in

Evolutionary origins of genomic adaptations in an invasive copepod

  • 1.

    Paini, D. R. et al. Global threat to agriculture from invasive species. Proc. Natl Acad. Sci. USA 113, 7575–7579 (2016).

    CAS  PubMed  Google Scholar 

  • 2.

    Bradshaw, C. J. A. et al. Massive yet grossly underestimated global costs of invasive insects. Nat. Commun. 7, 12986 (2016).

    CAS  PubMed  PubMed Central  Google Scholar 

  • 3.

    Bellard, C. et al. Will climate change promote future invasions? Glob. Change Biol. 19, 3740–3748 (2013).

    Google Scholar 

  • 4.

    Hellmann, J. J., Byers, J. E., Bierwagen, B. G. & Dukes, J. S. Five potential consequences of climate change for invasive species. Conserv. Biol. 22, 534–543 (2008).

    PubMed  Google Scholar 

  • 5.

    Chown, S. L. et al. Biological invasions, climate change and genomics. Evol. Appl. 8, 23–46 (2015).

    PubMed  Google Scholar 

  • 6.

    Rahel, F. J. & Olden, J. D. Assessing the effects of climate change on aquatic invasive species. Conserv. Biol. 22, 521–533 (2008).

    PubMed  Google Scholar 

  • 7.

    Chapman, D. S. et al. Modelling the introduction and spread of non-native species: international trade and climate change drive ragweed invasion. Glob. Change Biol. 22, 3067–3079 (2016).

    Google Scholar 

  • 8.

    Dam, H. G. Evolutionary adaptation of marine zooplankton to global change. Annu. Rev. Mar. Sci. 5, 349–370 (2013).

    Google Scholar 

  • 9.

    Blackburn, T. M. et al. A proposed unified framework for biological invasions. Trends Ecol. Evol. 26, 333–339 (2011).

    PubMed  Google Scholar 

  • 10.

    Lee, C. E. Evolutionary genetics of invasive species. Trends Ecol. Evol. 17, 386–391 (2002).

    Google Scholar 

  • 11.

    Lee, C. E. in Encyclopedia of Biological Invasions (eds Simberloff, D. & Rejmanek, M.) 215–222 (Univ. California Press 2010).

  • 12.

    Colautti, R. I., Alexander, J. M., Dlugosch, K. M., Keller, S. R. & Sultan, S. E. Invasions and extinctions through the looking glass of evolutionary ecology. Phil. Trans. R. Soc. B 372, 20160031 (2017).

    PubMed  Google Scholar 

  • 13.

    Williamson, M. & Fitter, A. The varying success of invaders. Ecology 77, 1661–1666 (1996).

    Google Scholar 

  • 14.

    Hayes, K. R. & Barry, S. C. Are there any consistent predictors of invasion success? Biol. Invasions 10, 483–506 (2008).

    Google Scholar 

  • 15.

    Bock, D. G. et al. What we still don’t know about invasion genetics. Mol. Ecol. 24, 2277–2297 (2015).

    PubMed  Google Scholar 

  • 16.

    Kolar, C. S. & Lodge, D. M. Progress in invasion biology: predicting invaders. Trends Ecol. Evol. 16, 199–204 (2001).

    PubMed  Google Scholar 

  • 17.

    Lee, C. E. & Bell, M. A. Causes and consequences of recent freshwater invasions by saltwater animals. Trends Ecol. Evol. 14, 284–288 (1999).

    CAS  PubMed  Google Scholar 

  • 18.

    Casties, I., Seebens, H. & Briski, E. Importance of geographic origin for invasion success: a case study of the North and Baltic seas versus the Great Lakes–St. Lawrence River region. Ecol. Evol. 6, 8318–8329 (2016).

    PubMed  PubMed Central  Google Scholar 

  • 19.

    Lee, C. E. & Gelembiuk, G. W. Evolutionary origins of invasive populations. Evol. Appl. 1, 427–448 (2008).

    PubMed  PubMed Central  Google Scholar 

  • 20.

    Winkler, G., Dodson, J. J. & Lee, C. E. Heterogeneity within the native range: population genetic analyses of sympatric invasive and noninvasive clades of the freshwater invading copepod Eurytemora affinis. Mol. Ecol. 17, 415–430 (2008).

