Concurrent invasions of European starlings in Australia and North America reveal population-specific differentiation in shared genomic regions.
genetic bottleneck
invasive species
natural selection
Journal
Molecular ecology
ISSN: 1365-294X
Titre abrégé: Mol Ecol
Pays: England
ID NLM: 9214478
Informations de publication
Date de publication:
07 Nov 2023
07 Nov 2023
Historique:
revised:
22
09
2023
received:
04
11
2022
accepted:
23
10
2023
medline:
7
11
2023
pubmed:
7
11
2023
entrez:
7
11
2023
Statut:
aheadofprint
Résumé
A species' success during the invasion of new areas hinges on an interplay between the demographic processes common to invasions and the specific ecological context of the novel environment. Evolutionary genetic studies of invasive species can investigate how genetic bottlenecks and ecological conditions shape genetic variation in invasions, and our study pairs two invasive populations that are hypothesized to be from the same source population to compare how each population evolved during and after introduction. Invasive European starlings (Sturnus vulgaris) established populations in both Australia and North America in the 19th century. Here, we compare whole-genome sequences among native and independently introduced European starling populations to determine how demographic processes interact with rapid evolution to generate similar genetic patterns in these recent and replicated invasions. Demographic models indicate that both invasive populations experienced genetic bottlenecks as expected based on invasion history, and we find that specific genomic regions have differentiated even on this short evolutionary timescale. Despite genetic bottlenecks, we suggest that genetic drift alone cannot explain differentiation in at least two of these regions. The demographic boom intrinsic to many invasions as well as potential inversions may have led to high population-specific differentiation, although the patterns of genetic variation are also consistent with the hypothesis that this infamous and highly mobile invader adapted to novel selection (e.g., extrinsic factors). We use targeted sampling of replicated invasions to identify and evaluate support for multiple, interacting evolutionary mechanisms that lead to differentiation during the invasion process.
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Subventions
Organisme : Newnham College, Cambridge
Organisme : The Winston Churchill Memorial Trust
Organisme : UK Biotechnology and Biological Sciences Research Council
ID : BB/P013759/1
Organisme : University of New South Wales
Informations de copyright
© 2023 John Wiley & Sons Ltd.
Références
Alexander, D. H., & Lange, K. (2011). Enhancements to the ADMIXTURE algorithm for individual ancestry estimation. BMC Bioinformatics, 12, 246.
Ball, G. F., & Wingfield, J. C. (1987). Changes in plasma levels of luteinizing hormone and sex steroid hormones in relation to multiple-broodedness and nest-site density in male starlings. Physiological Zoology, 60, 191-199.
Berthouly-Salazar, C., Hui, C., Blackburn, T. M., Gaboriaud, C., van Rensburg, B. J., van Vuuren, B. J., & Le Roux, J. J. (2013). Long-distance dispersal maximizes evolutionary potential during rapid geographic range expansion. Molecular Ecology, 22, 5793-5804.
Blackburn, T. M., Cassey, P., Lockwood, J. L., & Duncan, R. P. (2020). The relationship between propagule pressure and establishment success in alien bird populations: A re-analysis of Moulton & Cropper (2019). PeerJ, 8, e8766.
Blakeslee, A. M. H., Manousaki, T., Vasileiadou, K., & Tepolt, C. K. (2020). An evolutionary perspective on marine invasions. Evolutionary Applications, 13, 479-485.
Bock, D. G., Kantar, M. B., Caseys, C., Matthey-Doret, R., & Rieseberg, L. H. (2018). Evolution of invasiveness by genetic accommodation. Nature Ecology & Evolution, 2, 991-999.
Bodt, L. H., Rollins, L. A., & Zichello, J. M. (2020). Contrasting mitochondrial diversity of European starlings (Sturnus vulgaris) across three invasive continental distributions. Ecology and Evolution, 10, 10186-10195.
