Abstract
Understanding the source of non-native introduced populations is crucial for forecasting geographic invasion potential and understanding the ecological consequences of potential establishment. Here we use genomics to identify the source populations and invasion dynamics of two non-native introduced populations from the iconic avian lineage of ‘great speciators’ known as white-eyes (genus Zosterops). We established confidently for the first time that introduced Zosterops populations in Hawaii and southern California are completely unrelated and derived from independent introductions of the species Z. japonicus and Z. simplex, respectively. We used descriptive population genetic statistics to identify a reduction in genetic diversity and increase in private alleles in the southern California population supporting a recent, potentially ongoing, genetic bottleneck in this population. In contrast, the introduced population in Hawaii showed no such characteristics, likely due to a larger founding population size and repeated introductions in this intentionally introduced population. Ecological niche modeling indicated that there is little environmentally suitable habitat for Z. simplex across the continent of North America, suggesting limited invasion potential, assuming niche conservatism. Yet, portions of the introduced Z. simplex population have already surpassed areas projected as suitable, likely because the urbanized environment of southern California offers biotic resources and microhabitats not captured by our model. Because Z. simplex appears to have overcome both the ‘invasion paradox’ of low founding genetic diversity and relatively unfamiliar environmental conditions in southern California, we suggest that this population may continue expanding beyond our environmental niche model projections in other temperate, urban regions.
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Data availability
All code needed to reproduce the results of this study can be found by following the links on the homepage of the dedicated GitHub repository for this project at: https://github.com/DevonDeRaad/zosterops.rad. The entire repository is also permanently versioned and accessioned via Zenodo at: https://doi.org/10.5281/zenodo.10694997. The raw sequence data for each sample passing filtering protocols (i.e., all samples included in analyses presented in this manuscript) is available via NCBI's Sequence Read Archive, at the BioProject PRJNA1079333, which can be found at: https://www.ncbi.nlm.nih.gov/sra/PRJNA1079333.
References
Aagaard K, Lockwood JL (2016) Severe and rapid population declines in exotic birds. Biol Invas 18(6):1667–1678. https://doi.org/10.1007/s10530-016-1109-2
Alexander DH, Novembre J, Lange K (2009) Fast model-based estimation of ancestry in unrelated individuals. Genome Res 19(9):1655–1664. https://doi.org/10.1101/gr.094052.109
Anderson JT, Panetta AM, Mitchell-Olds T (2012) Evolutionary and ecological responses to anthropogenic climate change: update on anthropogenic climate change. Plant Physiol 160(4):1728–1740. https://doi.org/10.1104/pp.112.206219
Anderson RP, Lew D, Peterson AT (2003) Evaluating predictive models of species’ distributions: criteria for selecting optimal models. Ecol Model 162(3):211–232. https://doi.org/10.1016/S0304-3800(02)00349-6
Avery ML, Humphrey JS, Keacher KL, Bruce WE (2014) Detection and removal of invasive burmese pythons: methods development update. Proc Vertebr Pest Conf 26(26):1. https://doi.org/10.5070/V426110362
Banerjee AK, Mukherjee A, Guo W, Ng WL, Huang Y (2019) Combining ecological niche modeling with genetic lineage information to predict potential distribution of Mikania micrantha Kunth in South and Southeast Asia under predicted climate change. Glob Ecol Conserv 20:e00800. https://doi.org/10.1016/j.gecco.2019.e00800
Barton KE, Fortunel C (2023) Island plant functional syndromes and competition with invasive species. J Biogeogr 50(4):641–653. https://doi.org/10.1111/jbi.14568
Barton NH (1997) Natural selection and random genetic drift as causes of evolution on islands. Philos Trans R Soc Lond Ser B Biol Sci 351(1341):785–795. https://doi.org/10.1098/rstb.1996.0073