    PubMed  Google Scholar 

  • 21.

    Barrett, R. D. H. & Schluter, D. Adaptation from standing genetic variation. Trends Ecol. Evol. 23, 38–44 (2008).

    PubMed  Google Scholar 

  • 22.

    Lee, C. E. Evolutionary mechanisms of habitat invasions, using the copepod Eurytemora affinis as a model system. Evol. Appl. 9, 248–270 (2016).

    CAS  PubMed  Google Scholar 

  • 23.

    Peischl, S. & Excoffier, L. Expansion load: recessive mutations and the role of standing genetic variation. Mol. Ecol. 24, 2084–2094 (2015).

    PubMed  Google Scholar 

  • 24.

    Messer, P. W., Ellner, S. P. & Hairston, N. G. Can population genetics adapt to rapid evolution? Trends Genet. 32, 408–418 (2016).

    CAS  PubMed  Google Scholar 

  • 25.

    Lewontin, R. The Genetic Basis of Evolutionary Change (Columbia Univ. Press, 1974).

  • 26.

    Crow, J. F. Muller, Dobzhansky, and overdominance. J. Hist. Biol. 20, 351–380 (1987).

    Google Scholar 

  • 27.

    Beatty, J. Weighing the risks: stalemate in the classical/balance controversy. J. Hist. Biol. 20, 289–319 (1987).

    Google Scholar 

  • 28.

    Asthana, S., Schmidt, S. & Sunyaev, S. A limited role for balancing selection. Trends Genet. 21, 30–32 (2005).

    CAS  PubMed  Google Scholar 

  • 29.

    Muller, H. J. Our load of mutations. Am. J. Hum. Genet. 2, 111–176 (1950).

    CAS  PubMed  PubMed Central  Google Scholar 

  • 30.

    Dobzhansky, T. A review of some fundamental concepts and problems of population genetics. Cold Spring Harb. Symp. Quant. Biol. 20, 1–15 (1955).

    CAS  PubMed  Google Scholar 

  • 31.

    Hedrick, P. W. Genetic variation in a heterogeneous environment. I. Temporal heterogeneity and absolute dominance model. Genetics 78, 757–770 (1974).

    CAS  PubMed  PubMed Central  Google Scholar 

  • 32.

    Dempster, E. R. Maintenance of genetic heterogeneity. Cold Spring Harb. Symp. Quant. Biol. 20, 25–32 (1955).

    CAS  PubMed  Google Scholar 

  • 33.

    Haldane, J. B. S. & Jayakar, S. D. Polymorphism due to selection of varying direction. J. Genet. 58, 237–242 (1963).

    Google Scholar 

  • 34.

    Gillespie, J. Polymorphism in random environments. Theor. Popul. Biol. 4, 193–195 (1973).

    Google Scholar 

  • 35.

    Felsenstein, J. Theoretical population genetics of variable selection and migration. Annu. Rev. Genet. 10, 253–280 (1976).

    CAS  PubMed  Google Scholar 

  • 36.

    Holt, R. D., Barfield, M. & Gomulkiewicz, R. Temporal variation can facilitate niche evolution in harsh sink environments. Am. Nat. 164, 187–200 (2004).

    PubMed  Google Scholar 

  • 37.

    Huang, Y., Tran, I. & Agrawal, A. F. Does genetic variation maintained by environmental heterogeneity facilitate adaptation to novel selection? Am. Nat. 188, 27–37 (2016).

    PubMed  Google Scholar 

  • 38.

    de Filippo, C. et al. Recent selection changes in human genes under long-term balancing selection. Mol. Biol. Evol. 33, 1435–1447 (2016).

    PubMed  PubMed Central  Google Scholar 

  • 39.

    Hermisson, J. & Pennings, P. S. Soft sweeps: molecular population genetics of adaptation from standing genetic variation. Genetics 169, 2335–2352 (2005).

    CAS  PubMed  PubMed Central  Google Scholar 

  • 40.

    Hermisson, J. & Pennings, P. S. Soft sweeps and beyond: understanding the patterns and probabilities of selection footprints under rapid adaptation. Methods Ecol. Evol. 8, 700–716 (2017).

