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

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.

doi:10.1111/eva.13236

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

Journal Article · Wed Mar 31 00:00:00 EDT 2021 · Evolutionary Applications

DOI:https://doi.org/10.1111/eva.13236· OSTI ID:1783028

^[1]; McIntyre, Peter B. ^[2]; Lisi, Peter J. ^[3]; Prather, Jr., Robert B. ^[4]; Moody, Kristine N. ^[5]; Blum, Michael J. ^[6]; Hogan, James Derek ^[7];

^[3]

Univ. of Wisconsin, Madison, WI (United States); Univ. of Wyoming, Laramie, WY (United States)
Univ. of Wisconsin, Madison, WI (United States); Cornell Univ., Ithaca, NY (United States)
Univ. of Wisconsin, Madison, WI (United States)
Univ. of California, Riverside, CA (United States)
Univ. of Tennessee, Knoxville, TN (United States); Tulane Univ., New Orleans, LA (United States); Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
Univ. of Tennessee, Knoxville, TN (United States); Tulane Univ., New Orleans, LA (United States)
Texas A & M Univ., Corpus Christi, TX (United States)

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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Research Organization:: Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)

Sponsoring Organization:: USDOE; USDOD

Grant/Contract Number:: AC05-00OR22725; RC-1646; RC-2447

OSTI ID:: 1783028

Journal Information:: Evolutionary Applications, Vol. 14, Issue 7; ISSN 1752-4571

Publisher:: WileyCopyright Statement

Country of Publication:: United States

Language:: English

References (80)

