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Fresh start after rough rides: understanding patterns of genetic differentiation upon human-mediated translocations

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Abstract

Biological invasions via translocations are a textbook case of globalization’s impact on species distributions. Human-mediated transport helps species to overcome natural spatial boundaries and establish populations, often from a small number of individuals, in ecosystems previously unreachable through natural range expansion. The result is a discontinuous species distribution, with connectivity between the native and non-native range dependent on the recurrence of human-mediated species movement. The genetic diversity of introduced individuals represents a random fraction of the original diversity in the native range, but because connectivity is lost, non-native populations are bound to evolve independently. As a result, translocations can reshuffle genetic diversity in non-native populations, and thus, differentiation patterns arising after introduction may constitute the first step of novel evolutionary trajectories. By performing a meta-analysis on 5516 mitochondrial sequences of 20 different species, we explored whether life- and evolutionary history could explain differentiation among non-native populations of recently translocated organisms. We observed a general pattern consisting of reduced differentiation among non-native populations whose introduction derived from a single and intentional translocation, suggesting that these human actions play a role in reshaping genetic variance in non-native ranges. Additionally, we found geographic distance to be a poor predictor of population differentiation on the non-native range when compared to averaged evolutionary distances—the opposite being true for the native range—reinforcing connectivity break imposed by translocation events. Understanding the factors driving the distribution of genetic diversity upon translocations might not only facilitate the development of plans to mitigate the dispersal of invasive species but also to explore the emergence of novel evolutionary trajectories.

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Data availability

Original data utilized in this study can be consulted in Table S1.

Code availability

R code is available at: https://github.com/M-Heckwolf/gendiff_translocation.

References

  • Akaike H (1976) An information criterion (AIC) Mathematical Sciences 14

  • Allendorf FW, Lundquist LL (2003) Introduction: population biology, evolution, and control of invasive species. Conserv Biol 17:24–30

    Article  Google Scholar 

  • Alpert P (2006) The advantages and disadvantages of being introduced. Biol Invas 8:1523–1534. https://doi.org/10.1007/s10530-005-5844-z

    Article  Google Scholar 

  • Baltazar-Soares M, Blanchet S, Cote J, Tarkan AS, Záhorská E, Gozlan RE, Eizaguirre C (2019) Genomic footprints of a biological invasion: Introduction from Asia and dispersal in Europe of the topmouth gudgeon (Pseudorasbora parva). Mol Ecol. https://doi.org/10.1111/mec.15313

    Article  PubMed  PubMed Central  Google Scholar 

  • Barton NH (2000) Genetic Hitchhiking. Philos Trans R Soc Lond Ser b Biol Sci 355:1553–1562

    Article  CAS  Google Scholar 

  • Bates D, Mächler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48. https://doi.org/10.18637/jss.v067.i01

    Article  Google Scholar 

  • Berthouly-Salazar C, Hui C, Blackburn TM, Gaboriaud C, van Rensburg BJ, van Vuuren BJ, Le Roux JJ (2013) Long-distance dispersal maximizes evolutionary potential during rapid geographic range expansion. Mol Ecol 22:5793–5804. https://doi.org/10.1111/mec.12538

    Article  PubMed  Google Scholar 

  • Bock DG et al (2015) What we still don’t know about invasion genetics. Mol Ecol 24:2277–2297

    Article  PubMed  Google Scholar 

  • Bohonak AJ (1999) Dispersal, gene flow, and population structure. Q Rev Biol 74:21–45

    Article  CAS  PubMed  Google Scholar 

  • Briski E, Chan FT, Darling JA, Lauringson V, MacIsaac HJ, Zhan A, Bailey SA (2018) Beyond propagule pressure: importance of selection during the transport stage of biological invasions. Front Ecol Environ 16:345–353. https://doi.org/10.1002/fee.1820

    Article  PubMed  PubMed Central  Google Scholar 

  • Cain ML, Milligan BG, Strand AE (2000) Long-distance seed dispersal in plant populations. Am J Botany 87:1217–1227

    Article  CAS  Google Scholar 

  • Capinha C, Marcolin F, Reino L (2020) Human-induced globalization of insular herpetofaunas. Glob Ecol Biogeogr. https://doi.org/10.1111/geb.13109