Bourgeois, Y., Stritt, C., Walser, J., Gordon, S. P., Vogel, J. P., & Roulin, A. C. (2018). Genome-wide scans of selection highlight the impact of biotic and abiotic constraints in natural populations of the model grass Brachypodium distachyon. The Plant Journal, 96(2), 438-451. https://doi.org/10.1111/tpj.14042
Briski, E., Chan, F. T., Darling, J. A., Lauringson, V., Macisaac, H. J., Zhan, A., & Bailey, S. A. (2018). Beyond propagule pressure: Importance of selection during the transport stage of biological invasions. Frontiers in Ecology and the Environment, 16, 345-353.
Burtt, H. E., & Giltz, M. L. (1977). Seasonal directional patterns of movements and migrations of starlings. Bird-Banding, 48, 259-271.
Cardilini, A. P. A., Buchanan, K. L., Sherman, C. D. H., Cassey, P., & Symonds, M. R. E. (2016). Tests of ecogeographical relationships in a non-native species: What rules avian morphology? Oecologia, 181, 783-793.
Cardilini, A. P. A., Micallef, S., Bishop, V. R., Sherman, C. D. H., Meddle, S. L., & Buchanan, K. L. (2018). Environmental influences on neuromorphology in the non-native starling Sturnus vulgaris. Brain, Behavior and Evolution, 92, 63-70.
Cassey, P., Delean, S., Lockwood, J. L., Sadowski, J. S., & Blackburn, T. M. (2018). Dissecting the null model for biological invasions: A meta-analysis of the propagule pressure effect. PLoS Biology, 16, e2005987.
Cruickshank, T. E., & Hahn, M. W. (2014). Reanalysis suggests that genomic islands of speciation are due to reduced diversity, not reduced gene flow. Molecular Ecology, 23, 3133-3157.
Danecek, P., Auton, A., Abecasis, G., Albers, C. A., Banks, E., DePristo, M. A., Handsaker, R. E., Lunter, G., Marth, G. T., Sherry, S. T., et al. (2011). The variant call format and VCFtools. Bioinformatics, 27, 2156-2158.
Davis, M. A. (2020). Let's welcome a variety of voices to invasion biology. Conservation Biology, 34, 1329-1330.
Dawson, A. (1983). Plasma gonadal steroid levels in wild starlings (Sturnus vulgaris) during the annual cycle and in relation to the stages of breeding. General and Comparative Endocrinology, 49, 286-294.
Dlugosch, K. M., Anderson, S. R., Braasch, J., Cang, F. A., & Gillette, H. D. (2015). The devil is in the details: Genetic variation in introduced populations and its contributions to invasion. Molecular Ecology, 24, 2095-2111.
Dlugosch, K. M., & Parker, I. M. (2008). Founding events in species invasions: Genetic variation, adaptive evolution, and the role of multiple introductions. Molecular Ecology, 17, 431-449.
Dolbeer, R. A. (1982). Migration patterns of age and sex classes of blackbirds and starlings. Journal of Field Ornithology, 53, 28-46.
Dormontt, E. E., Lowe, A. J., & Prentis, P. J. (2011). Is rapid adaptive evolution important in successful invasions? In D. M. Richardson (Ed.), Fifty years of invasion ecology. Blackwell Publishing Ltd.
Early, R., Bradley, B. A., Dukes, J. S., Lawler, J. J., Olden, L. D., Blumenthal, D. M., Gonzalez, P., Grosholz, E. D., Ibañez, I., Miller, L. P., Sorte, C. J. B., & Tatem, A. J. (2016). Global threats from invasive alien species in the twenty-first century and national response capacities. Nature Communications, 7, 12485.
Enders, M., Havemann, F., Ruland, F., Bernard-Verdier, M., Catford, J. A., Gómez-Aparicio, L., Haider, S., Heger, T., Kueffer, C., Kühn, I., Meyerson, L. A., Musseau, C., Novoa, A., Ricciardi, A., Sagouis, A., Schittko, C., Strayer, D. L., Vilà, M., Essl, F., … Jeschke, J. M. (2020). A conceptual map of invasion biology: Integrating hypotheses into a consensus network. Global Ecology and Biogeography, 29, 978-991.