Aquatic surface respiration, an adaptive response to hypoxia in the guppy, Poecilia reticulata (Pisces, Poeciliidae) Kramer, Donald L.; Mehegan, John P. Environmental Biology of Fishes, Vol. 6, Issue 3-4 https://doi.org/10.1007/BF00005759	journal	November 1981
What we still don't know about invasion genetics Bock, Dan G.; Caseys, Celine; Cousens, Roger D. Molecular Ecology, Vol. 24, Issue 9 https://doi.org/10.1111/mec.13032	journal	January 2015
Differences in ecological structure, function, and native species abundance between native and invaded Hawaiian streams Holitzki, Tara M.; MacKenzie, Richard A.; Wiegner, Tracy N. Ecological Applications, Vol. 23, Issue 6 https://doi.org/10.1890/12-0529.1	journal	September 2013
A direct approach to false discovery rates Storey, John D. Journal of the Royal Statistical Society: Series B (Statistical Methodology), Vol. 64, Issue 3 https://doi.org/10.1111/1467-9868.00346	journal	August 2002
Genome-wide single nucleotide polymorphisms reveal population history and adaptive divergence in wild guppies Willing, Eva-Maria; Bentzen, Paul; van OOSTERHOUT, Cock Molecular Ecology, Vol. 19, Issue 5 https://doi.org/10.1111/j.1365-294X.2010.04528.x	journal	March 2010
G protein alpha subunit multigene family in the Japanese puffer fish Fugu rubripes: PCR from a compact vertebrate genome. Sarwal, M. M.; Sontag, J. M.; Hoang, L. Genome Research, Vol. 6, Issue 12 https://doi.org/10.1101/gr.6.12.1207	journal	December 1996
Response to selection and evolvability of invasive populations Lee, Carol Eunmi; Remfert, Jane Louise; Chang, Yu-Mei Genetica, Vol. 129, Issue 2 https://doi.org/10.1007/s10709-006-9013-9	journal	August 2006
Light environment and mating behavior in Trinidadian guppies (Poecilia reticulata) Archard, Gabrielle A.; Cuthill, Innes C.; Partridge, Julian C. Behavioral Ecology and Sociobiology, Vol. 64, Issue 2 https://doi.org/10.1007/s00265-009-0834-2	journal	August 2009
Adaptive evolution in invasive species Prentis, Peter J.; Wilson, John R. U.; Dormontt, Eleanor E. Trends in Plant Science, Vol. 13, Issue 6 https://doi.org/10.1016/j.tplants.2008.03.004	journal	June 2008
Overcoming urban stream syndrome: Trophic flexibility confers resilience in a Hawaiian stream fish Lisi, Peter J.; Childress, Evan S.; Gagne, Roderick B. Freshwater Biology, Vol. 63, Issue 5 https://doi.org/10.1111/fwb.13091	journal	March 2018
Adaptive Radiation and Genetic Differentiation in the Hawaiian Silversword Alliance (Compositae: Madiinae) Witter, Martha S.; Carr, Gerald D. Evolution, Vol. 42, Issue 6 https://doi.org/10.1111/j.1558-5646.1988.tb04187.x	journal	November 1988
An interplay between plasticity and parental phenotype determines impacts of ocean acidification on a reef fish Schunter, Celia; Welch, Megan J.; Nilsson, Göran E. Nature Ecology & Evolution, Vol. 2, Issue 2 https://doi.org/10.1038/s41559-017-0428-8	journal	December 2017
Experimentally induced life-history evolution in a natural population Reznick, David A.; Bryga, Heather; Endler, John A. Nature, Vol. 346, Issue 6282 https://doi.org/10.1038/346357a0	journal	July 1990
Inference of Population Splits and Mixtures from Genome-Wide Allele Frequency Data Pickrell, Joseph K.; Pritchard, Jonathan K. PLoS Genetics, Vol. 8, Issue 11 https://doi.org/10.1371/journal.pgen.1002967	journal	November 2012
Population Genomics of Parallel Adaptation in Threespine Stickleback using Sequenced RAD Tags Hohenlohe, Paul A.; Bassham, Susan; Etter, Paul D. PLoS Genetics, Vol. 6, Issue 2 https://doi.org/10.1371/journal.pgen.1000862	journal	February 2010
A Draft Sequence of the Neandertal Genome Green, R. E.; Krause, J.; Briggs, A. W. Science, Vol. 328, Issue 5979 https://doi.org/10.1126/science.1188021	journal	May 2010
Invasion of the Hawaiian Islands by a parasite infecting imperiled stream fishes Gagne, Roderick B.; Sprehn, C. Grace; Alda, Fernando Ecography, Vol. 41, Issue 3 https://doi.org/10.1111/ecog.02855	journal	May 2017
