Prior adaptation, diversity, and introduction frequency mediate the positive relationship between propagule pressure and the initial success of founding populations

  • Megan L. Vahsen
  • Katriona Shea
  • Ciara L. Hovis
  • Brittany J. Teller
  • Ruth A. Hufbauer
Original Paper
First Online:
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Accepted:

Abstract

Propagule pressure is often considered the most consistent predictor of the success of founding populations. This relationship could be mediated by the composition of the founding group (e.g. level of prior adaptation to the recipient environment or its diversity) as well as the introduction scenario (i.e. the frequency, size and timing of discrete introduction events). We introduced groups of Tribolium castaneum (red flour beetle) eggs across three levels of propagule pressure (n = 15, 30, 60), of three possible compositions (single, adapted lineage; single, unadapted lineage; mixed lineages) to a novel environment using six unique introduction scenarios, in a fully factorial design to evaluate the importance of composition and introduction scenario in influencing the relationship between propagule pressure and establishment. In our system, prior adaptation to the environment, including having some adapted individuals in mixed groups, rivaled the importance of propagule pressure in determining the establishment success and size of founding populations. More frequent introduction events resulted in fewer individuals that initially survived founding, but introduction scenario did not significantly influence establishment success or population size. This experimental evidence demonstrates the importance of context, both of the founding group and the recipient environment, in understanding how propagule pressure influences the success of founding populations.

Keywords

Propagule pressure Colonization Genetic diversity Invasive species Adaptation 
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Notes

Acknowledgements

We would like to thank graduate students S. Endriss and G. Tuttle and undergraduate lab assistants C. Reyes and M. Morris for their help with lab work. We are also grateful for input from members of the Shea lab at The Pennsylvania State University (especially J. Keller) and from B.A. Melbourne. Funding for this research was provided by the US National Science Foundation (DEB-0815373 and DEB-1556444 to KS and DEB-0949619 to RAH).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

10530_2018_1713_MOESM1_ESM.docx (592 kb)
Supplementary material 1 (DOCX 592 kb)