    Article  Google Scholar 

  • Chevan A, Sutherland M (1991) Hierarchical partitioning. Am Statis 45:90–96

    Google Scholar 

  • Clobert J, Le Galliard JF, Cote J, Meylan S, Massot M (2009) Informed dispersal, heterogeneity in animal dispersal syndromes and the dynamics of spatially structured populations. Ecol Lett 12:197–209

    Article  PubMed  Google Scholar 

  • Colautti RI, Grigorovich IA, MacIsaac HJ (2006) Propagule pressure: a null model for biological invasions. Biol Invas 8:1023–1037. https://doi.org/10.1007/s10530-005-3735-y

    Article  Google Scholar 

  • Consuegra S, John E, Verspoor E, de Leaniz CG (2015) Patterns of natural selection acting on the mitochondrial genome of a locally adapted fish species. Genet Sel Evol 47:58

    Article  PubMed  PubMed Central  Google Scholar 

  • Cousens R, Mortimer M (1995) Dynamics of weed populations. Cambridge University Press

    Book  Google Scholar 

  • Crawford K, Whitney K (2010) Population genetic diversity influences colonization success. Mol Ecol 19:1253–1263

    Article  CAS  PubMed  Google Scholar 

  • Crawley MJ et al (1986) The population biology of invaders. Philos Trans R Soc Lond B Biol Sci 314:711–731. https://doi.org/10.1098/rstb.1986.0082

    Article  Google Scholar 

  • Darling JA, Bagley MJ, Roman J, Tepolt CK, Geller JB (2008) Genetic patterns across multiple introductions of the globally invasive crab genus Carcinus. Mol Ecol 17:4992–5007

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Ehrenfeld JG (2010) Ecosystem consequences of biological invasions. Ann Rev Ecol Evolut Syst 41:59–80

    Article  Google Scholar 

  • Excoffier L, Ray N (2008) Surfing during population expansions promotes genetic revolutions and structuration. Trends Ecol Evolut 23:347–351

    Article  Google Scholar 

  • Excoffier L, Foll M, Petit RJ (2009) Genetic consequences of range expansions. Ann Rev Ecol Evolut Syst 40:481–501

    Article  Google Scholar 

  • Excoffier L, Lischer HE (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Resour 10:564–567

    Article  PubMed  Google Scholar 

  • Facon B, Pointier J-P, Jarne P, Sarda V, David P (2008) High genetic variance in life-history strategies within invasive populations by way of multiple introductions. Curr Biol 18:363–367. https://doi.org/10.1016/j.cub.2008.01.063

    Article  CAS  PubMed  Google Scholar 

  • Fitzpatrick BM, Fordyce JA, Niemiller ML, Reynolds RG (2012) What can DNA tell us about biological invasions? Biol Invas 14:245–253

    Article  Google Scholar 

  • Fox J, Weisberg S (2019) An R companion to applied regression, 3rd edn. Sage, Thousand Oaks CA

    Google Scholar 

  • Franks SJ, Munshi-South J (2014) Go forth, evolve and prosper: the genetic basis of adaptive evolution in an invasive species. Mol Ecol 23:2137–2140

    Article  PubMed  Google Scholar 

  • Gozlan RE et al (2010) Pan-continental invasion of Pseudorasbora parva: towards a better understanding of freshwater fish invasions. Fish Fish 11:315–340

    Article  Google Scholar 

  • Grismer JL et al (2016) The Eurasian invasion: phylogenomic data reveal multiple Southeast Asian origins for Indian Dragon Lizards. BMC Evol Biol 16:43

    Article  PubMed  PubMed Central  Google Scholar 

  • Gurnell J, Wauters LA, Lurz PW, Tosi G (2004) Alien species and interspecific competition: effects of introduced eastern grey squirrels on red squirrel population dynamics. J Anim Ecol 73:26–35

    Article  Google Scholar 

  • Hardouin EA et al (2019) Conservation of genetic uniqueness in remaining populations of red squirrels (Sciurus vulgaris L.) in the South of England. Ecol Evol 9:6547–6558

    PubMed  PubMed Central  Google Scholar 

  • He X et al (2020) Disturbance intensity overwhelms propagule pressure and litter resource in controlling the success of Pontoscolex corethrurus invasion in the tropics. Biol Invas. https://doi.org/10.1007/s10530-020-02214-8

