Biological Invasions

, Volume 18, Issue 11, pp 3175–3191

Contrasting patterns of genetic diversity and spatial structure in an invasive symbiont-host association

  • Alexandre Mestre
  • Roger K. Butlin
  • William E. Kelso
  • Robert Romaire
  • Christopher P. Bonvillain
  • Juan S. Monrós
  • Francesc Mesquita-Joanes
Original Paper

Abstract

Do host invaders and their associated symbiont co-invaders have different genetic responses to the same invasion process? To answer this question, we compared genetic patterns of native and exotic populations of an invasive symbiont-host association. This is an approach applied by very few studies, of which most are based on parasites with complex life cycles. We used the mitochondrial genetic marker cytochrome oxidase subunit I (COI) to investigate a non-parasitic freshwater ectosymbiont with direct life-cycle, low host specificity and well-documented invasion history. The study system was the crayfish Procambarus clarkii and its commensal ostracod Ankylocythere sinuosa, sampled in native (N American) and exotic (European) ranges. Results of analyses indicated: (1) higher genetic diversity in the symbiont than its host; (2) genetic diversity loss in the exotic range for both species, but less pronounced in the symbiont; (3) native populations genetically structured in space, with stronger patterns in the symbiont and (4) loss of spatial genetic structure in the exotic range in both species. The combination of historical, demographic and genetic data supports a higher genetic diversity of source populations and a higher propagule size that allowed the symbiont to overcome founder effects better than its host co-invader. Thus, the symbiont might be endowed with a higher adaptive potential to new hosts or off-host environmental pressures expected in the invasive range. We highlight the usefulness of this relatively unexplored kind of symbiont-host systems in the invasion context to test important ecological and evolutionary questions.

Keywords

Direct life-cycle Effective population size Founder effects Freshwater crustacean Dispersal Propagule size 

Supplementary material

10530_2016_1207_MOESM1_ESM.pdf (762 kb)
Supplementary material 1 (PDF 763 kb)