    Google Scholar 

  • 41.

    Jensen, J. D. On the unfounded enthusiasm for soft selective sweeps. Nat. Commun. 5, 6281 (2014).

    Google Scholar 

  • 42.

    Ralph, P. L. & Coop, G. The role of standing variation in geographic convergent adaptation. Am. Nat. 186, S5–S23 (2015).

    PubMed  PubMed Central  Google Scholar 

  • 43.

    Brennan, R. S., Garrett, A. D., Huber, K. E., Hargarten, H. & Pespeni, M. H. Rare genetic variation and balanced polymorphisms are important for survival in global change conditions. Proc. R. Soc. B 286, 20190943 (2019).

    CAS  PubMed  Google Scholar 

  • 44.

    Mallard, F., Nolte, V., Tobler, R., Kapun, M. & Schlotterer, C. A simple genetic basis of adaptation to a novel thermal environment results in complex metabolic rewiring in Drosophila. Genome Biol. 19, 119 (2018).

    PubMed  PubMed Central  Google Scholar 

  • 45.

    Kelly, J. K. & Hughes, K. A. Pervasive linked selection and intermediate-frequency alleles are implicated in an evolve-and-resequencing experiment of Drosophila simulans. Genetics 211, 943–961 (2019).

    CAS  PubMed  Google Scholar 

  • 46.

    Stern, D. L. The genetic causes of convergent evolution. Nat. Rev. Genet. 14, 751–764 (2013).

    CAS  PubMed  Google Scholar 

  • 47.

    Lee, K. M. & Coop, G. Population genomics perspectives on convergent adaptation. Phil. Trans. R. Soc. B 374, 20180236 (2019).

    PubMed  Google Scholar 

  • 48.

    Waldvogel, A. M. et al. Evolutionary genomics can improve prediction of species’ responses to climate change. Evol. Lett. 4, 4–18 (2019).

    Google Scholar 

  • 49.

    Lee, C. E. Rapid and repeated invasions of fresh water by the copepod Eurytemora affinis. Evolution 53, 1423–1434 (1999).

    PubMed  Google Scholar 

  • 50.

    Katajisto, T. Copepod eggs survive a decade in the sediments of the Baltic Sea. Hydrobiologia 320, 153–159 (1996).

    Google Scholar 

  • 51.

    Ban, S. & Minoda, T. Hatching of diapause eggs of Eurytemora affinis (Copepoda: Calanoida) collected from lake-bottom sediments. J. Crustac. Biol. 12, 51–56 (1992).

    Google Scholar 

  • 52.

    Glippa, O., Denis, L., Lesourd, S. & Souissi, S. Seasonal fluctuations of the copepod resting egg bank in the middle Seine estuary, France: impact on the nauplii recruitment. Estuar. Coast. Mar. Sci. 142, 60–67 (2014).

    Google Scholar 

  • 53.

    Posavi, M., Gelembiuk, G. W., Larget, B. & Lee, C. E. Testing for beneficial reversal of dominance during salinity shifts in the invasive copepod Eurytemora affinis, and implications for the maintenance of genetic variation. Evolution 68, 3166–3183 (2014).

    PubMed  Google Scholar 

  • 54.

    Lee, C. E. Global phylogeography of a cryptic copepod species complex and reproductive isolation between genetically proximate “populations”. Evolution 54, 2014–2027 (2000).

    CAS  PubMed  Google Scholar 

  • 55.

    Pickrell, J. K. & Pritchard, J. K. Inference of population splits and mixtures from genome-wide allele frequency data. PLoS Genet. 8, e1002967 (2012).

    CAS  PubMed  PubMed Central  Google Scholar 

  • 56.

    Foll, M., Gaggiotti, O. E., Daub, J. T., Vatsiou, A. & Excoffier, L. Widespread signals of convergent adaptation to high altitude in Asia and America. Am. J. Hum. Genet. 95, 394–407 (2014).

    CAS  PubMed  PubMed Central  Google Scholar 

  • 57.

    Foll, M. & Gaggiotti, O. A genome-scan method to identify selected loci appropriate for both dominant and codominant markers: a Bayesian perspective. Genetics 180, 977–993 (2008).