Estoup, A., Ravigné, V., Hufbauer, R., Vitalis, R., Gautier, M., & Facon, B. (2016). Is There a Genetic Paradox of Biological Invasion? Annual Review of Ecology, Evolution, and Systematics, 47(1), 51-72. https://doi.org/10.1146/annurev-ecolsys-121415-032116
Excoffier, L., Dupanloup, I., Huerta-Sanchez, E., Sousa, V. C., & Foll, M. (2013). Robust demographic inference from genomic and SNP data. PLoS Genetics, 9, e1003905-e1003917.
Feare, C. (1984). The starling. Oxford University Press.
Feare, C. J., & Forrester, G. J. (2002). The dynamics of a suburban nestbox breeding colony of Starlings Sturnus vulgaris. In H. Q. P. Crick, R. A. Robinson, G. F. Appleton, N. A. Clark, & A. D. Rickard (Eds.), Investigation into the causes of the decline of Starlings and House Sparrows in Great Britain. British Trust for Ornithology.
Forbush, E. H. (1915). The starling. Wright and Potter Printing Co.
Fumagalli, M., Vieira, F. G., Linderoth, T., & Nielsen, R. (2014). ngsTools: Methods for population genetics analyses from next-generation sequencing data. Bioinformatics, 30, 1486-1487.
Grabherr, M. G., Russell, P., Meyer, M., Mauceli, E., Alfoldi, J., Di Palma, F., & Lindblad-Toh, K. (2010). Genome-wide synteny through highly sensitive sequence alignment: Satsuma. Bioinformatics, 26, 1145-1151.
Gralka, M., Stiewe, F., Farrell, F., Möbius, W., Waclaw, B., & Hallatschek, O. (2016). Allele surfing promotes microbial adaptation from standing variation. Ecology Letters, 19, 889-898.
Hejase, H. A., Salman-Minkov, A., Campagna, L., Hubisz, M. J., Lovette, I. J., Gronau, I., & Siepel, A. (2020). Genomic islands of differentiation in a rapid avian radiation have been driven by recent selective sweeps. Proceedings of the National Academy of Sciences, 117(48), 30554-30565. https://doi.org/10.1073/pnas.2015987117
Higgins, P. J., Peter, J. M., & Cowling, S. J. (2006). Handbook of Australian, New Zealand & Antarctic birds. Volume 7. Boatbill to starlings. Oxford University Press.
Hofmeister, N. R., Werner, S. J., & Lovette, I. J. (2021). Environmental correlates of genetic variation in the invasive European starling in North America. Molecular Ecology, 30, 1251-1263.
Hubisz, M., & Siepel, A. (2020). Inference of Ancestral Recombination Graphs Using ARGweaver. Statistical Population Genomics, 231-266, https://doi.org/10.1007/978-1-0716-0199-0_10
Irwin, D. E., Milá, B., Toews, D. P. L., Brelsford, A., Kenyon, H. L., Porter, A. N., Grossen, C., Delmore, K. E., Alcaide, M., & Irwin, J. H. (2018). A comparison of genomic islands of differentiation across three young avian species pairs. Molecular Ecology, 27, 4839-4855.
Kawakami, T., Smeds, L., Backström, N., Husby, A., Qvarnström, A., Mugal, C. F., Olason, P., & Ellegren, H. (2014). A high-density linkage map enables a second-generation collared flycatcher genome assembly and reveals the patterns of avian recombination rate variation and chromosomal evolution. Molecular Ecology, 23, 4035-4058.
Kessel, B. (1953). Distribution and migration of the European starling in North America. The Condor, 55, 49-67.
Kim, S. Y., Lohmueller, K. E., Albrechtsen, A., Li, Y., Korneliussen, T., Tian, G., Grarup, N., Jiang, T., Andersen, G., Witte, D., Jorgensen, T., Hansen, T., Pedersen, O., Wang, J., & Nielsen, R. (2011). Estimation of allele frequency and association mapping using next-generation sequencing data. BMC Bioinformatics, 12, 231.
