Skip to main content
Log in

Priority effects can lead to underestimation of dispersal and invasion potential

  • Perpectives and paradigms
  • Published:
Biological Invasions Aims and scope Submit manuscript

Abstract

Molecular analyses are frequently used to assess biological gene flow and dispersal, yet recent data suggest that the operation of density-dependent priority effects often leads to underestimation of species movement patterns and associated invasive potential. Although individual movement is broadly considered to promote connectivity among populations, emerging genetic evidence on a range of scales indicates that it often fails to do so; instead, it can be a strategy that allows first colonizers to wedge a ‘foot in the door’ when new space becomes available. Founding lineages can then rapidly dominate, blocking colonization by later arrivals; subsequent invasion opportunities may be contingent on the extirpation of locals. Many contemporary studies, however, ignore the role of such density-dependent priority effects, and thus fail to assess major differences between movement and establishment. Understanding the role of these processes in the successful establishment of dispersing organisms is critical if we are to predict distributional range shifts and deal with invasive pest species.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Abdelkrim J, Pascal M, Samadi S (2007) Establishing causes of eradication failure based on genetics: case study of ship rat eradication in Ste. Anne Archipelago. Conserv Biol 21:719–730

    Article  PubMed  Google Scholar 

  • Almany GR (2003) Priority effects in coral reef fish communities. Ecology 84:1920–1935

    Article  Google Scholar 

  • Almany GR, Berumen ML, Thorrold SR et al (2007) Local replenishment of coral reef fish populations in a marine reserve. Science 316:742–744

    Article  CAS  PubMed  Google Scholar 

  • Amstrup S, MacDonald L, Manly B (2005) Handbook of Capture-Recapture Analysis. Princeton University Press, New Jersey

    Google Scholar 

  • Banks SC, Lindenmayer DB (2013) Inbreeding avoidance, patch isolation and matrix permeability influence dispersal and settlement choices by male agile antechinus in a fragmented landscape. J Anim Ecol 83:515–524

    Article  Google Scholar 

  • Barber PH, Palumbi SR, Erdmann MV et al (2002) Sharp genetic breaks among populations of Haptosquilla pulchella (Stomatopoda) indicate limits to larval transport: patterns, causes, and consequences. Mol Ecol 11:659–674

    Article  CAS  PubMed  Google Scholar 

  • Berry O, Tocher MD, Sarre SD (2004) Can assignment tests measure dispersal? Mol Ecol 13:551–561

    Article  PubMed  Google Scholar 

  • Boessenkool S, Austin JJ, Worthy TH et al (2009a) Relict or colonizer? Extinction and range expansion of penguins in southern New Zealand. Proc R Soc Biol Sci Ser B 276:815–821

    Article  CAS  Google Scholar 

  • Boessenkool S, Star B, Waters JM et al (2009b) Multilocus assignment analyses reveal multiple units and rare migration events in the recently expanded yellow-eyed penguin (Megadyptes antipodes). Mol Ecol 18:2390–2400

    Article  PubMed  Google Scholar 

  • Booth JD, Ovenden JR (2000) Distribution of Jasus spp. (Decapoda : Palinuridae) phyllosomas in southern waters: implications for larval recruitment. Mar Ecol Prog Ser 200:241–255

    Article  Google Scholar 

  • Bowler DE, Benton TG (2005) Causes and consequences of animal dispersal strategies: relating individual behaviour to spatial dynamics. Biol Rev 80:205–225

    Article  PubMed  Google Scholar 

  • Buckley HL, Paterson AM, Cruickshank RH et al (2013) The founder space race: a response to Waters et al. Trends Ecol Evol 28:189–190

    Article  PubMed  Google Scholar 

  • Buonaccorsi VP, Kimbrell CA, Lynn EA et al (2005) Limited realized dispersal and introgressive hybridization influence genetic structure and conservation strategies for brown rockfish, Sebastes auriculatus. Conserv Genet 6:697–713

    Article  Google Scholar 

  • Burgman MA, McCarthy MA, Robinson A et al (2013) Improving decisions for invasive species management: reformulation and extensions of the Panetta-Lawes eradication graph. Divers Distrib 19:603–607

    Article  Google Scholar 

  • Calmet C, Pascal M, Samadi S (2001) Is it worth eradicating the invasive pest Rattus norvegicus from Molène archipelago? Genetic structure as a decision-making tool. Biodivers Conserv 10:911–928

    Article  Google Scholar 

  • Chase JM (2003) Community assembly: when should history matter? Oecologia 136:489–498

    Article  PubMed  Google Scholar 

  • Clobert J, Le Galliard J-F, Cote J et al (2009) Informed dispersal, heterogeneity in animal dispersal syndromes and the dynamics of spatially structured populations. Ecol Lett 12:197–209

    Article  PubMed  Google Scholar 

  • De Meester L, Gomez A, Okamura B et al (2002) The monopolization hypothesis and the dispersal-gene flow paradox in aquatic organisms. Acta Oecol Int J Ecol 23:121–135