Battey CJ (2019) Ecological release of the Anna’s hummingbird during a Northern range expansion. Am Nat 194(3):306–315. https://doi.org/10.1086/704249
Belnap JYE, Ludwig JA, Wilcox BP, Betancourt JL, Dean WRJ, Hoffmann BD, Milton SJ (2012) Introduced and invasive species in novel rangeland ecosystems: friends or foes? Rangel Ecol Manag 65(6):569–578. https://doi.org/10.2111/REM-D-11-00157.1
Blackburn TM, Essl F, Evans T, Hulme PE, Jeschke JM, Kühn I, Kumschick S, Marková Z, Mrugała A, Nentwig W, Pergl J, Pyšek P, Rabitsch W, Ricciardi A, Richardson DM, Sendek A, Vilà M, Wilson JRU, Winter M, Bacher S (2014) A unified classification of alien species based on the magnitude of their environmental impacts. PLOS Biology 12(5):e1001850. https://doi.org/10.1371/journal.pbio.1001850
Brownrigg R (2013) R package “maps” [Computer software]
Caum EL (1933) The exotic birds of Hawaii. Occasion Pap Bernice Pauahi Bishop Museum Polynes Ethnol Nat Hist 10(9):1–55
Chng SCL, Shepherd CR, Eaton JA (2018) In the market for extinction: birds for sale at selected outlets in Sumatra. TRAFFIC Bull 30(1):1
Christie K, Strauss SY (2019) Reproductive isolation and the maintenance of species boundaries in two serpentine endemic Jewelflowers. Evolution 73(7):1375–1391. https://doi.org/10.1111/evo.13767
Clavero M, García-Berthou E (2005) Invasive species are a leading cause of animal extinctions. Trends Ecol Evol 20(3):110. https://doi.org/10.1016/j.tree.2005.01.003
Clegg SM, Degnan SM, Kikkawa J, Moritz C, Estoup A, Owens IPF (2002) Genetic consequences of sequential founder events by an island-colonizing bird. Proc Natl Acad Sci 99(12):8127–8132. https://doi.org/10.1073/pnas.102583399
Cobos ME, Owens HL, Soberón J, Peterson AT (2023) mop: Mobility Oriented-Parity Metric [R package]. https://CRAN.R-project.org/package=mop
Cobos ME, Peterson AT, Barve N, Osorio-Olvera L (2019) kuenm: an R package for detailed development of ecological niche models using Maxent. PeerJ 7:e6281. https://doi.org/10.7717/peerj.6281
Colautti RI, Bailey SA, van Overdijk CDA, Amundsen K, MacIsaac HJ (2006) Characterised and projected costs of nonindigenous species in Canada. Biol Invasions 8(1):45–59. https://doi.org/10.1007/s10530-005-0236-y
Cook P (2006) eBird Checklist: Https://ebird.org/checklist/S32428989. eBird: An online database of bird distribution and abundance [web application]. eBird, Ithaca, New York. http://www.ebird.org. (Accessed: Date [August 25, 2023]).
Crosby AW (2004) Ecological imperialism: the biological expansion of Europe, 900–1900 (2nd ed.). Cambridge University Press. https://doi.org/10.1017/CBO9780511805554
Daniels B (2011). eBird Checklist: Https://ebird.org/checklist/S50798538. eBird: An online database of bird distribution and abundance [web application]. eBird, Ithaca, New York. Http://www.ebird.org. (Accessed: Date [September 6, 2023]).
DeRaad DA (2022) SNPfiltR: an R package for interactive and reproducible SNP filtering. Mol Ecol Resour 22(6):2443–2453. https://doi.org/10.1111/1755-0998.13618
DeRaad DA, McCullough JM, DeCicco LH, Hime PM, Joseph L, Andersen MJ, Moyle RG (2023) Mitonuclear discordance results from incomplete lineage sorting, with no detectable evidence for gene flow, in a rapid radiation of Todiramphus kingfishers. Mol Ecol 32(17):4844–4862. https://doi.org/10.1111/mec.17080
Diamond JM, Gilpin ME, Mayr E (1976) Species-distance relation for birds of the Solomon Archipelago, and the paradox of the great speciators. Proc Natl Acad Sci 73(6):2160–2164. https://doi.org/10.1073/pnas.73.6.2160
Dong X, Ju T, Grenouillet G, Laffaille P, Lek S, Liu J (2020) Spatial pattern and determinants of global invasion risk of an invasive species, sharpbelly Hemiculter leucisculus (Basilesky, 1855). Sci Total Environ 711:134661. https://doi.org/10.1016/j.scitotenv.2019.134661
Early R, González-Moreno P, Murphy ST, Day R (2018) Forecasting the global extent of invasion of the cereal pest Spodoptera frugiperda, the fall armyworm. NeoBiota 40:25–50. https://doi.org/10.3897/neobiota.40.28165