Mutations in fam20b and xylt1 Reveal That Cartilage Matrix Controls Timing of Endochondral Ossification by Inhibiting Chondrocyte Maturation Eames, B. Frank; Yan, Yi-Lin; Swartz, Mary E. PLoS Genetics, Vol. 7, Issue 8 https://doi.org/10.1371/journal.pgen.1002246	journal	August 2011
Poppr : an R package for genetic analysis of populations with clonal, partially clonal, and/or sexual reproduction Kamvar, Zhian N.; Tabima, Javier F.; Grünwald, Niklaus J. PeerJ, Vol. 2 https://doi.org/10.7717/peerj.281	journal	January 2014
Dsuite ‐ Fast D ‐statistics and related admixture evidence from VCF files Malinsky, Milan; Matschiner, Michael; Svardal, Hannes Molecular Ecology Resources, Vol. 21, Issue 2 https://doi.org/10.1111/1755-0998.13265	journal	October 2020
Impacts of Human Disturbances on Biotic Communities in Hawaiian Streams Brasher, Anne M. D. BioScience, Vol. 53, Issue 11 https://doi.org/10.1641/0006-3568(2003)053[1052:IOHDOB]2.0.CO;2	journal	January 2003
Consequences of alternative dispersal strategies in a putatively amphidromous fish Hogan, J. Derek; Blum, Michael J.; Gilliam, James F. Ecology, Vol. 95, Issue 9 https://doi.org/10.1890/13-0576.1	journal	September 2014
Multiple origins of a spider radiation in Hawaii. Gillespie, R. G.; Croom, H. B.; Palumbi, S. R. Proceedings of the National Academy of Sciences, Vol. 91, Issue 6 https://doi.org/10.1073/pnas.91.6.2290	journal	March 1994
Distribution of guppies Poecilia reticulata (Peters, 1860) and Phalloceros caudimaculatus (Hensel, 1868) along a polluted stretch of the Paraíba do Sul River, Brazil Araújo, Fg.; Peixoto, Mg.; Pinto, Bct. Brazilian Journal of Biology, Vol. 69, Issue 1 https://doi.org/10.1590/S1519-69842009000100005	journal	February 2009
Genetic variation increases during biological invasion by a Cuban lizard Kolbe, Jason J.; Glor, Richard E.; Rodríguez Schettino, Lourdes Nature, Vol. 431, Issue 7005 https://doi.org/10.1038/nature02807	journal	September 2004
Parallel evolution of the sexes? Effects of predation and habitat features on the size and shape of wild guppies Hendry, A. P.; Kelly, M. L.; Kinnison, M. T. Journal of Evolutionary Biology, Vol. 19, Issue 3 https://doi.org/10.1111/j.1420-9101.2005.01061.x	journal	May 2006
Mate Choice Based upon Naturally Occurring Color-Pattern Variation in a Guppy Population Houde, Anne E. Evolution, Vol. 41, Issue 1 https://doi.org/10.1111/j.1558-5646.1987.tb05766.x	journal	January 1987
Correlated Evolution of Female Mating Preferences and Male Color Patterns in the Guppy Poecilia reticulata Houde, A. E.; Endler, J. A. Science, Vol. 248, Issue 4961 https://doi.org/10.1126/science.248.4961.1405	journal	June 1990
Contrasting post-settlement selection results in many-to-one mapping of high performance phenotypes in the Hawaiian waterfall-climbing goby Sicyopterus stimpsoni Moody, Kristine N.; Kawano, Sandy M.; Bridges, William C. Evolutionary Ecology, Vol. 31, Issue 4 https://doi.org/10.1007/s10682-017-9889-0	journal	February 2017
Biodiversity and ecosystem risks arising from using guppies to control mosquitoes El-Sabaawi, Rana W.; Frauendorf, Therese C.; Marques, Piata S. Biology Letters, Vol. 12, Issue 10 https://doi.org/10.1098/rsbl.2016.0590	journal	October 2016
Local adaptation despite high gene flow in the waterfall-climbing Hawaiian goby, Sicyopterus stimpsoni Moody, K. N.; Hunter, S. N.; Childress, M. J. Molecular Ecology, Vol. 24, Issue 3 https://doi.org/10.1111/mec.13016	journal	January 2015
Inferring the Joint Demographic History of Multiple Populations from Multidimensional SNP Frequency Data Gutenkunst, Ryan N.; Hernandez, Ryan D.; Williamson, Scott H. PLoS Genetics, Vol. 5, Issue 10 https://doi.org/10.1371/journal.pgen.1000695	journal	October 2009