    Article  Google Scholar 

  • Hedge LH, Leung B, O’Connor WA, Johnston EL (2014) The interacting effects of diversity and propagule pressure on early colonization and population size. J Anim Ecol 83:168–175. https://doi.org/10.1111/1365-2656.12125

    Article  PubMed  Google Scholar 

  • Hedrick P, Robinson J, Peterson RO, Vucetich JA (2019) Genetics and extinction and the example of Isle Royale wolves. Animal Conserv 22:302–309

    Article  Google Scholar 

  • Hofman CA, Rick TC (2018) Ancient biological invasions and island ecosystems: tracking translocations of wild plants and animals. J Archaeol Res 26:65–115

    Article  Google Scholar 

  • Hostetler JA, Onorato DP, Jansen D, Oli MK (2013) A cat’s tale: the impact of genetic restoration on Florida panther population dynamics and persistence. J Anim Ecol 82:608–620. https://doi.org/10.1111/1365-2656.12033

    Article  PubMed  Google Scholar 

  • Hothorn T, Bretz F, Westfall P (2008) Simultaneous inference in general parametric models. Biom J J Math Methods Biosci 50:346–363

    Google Scholar 

  • Hovick SM, Whitney KD (2019) Propagule pressure and genetic diversity enhance colonization by a ruderal species: a multi-generation field experiment. Ecol Monogr 89:e01368. https://doi.org/10.1002/ecm.1368

    Article  Google Scholar 

  • Hulme PE (2009) Trade, transport and trouble: managing invasive species pathways in an era of globalization. J Appl Ecol 46:10–18

    Article  Google Scholar 

  • Keller S, Taylor D (2010) Genomic admixture increases fitness during a biological invasion. J Evol Biol 23:1720–1731

    Article  CAS  PubMed  Google Scholar 

  • La Haye M, Reiners T, Raedts R, Verbist V, Koelewijn H (2017) Genetic monitoring to evaluate reintroduction attempts of a highly endangered rodent. Conserv Genet 18:877–892

    Article  Google Scholar 

  • Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452. https://doi.org/10.1093/bioinformatics/btp187

    Article  CAS  PubMed  Google Scholar 

  • Lockwood JL, Cassey P, Blackburn T (2005) The role of propagule pressure in explaining species invasions. Trends Ecol Evolut 20:223–228

    Article  Google Scholar 

  • Lockwood JL, Cassey P, Blackburn TM (2009) The more you introduce the more you get: the role of colonization pressure and propagule pressure in invasion ecology. Divers Distribut 15:904–910

    Article  Google Scholar 

  • Mueller SA, Reiners TE, Middelhoff TL, Anders O, Kasperkiewicz A, Nowak C (2020) The rise of a large carnivore population in Central Europe: genetic evaluation of lynx reintroduction in the Harz Mountains. Conserv Genet 21:577–587

    Article  Google Scholar 

  • Paulose J, Hallatschek O (2020) The impact of long-range dispersal on gene surfing. Proc Natl Acad Sci 117:7584–7593

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Paz-Vinas I et al (2021) Macrogenetic studies must not ignore limitations of genetic markers and scale. Ecol Lett 24:1282–1284. https://doi.org/10.1111/ele.13732

    Article  PubMed  Google Scholar 

  • Pearson DE, Ortega YK, Eren Ö, Hierro JL (2018) Community assembly theory as a framework for biological invasions. Trends Ecol Evol 33:313–325. https://doi.org/10.1016/j.tree.2018.03.002

    Article  PubMed  Google Scholar 

  • Peischl S, Gilbert KJ (2020) Evolution of dispersal can rescue populations from expansion load. Am Nat 195:349–360

    Article  PubMed  Google Scholar 

  • R Core Team (2020) R: a language and environment for statistical comput-ing Vienna, Austria: R Foundation for Statistical Computing

  • Ribeiro FS, Nichols E, Morato RG, Metzger JP, Pardini R (2019) Disturbance or propagule pressure? Unravelling the drivers and mapping the intensity of invasion of free-ranging dogs across the atlantic forest hotspot. Divers Distrib 25:191–204