Eaton JA, Leupen BTC, Krishnasamy K (2017) Songsters of Singapore: an overview of the bird species in Singapore Pet Shops. TRAFFIC Report, Petaling Jaya, Selangor, Malaysia
Estandía A, Sendell-Price AT, Oatley G, Robertson F, Potvin D, Massaro M, Robertson BC, Clegg SM (2023) Candidate gene polymorphisms are linked to dispersive and migratory behaviour: Searching for a mechanism behind the “paradox of the great speciators.” J Evol Biol 36(10):1503–1516. https://doi.org/10.1111/jeb.14222
Estoup A, Baird SJE, Ray N, Currat M, Cornuet J-M, Santos F, Beaumont MA, Excoffier L (2010) Combining genetic, historical and geographical data to reconstruct the dynamics of bioinvasions: application to the cane toad Bufo marinus. Mol Ecol Resource 10(5):886–901. https://doi.org/10.1111/j.1755-0998.2010.02882.x
Estoup A, Ravigné V, Hufbauer R, Vitalis R, Gautier M, Facon B (2016) Is there a genetic paradox of biological invasion? Annu Rev Ecol Evol Syst 47(1):51–72. https://doi.org/10.1146/annurev-ecolsys-121415-032116
Feeley KJ, Silman MR (2010) Biotic attrition from tropical forests correcting for truncated temperature niches. Glob Change Biol 16(6):1830–1836. https://doi.org/10.1111/j.1365-2486.2009.02085.x
Fell HG, Osborne OG, Jones MD, Atkinson S, Tarr S, Keddie SH, Algar AC (2022) Biotic factors limit the invasion of the plague pathogen (Yersinia pestis) in novel geographical settings. Glob Ecol Biogeogr 31(4):672–684. https://doi.org/10.1111/geb.13453
Filipová L, Grandjean F, Chucholl C, Soes DM, Petrusek A (2011) Identification of exotic North American crayfish in Europe by DNA barcoding. Knowl Manag Aquat Ecosyst 401:401. https://doi.org/10.1051/kmae/2011025
Frankel LE, Ané C (2023) Summary tests of introgression are highly sensitive to rate variation across lineages (p. 2023. 01. 26. 525396). bioRxiv. https://doi.org/10.1101/2023.01.26.525396
Garrett KL (1997) Population status and distribution of naturalized parrots in Southern California. Western Birds 28(4):181–195
Garrett KL (2018) Introducing change: a current look at naturalized bird species in western North America. In: Shuford WD, Gill RE Jr., Handel CM (eds) Trends and traditions: avifaunal change in western North America. In: Studies of Western birds 3, pp 116–130. Western Field Ornithologists. https://doi.org/10.21199/SWB3.5
GBIF (2023) GBIF.org; GBIF Occurrence Download [Computer software]. https://doi.org/10.15468/dl.77wduz
Gill F, Donsker D, Rasmussen P (2023) IOC World Bird List (v 13.1). https://doi.org/10.14344/IOC.ML.13.1. http://www.Worldbirdnames.Org/
Gleditsch JM, Sperry JH (2019) Rapid morphological change of nonnative frugivores on the Hawaiian island of O’ahu*. Evolution 73(7):1456–1465. https://doi.org/10.1111/evo.13744
Gorresen PM, Camp RJ, Pratt TK (2007) Forest Bird Distribution, Density and Trends in the Ka’u Region of Hawai’i Island. U.S. Geological Survey Open-File report., pp 1–101. https://pubs.usgs.gov/of/2007/1076/
Gotzek D, Brady SG, Kallal RJ, LaPolla JS (2012) The importance of using multiple approaches for identifying emerging invasive species: the case of the Rasberry crazy ant in the United States. PLoS ONE 7(9):e45314. https://doi.org/10.1371/journal.pone.0045314
Greenlees MJ, Harris S, White AW, Shine R (2018) The establishment and eradication of an extra-limital population of invasive cane toads. Biol Invas 20(8):2077–2089. https://doi.org/10.1007/s10530-018-1681-8
Guest SJ (1973) A reproductive biology and natural history of the Japanese White-eye (Zosterops japonica japonica) in urban Oahu (International Biological Program Technical Report 29). Island Ecosystems IRP, U.S. International Biological Program. http://hdl.handle.net/10125/25976
Gwee CY, Garg KM, Chattopadhyay B, Sadanandan KR, Prawiradilaga DM, Irestedt M, Lei F, Bloch LM, Lee JG, Irham M, Haryoko T, Soh MC, Peh KS-H, Rowe KM, Ferasyi TR, Wu S, Wogan GO, Bowie RC, Rheindt FE (2020) Phylogenomics of white-eyes, a ‘great speciator’, reveals Indonesian archipelago as the center of lineage diversity. eLife 9:e62765. https://doi.org/10.7554/eLife.62765
Halliburton R (2004) Introduction to Population Genetics. Pearson/Prentice Hall.