References

  1. Agashe D, Falk JJ, Bolnick DI (2011) Effects of founding genetic variation on adaptation to a novel resource. Evolution 65:2481–2491CrossRefPubMedGoogle Scholar
  2. Ahlroth P, Alatalo RV, Holopainen A, Kumpulainen T, Suhonen J (2003) Founder population size and number of source populations enhance colonization success in waterstriders. Oecologia 137:617–620CrossRefPubMedGoogle Scholar
  3. Albert A, Anderson JA (1984) On the existence of maximum-likelihood estimates in logistic-regression models. Biometrika 71:1–10CrossRefGoogle Scholar
  4. Birch LC, Park T, Frank MB (1951) The effect of intraspecies and interspecies competition on the fecundity of two species of flour beetles. Evolution 5:116–132CrossRefGoogle Scholar
  5. Blackburn TM, Lockwood JL, Cassey P (2015) The influence of numbers on invasion success. Mol Ecol 24:1942–1953CrossRefPubMedGoogle Scholar
  6. Britton JR, Gozlan RE (2013) How many founders for a biological invasion? Predicting introduction outcomes from propagule pressure. Ecology 94:2558–2566CrossRefPubMedGoogle Scholar
  7. Colautti RI, Grigorovich IA, MacIsaac HJ (2006) Propagule pressure: a null model for biological invasions. Biol Invasions 8:1023–1037CrossRefGoogle Scholar
  8. Crawford KM, Whitney KD (2010) Population genetic diversity influences colonization success. Mol Ecol 19:1253–1263CrossRefPubMedGoogle Scholar
  9. Crawley MJ (1986) The population biology of invaders. Philos Trans R Soc B 314:711–731CrossRefGoogle Scholar
  10. D’Antonio C, Levine J, Thomsen M (2001) Ecosystem resistance to invasion and the role of propagule supply: a California perspective. J Mediterr Ecol 2:233–245Google Scholar
  11. Dlugosch KM, Parker IM (2008) Founding events in species invasions: genetic variation, adaptive evolution, and the role of multiple introductions. Mol Ecol 17:431–449CrossRefPubMedGoogle Scholar
  12. Drake JM, Baggenstos P, Lodge DM (2005) Propagule pressure and persistence in experimental populations. Biol Lett 1:480–483CrossRefPubMedPubMedCentralGoogle Scholar
  13. Drolet D, Locke A (2016) Relative importance of propagule size and propagule number for establishment of non-indigenous species: a stochastic simulation study. Aquat Invasions 11:101–110CrossRefGoogle Scholar
  14. Duncan RP (2016) How propagule size and environmental suitability jointly determine establishment success: a test using dung beetle introductions. Biol Invasions 18:985–996CrossRefGoogle Scholar
  15. Elam DR, Ridley CE, Goodell K, Ellstrand NC (2007) Population size and relatedness affect fitness of a self-incompatible invasive plant. Proc Natl Acad Sci USA 104:549–552CrossRefPubMedGoogle Scholar
  16. Erfmeier A, Hantsch L, Bruelheide H (2013) The role of propagule pressure, genetic diversity and microsite availability for Senecio vernalis invasion. PLoS ONE 8:e57029CrossRefPubMedPubMedCentralGoogle Scholar
  17. Fauvergue X, Vercken E, Malausa T, Hufbauer RA (2012) The biology of small, introduced populations, with special reference to biological control. Evol Appl 5:424–443CrossRefPubMedPubMedCentralGoogle Scholar
  18. Grevstad FS (1999) Factors influencing the chance of population establishment: implications for release strategies in biological control. Ecol Appl 9:1439–1447CrossRefGoogle Scholar
  19. Gurevitch J, Fox GA, Wardle GM, Inderjit, Taub D (2011) Emergent insights from the synthesis of conceptual frameworks for biological invasions. Ecol Lett 14:407–418CrossRefPubMedGoogle Scholar
  20. Halekoh U, Hojsgaard S (2014) A Kenward-Roger approximation and parametric bootstrap methods for tests in linear mixed models—the R package pbkrtest. J Stat Softw 59:1–30CrossRefGoogle Scholar
  21. Halliday WD, Thomas AS, Blouin-Demers G (2015) High temperature intensifies negative density dependence of fitness in red flour beetles. Ecol Evol 5:1061–1067CrossRefPubMedPubMedCentralGoogle Scholar
  22. Hedge LH, O’Connor WA, Johnston EL (2012) Manipulating the intrinsic parameters of propagule pressure: implications for bio-invasion. Ecosphere 3:1–13CrossRefGoogle Scholar
  23. 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 83:168–175CrossRefPubMedGoogle Scholar
  24. Hufbauer RA, Facon B, Ravigné V, Turgeon J, Foucaud J, Lee CE, Rey O, Estoup A (2012) Anthropogenically induced adaptation to invade (AIAI): contemporary adaptation to human-altered habitats within the native range can promote invasions. Evol Appl 5:89–101CrossRefPubMedGoogle Scholar
  25. Hufbauer RA, Rutschmann A, Serrate B, Vermeil de Conchard H, Facon B (2013) Role of propagule pressure in colonization success: disentangling the relative importance of demographic, genetic and habitat effects. J Evol Biol 26:1691–1699CrossRefPubMedGoogle Scholar
  26. Hufbauer RA, Szűcs M, Kasyon E, Youngberg C, Koontz MJ, Richards C, Tuff T, Melbourne BA (2015) Three types of rescue can avert extinction in a changing environment. Proc Natl Acad Sci USA 112:10557–10562CrossRefPubMedPubMedCentralGoogle Scholar
  27. Hughes AR, Inouye BD, Johnson MTJ, Underwood N, Vellend M (2008) Ecological consequences of genetic diversity. Ecol Lett 11:609–623CrossRefPubMedGoogle Scholar
  28. Hui C, Richardson DM (2017) Invasion dynamics. Oxford University Press, New YorkCrossRefGoogle Scholar