    Article  Google Scholar 

  • Donlan CJ, Tershy BR, Campbell K et al (2003) Research for requiems: the need for more collaborative action in eradication of invasive species. Conserv Biol 17:1850–1851

    Article  Google Scholar 

  • Eitam A, Blaustein L, Mangel M (2005) Density and intercohort priority effects on larval Salamandra salamandra in temporary pools. Oecologia 146:36–42

    Article  PubMed  Google Scholar 

  • Emerson BC, Gillespie RG (2008) Phylogenetic analysis of community assembly and structure over space and time. Trends Ecol Evol 23:619–630

    Article  PubMed  Google Scholar 

  • Esher RJ, Wolfe JL, Layne JN (1978) Swimming behavior of rice rats (Oryzomys palustris) and cotton rats (Sigmodon hispidus). J Mammal 59:551–558

    Article  Google Scholar 

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

    Article  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Fraser CI, Nikula R, Spencer HG et al (2009) Kelp genes reveal effects of subantarctic sea ice during the Last Glacial Maximum. Proc Natl Acad Sci USA 106:3249–3253

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Fraser CI, Nikula R, Waters JM (2011) Oceanic rafting by a coastal community. Proc R Soc Biol Sci Ser B 278:649–655

    Article  Google Scholar 

  • Fretwell SD, Calver JS (1969) On territorial behavior and other factors influencing habitat distribution in birds. Acta Biotheor 19:37–44

    Article  Google Scholar 

  • Gauffre B, Petit E, Brodier S et al (2009) Sex-biased dispersal patterns depend on the spatial scale in a social rodent. Proc R Soc B-Biol Sci 276:3487–3494

    Article  CAS  Google Scholar 

  • Geange SW, Stier AC (2009) Order of arrival affects competition in two reef fishes. Ecology 90:2868–2878

    Article  PubMed  Google Scholar 

  • Glen AS, Atkinson R, Campbell KJ et al (2013) Eradicating multiple invasive species on inhabited islands: the next big step in island restoration? Biol Invasions 15:2589–2603

  • Hallatschek O, Hersen P, Ramanathan S et al (2007) Genetic drift at expanding frontiers promotes gene segregation. Proc Natl Acad Sci USA 104:19926–19930

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Hardouin EA, Chapuis JL, Stevens MI et al (2010) House mouse colonization patterns on the sub-Antarctic Kerguelen Archipelago suggest singular primary invasions and resilience against re-invasion. BMC Evol Biol 10:325

    Article  PubMed Central  PubMed  Google Scholar 

  • Harris DB, Gregory SD, Bull LS et al (2012) Island prioritization for invasive rodent eradications with an emphasis on reinvasion risk. Biol Invasions 14:1251–1263

    Article  Google Scholar 

  • Hewitt GM (1993) Postglacial distribution and species substructure: lessons from pollen, insects and hybrid zones. In: Lees DR, Edwards D (eds) Evolutionary Patterns and Processes. Academic Press, London, pp 97–103

    Google Scholar 

  • Hewitt GM (1996) Some genetic consequences of ice ages, and their role in divergence and speciation. Biol J Linn Soc 58:247–276

    Article  Google Scholar 

  • Hewitt G (2000) The genetic legacy of the quaternary ice ages. Nature 405:907–913

    Article  CAS  PubMed  Google Scholar 

  • Howald G, Donlan CJ, Galvan JP et al (2007) Invasive rodent eradication on islands. Conserv Biol 21:1258–1268

    Article  PubMed  Google Scholar 

  • Hubbell SP (2001) The unified neutral theory of biodiversity and biogeography. Princeton University Press, Princeton

    Google Scholar 

  • Keitt B, Campbell K, Saunders A et al (2011) The Global Islands Invasive Vertebrate Eradication Database: a tool to improve and facilitate restoration of island ecosystems. In: Veitch CR, Clout MN, Towns DR (eds) Island invasives: eradication and management. IUCN, Gland, pp 74–77

    Google Scholar 

  • Kerth G, Petit E (2005) Colonization and dispersal in a social species, the Bechstein’s bat (Myotis bechsteinii). Mol Ecol 14:3943–3950

    Article  PubMed  Google Scholar 

  • Kueffer C (2013) Integrating natural and social sciences for understanding and managing plant invasions. In: Larrue S (ed) Biodiversity and Society in the Pacific Islands. ANU ePress, Canberra, pp 71–95

    Google Scholar 

  • Kuussaari M, Nieminen M, Hanski I (1996) An experimental study of migration in the Glanville fritillary butterfly Melitaea cinxia. J Anim Ecol 65:791–801

    Article  Google Scholar 

  • Lee WG, Tanentzap AJ, Heenan PB (2012) Plant radiation history affects community assembly: evidence from the New Zealand alpine. Biol Lett 8:558–561

    Article  PubMed Central  PubMed  Google Scholar 

  • Lowe WH, Allendorf FW (2010) What can genetics tell us about population connectivity? Mol Ecol 19:3038–3051