Harper GA, Bunbury N (2015) Invasive rats on tropical islands: their population biology and impacts on native species. Glob Ecol Conserv 3:607–627. https://doi.org/10.1016/j.gecco.2015.02.010
Heller R, Chikhi L, Siegismund HR (2013) The confounding effect of population structure on Bayesian Skyline Plot inferences of demographic history. PLoS ONE 8(5):e62992. https://doi.org/10.1371/journal.pone.0062992
Hewett AM, Stoffel MA, Peters L, Johnston SE, Pemberton JM (2023) Selection, recombination and population history effects on runs of homozygosity (ROH) in wild red deer (Cervus elaphus). Heredity 130(4):4. https://doi.org/10.1038/s41437-023-00602-z
Hijmans R (2023) Terra: Spatial Data Analysis. [R package]. https://CRAN.R-project.org/package=terra
Hijmans R, Barbosa M, Ghosh A, Mandel A (2023) Geodata: Download Geographic Data. R Package. R, 2023. Https://CRAN.R-project.org/package=geodata. [Computer software]
Hofmeister NR, Werner SJ, Lovette IJ (2021) Environmental correlates of genetic variation in the invasive European starling in North America. Mol Ecol 30(5):1251–1263. https://doi.org/10.1111/mec.15806
Hudson J, Castilla JC, Teske PR, Beheregaray LB, Haigh ID, McQuaid CD, Rius M (2021) Genomics-informed models reveal extensive stretches of coastline under threat by an ecologically dominant invasive species. Proc Natl Acad Sci 118(23):e2022169118. https://doi.org/10.1073/pnas.2022169118
Hulme PE (2009) Trade, transport and trouble: managing invasive species pathways in an era of globalization. J Appl Ecol 46(1):10–18. https://doi.org/10.1111/j.1365-2664.2008.01600.x
Huson DH, Bryant D (2006) Application of phylogenetic networks in evolutionary studies. Mol Biol Evol 23(2):254–267. https://doi.org/10.1093/molbev/msj030
James JE, Lanfear R, Eyre-Walker A (2016) Molecular evolutionary consequences of Island Colonization. Genome Biol Evol 8(6):1876–1888. https://doi.org/10.1093/gbe/evw120
Jamieson IG (2011) Founder effects, inbreeding, and loss of genetic diversity in four avian reintroduction programs. Conserv Biol 25(1):115–123. https://doi.org/10.1111/j.1523-1739.2010.01574.x
Jiménez L, Soberón J, Christen JA, Soto D (2019) On the problem of modeling a fundamental niche from occurrence data. Ecol Model 397:74–83. https://doi.org/10.1016/j.ecolmodel.2019.01.020
Jombart T (2008) adegenet: a R package for the multivariate analysis of genetic markers. Bioinformatics 24(11):1403–1405. https://doi.org/10.1093/bioinformatics/btn129
Knaus BJ, Grünwald NJ (2017) vcfr: a package to manipulate and visualize variant call format data in R. Mol Ecol Resour 17(1):44–53. https://doi.org/10.1111/1755-0998.12549
Kolbe JJ, Glor RE, Rodríguez Schettino L, Lara AC, Larson A, Losos JB (2004) Genetic variation increases during biological invasion by a Cuban lizard. Nature 431(7005):7005. https://doi.org/10.1038/nature02807
Kumar S, LeBrun EG, Stohlgren TJ, Stabach JA, McDonald DL, Oi DH, LaPolla JS (2015) Evidence of niche shift and global invasion potential of the Tawny Crazy ant, Nylanderia Fulva. Ecol Evol 5(20):4628–4641. https://doi.org/10.1002/ece3.1737
Lee CE (2002) Evolutionary genetics of invasive species. Trends Ecol Evol 17(8):386–391. https://doi.org/10.1016/S0169-5347(02)02554-5
Lee CE (2016) Evolutionary mechanisms of habitat invasions, using the copepod Eurytemora affinis as a model system. Evol Appl 9(1):248–270. https://doi.org/10.1111/eva.12334
Li H, Durbin R (2009) Fast and accurate short read alignment with Burrows–Wheeler transform. Bioinformatics (oxford, England) 25(14):1754–1760. https://doi.org/10.1093/bioinformatics/btp324
Li H, Durbin R (2011) Inference of human population history from individual whole-genome sequences. Nature 475(7357):7357. https://doi.org/10.1038/nature102316
Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R, 1000 Genome Project Data Processing Subgroup (2009) The sequence alignment/map format and SAMtools. Bioinformatics 25(16):2078–2079. https://doi.org/10.1093/bioinformatics/btp352