    Article  Google Scholar 

  • Rollins LA, Richardson MF, Shine R (2015) A genetic perspective on rapid evolution in cane toads (Rhinella marina). Mol Ecol 24:2264–2276

    Article  PubMed  Google Scholar 

  • Roman J, Darling JA (2007) Paradox lost: genetic diversity and the success of aquatic invasions. Trends Ecol Evolut 22:454–464

    Article  Google Scholar 

  • Ruthrof KX, Loneragan WA, Yates CJ (2003) Comparative population dynamics of Eucalyptus cladocalyx in its native habitat and as an invasive species in an urban bushland in south-western Australia. Divers Distrib 9:469–483

    Article  Google Scholar 

  • Schmidt C, Garroway CJ (2021) The conservation utility of mitochondrial genetic diversity in macrogenetic research. Conserv Genet 22:323–327. https://doi.org/10.1007/s10592-021-01333-6

    Article  Google Scholar 

  • Seebens H (2019) Invasion ecology: expanding trade and the dispersal of alien species. Curr Biol 29:R120–R122. https://doi.org/10.1016/j.cub.2018.12.047

    Article  CAS  PubMed  Google Scholar 

  • Simberloff D (2009) The role of propagule pressure in biological invasions annual review of ecology. Evolut Syst 40:81–102

    Article  Google Scholar 

  • Stuart KC, Cardilini AP, Cassey P, Richardson MF, Sherwin WB, Rollins LA, Sherman CD (2020) Signatures of selection in a recent invasion reveal adaptive divergence in a highly vagile invasive species. Mol Ecol 101:451

    Google Scholar 

  • Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol. https://doi.org/10.1093/molbev/mst197

    Article  PubMed  PubMed Central  Google Scholar 

  • Tamura K, Kumar S (2002) Evolutionary distance estimation under heterogeneous substitution pattern among lineages. Mol Biol Evol 19:1727–1736

    Article  CAS  PubMed  Google Scholar 

  • Teske PR et al (2018) Mitochondrial DNA is unsuitable to test for isolation by distance. Sci Rep 8:8448. https://doi.org/10.1038/s41598-018-25138-9

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Toews DP, Brelsford A (2012) The biogeography of mitochondrial and nuclear discordance in animals. Mol Ecol 21:3907–3930

    Article  CAS  PubMed  Google Scholar 

  • Uller T, Leimu R (2011) Founder events predict changes in genetic diversity during human-mediated range expansions. Glob Change Biol 17:3478–3485

    Article  Google Scholar 

  • Venesky MD, Mendelson JR III, Sears BF, Stiling P, Rohr JR (2012) Selecting for tolerance against pathogens and herbivores to enhance success of reintroduction and translocation. Conserv Biol 26:586–592

    Article  PubMed  Google Scholar 

  • Veness C (2018) Latitude/longitude spherical geodesy tools

  • Walsh C, Mac Nally R (2013) Package hier: part—hierarchical partitioning, version 1.0–4 R foundation for statistical computing, Vienna, Austria

  • Weersing K, Toonen RJ (2009) Population genetics, larval dispersal, and connectivity in marine systems. Mar Ecol Prog Ser 393:1–12

    Article  Google Scholar 

  • Wright S (1943) Isolation by distance. Genetics 28:114

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zug GR, Zug PB (1979) The marine toad, Bufo marinus: a natural history resume of native populations. Smithson Contrib Zool. https://doi.org/10.5479/si.00810282.284

    Article  Google Scholar 

Download references

Acknowledgements

We would like to thank two anonymous reviewers and the editor for comments and suggestions that undoubtfully improved the quality of our manuscript.

Funding

The work was supported by a MSCA-IF (ADAPTATION) attributed to MBS.

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MBS and MJH designed the experiment. FR and TM collected and curated the data. All authors contributed to the analysis. MBS led the writing of the manuscript. All authors contributed to revising the manuscript and all authors approved its submission.

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Correspondence to Miguel Baltazar-Soares.

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Heckwolf, M.J., Morim, T., Riccioli, F. et al. Fresh start after rough rides: understanding patterns of genetic differentiation upon human-mediated translocations. Biol Invasions 23, 3625–3639 (2021). https://doi.org/10.1007/s10530-021-02605-5

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