References

  1. Allendorf FW, Lundquist LL (2003) Introduction: population biology, evolution, and control of invasive species. Conserv Biol 17:24–30CrossRefGoogle Scholar
  2. Avise JC (1994) Molecular markers, natural history and evolution, 2nd edn. Chapman & Hall, LondonCrossRefGoogle Scholar
  3. Baker JH (1969) On the relationship of Ankylocythere sinuosa (Rioja 1942) (Ostracoda, Entocytheridae) to the crayfish Procambarus simulans simulans (Faxon 1884). Trans Am Microsc Soc 88:293–294CrossRefGoogle Scholar
  4. Barbaresi S, Gherardi F, Mengoni A, Souty-Grosset C (2007) Genetics and invasion biology in fresh waters: a pilot study of Procambarus clarkii in Europe. In: Gherardi F (ed) Biological invaders in inland waters: profiles, distribution, and threats. Springer, Dordrecht, pp 381–400CrossRefGoogle Scholar
  5. Bazin E, Glémin S, Galtier N (2006) Population size does not influence mitochondrial genetic diversity in animals. Science 312:570–572CrossRefPubMedGoogle Scholar
  6. Bivand R, Piras G (2015) Comparing implementations of estimation methods for spatial econometrics. J Stat Softw 63:1–36Google Scholar
  7. Blakeslee AM, Byers JE, Lesser MP (2008) Solving cryptogenic histories using host and parasite molecular genetics: the resolution of Littorina littorea’s North American origin. Mol Ecol 17:3684–3696CrossRefPubMedGoogle Scholar
  8. Blouin MS, Yowell CA, Courtney CH, Dame JB (1995) Host movement and the genetic structure of populations of parasitic nematodes. Genetics 141:1007–1014PubMedPubMedCentralGoogle Scholar
  9. Burbrink FT, Fontanella F, Pyron RA, Guiher TJ, Jimenez C (2008) Phylogeography across a continent: the evolutionary and demographic history of the North American racer (Serpentes: Colubridae: Coluber constrictor). Mol Phylogenet Evol 47:274–288CrossRefPubMedGoogle Scholar
  10. Castillo-Escrivà A, Mestre A, Monrós JS, Mesquita-Joanes F (2013) Population dynamics of an epibiont Ostracoda on the invasive red swamp crayfish Procambarus clarkii in a western Mediterranean wetland. Hydrobiologia 714:217–228CrossRefGoogle Scholar
  11. Charlesworth D (2003) Effects of inbreeding on the genetic diversity of populations. Philos Trans R Soc Lond Ser B 258:1051–1070CrossRefGoogle Scholar
  12. Combes C (2004) Parasitism: the ecology and evolution of intimate interactions. University of Chicago Press, ChicagoGoogle Scholar
  13. Cox GW (2004) Founder effects and exotic variability. In: Cox GW (ed) Alien species and evolution: the evolutionary ecology of exotic plants, animals, microbes, and interacting native species. Island Press, Washington, pp 32–46Google Scholar
  14. Criscione CD, Blouin MS (2004) Life cycles shape parasite evolution: comparative population genetics of salmond trematodes. Evolution 58:198–202CrossRefPubMedGoogle Scholar
  15. Criscione CD, Poulin R, Blouin MS (2005) Molecular ecology of parasites: elucidating ecological and microevolutionary processes. Mol Ecol 14:2247–2257CrossRefPubMedGoogle Scholar
  16. Darriba D, Taboada GL, Doallo R, Posada D (2012) jModelTest 2: more models, new heuristics and parallel computing. Nat Methods 9:772CrossRefPubMedPubMedCentralGoogle Scholar
  17. Dray S (2013) spacemakeR: spatial modelling. R package version 0.0-5/r113Google Scholar
  18. Dray S, Dufour AB (2007) The ade4 package: implementing the duality diagram for ecologists. J Stat Softw 22:1–20CrossRefGoogle Scholar
  19. Dray S, Legendre P, Blanchet G (2013) packfor: forward selection with permutation (Canoco p.46). R package version 0.0-8/r109Google Scholar
  20. Excoffier L, Dupanloup I, Huerta-Sánchez E, Foll M (2013) Robust demographic inference from genomic and SNP data. PLoS Genet 9:e1003905CrossRefPubMedPubMedCentralGoogle Scholar
  21. Gaither MR, Aeby G, Vignon M, Meguro Y, Rigby M, Runyon C et al (2013) An invasive fish and the time-lagged spread of its parasite across the Hawaiian archipelago. PLoS ONE 8:e56940CrossRefPubMedPubMedCentralGoogle Scholar
  22. Galpern P, Peres-Neto PR, Polfus J, Manseau M (2014) MEMGENE: spatial pattern detection in genetic distance data. Methods Ecol Evol 5:1116–1120CrossRefGoogle Scholar
  23. Goodall-Copestake W, Tarling G, Murphy E (2012) On the comparison of population-level estimates of haplotype and nucleotide diversity: a case study using the gene cox1 in animals. Heredity 109:50–56CrossRefPubMedPubMedCentralGoogle Scholar