Lim BTM, Sadanandan KR, Dingle C, Leung YY, Prawiradilaga DM, Irham M, Ashari H, Lee JGH, Rheindt FE (2019) Molecular evidence suggests radical revision of species limits in the great speciator white-eye genus Zosterops. J Ornithol 160(1):1–16. https://doi.org/10.1007/s10336-018-1583-7
Linz GM, Homan HJ, Gaulker SM, Penry LB, Bleier WJ (2007) European starlings: a review of an invasive species with far-reaching impacts. USDA National Wildlife Research Symposia, Managing vertebrate invasive species
Linz GM, Thiele J, Johnson R (2018) European starlings. Ecology and management of terrestrial vertebrate invasive species in the United States, pp 311–332
Liu S, Hansen MM (2017) PSMC (pairwise sequentially Markovian coalescent) analysis of RAD (restriction site associated DNA) sequencing data. Mol Ecol Resour 17(4):631–641. https://doi.org/10.1111/1755-0998.12606
Losos JB (2008) Phylogenetic niche conservatism, phylogenetic signal and the relationship between phylogenetic relatedness and ecological similarity among species. Ecol Lett 11(10):995–1003. https://doi.org/10.1111/j.1461-0248.2008.01229.x
Machado-Stredel F, Cobos ME, Peterson AT (2021) A simulation-based method for selecting calibration areas for ecological niche models and species distribution models. Front Biogeogr 13(4):1. https://doi.org/10.2125/F5FBG488144
Maddison WP, Knowles LL (2006) Inferring phylogeny despite incomplete lineage sorting. Syst Biol 55(1):21–30. https://doi.org/10.1080/10635150500354928
Manthey JD, Moyle RG (2015) Isolation by environment in White-breasted Nuthatches (Sitta carolinensis) of the Madrean Archipelago sky islands: a landscape genomics approach. Mol Ecol 24(14):3628–3638. https://doi.org/10.1111/mec.13258
Manthey JD, Oliveros CH, Andersen MJ, Filardi CE, Moyle RG (2020) Gene flow and rapid differentiation characterize a rapid insular radiation in the southwest Pacific (Aves: Zosterops). Evolution 74(8):1788–1803. https://doi.org/10.1111/evo.14043
Mathys BA, Lockwood JL (2011) Contemporary morphological diversification of passerine birds introduced to the Hawaiian archipelago. Proc R Soc b: Biol Sci 278(1716):2392–2400. https://doi.org/10.1098/rspb.2010.2302
Mayr E (1942) Systematics and the origin of species. Columbia University Press, New York
Mazzamuto MV, Galimberti A, Cremonesi G, Pisanu B, Chapuis J-L, Stuyck J, Amori G, Su H, Aloise G, Preatoni DG, Wauters LA, Casiraghi M, Martinoli A (2016) Preventing species invasion: a role for integrative taxonomy? Integrative Zoology 11(3):214–228. https://doi.org/10.1111/1749-4877.12185
Mittan-Moreau CS, Kelehear C, Toledo LF, Bacon J, Guayasamin JM, Snyder A, Zamudio KR (2022) Cryptic lineages and standing genetic variation across independent cane toad introductions. Mol Ecol 31(24):6440–6456. https://doi.org/10.1111/mec.16713
Moyle RG, Filardi CE, Smith CE, Diamond J (2009) Explosive Pleistocene diversification and hemispheric expansion of a “great speciator.” Proc Natl Acad Sci 106(6):1863–1868
Mungomery RW (1935) The giant American toad (Bufo marinus). Cane Growers Q Bull 3:21–27
Mutamiswa R, Machekano H, Singano C, Joseph V, Chidawanyika F, Nyamukondiwa C (2021) Desiccation and temperature resistance of the larger grain borer, Prostephanus truncatus (Horn) (Coleoptera: Bostrichidae): pedestals for invasion success? Physiol Entomol 46(2):157–166. https://doi.org/10.1111/phen.12355
Natola L, Seneviratne SS, Irwin D (2022) Population genomics of an emergent tri-species hybrid zone. Mol Ecol 31(20):5356–5367. https://doi.org/10.1111/mec.16650
Nei M (1972) Genetic distance between populations. Am Nat 106:283–292. https://doi.org/10.1086/282771
Nei M, Maruyama T, Chakraborty R (1975) The bottleneck effect and genetic variability in populations. Evolution 29(1):1–10. https://doi.org/10.2307/2407137
Ng PKL, Wee YC (1994) The Singapore red data book: Threatened plants and animals of Singapore. The Nature Society (Singapore). https://cir.nii.ac.jp/crid/1130000795400296576
Nuñez-Penichet C, Osorio-Olvera L, Gonzalez VH, Cobos ME, Jiménez L, DeRaad DA, Alkishe A, Contreras-Díaz RG, Nava-Bolaños A, Utsumi K, Ashraf U, Adeboje A, Peterson AT, Soberon J (2021) Geographic potential of the world’s largest hornet, Vespa mandarinia Smith (Hymenoptera: Vespidae), worldwide and particularly in North America. PeerJ 9:e10690. https://doi.org/10.7717/peerj.10690