Increased genetic variation and evolutionary potential drive the success of an invasive grass Lavergne, S.; Molofsky, J. Proceedings of the National Academy of Sciences, Vol. 104, Issue 10 https://doi.org/10.1073/pnas.0607324104	journal	February 2007
Admixture, Population Structure, and F -Statistics Peter, Benjamin M. Genetics, Vol. 202, Issue 4 https://doi.org/10.1534/genetics.115.183913	journal	February 2016
Paradox lost: genetic diversity and the success of aquatic invasions Roman, J.; Darling, J. Trends in Ecology & Evolution, Vol. 22, Issue 9 https://doi.org/10.1016/j.tree.2007.07.002	journal	September 2007
Diet quality and prey selectivity correlate with life histories and predation regime in Trinidadian guppies: Diet correlates with life histories in guppy Zandonà, Eugenia; Auer, Sonya K.; Kilham, Susan S. Functional Ecology, Vol. 25, Issue 5 https://doi.org/10.1111/j.1365-2435.2011.01865.x	journal	May 2011
Transcriptome assemblies for studying sex-biased gene expression in the guppy, Poecilia reticulata Sharma, Eshita; Künstner, Axel; Fraser, Bonnie A. BMC Genomics, Vol. 15, Issue 1 https://doi.org/10.1186/1471-2164-15-400	journal	January 2014
Behavioral and genomic impacts of a wastewater effluent on the fathead minnow Garcia-Reyero, Natàlia; Lavelle, Candice M.; Escalon, B. Lynn Aquatic Toxicology, Vol. 101, Issue 1 https://doi.org/10.1016/j.aquatox.2010.08.014	journal	January 2011
Phylogenetic relationships among the mollies (Poeciliidae: Poecilia: Mollienesia group) based on mitochondrial DNA sequences Ptacek, M. B.; Breden†, F. Journal of Fish Biology, Vol. 53, Issue sA https://doi.org/10.1111/j.1095-8649.1998.tb01018.x	journal	December 1998
Parallel Evolution and Vicariance in the Guppy (Poecilia Reticulata) over Multiple Spatial and Temporal Scales Alexander, Heather J.; Taylor, John S.; Wu, Sampson Sze-Tsun Evolution, Vol. 60, Issue 11 https://doi.org/10.1111/j.0014-3820.2006.tb01870.x	journal	November 2006
Spread of an introduced parasite across the Hawaiian archipelago independent of its introduced host Gagne, Roderick B.; Hogan, J. Derek; Pracheil, Brenda M. Freshwater Biology, Vol. 60, Issue 2 https://doi.org/10.1111/fwb.12491	journal	November 2014
Evaluation of the Rate of Evolution in Natural Populations of Guppies (Poecilia reticulata) Reznick, D. N. Science, Vol. 275, Issue 5308 https://doi.org/10.1126/science.275.5308.1934	journal	March 1997
Non-adaptive plasticity potentiates rapid adaptive evolution of gene expression in nature Ghalambor, Cameron K.; Hoke, Kim L.; Ruell, Emily W. Nature, Vol. 525, Issue 7569 https://doi.org/10.1038/nature15256	journal	September 2015
UniProt: a worldwide hub of protein knowledge Consortium, The UniProt Nucleic Acids Research https://doi.org/10.1093/nar/gky1049		November 2018
Are sex-biased genes more dispensable? Mank, Judith E.; Ellegren, Hans Biology Letters, Vol. 5, Issue 3 https://doi.org/10.1098/rsbl.2008.0732	journal	January 2009
The evolutionary causes and consequences of sex-biased gene expression Parsch, John; Ellegren, Hans Nature Reviews Genetics, Vol. 14, Issue 2 https://doi.org/10.1038/nrg3376	journal	January 2013
Adaptive Genetic Variation on the Landscape: Methods and Cases Schoville, Sean D.; Bonin, Aurélie; François, Olivier Annual Review of Ecology, Evolution, and Systematics, Vol. 43, Issue 1 https://doi.org/10.1146/annurev-ecolsys-110411-160248	journal	December 2012
Variation in the appearance of guppy color patterns to guppies and their predators under different visual conditions Endler, John A. Vision Research, Vol. 31, Issue 3 https://doi.org/10.1016/0042-6989(91)90109-I	journal	January 1991
How Reproductive Ecology Contributes to the Spread of a Globally Invasive Fish Deacon, Amy E.; Ramnarine, Indar W.; Magurran, Anne E. PLoS ONE, Vol. 6, Issue 9 https://doi.org/10.1371/journal.pone.0024416	journal	September 2011