    PubMed  PubMed Central  Google Scholar 

  • 58.

    Gautier, M. Genome-wide scan for adaptive divergence and association with population-specific covariates. Genetics 201, 1555–1579 (2015).

    CAS  PubMed  PubMed Central  Google Scholar 

  • 59.

    Jones, F. C. et al. The genomic basis of adaptive evolution in threespine sticklebacks. Nature 484, 55–61 (2012).

    CAS  PubMed  PubMed Central  Google Scholar 

  • 60.

    Alberto, F. J. et al. Convergent genomic signatures of domestication in sheep and goats. Nat. Commun. 9, 813 (2018).

    PubMed  PubMed Central  Google Scholar 

  • 61.

    Gerber, L. et al. The legs have it: in situ expression of ion transporters V-Type H+ ATPase and Na+/K+-ATPase in osmoregulatory leg organs of the invading copepod Eurytemora affinis. Physiol. Biochem. Zool. 89, 233–250 (2016).

    PubMed  Google Scholar 

  • 62.

    Johnson, K. E., Perreau, L., Charmantier, G., Charmantier-Daures, M. & Lee, C. E. Without gills: localization of osmoregulatory function in the copepod Eurytemora affinis. Physiol. Biochem. Zool. 87, 310–324 (2014).

    CAS  PubMed  Google Scholar 

  • 63.

    Lee, C. E., Kiergaard, M., Gelembiuk, G. W., Eads, B. D. & Posavi, M. Pumping ions: rapid parallel evolution of ionic regulation following habitat invasions. Evolution 65, 2229–2244 (2011).

    CAS  PubMed  Google Scholar 

  • 64.

    Siewert, K. M. & Voight, B. F. Detecting long-term balancing selection using allele frequency correlation. Mol. Biol. Evol. 34, 2996–3005 (2017).

    CAS  PubMed  PubMed Central  Google Scholar 

  • 65.

    Bitarello, B. D. et al. Signatures of long-term balancing selection in human genomes. Genome Biol. Evol. 10, 939–955 (2018).

    CAS  PubMed  PubMed Central  Google Scholar 

  • 66.

    Siewert, K. M. & Voight, B. F. BetaScan2: standardized statistics to detect balancing selection utilizing substitution data. Genome Biol. Evol. 12, 3873–3877 (2020).

    PubMed  PubMed Central  Google Scholar 

  • 67.

    Tajima, F. Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123, 585–595 (1989).

    CAS  PubMed  PubMed Central  Google Scholar 

  • 68.

    Bolnick, D. I., Barrett, R. D. H., Oke, K. B., Rennison, D. J. & Stuart, Y. E. (Non)parallel evolution. Ann. Rev. Ecol. Evol. Syst. 49, 303–330 (2018).

    Google Scholar 

  • 69.

    Hedrick, P. W., Ginevan, M. E. & Ewing, E. P. Genetic polymorphism in heterogeneous environments. Ann. Rev. Ecol. Syst. 7, 1–32 (1976).

    Google Scholar 

  • 70.

    Wittmann, M. J., Bergland, A. O., Feldman, M. W., Schmidt, P. S. & Petrov, D. A. Seasonally fluctuating selection can maintain polymorphism at many loci via segregation lift. Proc. Natl Acad. Sci. USA 114, E9932–E9941 (2017).

    CAS  PubMed  Google Scholar 

  • 71.

    Bergland, A. O., Behrman, E. L., O’Brien, K. R., Schmidt, P. S. & Petrov, D. A. Genomic evidence of rapid and stable adaptive oscillations over seasonal time scales in Drosophila. PLoS Genet. 10, e1004775 (2014).

    PubMed  PubMed Central  Google Scholar 

  • 72.

    Troth, A., Puzey, J. R., Kim, R. S., Willis, J. H. & Kelly, J. K. Selective trade-offs maintain alleles underpinning complex trait variation in plants. Science 361, 475–478 (2018).

    CAS  PubMed  Google Scholar 

  • 73.

    Siepielski, A. M., DiBattista, J. D. & Carlson, S. M. It’s about time: the temporal dynamics of phenotypic selection in the wild. Ecol. Lett. 12, 1261–1276 (2009).