Oatley G, De Swardt DH, Nuttall RJ, Crowe TM, Bowie RCK (2017) Phenotypic and genotypic variation across a stable white-eye (Zosterops sp.) hybrid zone in central South Africa. Biol J Linnean Soc 121(3):670–684. https://doi.org/10.1093/biolinnean/blx012
Okamiya H, Inoue Y, Takai K, Crossland MR, Kishida O (2021) Native frogs (Rana pirica) do not respond adaptively to alien toads (Bufo japonicus formosus) 100 years after introduction. Ecol Res 36(6):1005–1014. https://doi.org/10.1111/1440-1703.12259
Osborne MA (2000) Acclimatizing the world: a history of the paradigmatic colonial science. Osiris 15:135–151
Owens HL, Campbell LP, Dornak LL, Saupe EE, Barve N, Soberón J, Ingenloff K, Lira-Noriega A, Hensz CM, Myers CE, Peterson AT (2013) Constraints on interpretation of ecological niche models by limited environmental ranges on calibration areas. Ecol Model 263:10–18. https://doi.org/10.1016/j.ecolmodel.2013.04.011
Pebesma E (2018) Simple features for R: standardized support for spatial vector data. The R J 10(1):439. https://doi.org/10.3214/RJ-2018-009
Pembleton LW, Cogan NOI, Forster JW (2013) StAMPP: an R package for calculation of genetic differentiation and structure of mixed-ploidy level populations. Mol Ecol Resour 13(5):946–952. https://doi.org/10.1111/1755-0998.12129
Peterson AT (2003) Predicting the geography of species’ invasions via ecological niche modeling. Q Rev Biol 78(4):419–433. https://doi.org/10.1086/378926
Peterson AT (2011) Ecological niche conservatism: a time-structured review of evidence. J Biogeogr 38(5):817–827. https://doi.org/10.1111/j.1365-2699.2010.02456.x
Peterson AT, Papeş M, Soberón J (2008) Rethinking receiver operating characteristic analysis applications in ecological niche modeling. Ecol Model 213(1):63–72. https://doi.org/10.1016/j.ecolmodel.2007.11.008
Peterson AT, Soberón J, Pearson RG, Anderson RP, Martínez-Meyer E, Nakamura M, Araújo MB (2011) Ecological niches and geographic distributions. Princeton University Press. https://www.jstor.org/stable/j.ctt7stnh
Peterson AT, Soberón J, Sánchez-Cordero V (1999) Conservatism of ecological niches in evolutionary time. Science 285(5431):1265–1267. https://doi.org/10.1126/science.285.5431.1265
Peterson AT, Vieglais DA (2001) Predicting species invasions using ecological niche modeling: new approaches from bioinformatics attack a pressing problem. Bioscience 51(5):363–371. https://doi.org/10.1641/0006-3568(2001)051[0363:PSIUEN]2.0.CO;2
Phillips SJ, Anderson RP, Dudík M, Schapire RE, Blair ME (2017) Opening the black box: an open-source release of Maxent. Ecography 40(7):887–893. https://doi.org/10.1111/ecog.03049
Pimentel D, Zuniga R, Morrison D (2005) Update on the environmental and economic costs associated with alien-invasive species in the United States. Ecol Econ 52(3):273–288. https://doi.org/10.1016/j.ecolecon.2004.10.002
Pruett-Jones S (2021) Naturalized parrots of the world: distribution, ecology, and impacts of the world’s most colorful colonizers. Princeton University Press
Pyron RA, Costa GC, Patten MA, Burbrink FT (2015) Phylogenetic niche conservatism and the evolutionary basis of ecological speciation. Biol Rev 90(4):1248–1262. https://doi.org/10.1111/brv.12154
R Core Team (2019) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria [Computer software]
Rochette NC, Rivera-Colón AG, Catchen JM (2019) Stacks 2: analytical methods for paired-end sequencing improve RADseq-based population genomics. Mol Ecol 28(21):4737–4754. https://doi.org/10.1111/mec.15253
Roemer GW, Donlan CJ, Courchamp F (2002) Golden eagles, feral pigs, and insular carnivores: how exotic species turn native predators into prey. Proc Natl Acad Sci 99(2):791–796. https://doi.org/10.1073/pnas.012422499
Roy HE, Lawson Handley L-J, Schönrogge K, Poland RL, Purse BV (2011) Can the enemy release hypothesis explain the success of invasive alien predators and parasitoids? Biocontrol 56(4):451–468. https://doi.org/10.1007/s10526-011-9349-7