    Article  PubMed  Google Scholar 

  • Miller MP, Haig SM, Ledig DB et al (2011) Will an “island” population of voles be recolonized if eradicated? insights from molecular genetic analyses. J Wildl Manag 75:1812–1818

    Article  Google Scholar 

  • Münkemüller T, Travis JMJ, Burton OJ et al (2011) Density-regulated population dynamics and conditional dispersal alter the fate of mutations occurring at the front of an expanding population. Heredity 106:678–689

    Article  PubMed Central  PubMed  Google Scholar 

  • Parker JD, Hay ME (2005) Biotic resistance to plant invasions? Native herbivores prefer non-native plants. Ecol Lett 8:959–967

    Article  Google Scholar 

  • Peay KG, Belisle M, Fukami T (2012) Phylogenetic relatedness predicts priority effects in nectar yeast communities. Proc R Soc Biol Sci Ser B 279:749–758

    Article  Google Scholar 

  • Planes S, Jones GP, Thorrold SR (2009) Larval dispersal connects fish populations in a network of marine protected areas. Proc Natl Acad Sci USA 106:5693–5697

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Pulliam HR, Danielson BJ (1991) Sources, sinks, and habitat selection - a landscape perspective on population dynamics. Am Nat 137:S50–S66

    Article  Google Scholar 

  • Ricklefs RE (2010) Dynamics of colonization and extinction on islands: insights from Lesser Antillean birds. In: Losos JB, Ricklefs RE (eds) The Theory of Island Biogeography Revisited. Princeton University Press, Princeton, pp 388–414

    Google Scholar 

  • Rius M, Darling JA (2014) How important is intraspecific genetic admixture to the success of colonising populations? Trends Ecol Evol 29:233–242

    Article  PubMed  Google Scholar 

  • Roques L, Garnier J, Hamel F et al (2012) Allee effect promotes diversity in traveling waves of colonization. Proc Natl Acad Sci USA 109:8828–8833

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Russell JC, Towns DR, Clout MN (2008) Review of rat invasion biology: implications for island biosecurity. Science for Conservation, 286. Department of Conservation, Wellington

  • Russell JC, Miller SD, Harper GA et al (2010) Survivors or reinvaders? Using genetic assignment to identify invasive pests following eradication. Biol Invasions 12:1747–1757

    Article  Google Scholar 

  • Shulman MJ, Ogden JC, Ebersole JP et al (1983) Priority effects in the recruitment of juvenile coral-reef fishes. Ecology 64:1508–1513

    Article  Google Scholar 

  • Tan JQ, Pu ZC, Ryberg WA et al (2012) Species phylogenetic relatedness, priority effects, and ecosystem functioning. Ecology 93:1164–1172

    Article  PubMed  Google Scholar 

  • Towns DR (2011) Eradications of vertebrate pests from islands around New Zealand: what have we delivered and what have we learned? In: Veitch CR, Clout MN, Towns DR (eds) Island invasives: eradication and management. IUCN, Gland, pp 364–371

    Google Scholar 

  • Travis JMJ, Munkemuller T, Burton OJ (2010) Mutation surfing and the evolution of dispersal during range expansions. J Evol Biol 23:2656–2667

    Article  CAS  PubMed  Google Scholar 

  • Veale AJ, Clout MN, Gleeson DM (2012) Genetic population assignment reveals a long-distance incursion to an island by a stoat (Mustela erminea). Biol Invasions 14:735–742

    Article  Google Scholar 

  • Votier SC, Grecian WJ, Patrick S et al (2011) Inter-colony movements, at-sea behaviour and foraging in an immature seabird: results from GPS-PPT tracking, radio-tracking and stable isotope analysis. Mar Biol 158:355–362

    Article  CAS  Google Scholar 

  • Waters JM, Fraser CI, Banks SC et al (2013a) The founder space race: a reply to Buckley et al. Trends Ecol Evol 28:190–191

    Article  PubMed  Google Scholar 

  • Waters JM, Fraser CI, Hewitt GM (2013b) Founder takes all: density-dependent processes structure biodiversity. Trends Ecol Evol 28:78–85

    Article  PubMed  Google Scholar 

  • White TA, Perkins SE, Heckel G et al (2013) Adaptive evolution during an ongoing range expansion: the invasive bank vole (Myodes glareolus) in Ireland. Mol Ecol 22:2971–2985

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We thank J. Russell and A. Veale for information on rodent and stoat invasions; G. Hewitt for crucial insights into density blocking processes; K. Ikin and A. Veale for comments on early drafts; and H. Buckley and an anonymous reviewer for comments that improved the manuscript. Images used in figures were free-use and/or used with permission: S. Boessenkool (Megadyptes antipodes); R. McKenna (Rattus norvegicus); P. Garvey (Mustela erminea).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Ceridwen I. Fraser.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Fraser, C.I., Banks, S.C. & Waters, J.M. Priority effects can lead to underestimation of dispersal and invasion potential. Biol Invasions 17, 1–8 (2015). https://doi.org/10.1007/s10530-014-0714-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10530-014-0714-1

Keywords

Navigation