Skip to main content

Advertisement

SpringerLink
Log in

The effect of mating system on invasiveness: some genetic load may be advantageous when invading new environments

  • Original Paper
  • Published:
Biological Invasions Aims and scope Submit manuscript

Abstract

The role of adaptation in determining invasion success has been acknowledged recently, notably through the accumulation of case studies of rapid evolution during bioinvasions. Despite this growing body of empirical evidence, there is still a need to develop the theoretical background of invasions with adaptation. Specifically, the impact of mating system on the dynamics of adaptation during invasion of a new environment remains only partially understood. Here, we analyze a simulation demo-genetic model of bioinvasion accounting for partial asexuality rates. We simulate two levels of recurrent immigration from a source population at mutation–drift–selection equilibrium to a new empty environment with a different adaptive landscape (black-hole sink). Adaptation relies on a quantitative trait coded explicitly by 10 loci under mutation, selection and genetic drift. Using this model, we confirm previous results on the positive effects on invasiveness of migration, mutation and similarity of local phenotypic optima. We further show how the invasion dynamics of the introduced population is affected by the rate of asexuality. Purely asexual species have lower invasion success in terms of probability and time to invasion than species with other mating systems. Among species with mixed mating systems, the greatest invasiveness is observed for species with high asexual rates. We suggest that this pattern is due to inflated genetic variance in the source population through the Hill-Robertson effect (i.e., clonal interference). An interesting consequence is that species with the highest genetic load in their source environment have greatest invasiveness in the new environment.

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

Access this article

Log in via an institution

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
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Amsellem L, Noyer J-L, Hossaert-McKey M (2001) Evidence for a switch in the reproductive biology of Rubus alceifolius (Rosaceae) towards apomixis, between its native range and its area of introduction. Am J Bot 88:2243–2251

    Article  CAS  PubMed  Google Scholar 

  • Baker HG (1955) Self-compatibility and establishment after ‘long-distance’ dispersal. Evolution 9:347–349

    Article  Google Scholar 

  • Barrett SCH (2011) Why reproductive systems matter for the invasion biology of plants. In: Richardson DM (ed) Fifty years of invasion ecology: the legacy of Charles Elton, 1st edn. Blackwell Publishing Ltd, Hoboken, pp 195–210

    Google Scholar 

  • Barrett RDH, Schluter D (2008) Adaptation from standing genetic variation. Trends Ecol Evol 23:38–44

    Article  PubMed  Google Scholar 

  • Barrett SCH, Colautti RI, Eckert CG (2008) Plant reproductive systems and evolution during biological invasion. Mol Ecol 17:373–383

    Article  PubMed  Google Scholar 

  • Behrman KD, Kirkpatrick M (2011) Species range expansion by beneficial mutations. J Evol Biol 24:665–675

    Article  CAS  PubMed  Google Scholar 

  • Bridle JR, Polechová J, Kawata M, Butlin RK (2010) Why is adaptation prevented at ecological margins? New insights from individual-based simulations. Ecol Lett 13:485–494

    Article  PubMed  Google Scholar 

  • Brown AHD, Burdon JJ (1987) Mating systems and colonizing success in plants. In: Cary AJ, Crawley MJ, Edwards PJ (eds) Colonization, succession and stability. Blackwell Scientific Publications, Oxford, pp 115–131

    Google Scholar 

  • Bürger R (1989) Linkage and the maintenance of heritable variation by mutation–selection balance. Genetics 121:175–184

    PubMed Central  PubMed  Google Scholar 

  • Bürger R, Lynch M (1995) Evolution and extinction in a changing environment: a quantitative-genetic analysis. Evolution 49:151–163

    Article  Google Scholar 

  • Bürger R, Lynch M (1997) Adaptation and extinction in changing environments. Genetics 83:209–239

    Google Scholar 

  • Burns JH, Ashman TL, Steets JA et al (2011) A phylogenetically controlled analysis of the roles of reproductive traits in plant invasions. Oecologia 166:1009–1017

    Article  PubMed  Google Scholar 

  • Burt A (2000) Perspective: sex, recombination, and the efficacy of selection—was Weismann right? Evolution 54:337–351

    CAS  PubMed  Google Scholar 

  • Charlesworth D, Morgan MT, Charlesworth B (1993) Mutation accumulation in finite outbreeding and inbreeding populations. Genet Res 61:39–56

    Article  Google Scholar 

  • Cox GW (2004) Alien species and evolution. Island Press, Washington, D C

    Google Scholar 

  • D’Souza TG, Michiels NK (2010) The costs and benefits of occasional sex: theoretical predictions and a case study. J Hered 101(Suppl):S34–S41