Roy HE, Pauchard A, Stoett P, Renard Truong T, Bacher S, Galil BS, Hulme PE, Ikeda T, Sankaran KV, McGeoch MA, Meyerson LA, Nuñez MA, Ordonez A, Rahlao SJ, Schwindt E, Seebens H, Sheppard AW, Vandvik V (2023) Summary for policymakers of the thematic assessment report on invasive alien species and their control of the intergovernmental science-policy platform on biodiversity and ecosystem services. Zenodo. https://doi.org/10.5281/zenodo.8314303
Scott JM, Mountainspring S, Ramsey FL, Kepler CB (1986) Forest bird communities of the Hawaiian Islands: their dynamics, ecology, and conservation, vol 9. Cooper Ornithological Society
Sendell-Price AT, Ruegg KC, Anderson EC, Quilodrán CS, Van Doren BM, Underwood VL, Coulson T, Clegg SM (2020a) The genomic landscape of divergence across the speciation continuum in island-colonising silvereyes (Zosterops lateralis). G3 Genes Genom Genet 10(9):3147–3163. https://doi.org/10.1534/g3.120.401352
Sendell-Price AT, Ruegg KC, Clegg SM (2020b) Rapid morphological divergence following a human-mediated introduction: the role of drift and directional selection. Heredity 124(4):4. https://doi.org/10.1038/s41437-020-0298-8
Sendell-Price AT, Ruegg KC, Robertson BC, Clegg SM (2021) An island-hopping bird reveals how founder events shape genome-wide divergence. Mol Ecol 30(11):2495–2510. https://doi.org/10.1111/mec.15898
Shafer ABA, Peart CR, Tusso S, Maayan I, Brelsford A, Wheat CW, Wolf JBW (2017) Bioinformatic processing of RAD-seq data dramatically impacts downstream population genetic inference. Methods Ecol Evol 8(8):907–917. https://doi.org/10.1111/2041-210X.12700
Sharaf MR, Gotzek D, Guénard B, Fisher BL, Aldawood AS, Al Dhafer HM, Mohamed AA (2020) Molecular phylogenetic analysis and morphological reassessments of thief ants identify a new potential case of biological invasions. Sci Rep 10(1):1. https://doi.org/10.1038/s41598-020-69029-4
Shchur V, Brandt DYC, Ilina A, Nielsen R (2022) Estimating population split times and migration rates from historical effective population sizes, p. 2022.06.17.496540. bioRxiv. https://doi.org/10.1101/2022.06.17.496540
Shultz AJ, Baker AJ, Hill GE, Nolan PM, Edwards SV (2016) SNPs across time and space: population genomic signatures of founder events and epizootics in the House Finch (Haemorhous mexicanus). Ecol Evol 6(20):7475–7489. https://doi.org/10.1002/ece3.2444
Soberón J, Peterson AT (2005) Interpretation of models of fundamental ecological niches and species’ distributional areas. Biodivers Inf 2:1. https://doi.org/10.1761/bi.v2i0.4
Stager M, Senner NR, Swanson DL, Carling MD, Eddy DK, Greives TJ, Cheviron ZA (2021) Temperature heterogeneity correlates with intraspecific variation in physiological flexibility in a small endotherm. Nat Commun 12(1):1. https://doi.org/10.1038/s41467-021-24588-6
Strayer DL, D’Antonio CM, Essl F, Fowler MS, Geist J, Hilt S, Jarić I, Jöhnk K, Jones CG, Lambin X, Latzka AW, Pergl J, Pyšek P, Robertson P, von Schmalensee M, Stefansson RA, Wright J, Jeschke JM (2017) Boom-bust dynamics in biological invasions: towards an improved application of the concept. Ecol Lett 20(10):1337–1350. https://doi.org/10.1111/ele.12822
Stuart KC, Hofmeister NR, Zichello JM, Rollins LA (2023) Global invasion history and native decline of the common starling: insights through genetics. Biol Invasions 25(5):1291–1316. https://doi.org/10.1007/s10530-022-02982-5
Sullivan BL, Wood CL, Iliff MJ, Bonney RE, Fink D, Kelling S (2009) eBird: A citizen-based bird observation network in the biological sciences. Biol Cons 142(10):2282–2292. https://doi.org/10.1016/j.biocon.2009.05.006
Unitt P, Klovstad AE (2004) San Diego county bird atlas, vol 39. San Diego Natural History Museum
Vega GC, Pertierra LR, Benayas J, Olalla-Tárraga MÁ (2021) Ensemble forecasting of invasion risk for four alien springtail (Collembola) species in Antarctica. Polar Biol 44(11):2151–2164. https://doi.org/10.1007/s00300-021-02949-7
Vega GC, Pertierra LR, Olalla-Tárraga MÁ (2017) MERRAclim, a high-resolution global dataset of remotely sensed bioclimatic variables for ecological modelling. Sci Data 4(1):1. https://doi.org/10.1038/sdata.2017.78