Knief, U., & Forstmeier, W. (2016). Mapping centromeres of microchromosomes in the zebra finch (Taeniopygia guttata) using half-tetrad analysis. Chromosoma, 125, 1-12.
Kolbe, J. J., Glor, R. E., Rodriguez Schettino, L., Chamizo Lara, A., Larson, A., & Losos, J. B. (2004). Genetic variation increases during biological invasion by a Cuban lizard. Nature, 431, 177-181.
Korneliussen, T. S., Albrechtsen, A., & Nielsen, R. (2014). ANGSD: Analysis of next generation sequencing data. BMC Bioinformatics, 15, 356.
Langmead, B., & Salzberg, S. L. (2012). Fast gapped-read alignment with bowtie 2. Nature Methods, 9, 357-359.
Linz, G. M., Homan, H. J., Gaulker, S. M., Penry, L. B., & Bleier, W. J. (2007). European starlings: A review of an invasive species with far-reaching impacts. http://digitalcommons.unl.edu/nwrcinvasive/24
Lowe, W. H., Kovach, R. P., & Allendorf, F. W. (2017). Population genetics and demography unite ecology and evolution. Trends in Ecology & Evolution, 32, 141-152.
Lu-Irving, P., Marx, H. E., & Dlugosch, K. M. (2018). ScienceDirect leveraging contemporary species introductions to test phylogenetic hypotheses of trait evolution. Current Opinion in Plant Biology, 42, 95-102.
Marques, D. A., Jones, F. C., Di Palma, F., Kingsley, D. M., & Reimchen, T. E. (2018). Experimental evidence for rapid genomic adaptation to a new niche in an adaptive radiation. Nature Ecology & Evolution, 2, 1128-1138.
McKenna, A., Hanna, M., Banks, E., Sivachenko, A., Cibulskis, K., Kernytsky, A., Garimella, K., Altshuler, D., Gabriel, S., Daly, M., & DePristo, M. A. (2010). The genome analysis toolkit: A MapReduce framework for analyzing next-generation DNA sequencing data. Genome Research, 20, 1297-1303.
Miller, T. E. X., Angert, A. L., Brown, C. D., Lee-Yaw, J. A., Lewis, M., Lutscher, F., Marculis, N. G., Melbourne, B. A., Shaw, A. K., Szúcs, M., Tabares, O., Usui, T., Weiss-Lehman, C., & Williams, J. L. (2020). Eco-evolutionary dynamics of range expansion. Ecology, 101(10), e03139.
Moinet, A., Schlichta, F., Peischl, S., & Excoffier, L. (2022). Strong neutral sweeps occurring during a population contraction. Genetics, 220, iyac021.
Moulton, M. P., & Cropper, W. P., Jr. (2019). Propagule pressure does not consistently predict the outcomes of exotic bird introductions. PeerJ, 7, e7637.
Nielsen, R., Korneliussen, T., Albrechtsen, A., Li, Y., & Wang, J. (2012). SNP calling, genotype calling, and sample allele frequency estimation from new-generation sequencing data. PLoS One, 7, e37558.
North, H. L., McGaughran, A., & Jiggins, C. D. (2021). Insights into invasive species from whole-genome resequencing. Molecular Ecology, 30(23), 6289-6308. https://doi.org/10.1111/mec.15999
Okonechnikov, K., Conesa, A., & García-Alcalde, F. (2015). Qualimap 2: Advanced multi-sample quality control for high-throughput sequencing data. Bioinformatics, 32, btv566.
Parvizi, E., Dhami, M. K., Yan, J., & McGaughran, A. (2023). Population genomic insights into invasion success in a polyphagous agricultural pest, Halyomorpha halys. Molecular Ecology, 32(1), 138-151.
Rasmussen, M. D., Hubisz, M. J., Gronau, I., & Siepel, A. (2014). Genome-wide inference of ancestral recombination graphs. PLoS Genetics, 10(5), e1004342.