Testing for Associations between Loci and Environmental Gradients Using Latent Factor Mixed Models Frichot, Eric; Schoville, Sean D.; Bouchard, Guillaume Molecular Biology and Evolution, Vol. 30, Issue 7 https://doi.org/10.1093/molbev/mst063	journal	March 2013
Genotype Imputation with Millions of Reference Samples Browning, Brian L.; Browning, Sharon R. The American Journal of Human Genetics, Vol. 98, Issue 1 https://doi.org/10.1016/j.ajhg.2015.11.020	journal	January 2016
Basic local alignment search tool Altschul, Stephen F.; Gish, Warren; Miller, Webb Journal of Molecular Biology, Vol. 215, Issue 3, p. 403-410 https://doi.org/10.1016/S0022-2836(05)80360-2	journal	October 1990
Mitochondrial energetic metabolism perturbations in skeletal muscles and brain of zebrafish (Danio rerio) exposed to low concentrations of waterborne uranium Lerebours, Adélaïde; Adam-Guillermin, Christelle; Brèthes, Daniel Aquatic Toxicology, Vol. 100, Issue 1 https://doi.org/10.1016/j.aquatox.2010.07.007	journal	October 2010
Genetic diversity and species diversity of stream fishes covary across a land-use gradient Blum, Michael J.; Bagley, Mark J.; Walters, David M. Oecologia, Vol. 168, Issue 1 https://doi.org/10.1007/s00442-011-2078-x	journal	July 2011
Stacks: an analysis tool set for population genomics Catchen, Julian; Hohenlohe, Paul A.; Bassham, Susan Molecular Ecology, Vol. 22, Issue 11 https://doi.org/10.1111/mec.12354	journal	May 2013
A practical guide to environmental association analysis in landscape genomics Rellstab, Christian; Gugerli, Felix; Eckert, Andrew J. Molecular Ecology, Vol. 24, Issue 17 https://doi.org/10.1111/mec.13322	journal	August 2015
Female choice in the guppy ( Poecilia reticulata ): the interaction between male color and display Kodric-Brown, Astrid; Nicoletto, Paul Behavioral Ecology and Sociobiology, Vol. 50, Issue 4 https://doi.org/10.1007/s002650100374	journal	September 2001
Hybridization as a stimulus for the evolution of invasiveness in plants? Ellstrand, N. C.; Schierenbeck, K. A. Proceedings of the National Academy of Sciences, Vol. 97, Issue 13 https://doi.org/10.1073/pnas.97.13.7043	journal	June 2000
Evidence of local adaptation in a waterfall-climbing Hawaiian goby fish derived from coupled biophysical modeling of larval dispersal and post-settlement selection Moody, Kristine N.; Wren, Johanna L. K.; Kobayashi, Donald R. BMC Evolutionary Biology, Vol. 19, Issue 1 https://doi.org/10.1186/s12862-019-1413-4	journal	April 2019
Estimating F-Statistics Weir, B. S.; Hill, W. G. Annual Review of Genetics, Vol. 36, Issue 1 https://doi.org/10.1146/annurev.genet.36.050802.093940	journal	December 2002
Contemporary evolution during invasion: evidence for differentiation, natural selection, and local adaptation Colautti, Robert I.; Lau, Jennifer A. Molecular Ecology, Vol. 24, Issue 9 https://doi.org/10.1111/mec.13162	journal	April 2015
The Genome of the Trinidadian Guppy, Poecilia reticulata, and Variation in the Guanapo Population Künstner, Axel; Hoffmann, Margarete; Fraser, Bonnie A. PLOS ONE, Vol. 11, Issue 12 https://doi.org/10.1371/journal.pone.0169087	journal	December 2016
Global threats from invasive alien species in the twenty-first century and national response capacities Early, Regan; Bradley, Bethany A.; Dukes, Jeffrey S. Nature Communications, Vol. 7, Issue 1 https://doi.org/10.1038/ncomms12485	journal	August 2016
Exploring population size changes using SNP frequency spectra Liu, Xiaoming; Fu, Yun-Xin Nature Genetics, Vol. 47, Issue 5 https://doi.org/10.1038/ng.3254	journal	April 2015
Comparative Genome Analysis of the Neurexin Gene Family in Danio rerio: Insights into Their Functions and Evolution Rissone, Alberto; Monopoli, Matteo; Beltrame, Monica Molecular Biology and Evolution, Vol. 24, Issue 1 https://doi.org/10.1093/molbev/msl147	journal	October 2006