Venkatraman M, Fleischer RC, Tsuchiya MTN (2021) Comparative analysis of annotation pipelines using the first Japanese white-eye (Zosterops japonicus) genome. Genome Biol Evol 13(5):63. https://doi.org/10.1093/gbe/evab063
Vinciguerra NT, Oliveros CH, Moyle RG, Andersen MJ (2023) Island life accelerates geographic radiation in the white-eyes (Zosteropidae). Ibis. https://doi.org/10.1111/ibi.13177
Wang S, Chu LM (2021) Microhabitat characteristics related to seasonal roost switching: implications from a threatened and introduced cockatoo species in an urban landscape. Avian Res 12(1):35. https://doi.org/10.1186/s40657-021-00270-9
Warren DL, Seifert SN (2011) Ecological niche modeling in Maxent: the importance of model complexity and the performance of model selection criteria. Ecol Appl 21(2):335–342. https://doi.org/10.1890/10-1171.1
Wickham H, Chang W, Henry L, Pedersen TL, Takahashi K, Wilke C, Woo K, Yutani H, Dunnington D (2020) ggplot2: Create elegant data visualisations using the grammar of graphics (R package, version 3.3.2) [R package, version 3.3.2]. https://CRAN.R-project.org/package=ggplot2
Wilson JRU, Dormontt EE, Prentis PJ, Lowe AJ, Richardson DM (2009) Something in the way you move: dispersal pathways affect invasion success. Trends Ecol Evol 24(3):136–144. https://doi.org/10.1016/j.tree.2008.10.007
Yates KL, Bouchet PJ, Caley MJ, Mengersen K, Randin CF, Parnell S, Fielding AH, Bamford AJ, Ban S, Barbosa AM, Dormann CF, Elith J, Embling CB, Ervin GN, Fisher R, Gould S, Graf RF, Gregr EJ, Halpin PN, Sequeira AMM (2018) Outstanding challenges in the transferability of ecological models. Trends Ecol Evol 33(10):790–802. https://doi.org/10.1016/j.tree.2018.08.001
Acknowledgements
Each Zosterops illustration shown in this manuscript is an original creation of H. Douglas Pratt and has been subsequently licensed and reproduced via the Cornell Lab of Ornithology Birds of the World, with permission from Lynx Edicions. We thank the Urban Nature Research Center for helpful feedback on an in-progress draft of this manuscript. We would like to thank the Volcano Islands Research Team of Tokyo Metropolitan Government; the National Museum of Science and Nature, Tokyo; the South China Institute for Endangered Animals; the University of Washington Burke Museum; the Cincinnati Museum Center; the American Museum of Natural History; the Field Museum; Natural History Museum of Los Angeles County; the Smithsonian National Museum of Natural History; and the University of Kansas Natural History Museum for providing the sampling necessary to complete this project.
Funding
This work was supported in part by National Science Foundation grant to RGM (DEB-1557053). This work was performed in part using the HPC facilities operated by the Center for Research Computing at the University of Kansas supported in part through the National Science Foundation MRI Award #2117449. DAD was supported by the Lila and Madison Self Graduate Fellowship during a portion of this project. HLM was supported through NSF Award #2322123. SMA was supported by a Stanford Science Fellowship.
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DAD and AJS conceptualized and designed the study. DAD performed molecular lab work, genomic data analysis, and wrote the first draft of the manuscript. MEC and ATP performed ecological niche modeling analyses. RGM, AJS, KLG, IN, BM, FSZ, KK, CHK, RSY, CTY, and HLMJ all contributed crucial specimens and tissue samples to the project. RGM secured funding for genomic sequencing. All authors contributed substantial feedback on the analysis and interpretation of data across multiple drafts of this manuscript, and approved the final submitted version of the manuscript.
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DeRaad, D.A., Cobos, M.E., Hofmeister, N.R. et al. On the brink of explosion? Identifying the source and potential spread of introduced Zosterops white-eyes in North America. Biol Invasions (2024). https://doi.org/10.1007/s10530-024-03268-8
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DOI: https://doi.org/10.1007/s10530-024-03268-8