomics

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