    PubMed  Google Scholar 

  • 74.

    Thurman, T. J. & Barrett, R. D. H. The genetic consequences of selection in natural populations. Mol. Ecol. 25, 1429–1448 (2016).

    PubMed  Google Scholar 

  • 75.

    Gelembiuk, G. W., May, G. E. & Lee, C. E. Phylogeography and systematics of zebra mussels and related species. Mol. Ecol. 15, 1033–1050 (2006).

    CAS  PubMed  Google Scholar 

  • 76.

    May, G. E., Gelembiuk, G. W., Panov, V. E., Orlova, M. I. & Lee, C. E. Molecular ecology of zebra mussel invasions. Mol. Ecol. 15, 1021–1031 (2006).

    CAS  PubMed  Google Scholar 

  • 77.

    Bertram, J. & Masel, J. Different mechanisms drive the maintenance of polymorphism at loci subject to strong versus weak fluctuating selection. Evolution 73, 883–896 (2019).

    PubMed  Google Scholar 

  • 78.

    Chen, J., Nolte, V. & Schlotterer, C. Temperature stress mediates decanalization and dominance of gene expression in Drosophila melanogaster. PLoS Genet. 11, e1004883 (2015).

    PubMed  PubMed Central  Google Scholar 

  • 79.

    Panov, V. E., Krylov, P. I. & Riccardi, N. Role of diapause in dispersal and invasion success by aquatic invertebrates. J. Limnol. 63, 56–69 (2004).

    Google Scholar 

  • 80.

    Lee, C. E. & Frost, B. W. Morphological stasis in the Eurytemora affinis species complex (Copepoda: Temoridae). Hydrobiologia 480, 111–128 (2002).

    CAS  Google Scholar 

  • 81.

    Alekseev, V. R. & Souissi, A. A new species within the Eurytemora affinis complex (Copepoda: Calanoida) from the Atlantic Coast of USA, with observations on eight morphologically different European populations. Zootaxa 2767, 41–56 (2011).

  • 82.

    Smit, A. F. A., Hubley, R. & Green, P. RepeatMasker Open-4.0 (2013–2015); http://www.repeatmasker.org

  • 83.

    Eyun, S. I. et al. Evolutionary history of chemosensory-related gene families across the Arthropoda. Mol. Biol. Evol. 34, 1838–1862 (2017).

    CAS  PubMed  PubMed Central  Google Scholar 

  • 84.

    Li, H. & Durbin, R. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25, 1754–1760 (2009).

    CAS  PubMed  PubMed Central  Google Scholar 

  • 85.

    Sedlazeck, F. J., Rescheneder, P. & von Haeseler, A. NextGenMap: fast and accurate read mapping in highly polymorphic genomes. Bioinformatics 29, 2790–2791 (2013).

    CAS  PubMed  Google Scholar 

  • 86.

    McKenna, A. et al. The Genome Analysis Toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res. 20, 1297–1303 (2010).

    CAS  PubMed  PubMed Central  Google Scholar 

  • 87.

    Kofler, R., Pandey, R. V. & Schlotterer, C. PoPoolation2: identifying differentiation between populations using sequencing of pooled DNA samples (Pool-Seq). Bioinformatics 27, 3435–3436 (2011).

    CAS  PubMed  PubMed Central  Google Scholar 

  • 88.

    Hivert, V., Leblois, R., Petit, E. J., Gautier, M. & Vitalis, R. Measuring genetic differentiation from Pool-Seq data. Genetics 210, 315–330 (2018).

    CAS  PubMed  PubMed Central  Google Scholar 

  • 89.

    Kofler, R. et al. PoPoolation: a toolbox for population genetic analysis of next generation sequencing data from pooled individuals. PLoS ONE 6, e0015925 (2011).

    Google Scholar 

  • 90.

    Revell, L. J. phytools: an R package for phylogenetic comparative biology (and other things). Methods Ecol. Evol. 3, 217–223 (2012).

    Google Scholar 

  • 91.

    Ives, A. R., Midford, P. E. & Garland, T. Within-species variation and measurement error in phylogenetic comparative methods. Syst. Biol. 56, 252–270 (2007).

    PubMed  Google Scholar 

  • 92.