    Article  PubMed  Google Scholar 

  • Desprez-Loustau M-L, Robin C, Buée M et al (2007) The fungal dimension of biological invasions. Trends Ecol Evol 22:472–480

    Article  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

    Article  CAS  PubMed  Google Scholar 

  • Ellstrand NC, Schierenbeck KA (2000) Hybridization as a stimulus for the evolution of invasiveness in plants? Proc Natl Acad Sci USA 97:7043–7050

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Facon B, Pointier J-P, Jarne P et al (2008) High genetic variance in life-history strategies within invasive populations by way of multiple introductions. Curr Biol 18:363–367

    Article  CAS  PubMed  Google Scholar 

  • Felsenstein J (1974) The evolutionary advantage of recombination. Genetics 78:737–756

    CAS  PubMed Central  PubMed  Google Scholar 

  • Gomulkiewicz R, Holt RD, Barfield M (1999) The effects of density dependence and immigration on local adaptation and niche evolution in a black-hole sink environment. Theor Popul Biol 55:283–296

    Article  CAS  PubMed  Google Scholar 

  • Green RF, Noakes DLG (1995) Is a little bit of sex as good as a lot? J Theor Biol 174:87–96

    Article  Google Scholar 

  • Grether G (2005) Environmental change, phenotypic plasticity, and genetic compensation. Am Nat 166:E115–E123

    Article  PubMed  Google Scholar 

  • Hayes K, Barry S (2008) Are there any consistent predictors of invasion success? Biol Invasions 10:483–506

    Article  Google Scholar 

  • Hedrick PW, Whittam TS (1989) Sex in diploids. Nature 342:231

    Article  Google Scholar 

  • Hill WG, Robertson A (1966) Linkage disequilibrium in finite populations. Theor Appl Genet 38:226–231

    Article  Google Scholar 

  • Holt RD (1983) Models for peripheral populations: the role of immigration. In: Freedman HI, Strobeck C (eds) Lecture notes in biomathematics. Springer, Berlin, pp 25–32

    Google Scholar 

  • Holt RD (1996) Demographic constraints in evolution: towards unifying the evolutionary theories of senescence and niche conservatism. Evol Ecol 10:1–11

    Article  Google Scholar 

  • Holt RD, Gaines M (1992) The analysis of adaptation in heterogeneous landscapes: implications for the evolution of fundamental niches. Evol Ecol 6:433–447

    Article  Google Scholar 

  • Holt RD, Gomulkiewicz R (1997a) How does immigration influence local adaptation? A reexamination of a familiar paradigm. Am Nat 149:563–572

    Article  Google Scholar 

  • Holt RD, Gomulkiewicz R (1997b) The evolution of species’ niches: a population dynamic perspective. In: Othmer H, Adler F, Lewis M, Dallon J (eds) Case studies in mathematical modeling: ecology, physiology, and cell biology. Prentice-Hall, New Jersey, pp 25–50

    Google Scholar 

  • Holt RD, Gomulkiewicz R, Barfield M (2003) The phenomenology of niche evolution via quantitative traits in a “black-hole” sink. Proc R Soc Lond B Biol Sci 270:215–224

    Article  CAS  Google Scholar 

  • Holt RD, Knight TM, Barfield M (2004) Allee effects, immigration, and the evolution of species’ niches. Am Nat 163:253–262

    Article  PubMed  Google Scholar 

  • Holt RD, Barfield M, Gomulkiewicz R (2005) Theories of Niche conservatism and evolution. Could exotic species be potential tests? In: Sax DF, Stachowicz JJ, Gaines SD (eds) Species invasions. Insights into ecology, evolution, and biogeography. Sinauer, Sunderland, pp 269–279

    Google Scholar 

  • Hufbauer RA, Facon B, Ravigné V et al (2012) Anthropogenically induced adaptation to invade (AIAI): contemporary adaptation to human-altered habitats within the native range can promote invasions. Evol Appl 5:89–101

    Article  PubMed Central  Google Scholar 

  • Kanarek AR, Webb CT (2010) Allee effects, adaptive evolution, and invasion success. Evol Appl 3:122–135

    Article  PubMed Central  Google Scholar 

  • Kawecki TJ (1995) Demography of source-sink populations and the evolution of ecological niches. Evol Ecol 9:38–44

