Abstract
The house sparrow is one of the most widely introduced vertebrate species around the world, making it an important model species for the study of invasion ecology. Population genetic studies of these invasions provide important insights into colonisation processes and adaptive responses occurring during invasion. Here we use microsatellite data to infer the population structure and invasion history of the introduced house sparrow (Passer domesticus) in Australia and New Zealand. Our results identify stronger population structure within Australia in comparison to New Zealand and patterns are consistent with historical records of multiple introduction sites across both countries. Within the five population clusters identified in Australia, we find declines in genetic diversity as we move away from the reported introduction site within each cluster. This pattern is consistent with sequential founder events. Interestingly, an even stronger decline in genetic diversity is seen across Australia as we move away from the Melbourne introduction site; secondary historical reports suggest this site imported a large number of sparrows and was possible the source of a single range expansion across Australia. However, private allele numbers are highest in the north, away from Melbourne, which could be a result of drift increasing the frequency of rare alleles in areas of smaller population size or due to an independent introduction that seeded or augmented the northern population. This study highlights the difficulties of elucidating population dynamics in introduced species with complex introduction histories and suggests that a combination of historical and genetic data can be useful.
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References
Anderson TR (2006) Biology of the ubiquitous house sparrow: from genes to populations. University Press, New York
Andrew SC, Griffith SC (2016) Inaccuracies in the history of a well-known introduction: a case study of the Australian House Sparrow (Passer domesticus). Avian Res 7:9. https://doi.org/10.1186/s40657-016-0044-3
Baalsrud HT, Saether B-E, Hagen IJ et al (2014) Effects of population characteristics and structure on estimates of effective population size in a house sparrow metapopulation. Mol Ecol 23:2653–2668. https://doi.org/10.1111/mec.12770
Balmford R (1981) Early introductions of birds to Victoria. Vic Nat 98:96–105
Barrett SCH (2014) Foundations of invasion genetics: the Baker and Stebbins legacy. Mol Ecol 24:1927–1941. https://doi.org/10.1111/mec.13014
Bates D, Maechler M, Bolker B, Walker S (2015) lme4: linear mixed-effects models using Eigen and S4. R package version 1.1-8. https://CRAN.R-project.org/package=lme4
Benazzo A, Ghirotto S, Vilaça ST, Hoban S (2015) Using ABC and microsatellite data to detect multiple introductions of invasive species from a single source. Heredity (Edinb) 115:262–272. https://doi.org/10.1038/hdy.2015.38
Blackburn TM (2008) Using aliens to explore how our planet works. Proc Natl Acad Sci 105:9–10
Cavalli-Sforza LL, Edwards AWF (1967) Phylogenetic analysis models and estimation procedures. Am J Hum Genet 19:233–257. https://doi.org/10.2307/2406616
Colautti RI, Lau JA (2015) Contemporary evolution during invasion: evidence for differentiation, natural selection, and local adaptation. Mol Ecol 24:1999–2017
Cole SR, Parkin DT (1986) Adenosine-deaminase polymorphism in house sparrow, Passer-domesticus. Anim Genet 17:77–88
Cristescu ME (2015) Genetic reconstructions of invasion history. Mol Ecol 24:2212–2225. https://doi.org/10.1111/mec.13117
Dawson DA, Horsburgh GJ, Krupa AP et al (2012) Microsatellite resources for Passeridae species: a predicted microsatellite map of the house sparrow Passer domesticus. Mol Ecol Resour 12:501–523. https://doi.org/10.1111/j.1755-0998.2012.03115.x