Parallel genetic basis for repeated evolution of armor loss in Alaskan threespine stickleback populations Cresko, W. A.; Amores, A.; Wilson, C. Proceedings of the National Academy of Sciences, Vol. 101, Issue 16 https://doi.org/10.1073/pnas.0308479101	journal	April 2004
Pla2g6 Deficiency in Zebrafish Leads to Dopaminergic Cell Death, Axonal Degeneration, Increased β-Synuclein Expression, and Defects in Brain Functions and Pathways Sánchez, Elena; Azcona, Luis J.; Paisán-Ruiz, Coro Molecular Neurobiology, Vol. 55, Issue 8 https://doi.org/10.1007/s12035-017-0846-2	journal	January 2018
A Robust, Simple Genotyping-by-Sequencing (GBS) Approach for High Diversity Species Elshire, Robert J.; Glaubitz, Jeffrey C.; Sun, Qi PLoS ONE, Vol. 6, Issue 5, Article No. e19379 https://doi.org/10.1371/journal.pone.0019379	journal	May 2011
Migratory gauntlets on oceanic islands: Watershed disturbance increases the cost of amphidromy Hain, Ernie F.; Moody, Kristine N.; Lamphere, Bradley A. Ecology of Freshwater Fish, Vol. 28, Issue 3 https://doi.org/10.1111/eff.12467	journal	December 2018
Adaptive Changes in Life History and Survival following a New Guppy Introduction Gordon, Swanne P.; Reznick, David N.; Kinnison, Michael T. The American Naturalist, Vol. 174, Issue 1 https://doi.org/10.1086/599300	journal	July 2009
Multilocus Resolution of Phylogeny and Timescale in the Extant Adaptive Radiation of Hawaiian Honeycreepers Lerner, Heather R. L.; Meyer, Matthias; James, Helen F. Current Biology, Vol. 21, Issue 21 https://doi.org/10.1016/j.cub.2011.09.039	journal	November 2011
Disentangling the Effects of Geographic and Ecological Isolation on Genetic Differentiation: Isolation by Geographic and Ecological Distance Bradburd, Gideon S.; Ralph, Peter L.; Coop, Graham M. Evolution, Vol. 67, Issue 11 https://doi.org/10.1111/evo.12193	journal	July 2013
Biotic Interactions, Rapid Evolution, and the Establishment of Introduced Species Jones, Emily I.; Gomulkiewicz, Richard The American Naturalist, Vol. 179, Issue 2 https://doi.org/10.1086/663678	journal	February 2012
Rapid evolution in introduced species, ‘invasive traits’ and recipient communities: challenges for predicting invasive potential: Evolution and invasion predictions Whitney, Kenneth D.; Gabler, Christopher A. Diversity and Distributions, Vol. 14, Issue 4 https://doi.org/10.1111/j.1472-4642.2008.00473.x	journal	April 2008
Salinity tolerance of the guppy, Poecilia reticulata Peters Chervinski, J. Journal of Fish Biology, Vol. 24, Issue 4 https://doi.org/10.1111/j.1095-8649.1984.tb04815.x	journal	April 1984
`LEA` : An `R` package for landscape and ecological association studies Frichot, Eric; François, Olivier Methods in Ecology and Evolution, Vol. 6, Issue 8 https://doi.org/10.1111/2041-210X.12382	journal	May 2015
Introduction: Population Biology, Evolution, and Control of Invasive Species Allendorf, Fred W.; Lundquist, Laura L. Conservation Biology, Vol. 17, Issue 1 https://doi.org/10.1046/j.1523-1739.2003.02365.x	journal	February 2003
Life‐History Evolution in Guppies. VII. The Comparative Ecology of High‐ and Low‐Predation Environments Reznick, David; Butler IV, Mark J.; Rodd, Helen The American Naturalist, Vol. 157, Issue 2 https://doi.org/10.1086/318627	journal	February 2001
Fast gapped-read alignment with Bowtie 2 Langmead, Ben; Salzberg, Steven L. Nature Methods, Vol. 9, Issue 4 https://doi.org/10.1038/nmeth.1923	journal	March 2012
Leptin Selectively Regulates Nutrients Metabolism in Nile Tilapia Fed on High Carbohydrate or High Fat Diet Liu, Cai-Zhi; He, An-Yuan; Ning, Li-Jun Frontiers in Endocrinology, Vol. 9 https://doi.org/10.3389/fendo.2018.00574	journal	September 2018

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59 BASIC BIOLOGICAL SCIENCES
biological adaptation
Hawai‘i introduced species
molecular evolution
population genomics

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

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