  24. Gotelli NJ, Colwell RK (2010) Estimating species richness. In: Magurran AE, McGill BJ (eds) Biological diversity: frontiers in measurement and assessment. Oxford University Press, Oxford, pp 39–54Google Scholar
  25. Gutiérrez-Yurrita PJ, Martínez JM, Bravo-Utrera MA, Montes C, Ilhéu M, Bernardo JM (1999) The status of crayfish populations in Spain and Portugal. In: Gherardi F, Holdich DM (eds) Crayfish in Europe as alien species: How to make the best of a bad situation?. A. A. Balkema, Rotterdam, pp 161–192Google Scholar
  26. Hart DG, Hart CW Jr (1974) The ostracod family Entocytheridae. Fulton Press Inc., LancasterGoogle Scholar
  27. Hobbs HH Jr (1972) Biota of freshwater ecosystems, identification manual 9: Crayfishes (Astacidae) of North and Middle America. US Environmental Protection Agency, WashingtonGoogle Scholar
  28. Huey RB, Gilchrist GW, Carlson ML, Berrigan D, Serra L (2000) Rapid evolution of a geographic cline in size in an introduced fly. Science 287:308–309CrossRefPubMedGoogle Scholar
  29. Huner JV, Barr JAE (1991) Red swamp crayfish, biology and exploitation, 3rd edn. Louisiana State University, Baton RougeGoogle Scholar
  30. Jarne P (1995) Mating system, bottlenecks and genetic polymorphism in hermaphroditic animals. Genet Res 65:193–207CrossRefGoogle Scholar
  31. Jensen JD, Kim Y, DuMont VB, Aquadro CF, Bustamante CD (2005) Distinguishing between selective sweeps and demography using DNA polymorphism data. Genetics 170:1401–1410CrossRefPubMedPubMedCentralGoogle Scholar
  32. Kolbe JJ, Larson A, Losos JB, de Queiroz K (2008) Admixture determines genetic diversity and population differentiation in the biological invasion of a lizard species. Biol Lett 4:434–437CrossRefPubMedPubMedCentralGoogle Scholar
  33. Kouba A, Petrusek A, Kozák P (2014) Continental-wide distribution of crayfish species in Europe: update and maps. Knowl Manag Aquat Ecosyst 413:05CrossRefGoogle Scholar
  34. Legendre P (2014) lmodel2: model II regression. R package version 1.7-2Google Scholar
  35. Li Y, Guo X, Cao X, Deng W, Luo W, Wang W (2012) Population genetic structure and post-establishment dispersal patterns of the red swamp crayfish Procambarus Clarkii in China. PLoS ONE 7:e40652CrossRefPubMedPubMedCentralGoogle Scholar
  36. Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452CrossRefPubMedGoogle Scholar
  37. Lockwood JL, Cassey P, Blackburn T (2005) The role of propagule pressure in explaining species invasions. Trends Ecol Evol 20:223–228CrossRefPubMedGoogle Scholar
  38. McCoy KD, Boulinier T, Tirard C, Michalakis Y (2001) Host specificity of a generalist parasite: genetic evidence of sympatric host races in the seabird tick Ixodes uriae. J Evol Biol 14:395–405CrossRefGoogle Scholar
  39. Meirmans PG (2006) Using the AMOVA framework to estimate a standardized genetic differentiation measure. Evolution 60:2399–2402CrossRefPubMedGoogle Scholar
  40. Mestre A, Monrós JS, Mesquita-Joanes F (2011) Comparison of two chemicals for removing an entocytherid (Ostracoda: Crustacea) species from its host crayfish (Cambaridae: Crustacea). Int Rev Hydrobiol 96:347–355CrossRefGoogle Scholar
  41. Mestre A, Aguilar-Alberola JA, Baldry D, Balkis H, Ellis A, Gil-Delgado JA et al (2013) Invasion biology in non-free-living species: interactions between abiotic (climatic) and biotic (host availability) factors in geographical space in crayfish commensals (Ostracoda, Entocytheridae). Ecol Evol 3:5237–5253CrossRefPubMedPubMedCentralGoogle Scholar
  42. Mestre A, Monrós JS, Mesquita-Joanes F (2014a) A review of the Entocytheridae (Ostracoda) of the world: updated bibliographic and species checklists and global georeferenced database, with insights into host specificity and latitudinal patterns of species richness. Crustaceana 87:923–951CrossRefGoogle Scholar
  43. Mestre A, Monrós JS, Mesquita-Joanes F (2014b) The influence of environmental factors on abundance and prevalence of a commensal ostracod hosted by an invasive crayfish: are ‘parasite rules’ relevant to non-parasitic symbionts? Freshw Biol 59:2107–2121CrossRefGoogle Scholar
  44. Mestre A, Castillo-Escrivà A, Rueda J, Monrós JS, Mesquita-Joanes F (2015) Experimental spillover of an exotic ectosymbiont on an European native crayfish: the importance of having a chance. Hydrobiologia 755:225–237CrossRefGoogle Scholar
  45. Miura O, Torchin ME, Kuris AM, Hechinger RF, Chiba S (2006) Introduced cryptic species of parasites exhibit different invasion pathways. Proc Natl Acad Sci USA 103:19818–19823CrossRefPubMedPubMedCentralGoogle Scholar