De Mita S, Thuillet A-C, Gay L et al (2013) Detecting selection along environmental gradients: analysis of eight methods and their effectiveness for outbreeding and selfing populations. Mol Ecol 22:1383–1399. https://doi.org/10.1111/mec.12182
de Villemereuil P, Frichot É, Bazin É et al (2014) Genome scan methods against more complex models: When and how much should we trust them? Mol Ecol 23:2006–2019. https://doi.org/10.1111/mec.12705
Dlugosch KM, Parker IM (2008) Founding events in species invasions: genetic variation, adaptive evolution, and the role of multiple introductions. Mol Ecol 17:431–449. https://doi.org/10.1111/j.1365-294X.2007.03538.x
Earl DA, VonHoldt BM (2012) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genet Resour 4:359–361. https://doi.org/10.1007/s12686-011-9548-7
Estoup A, Guillemaud T (2010) Reconstructing routes of invasion using genetic data: Why, how and so what? Mol Ecol 19:4113–4130. https://doi.org/10.1111/j.1365-294X.2010.04773.x
Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software structure: a simulation study. Mol Ecol 14:2611–2620. https://doi.org/10.1111/j.1365-294X.2005.02553.x
Excoffier L, Laval G, Schneider S (2005) Arlequin (version 3.0): an integrated software package for population genetics data analysis. Evol Bioinform Online 1:47
Excoffier L, Foll M, Petit RJ (2009a) Genetic consequences of range expansions. Annu Rev Ecol Evol Syst 40:481–501. https://doi.org/10.1146/annurev.ecolsys.39.110707.173414
Excoffier L, Hofer T, Foll M (2009b) Detecting loci under selection in a hierarchically structured population. Heredity (Edinb) 103:285–298. https://doi.org/10.1038/hdy.2009.74
Francois O, Martins H, Caye K, Schoville S (2016) A tutorial on controlling false discoveries in genome scans for selection. Mol Ecol 25:454–469. https://doi.org/10.1111/mec.13513
Frantz AC, Cellina S, Krier A et al (2009) Using spatial Bayesian methods to determine the genetic structure of a continuously distributed population: Clusters or isolation by distance? J Appl Ecol 46:493–505. https://doi.org/10.1111/j.1365-2664.2008.01606.x
Goudet J (1995) FSTAT (version 1.2): a computer program to calculate F-statistics. J Hered 86:485–486. https://doi.org/10.1093/jhered/esh074
Günther T, Coop G (2013) Robust identification of local adaptation from allele frequencies. Genetics 195:205–220. https://doi.org/10.1534/genetics.113.152462
Hagen IJ, Billing AM, Rønning B et al (2013) The easy road to genome-wide medium density SNP screening in a non-model species: development and application of a 10 K SNP-chip for the house sparrow (Passer domesticus). Mol Ecol Resour 13:429–439. https://doi.org/10.1111/1755-0998.12088
Higgins PJ, Peter JM, Cowling SJ (2006) Handbook of Australian, New Zealand and Antarctic birds: Boatbill to starlings, vol 7. Oxford University Press, Melbourne, pp 1102–1126
Jakobsson M, Rosenberg NA (2007) CLUMPP: a cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinformatics 23:1801–1806. https://doi.org/10.1093/bioinformatics/btm233
Jakobsson M, Edge MD, Rosenberg NA (2013) The relationship between FST and the frequency of the most frequent allele. Genetics 193:515–528. https://doi.org/10.1534/genetics.112.144758
Jensen H, Moe R, Hagen IJ et al (2013) Genetic variation and structure of house sparrow populations: Is there an island effect? Mol Ecol 22:1792–1805. https://doi.org/10.1111/mec.12226
Johnson MTJ, Munshi-South J (2017) Evolution of life in urban environments. Science 358:eaam8327
Jombart T (2008) Adegenet: a R package for the multivariate analysis of genetic markers. Bioinformatics 24:1403–1405. https://doi.org/10.1093/bioinformatics/btn129
Jombart T, Pontier D, Dufour A-B (2009) Genetic markers in the playground of multivariate analysis. Heredity (Edinb) 102:330–341. https://doi.org/10.1038/hdy.2008.130
Jombart T, Devillard S, Balloux F et al (2010) Discriminant analysis of principal components: a new method for the analysis of genetically structured populations. BMC Genet 11:94. https://doi.org/10.1186/1471-2156-11-94