    Quinlan, A. R. & Hall, I. M. BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics 26, 841–842 (2010).

    CAS  PubMed  PubMed Central  Google Scholar 

  • 93.

    Neph, S. et al. BEDOPS: high-performance genomic feature operations. Bioinformatics 28, 1919–1920 (2012).

    CAS  PubMed  PubMed Central  Google Scholar 

  • 94.

    Lee, E. et al. Web Apollo: a web-based genomic annotation editing platform. Genome Biol. 14, R93 (2013).

  • 95.

    Kofler, R. & Schlotterer, C. Gowinda: unbiased analysis of gene set enrichment for genome-wide association studies. Bioinformatics 28, 2084–2085 (2012).

    CAS  PubMed  PubMed Central  Google Scholar 

  • 96.

    Benjamini, Y. & Hochberg, Y. Controlling the false discovery rate—a practical and powerful approach to multiple testing. J. R. Stat. Soc. B 57, 289–300 (1995).

    Google Scholar 

  • 97.

    Foley, B. R.et al. A gene-based SNP resource and linkage map for the copepod Tigriopus californicus. BMC Genom. 12, 568 (2011).

  • 98.

    Dymowska, A. K., Hwang, P. P. & Goss, G. G. Structure and function of ionocytes in the freshwater fish gill. Respir. Physiol. Neurobiol. 184, 282–292 (2012).

    CAS  PubMed  Google Scholar 

  • 99.

    Lee, C. E. & Petersen, C. H. Effects of developmental acclimation on adult salinity tolerance in the freshwater-invading copepod Eurytemora affinis. Physiol. Biochem. Zool. 76, 296–301 (2003).

    PubMed  Google Scholar 

  • 100.

    Lee, C. E., Remfert, J. L. & Chang, Y. M. Response to selection and evolvability of invasive populations. Genetica 129, 179–192 (2007).

    PubMed  Google Scholar 

  • 101.

    Lee, C. E., Remfert, J. L. & Gelembiuk, G. W. Evolution of physiological tolerance and performance during freshwater invasions. Integr. Comp. Biol. 43, 439–449 (2003).

    PubMed  Google Scholar 

  • 102.

    Ellner, S. & Sasaki, A. Patterns of genetic polymorphism maintained by fluctuating selection with overlapping generations. Theor. Popul. Biol. 50, 31–65 (1996).

    CAS  PubMed  Google Scholar 

  • 103.

    Turelli, M. & Barton, N. H. Polygenic variation maintained by balancing selection: pleiotropy, sex-dependent allelic effects and GxE interactions. Genetics 166, 1053–1079 (2004).

    PubMed  PubMed Central  Google Scholar 

  • 104.

    Turelli, M., Schemske, D. W. & Bierzychudek, P. Stable two-allele polymorphisms maintained by fluctuating fitnesses and seed banks: protecting the blues in Linanthus parryae. Evolution 55, 1283–1298 (2001).

    CAS  PubMed  Google Scholar 

  • 105.

    Ellner, S. & Hairston, N. G. Role of overlapping generations in maintaining genetic variation in a fluctuating environment. Am. Nat. 143, 403–417 (1994).

  • 106.

    Wright, S. Physiological and evolutionary theories of dominance. Am. Nat. 68, 24–53 (1934).

  • 107.

    Curtsinger, J. W., Service, P. M. & Prout, T. Antagonistic pleiotropy, reversal of dominance, and genetic polymorphism. Am. Nat. 144, 210–228 (1994).

  • 108.

    Gulisija, D., Kim, Y. & Plotkin, J. B. Phenotypic plasticity promotes balanced polymorphism in periodic environments by a genomic storage effect. Genetics 202, 1437–1448 (2016).

    CAS  PubMed  PubMed Central  Google Scholar 

  • 109.

    Gulisija, D. & Plotkin, J. B. Phenotypic plasticity promotes recombination and gene clustering in periodic environments. Nat. Commun. 8, 2041 (2017).

    PubMed  PubMed Central  Google Scholar 


  • Source: Ecology - nature.com

    Dimorphic flowers modify the visitation order of pollinators from male to female flowers

    Climate change will affect global water availability through compounding changes in seasonal precipitation and evaporation