  46. Mulligan CJ, Kitchen A, Miyamoto MM (2006) Comment on “Population size does not influence mitochondrial genetic diversity in animals”. Science 314:1390CrossRefPubMedGoogle Scholar
  47. Novak SJ, Mack RN (2005) Genetic bottlenecks in alien plant species: influence of mating systems. In: Sax DF, Stachowicz JJ, Gaines SD (eds) Species invasions: insights into ecology, evolution, and biogeography. Sinauer Associates Inc, Sunderland, pp 201–228Google Scholar
  48. Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin PR, O’Hara RB et al (2015) vegan: community ecology package. R package version 2.2-1Google Scholar
  49. Paradis E (2010) pegas: an R package for population genetics with an integrated-modular approach. Bioinformatics 26:419–420CrossRefPubMedGoogle Scholar
  50. Paradis E, Claude J, Strimmer K (2004) APE: analyses of phylogenetics and evolution in R language. Bioinformatics 20:289–290CrossRefPubMedGoogle Scholar
  51. Paulson EL, Martin AP (2014) Discerning invasion history in an ephemerally connected system: landscape genetics of Procambarus clarkii in Ash Meadows, Nevada. Biol Invasions 16:1719–1734CrossRefGoogle Scholar
  52. Poulin R (2007) Evolutionary ecology of parasites, 2nd edn. Princeton University Press, PrincetonGoogle Scholar
  53. Poulin R, Morand S (2005) Parasite biodiversity. Smithsonian Institution Scholarly Press, WashingtonGoogle Scholar
  54. Roy HE, Handley LJL (2012) Networking: a community approach to invaders and their parasites. Funct Ecol 26:1238–1248CrossRefGoogle Scholar
  55. Sax DF, Stachowicz JJ, Brown JH, Bruno JF, Dawson MN, Gaines SD et al (2007) Ecological and evolutionary insights from species invasions. Trends Ecol Evol 22:465–471CrossRefPubMedGoogle Scholar
  56. Siesa ME, Manenti R, Padoa-Schioppa E, Bernardi FD, Ficetola GF (2011) Spatial autocorrelation and the analysis of invasion processes from distribution data: a study with the crayfish Procambarus clarkii. Biol Invasions 13:2147–2160CrossRefGoogle Scholar
  57. Stefani F, Aquaro G, Azzurro E, Colorni A, Galli P (2012) Patterns of genetic variation of a Lessepsian parasite. Biol Invasions 14:1725–1736CrossRefGoogle Scholar
  58. Tamura K, Nei M (1993) Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol Biol Evol 10:512–526PubMedGoogle Scholar
  59. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729CrossRefPubMedPubMedCentralGoogle Scholar
  60. Torchin ME, Lafferty KD, Dobson AP, McKenzie VJ, Kuris AM (2003) Introduced species and their missing parasites. Nature 421:628–630CrossRefPubMedGoogle Scholar
  61. Untergrasser A, Cutcutache I, Koressaar T, Ye J, Faircloth BC, Remm M, Rozen SG (2012) Primer3—new capabilities and interfaces. Nucleic Acids Res 40:e115CrossRefGoogle Scholar
  62. Vavrek MJ (2011) Fossil: palaeoecological and palaeogeographical analysis tools. Palaeontol Electron 14:1TGoogle Scholar
  63. Wares JP, Hughes AR, Grosberg RK (2005) Mechanisms that drive evolutionary change: insights from species introductions and invasions. In: Sax DF, Stachowicz JJ, Gaines SD (eds) Species invasions: insights into ecology, evolution, and biogeography. Sinauer Associates Inc, Sunderland, pp 229–258Google Scholar
  64. Young W (1971) Ecological studies of Entocytheridae (Ostracoda). Am Midl Nat 85:399–409CrossRefGoogle Scholar
  65. Yue GH, Li J, Bai Z, Wang CM, Feng F (2010) Genetic diversity and population structure of the invasive alien red swamp crayfish. Biol Invasions 12:2697–2706CrossRefGoogle Scholar
  66. Zhang Z, Schwartz S, Wagner L, Miller W (2000) A greedy algorithm for aligning DNA sequences. J Comput Biol 7:203–214CrossRefPubMedGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2016

Authors and Affiliations

  • Alexandre Mestre
    • 1
  • Roger K. Butlin
    • 2
  • William E. Kelso
    • 3
  • Robert Romaire
    • 4
  • Christopher P. Bonvillain
    • 5
  • Juan S. Monrós
    • 1
  • Francesc Mesquita-Joanes
    • 1
  1. 1.Department of Microbiology and Ecology, Cavanilles Institute of Biodiversity and Evolutionary BiologyUniversity of ValenciaBurjassotSpain
  2. 2.Department of Animal and Plant SciencesUniversity of SheffieldSheffieldUK
  3. 3.School of Renewable Natural ResourcesLouisiana State UniversityBaton RougeUSA
  4. 4.Aquaculture Research StationLouisiana State University Agricultural CenterBaton RougeUSA
  5. 5.Department of Biological SciencesNicholls State UniversityThibodauxUSA

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