  29. Järemo J, Bengtsson G (2011) On the importance of life history and age structure in biological invasions. Ecol Model 222:485–492CrossRefGoogle Scholar
  30. Johnson DW, Freiwald J, Bernardi G (2016) Genetic diversity affects the strength of population regulation in a marine fish. Ecology 97:627–639PubMedGoogle Scholar
  31. Koontz MJ, Oldfather MF, Melbourne BA, Hufbauer RA (2017) Parsing propagule pressure: Number, not size, of introductions drives colonization success in a novel environment. bioRxiv.  https://doi.org/10.1101/108324 Google Scholar
  32. Kowarik I (1995) Time lags in biological invasions with regard to the success and failure of alien species. In: Pyšek P, Prach K, Rejmánek M, Wade M (eds) Plant invasions, general aspects and special problems. SPB Academic Publishers, Amsterdam, pp 15–38Google Scholar
  33. Lande R (1988) Genetics and demography in biological conservation. Science 241:1455–1460CrossRefPubMedGoogle Scholar
  34. Lockwood JL, Cassey P, Blackburn T (2005) The role of propagule pressure in explaining species invasions. Trends Ecol Evol 20:223–228CrossRefPubMedGoogle Scholar
  35. Loreau M, Hector A (2001) Partitioning selection and complementarity in biodiversity experiments. Nature 412:72–76CrossRefPubMedGoogle Scholar
  36. MacArthur RH, Wilson EO (1967) The theory of island biogeography. Princeton University Press, PrincetonGoogle Scholar
  37. Maron JL (2006) The relative importance of latitude matching and propagule pressure in the colonization success of an invasive forb. Ecography 29:819–826CrossRefGoogle Scholar
  38. Mertz DB, Cawthon DA (1973) Sex differences in the cannibalistic roles of adult flour beetles. Ecology 54:1400–1402CrossRefGoogle Scholar
  39. Nuñez MA, Moretti A, Simberloff D (2011) Propagule pressure hypothesis not supported by an 80-year experiment on woody species invasion. Oikos 120:1311–1316CrossRefGoogle Scholar
  40. R Core Team (2017) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/ Google Scholar
  41. Rouget M, Richardson DM (2003) Inferring process from pattern in plant invasions: a semimechanistic model incorporating propagule pressure and environmental factors. Am Nat 162:713–724CrossRefPubMedGoogle Scholar
  42. Shea K, Possingham HP (2000) Optimal release strategies for biological control agents: an application of stochastic dynamic programming to population management. J Appl Ecol 37:77–86CrossRefGoogle Scholar
  43. Simberloff D (2009) The role of propagule pressure in biological invasions. Annu Rev Ecol Evol Syst 40:81–102CrossRefGoogle Scholar
  44. Sinclair JS, Arnott SE (2016) Strength in size not numbers: propagule size more important than number in sexually reproducing populations. Biol Invasions 18:497–505CrossRefGoogle Scholar
  45. Sol D (2007) Do successful invaders exist? Pre-adaptations to novel environments in terrestrial vertebrates. In: Nentwig W (ed) Biological invasions. Springer, Heidelberg, pp 127–141CrossRefGoogle Scholar
  46. Szűcs M, Melbourne BA, Tuff T, Hufbauer RA (2014) The roles of demography and genetics in the early stages of colonization. Proc R Soc B Biol Sci 281:20141073CrossRefGoogle Scholar
  47. Szűcs M, Melbourne BA, Tuff T, Weiss-Lehman C, Hufbauer RA (2017) Genetic and demographic founder effects have long-term fitness consequences for colonising populations. Ecol Lett 20:436–444CrossRefPubMedGoogle Scholar
  48. Van Allen BG, Rudolf VHW (2013) Ghosts of habitats past: environmental carry-over effects drive population dynamics in novel habitat. Am Nat 181:596–608CrossRefPubMedGoogle Scholar
  49. Van Allen BG, Rudolf VHW (2016) Carryover effects drive competitive dominance in spatially structure environments. Proc Natl Acad Sci USA 113:6939–6944CrossRefPubMedPubMedCentralGoogle Scholar
  50. Williamson M (1996) Biological invasions. Chapman & Hall, LondonGoogle Scholar
  51. Wong N, Lee C (2011) Relationship between population growth of the red flour beetle Tribolium castaneum and protein and carbohydrate content in flour and starch. J Econ Entomol 104:2087–2094CrossRefPubMedGoogle Scholar
  52. Wootton JT, Pfister CA (2013) Experimental separation of genetic and demographic factors on extinction risk in wild populations. Ecology 94:2117–2123CrossRefPubMedGoogle Scholar
  53. Yamamichi M, Yoshida T, Sasaki A (2014) Timing and propagule size of invasion determine its success by a time-varying threshold of demographic regime shift. Ecology 95:2303–2315CrossRefPubMedGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  • Megan L. Vahsen
    • 1
    • 2
    • 3
  • Katriona Shea
    • 4
  • Ciara L. Hovis
    • 4
    • 5
  • Brittany J. Teller
    • 4
  • Ruth A. Hufbauer
    • 1
    • 2
  1. 1.Department of Bioagricultural Sciences and Pest ManagementColorado State UniversityFort CollinsUSA
  2. 2.Graduate Degree Program in EcologyColorado State UniversityFort CollinsUSA
  3. 3.Department of Biological SciencesUniversity of Notre DameSouth BendUSA
  4. 4.Department of BiologyThe Pennsylvania State UniversityUniversity ParkUSA
  5. 5.Center for Systems Integration and SustainabilityMichigan State UniversityEast LansingUSA

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