    Article  Google Scholar 

  • Kawecki TJ (2000) Adaptation to marginal habitats: contrasting influence of the dispersal rate on the fate of alleles with small and large effects. Proc R Soc Lond B Biol Sci 267:1315–1320

    Article  CAS  Google Scholar 

  • Kawecki TJ (2008) Adaptation to marginal habitats. Annu Rev Ecol Evol Syst 39:321–342

    Article  Google Scholar 

  • Keane RM, Crawley MJ (2002) Exotic plant invasions and the enemy release hypothesis. Trends Ecol Evol 17:164–170

    Article  Google Scholar 

  • Kimbrell T, Holt RD (2007) Canalization breakdown and evolution in a source-sink system. Am Nat 169:370–382

    Article  PubMed  Google Scholar 

  • Kirkpatrick M, Barton NH (1997) Evolution of a species’ range. Am Nat 150:1–23

    Article  CAS  PubMed  Google Scholar 

  • Kolar CS, Lodge DM (2001) Progress in invasion biology: predicting invaders. Trends Ecol Evol 16:199–204

    Article  PubMed  Google Scholar 

  • Lambrinos JG (2004) How interactions between ecology and evolution influence contemporary invasion dynamics. Ecology 85:2061–2070

    Article  Google Scholar 

  • Larkin DJ (2012) Lengths and correlates of lag phases in upper-Midwest plant invasions. Biol Invasions 14:827–838

    Article  Google Scholar 

  • Lee CE (2002) Evolutionary genetics of invasive species. Trends Ecol Evol 17:386–391

    Article  Google Scholar 

  • Liu H, Stiling P (2006) Testing the enemy release hypothesis: a review and meta-analysis. Biol Invasions 8:1535–1545

    Article  Google Scholar 

  • Lloret F, Medail F, Brundu G et al (2005) Species attributes and invasion success by alien plants on Mediterranean islands. J Ecol 93:512–520

    Article  Google Scholar 

  • Lynch M, Gabriel W (1983) Phenotypic evolution and parthenogenesis. Am Nat 122:745–764

    Article  Google Scholar 

  • Martin G, Otto SP, Lenormand T (2006) Selection for recombination in structured populations. Genetics 172:593–609

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • McDonald BA, Linde CC (2002) Pathogen population genetics, evolutionary potential, and durable resistance. Annu Rev Phytopathol 40:349–379

    Article  CAS  PubMed  Google Scholar 

  • Muller-Scharer H, Schaffner U, Steinger T (2004) Evolution in invasive plants: implications for biological control. Trends Ecol Evol 19:417–422

    Article  PubMed  Google Scholar 

  • Neuenschwander S, Hospital F, Guillaume F, Goudet J (2008) quantiNemo: an individual-based program to simulate quantitative traits with explicit genetic architecture in a dynamic metapopulation. Bioinformatics 24:1552–1553

    Article  CAS  PubMed  Google Scholar 

  • Otto SP, Lenormand T (2002) Resolving the paradox of sex and recombination. Nat Rev Genet 3:252–261

    Article  CAS  PubMed  Google Scholar 

  • Pannell JR, Barrett SCH (1998) Baker’s law revisited: reproductive assurance in a metapopulation. Evolution 52:657–668

    Article  Google Scholar 

  • Pannell JR, Dorken ME (2006) Colonisation as a common denominator in plant metapopulations and range expansions: effects on genetic diversity and sexual systems. Landsc Ecol 21:837–848

    Article  Google Scholar 

  • Parker IM, Gilbert GS (2004) The evolutionary ecology of novel plant–pathogen interactions. Annu Rev Ecol Evol Syst 35:675–700

    Article  Google Scholar 

  • Peck JR, Yearsley JM, Waxman D (1998) Explaining the geographic distributions of sexual and asexual populations. Nature 391:889–892

    Article  CAS  Google Scholar 

  • Philibert A, Desprez-Loustau M-L, Fabre B et al (2011) Predicting invasion success of forest pathogenic fungi from species traits. J Appl Ecol 48:1381–1390

    Article  Google Scholar 

  • Pigliucci M, Murren CJ (2003) Perspective: genetic assimilation and a possible evolutionary paradox: can macroevolution sometimes be so fast as to pass us by? Evolution 57:1455–1464

    PubMed  Google Scholar 

  • Prentis PJ, Wilson JRU, Dormontt EE et al (2008) Adaptive evolution in invasive species. Trends Plant Sci 13:288–294

    Article  CAS  PubMed  Google Scholar 

  • Reichard SH, Hamilton CW (1997) Predicting invasions of woody plants introduced into North America. Conserv Biol 11:193–203