Redding, D. W., Pigot, A. L., Dyer, E. E., Şekercioğlu, Ç. H., Kark, S., & Blackburn, T. M. (2019). Location-level processes drive the establishment of alien bird populations worldwide. Nature, 571, 103-106.
Revell, L. (2012). Phytools: An R package for phylogenetic comparative biology (and other things). Methods in Ecology and Evolution, 3, 217-223.
Ricciardi, A., & Ryan, R. (2017). The exponential growth of invasive species denialism. Biological Invasions, 20, 549-553.
Rollins, L. A., Woolnough, A. P., Wilton, A. N., Sinclair, R., & Sherwin, W. B. (2009). Invasive species can't cover their tracks: Using microsatellites to assist management of starling (Sturnus vulgaris) populations in Western Australia. Molecular Ecology, 18, 1560-1573.
Russell, J. C., & Blackburn, T. M. (2017). The rise of invasive species denialism. Trends in Ecology & Evolution, 32, 3-6.
Sagoff, M. (2019). Fact and value in invasion biology. Conservation Biology, 34, 581-588.
Saxonov, S., Berg, P., & Brutlag, D. L. (2006). A genome-wide analysis of CpG dinucleotides in the human genome distinguishes two distinct classes of promoters. Proceedings of the National Academy of Sciences of the United States of America, 103, 1412-1417.
Schneider, K., White, T. J., Mitchell, S., Adams, C. E., Reeve, R., & Elmer, K. R. (2021). The pitfalls and virtues of population genetic summary statistics: Detecting selective sweeps in recent divergences. Journal of Evolutionary Biology, 34, 893-909.
Schubert, M., Lindgreen, S., & Orlando, L. (2016). AdapterRemoval v2: Rapid adapter trimming, identification, and read merging. BMC Research Notes, 9, 88.
Sheldon, E. L., Schrey, A., Andrew, S. C., Ragsdale, A., & Griffith, S. C. (2018). Epigenetic and genetic variation among three separate introductions of the house sparrow (Passer domesticus) into Australia. Royal Society Open Science, 5, 172185.
Simberloff, D. (2009). The role of propagule pressure in biological invasions. Annual Review of Ecology, Evolution, and Systematics, 40, 81-102.
Simmen, M. (2008). Genome-scale relationships between cytosine methylation and dinucleotide abundances in animals. Genomics, 92, 33-40.
Skotte, L., Korneliussen, T. S., & Albrechtsen, A. (2013). Estimating individual admixture proportions from next generation sequencing data. Genetics, 195, 693-702.
Smith, A. L., Hodkinson, T. R., Villellas, J., Catford, J. A., Csergő, A. M., Blomberg, S. P., Crone, E. E., Ehrlén, J., Garcia, M. B., Laine, A.-L., Roach, D. A., Salguero-Gómez, R., Wardle, G. M., Childs, D. Z., Elderd, B. D., Finn, A., Munné-Bosch, S., Baudraz, M. E. A., Bódis, J., … Buckley, Y. M. (2020). Global gene flow releases invasive plants from environmental constraints on genetic diversity. Proceedings of the National Academy of Sciences of the United States of America, 117, 4218-4227.
Stapley, J., Reger, J., Feulner, P. G. D., Smadja, C., Galindo, J., Ekblom, R., Bennison, C., Ball, A. D., Beckerman, A. P., & Slate, J. (2010). Adaptation genomics: The next generation. Trends in Ecology & Evolution, 25, 705-712.
