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

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‐n...

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Main Authors: William C. Rosenthal, Peter B. McIntyre, Peter J. Lisi, Robert B. Prather Jr., Kristine N. Moody, Michael J. Blum, James Derek Hogan, Sean D. Schoville
Format: Article
Language:English
Published: Wiley 2021-07-01
Series:Evolutionary Applications
Subjects:
Online Access:https://doi.org/10.1111/eva.13236
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author William C. Rosenthal
Peter B. McIntyre
Peter J. Lisi
Robert B. Prather Jr.
Kristine N. Moody
Michael J. Blum
James Derek Hogan
Sean D. Schoville
author_facet William C. Rosenthal
Peter B. McIntyre
Peter J. Lisi
Robert B. Prather Jr.
Kristine N. Moody
Michael J. Blum
James Derek Hogan
Sean D. Schoville
author_sort William C. Rosenthal
collection DOAJ
description 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.
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spelling doaj.art-cb08424844fd4e78a19c6e217ce71d792022-12-21T20:12:32ZengWileyEvolutionary Applications1752-45712021-07-011471747176110.1111/eva.13236Invasion and rapid adaptation of guppies (Poecilia reticulata) across the Hawaiian ArchipelagoWilliam C. Rosenthal0Peter B. McIntyre1Peter J. Lisi2Robert B. Prather Jr.3Kristine N. Moody4Michael J. Blum5James Derek Hogan6Sean D. Schoville7Center for Limnology University of Wisconsin‐Madison Madison WI USACenter for Limnology University of Wisconsin‐Madison Madison WI USACenter for Limnology University of Wisconsin‐Madison Madison WI USADepartment of Evolution, Ecology, and Organismal Biology University of California Riverside Riverside CA USADepartment of Ecology and Evolutionary Biology University of Tennessee Knoxville Knoxville TN USADepartment of Ecology and Evolutionary Biology University of Tennessee Knoxville Knoxville TN USADepartment of Life Sciences Texas A&M University‐Corpus Christi Corpus Christi TX USADepartment of Entomology University of Wisconsin‐Madison Madison WI USAAbstract 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.https://doi.org/10.1111/eva.13236biological adaptationHawai‘iintroduced speciesmolecular evolutionpopulation genomics
spellingShingle William C. Rosenthal
Peter B. McIntyre
Peter J. Lisi
Robert B. Prather Jr.
Kristine N. Moody
Michael J. Blum
James Derek Hogan
Sean D. Schoville
Invasion and rapid adaptation of guppies (Poecilia reticulata) across the Hawaiian Archipelago
Evolutionary Applications
biological adaptation
Hawai‘i
introduced species
molecular evolution
population genomics
title Invasion and rapid adaptation of guppies (Poecilia reticulata) across the Hawaiian Archipelago
title_full Invasion and rapid adaptation of guppies (Poecilia reticulata) across the Hawaiian Archipelago
title_fullStr Invasion and rapid adaptation of guppies (Poecilia reticulata) across the Hawaiian Archipelago
title_full_unstemmed Invasion and rapid adaptation of guppies (Poecilia reticulata) across the Hawaiian Archipelago
title_short Invasion and rapid adaptation of guppies (Poecilia reticulata) across the Hawaiian Archipelago
title_sort invasion and rapid adaptation of guppies poecilia reticulata across the hawaiian archipelago
topic biological adaptation
Hawai‘i
introduced species
molecular evolution
population genomics
url https://doi.org/10.1111/eva.13236
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