    Article  Google Scholar 

  • Robert S, Ravigné V, Zapater M-F et al (2012) Contrasting introduction patterns among continents in the worldwide invasion of the banana fungal pathogen Mycosphaerella fijiensis. Mol Ecol 21:1098–1114

    Article  CAS  PubMed  Google Scholar 

  • Roels SAB, Kelly JR (2011) Rapid evolution caused by pollinator loss in Mimulus guttatus. Evolution 65:2541–2552

    Article  PubMed  Google Scholar 

  • Sakai AK, Allendorf FW, Holt JS et al (2001) The population biology of invasive species. Annu Rev Ecol Syst 32:305–332

    Article  Google Scholar 

  • Saleh D, Xu P, Shen Y et al (2012) Sex at the origin: an Asian population of the rice blast fungus Magnaporthe oryzae reproduces sexually. Mol Ecol 21:1330–1344

    Article  PubMed  Google Scholar 

  • Sax DF, Stachowicz JJ, Brown JH et al (2007) Ecological and evolutionary insights from species invasions. Trends Ecol Evol 22:465–471

    Article  PubMed  Google Scholar 

  • Singh RP, Hodson DP, Huerta-Espino J et al (2011) The emergence of Ug99 races of the stem rust fungus is a threat to world wheat production. Annu Rev Phytopathol 49:465–481

    Article  CAS  PubMed  Google Scholar 

  • Stukenbrock EH, McDonald BA (2008) The origins of plant pathogens in agro-ecosystems. Annu Rev Phytopathol 46:75–100

    Article  CAS  PubMed  Google Scholar 

  • Sutherland S (2004) What makes a weed a weed: life history traits of native and exotic plants in the USA. Oecologia 141:24–39

    Article  PubMed  Google Scholar 

  • Travis JMJ, Hammershøj M, Stephenson C (2005) Adaptation and propagule pressure determine invasion dynamics: insights from a spatially explicit model for sexually reproducing species. Evol Ecol Res 7:37–51

    Google Scholar 

  • Wiens JJ, Graham CH (2005) Niche conservatism: integrating evolution, ecology, and conservation biology. Annu Rev Ecol Evol Syst 36:519–539

    Article  Google Scholar 

  • Williamson MH, Fitter A (1996) The characters of successful invaders. Biol Conserv 78:163–170

    Article  Google Scholar 

  • Wloch DM, Szafraniec K, Borts RH, Korona R (2001) Direct estimate of the mutation rate and the distribution of fitness effects in the yeast Saccharomyces cerevisiae. Genetics 159:441–452

    CAS  PubMed Central  PubMed  Google Scholar 

  • Zaykin DV, Pudovkin A, Weir BS (2008) Correlation-based inference for linkage disequilibrium with multiple alleles. Genetics 180:533–545

    Article  PubMed Central  PubMed  Google Scholar 

Download references

Acknowledgments

We are grateful to F. Halkett, BECPHY team of UMR BGPI, and people attending the various EMERFUNDIS workshops for helpful discussions. We also wish to thank S. Neuenschwander for providing quantiNEMO code and his help. The manuscript benefitted much from comments by the Editor, two reviewers and Mike Barfield. EB was funded by an ANR post-doctoral fellowship as part of the project EMERFUNDIS (ANR 07-BDIV-003) of the French “Agence Nationale de la Recherche” (ANR). This work was also supported by the French Agropolis Fondation (Labex Agro—Montpellier, BIOFIS Project Number 1001-001).

Author information

Authors and Affiliations

  1. UMR LECA, Université Joseph Fourier, 38041, Grenoble Cedex 9, France

    Éric Bazin

  2. UMR ISA, Université de Nice, 06090, Sophia-Antipolis, France

    Hugo Mathé-Hubert

  3. UMR BGPI, CIRAD, 34398, Montpellier, France

    Éric Bazin, Hugo Mathé-Hubert, Jean Carlier & Virginie Ravigné

  4. UMR CBGP, INRA, 34398, Montpellier, France

    Benoît Facon

Authors
  1. Éric Bazin
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Hugo Mathé-Hubert
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Benoît Facon
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jean Carlier
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Virginie Ravigné
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Virginie Ravigné.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 1193 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Bazin, É., Mathé-Hubert, H., Facon, B. et al. The effect of mating system on invasiveness: some genetic load may be advantageous when invading new environments. Biol Invasions 16, 875–886 (2014). https://doi.org/10.1007/s10530-013-0544-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10530-013-0544-6

Keywords

Search

Navigation