Stuart, K. C., Cardilini, A. P. A., Cassey, P., Richardson, M. F., Sherwin, W., Rollins, L. A., & Sherman, C. D. H. (2020). Signatures of selection in a recent invasion reveals adaptive divergence in a highly vagile invasive species. Molecular Ecology, 30(6), 1419-1434. https://doi.org/10.1111/mec.15601
Stuart, K. C., Edwards, R. J., Cheng, Y., Warren, W. C., Burt, D. W., Sherwin, W. B., Hofmeister, N. R., Werner, S. J., Ball, G. F., Bateson, M., et al. (2021). Transcript- and annotation-guided genome assembly of the European starling. bioRxiv. 10.1101/2021.04.07.438753
Stuart, K. C., Hofmeister, N. R., Zichello, J. M., & Rollins, L. A. (2023). Global invasion history and native decline of the common starling: Insights through genetics. Biological Invasions, 25, 1291-1316. https://doi.org/10.1007/s10530-022-02982-5
Stuart, K. C., Sherwin, W. B., Austin, J. J., Bateson, M., Eens, M., Brandley, M. C., & Rollins, L. A. (2022). Historical museum samples enable the examination of divergent and parallel evolution during invasion. Molecular Ecology, 31, 1836-1852. https://doi.org/10.1111/mec.16353
Stuart, K. C., Sherwin, W. B., Cardilini, A. P. A., & Rollins, L. A. (2022). Genetics and plasticity are responsible for climate induced ecogeographical patterns in a recent invasion. Frontiers in Genetics, 13, 824424. https://doi.org/10.3389/fgene.2022.824424
Supek, F., Bosnjak, M., Skunca, N., & Smuc, T. (2011). REVIGO summarizes and visualizes long lists of gene ontology terms. PLoS One, 6, e21800.
Sved, J., & Bird, A. (1990). The expected equilibrium of the CpG dinucleotide in vertebrate genomes under a mutation model. Proceedings of the National Academy of Sciences of the United States of America, 87, 4692-4696.
Terhorst, J., Kamm, J. A., & Song, Y. S. (2017). Robust and scalable inference of population history from hundreds of unphased whole genomes. Nature Genetics, 49, 303-309.
Tsutsui, N. D., Suarez, A. V., Holway, D. A., & Case, T. J. (2000). Reduced genetic variation and the success of an invasive species. Proceedings of the National Academy of Sciences of the United States of America, 97, 5948-5953.
Verhoeven, K. J. F., Macel, M., Wolfe, L. M., & Biere, A. (2011). Population admixture, biological invasions and the balance between local adaptation and inbreeding depression. Proceedings of the Royal Society B: Biological Sciences, 278, 2-8.
Waterman, M., Fuller, C., & Murray, M. D. (2008). Studies of roosting common starlings Sturnus vulgaris in South Australia. Corella, 32, 25-29.
Werner, S. J., Fischer, J. W., & Hobson, K. A. (2020). Multi-isotopic (δ2H, δ13C, δ15N) tracing of molt origin for European starlings associated with U.S. dairies and feedlots. PLoS One, 15, e0237137.
White, T. A., Perkins, S. E., Heckel, G., & Searle, J. B. (2013). Adaptive evolution during an ongoing range expansion: The invasive bank vole (Myodes glareolus) in Ireland. Molecular Ecology, 22, 2971-2985.
Williams, J. L., Hufbauer, R. A., & Miller, T. E. X. (2019). How evolution modifies the variability of range expansion. Trends in Ecology & Evolution, 34, 903-913.
Willoughby, J. R., Harder, A. M., Tennessen, J. A., Scribner, K. T., & Christie, M. R. (2018). Rapid genetic adaptation to a novel environment despite a genome-wide reduction in genetic diversity. Molecular Ecology, 17, 675-4051.
Yang, J., Benyamin, B., McEvoy, B. P., Gordon, S., Henders, A. K., Nyholt, D. R., Madden, P. A., Heath, A. C., Martin, N. G., Montgomery, G. W., Goddard, M. E., & Visscher, P. M. (2010). Common SNPs explain a large proportion of the heritability for human height. Nature Genetics, 42(7), 565-569. https://doi.org/10.1038/ng.608
Zheng, X., Levine, D., Shen, J., Gogarten, S. M., Laurie, C., & Weir, B. S. (2012). A high-performance computing toolset for relatedness and principal component analysis of SNP data. Bioinformatics, 28, 3326-3328.