Kekkonen J, Hanski IK, Jensen H et al (2011a) Increased genetic differentiation in house sparrows after a strong population decline: from panmixia towards structure in a common bird. Biol Conserv 144:2931–2940. https://doi.org/10.1016/j.biocon.2011.08.012
Kekkonen J, Seppä P, Hanski IK et al (2011b) Low genetic differentiation in a sedentary bird: house sparrow population genetics in a contiguous landscape. Heredity (Edinb) 106:183–190. https://doi.org/10.1038/hdy.2010.32
Keller LF, Waller DM (2002) Inbreeding effects in wild populations. Trends Ecol Evol 17:230–241
Kuznetsova A, Brockhoff PB, Christensen RHB (2016) lmerTest: tests in linear mixed effects models. R package version 2.0-32. https://CRAN.R-project.org/package=lmerTest
Langella O (2002) POPULATIONS. Bioinformatics. http://bioinformatics.org/project/?group_id=84
Lee CEE (2002) Evolutionary genetics of invasive species. Trends Ecol Evol 17:386–391. https://doi.org/10.1016/S0169-5347(02)02554-5
Lever C (1985) Naturalized Mammals of the World. Longman, London
Lever C (1992) They dined on eland. Quiller Press Ltd, London
Lever C (2005) Naturalised birds of the world. T & A D Poyser, London, pp 204–218
Liebl AL, Schrey AW, Andrew SC et al (2015) Invasion genetics: lessons from a ubiquitous bird, the house sparrow Passer domesticus. Curr Zool 61:465–476. https://doi.org/10.1093/czoolo/61.3.465
Lima MR, Macedo RHF, Martins TLF et al (2012) Genetic and morphometric divergence of an invasive bird: the introduced house sparrow (Passer domesticus) in Brazil. PLoS ONE. https://doi.org/10.1371/journal.pone.0053332
Long JL (1981) Introduced birds of the world: the worldwide history, distribution and influence of birds introduced to new environments. Universe Books, Campbelltown, pp 372–381
Long JL (1988) Introduced birds and mammals in Western Australia. Agric. Prot. Board West. Aust. Agriculture Protection Board, Perth, pp 13–14
Lotterhos KE, Whitlock MC (2014) Evaluation of demographic history and neutral parameterization on the performance of FST outlier tests. Mol Ecol 23:2178–2192. https://doi.org/10.1111/mec.12725
Marshall TC, Slate J, Kruuk LEB, Pemberton JM (1997) Statistical confidence for likelihood-based paternity. Mol Ecol 7:639–655
Miller N, Estoup A, Toepfer S et al (2005) Multiple transatlantic introductions of the western corn rootworm. Science 310:992. https://doi.org/10.1126/science.1115871
Nakagawa S, Schielzeth H (2013) A general and simple method for obtaining R2 from generalized linear mixed-effects models. Methods Ecol Evol 4:133–142. https://doi.org/10.1111/j.2041-210x.2012.00261.x
Ockendon N, Griffith SC, Burke T (2009) Extrapair paternity in an insular population of house sparrows after the experimental introduction of individuals from the mainland. Behav Ecol 20:305–312. https://doi.org/10.1093/beheco/arp006
Orsini L, Vanoverbeke J, Swillen I et al (2013) Drivers of population genetic differentiation in the wild: isolation by dispersal limitation, isolation by adaptation and isolation by colonization. Mol Ecol 22:5983–5999. https://doi.org/10.1111/mec.12561
Parkin DT, Cole SR (1985) Genetic differentiation and rates of evolution in some introduced populations of the house sparrow, Passer domesticus in Australia and New Zealand. Heredity (Edinb) 54:15–23. https://doi.org/10.1038/hdy.1985.4
Pascual M, Chapuis MP, Mestres F et al (2007) Introduction history of Drosophila subobscura in the New World: a microsatellite-based survey using ABC methods. Mol Ecol 16:3069–3083. https://doi.org/10.1111/j.1365-294X.2007.03336.x
Peakall R, Smouse PE (2006) GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol Ecol Notes 6:288–295. https://doi.org/10.1111/j.1471-8286.2005.01155.x
Peakall R, Smouse PE (2012) GenALEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research-an update. Bioinformatics 28:2537–2539. https://doi.org/10.1093/bioinformatics/bts460
