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Title: 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-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 nutrientmore » 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.« less

Authors:
ORCiD logo [1];  [2];  [3];  [4];  [5];  [6];  [7]; ORCiD logo [3]
  1. Univ. of Wisconsin, Madison, WI (United States); Univ. of Wyoming, Laramie, WY (United States)
  2. Univ. of Wisconsin, Madison, WI (United States); Cornell Univ., Ithaca, NY (United States)
  3. Univ. of Wisconsin, Madison, WI (United States)
  4. Univ. of California, Riverside, CA (United States)
  5. Univ. of Tennessee, Knoxville, TN (United States); Tulane Univ., New Orleans, LA (United States); Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
  6. Univ. of Tennessee, Knoxville, TN (United States); Tulane Univ., New Orleans, LA (United States)
  7. Texas A & M Univ., Corpus Christi, TX (United States)
Publication Date:
Research Org.:
Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)
Sponsoring Org.:
USDOE; USDOD
OSTI Identifier:
1783028
Grant/Contract Number:  
AC05-00OR22725; RC-1646; RC-2447
Resource Type:
Accepted Manuscript
Journal Name:
Evolutionary Applications
Additional Journal Information:
Journal Volume: 14; Journal Issue: 7; Journal ID: ISSN 1752-4571
Publisher:
Wiley
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; biological adaptation; Hawai‘i introduced species; molecular evolution; population genomics

Citation Formats

Rosenthal, William C., McIntyre, Peter B., Lisi, Peter J., Prather, Jr., Robert B., Moody, Kristine N., Blum, Michael J., Hogan, James Derek, and Schoville, Sean D. Invasion and rapid adaptation of guppies (Poecilia reticulata) across the Hawaiian Archipelago. United States: N. p., 2021. Web. doi:10.1111/eva.13236.
Rosenthal, William C., McIntyre, Peter B., Lisi, Peter J., Prather, Jr., Robert B., Moody, Kristine N., Blum, Michael J., Hogan, James Derek, & Schoville, Sean D. Invasion and rapid adaptation of guppies (Poecilia reticulata) across the Hawaiian Archipelago. United States. https://doi.org/10.1111/eva.13236
Rosenthal, William C., McIntyre, Peter B., Lisi, Peter J., Prather, Jr., Robert B., Moody, Kristine N., Blum, Michael J., Hogan, James Derek, and Schoville, Sean D. Wed . "Invasion and rapid adaptation of guppies (Poecilia reticulata) across the Hawaiian Archipelago". United States. https://doi.org/10.1111/eva.13236. https://www.osti.gov/servlets/purl/1783028.
@article{osti_1783028,
title = {Invasion and rapid adaptation of guppies (Poecilia reticulata) across the Hawaiian Archipelago},
author = {Rosenthal, William C. and McIntyre, Peter B. and Lisi, Peter J. and Prather, Jr., Robert B. and Moody, Kristine N. and Blum, Michael J. and Hogan, James Derek and Schoville, Sean D.},
abstractNote = {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.},
doi = {10.1111/eva.13236},
journal = {Evolutionary Applications},
number = 7,
volume = 14,
place = {United States},
year = {Wed Mar 31 00:00:00 EDT 2021},
month = {Wed Mar 31 00:00:00 EDT 2021}
}

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