Peter BM, Slatkin M (2015) The effective founder effect in a spatially expanding population. Evolution 69:721–734. https://doi.org/10.1111/evo.12609.This
Preuss S, Berggren Å, Cassel-Lundhagen A (2015) Genetic patterns reveal an old introduction event and dispersal limitations despite rapid distribution expansion. Biol Invasions 17:2851–2862. https://doi.org/10.1007/s10530-015-0915-2
Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959
R Core Team (2017) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. URL https://www.R-project.org
Raymond M, Rousset F (1993) GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. J Hered 86:248–249
Rellstab C, Gugerli F, Eckert AJ et al (2015) A practical guide to environmental association analysis in landscape genomics. Mol Ecol 24:4348–4370. https://doi.org/10.1111/mec.13322
Rollins LA, Woolnough AP, Wilton AN et al (2009) Invasive species can’t cover their tracks: using microsatellites to assist management of starling (Sturnus vulgaris) populations in Western Australia. Mol Ecol 18:1560–1573. https://doi.org/10.1111/j.1365-294X.2009.04132.x
Rosenberg NA (2004) Distruct: a program for the graphical display of population structure. Mol Ecol Notes 4:137–138. https://doi.org/10.1046/j.1471-8286.2003.00566.x
Sætre G-P, Riyahi S, Aliabadian M et al (2012) Single origin of human commensalism in the house sparrow. J Evol Biol 25:788–796. https://doi.org/10.1111/j.1420-9101.2012.02470.x
Sax DF, Stachowicz JJ, Brown JH et al (2007) Ecological and evolutionary insights from species invasions. Trends Ecol Evol 22:465–471. https://doi.org/10.1016/j.tree.2007.06.009
Schrey AW, Grispo M, Awad M et al (2011) Broad-scale latitudinal patterns of genetic diversity among native European and introduced house sparrow (Passer domesticus) populations. Mol Ecol 20:1133–1143. https://doi.org/10.1111/j.1365-294X.2011.05001.x
Schrey AW, Liebl AL, Richards CL, Martin LB (2014) Range expansion of house sparrows (Passer domesticus) in Kenya: evidence of genetic admixture and human-mediated dispersal. J Hered 105:60–69. https://doi.org/10.1093/jhered/est085
Thomson GM (1922) The Naturalisation of Animals and Plants in New Zealand. University Press, Cambridge
Tufto J, Ringsby T, Dhondt AA et al (2005) A parametric model for estimation of dispersal patterns applied to five passerine spatially structured populations. Am Nat 165:E13–E26
Vangestel C, Mergeay J, Dawson DA et al (2011) Spatial heterogeneity in genetic relatedness among house sparrows along an urban-rural gradient as revealed by individual-based analysis. Mol Ecol 20:4643–4653. https://doi.org/10.1111/j.1365-294X.2011.05316.x
Wagner CH (1982) Simpson’s paradox in real life. Am Stat 36:46–48
Acknowledgements
For funding support: SCA was supported by Macquarie University Research Excellence Scholarships (No. 2013077). SCG was supported by an Australian Research Council Future Fellowship (FT130101253). SN was supported by a Rutherford Discovery Fellowship (New Zealand) and an Australian Research Council Future Fellowship (FT130100268). Fragment analysis was conducted at Macrogen, Inc. We would like to thank the large number of people who helped us with access to urban catch sites for sampling the human commensal house sparrow. We would also like to thank, Amanda D. Griffith, Elizabeth L. Sheldon, Anna Feit, Ondi Crino and Peter Bird for their participation with field work in Australia and Karin Ludwig in New Zealand. We would also like to thank Elizabeth L. Sheldon for their assistance with lab work.
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Andrew, S.C., Awasthy, M., Bolton, P.E. et al. The genetic structure of the introduced house sparrow populations in Australia and New Zealand is consistent with historical descriptions of multiple introductions to each country. Biol Invasions 20, 1507–1522 (2018). https://doi.org/10.1007/s10530-017-1643-6
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DOI: https://doi.org/10.1007/s10530-017-1643-6