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

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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.

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References

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

    Article  Google Scholar 

  • Avise JC (1994) Molecular markers, natural history and evolution, 2nd edn. Chapman & Hall, London

    Book  Google Scholar 

  • 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 88:293–294

    Article  Google Scholar 

  • 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 381–400

    Chapter  Google Scholar 

  • Bazin E, Glémin S, Galtier N (2006) Population size does not influence mitochondrial genetic diversity in animals. Science 312:570–572

    Article  CAS  PubMed  Google Scholar 

  • Bivand R, Piras G (2015) Comparing implementations of estimation methods for spatial econometrics. J Stat Softw 63:1–36

    Google Scholar 

  • 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 17:3684–3696

    Article  CAS  PubMed  Google Scholar 

  • Blouin MS, Yowell CA, Courtney CH, Dame JB (1995) Host movement and the genetic structure of populations of parasitic nematodes. Genetics 141:1007–1014

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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 47:274–288

    Article  CAS  PubMed  Google Scholar 

  • 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 714:217–228

    Article  Google Scholar 

  • Charlesworth D (2003) Effects of inbreeding on the genetic diversity of populations. Philos Trans R Soc Lond Ser B 258:1051–1070

    Article  Google Scholar 

  • Combes C (2004) Parasitism: the ecology and evolution of intimate interactions. University of Chicago Press, Chicago

    Google Scholar 

  • 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 32–46

    Google Scholar 

  • Criscione CD, Blouin MS (2004) Life cycles shape parasite evolution: comparative population genetics of salmond trematodes. Evolution 58:198–202

    Article  PubMed  Google Scholar 

  • Criscione CD, Poulin R, Blouin MS (2005) Molecular ecology of parasites: elucidating ecological and microevolutionary processes. Mol Ecol 14:2247–2257

    Article  CAS  PubMed  Google Scholar 

  • Darriba D, Taboada GL, Doallo R, Posada D (2012) jModelTest 2: more models, new heuristics and parallel computing. Nat Methods 9:772

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dray S (2013) spacemakeR: spatial modelling. R package version 0.0-5/r113

  • Dray S, Dufour AB (2007) The ade4 package: implementing the duality diagram for ecologists. J Stat Softw 22:1–20

    Article  Google Scholar 

  • Dray S, Legendre P, Blanchet G (2013) packfor: forward selection with permutation (Canoco p.46). R package version 0.0-8/r109

  • Excoffier L, Dupanloup I, Huerta-Sánchez E, Foll M (2013) Robust demographic inference from genomic and SNP data. PLoS Genet 9:e1003905

    Article  PubMed  PubMed Central  Google Scholar 

  • 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:e56940

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Galpern P, Peres-Neto PR, Polfus J, Manseau M (2014) MEMGENE: spatial pattern detection in genetic distance data. Methods Ecol Evol 5:1116–1120

    Article  Google Scholar 

  • 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 109:50–56

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 39–54

    Google Scholar 

  • 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 161–192

    Google Scholar 

  • Hart DG, Hart CW Jr (1974) The ostracod family Entocytheridae. Fulton Press Inc., Lancaster

    Google Scholar 

  • Hobbs HH Jr (1972) Biota of freshwater ecosystems, identification manual 9: Crayfishes (Astacidae) of North and Middle America. US Environmental Protection Agency, Washington

    Google Scholar 

  • Huey RB, Gilchrist GW, Carlson ML, Berrigan D, Serra L (2000) Rapid evolution of a geographic cline in size in an introduced fly. Science 287:308–309

    Article  CAS  PubMed  Google Scholar 

  • Huner JV, Barr JAE (1991) Red swamp crayfish, biology and exploitation, 3rd edn. Louisiana State University, Baton Rouge

    Google Scholar 

  • Jarne P (1995) Mating system, bottlenecks and genetic polymorphism in hermaphroditic animals. Genet Res 65:193–207

    Article  Google Scholar 

  • Jensen JD, Kim Y, DuMont VB, Aquadro CF, Bustamante CD (2005) Distinguishing between selective sweeps and demography using DNA polymorphism data. Genetics 170:1401–1410

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 4:434–437

    Article  PubMed  PubMed Central  Google Scholar 

  • Kouba A, Petrusek A, Kozák P (2014) Continental-wide distribution of crayfish species in Europe: update and maps. Knowl Manag Aquat Ecosyst 413:05

    Article  Google Scholar 

  • Legendre P (2014) lmodel2: model II regression. R package version 1.7-2

  • 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:e40652

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452

    Article  CAS  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • 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 14:395–405

    Article  Google Scholar 

  • Meirmans PG (2006) Using the AMOVA framework to estimate a standardized genetic differentiation measure. Evolution 60:2399–2402

    Article  PubMed  Google Scholar 

  • 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 96:347–355

    Article  CAS  Google Scholar 

  • 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 3:5237–5253

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 87:923–951

    Article  Google Scholar 

  • 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 59:2107–2121

    Article  Google Scholar 

  • 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 755:225–237

    Article  Google Scholar 

  • 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 103:19818–19823

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mulligan CJ, Kitchen A, Miyamoto MM (2006) Comment on “Population size does not influence mitochondrial genetic diversity in animals”. Science 314:1390

    Article  PubMed  Google Scholar 

  • 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 201–228

    Google Scholar 

  • Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin PR, O’Hara RB et al (2015) vegan: community ecology package. R package version 2.2-1

  • Paradis E (2010) pegas: an R package for population genetics with an integrated-modular approach. Bioinformatics 26:419–420

    Article  CAS  PubMed  Google Scholar 

  • Paradis E, Claude J, Strimmer K (2004) APE: analyses of phylogenetics and evolution in R language. Bioinformatics 20:289–290

    Article  CAS  PubMed  Google Scholar 

  • Paulson EL, Martin AP (2014) Discerning invasion history in an ephemerally connected system: landscape genetics of Procambarus clarkii in Ash Meadows, Nevada. Biol Invasions 16:1719–1734

    Article  Google Scholar 

  • Poulin R (2007) Evolutionary ecology of parasites, 2nd edn. Princeton University Press, Princeton

    Google Scholar 

  • Poulin R, Morand S (2005) Parasite biodiversity. Smithsonian Institution Scholarly Press, Washington

    Google Scholar 

  • Roy HE, Handley LJL (2012) Networking: a community approach to invaders and their parasites. Funct Ecol 26:1238–1248

    Article  Google Scholar 

  • 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 22:465–471

    Article  PubMed  Google Scholar 

  • 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 13:2147–2160

    Article  Google Scholar 

  • Stefani F, Aquaro G, Azzurro E, Colorni A, Galli P (2012) Patterns of genetic variation of a Lessepsian parasite. Biol Invasions 14:1725–1736

    Article  Google Scholar 

  • 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 10:512–526

    CAS  PubMed  Google Scholar 

  • Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Torchin ME, Lafferty KD, Dobson AP, McKenzie VJ, Kuris AM (2003) Introduced species and their missing parasites. Nature 421:628–630

    Article  CAS  PubMed  Google Scholar 

  • Untergrasser A, Cutcutache I, Koressaar T, Ye J, Faircloth BC, Remm M, Rozen SG (2012) Primer3—new capabilities and interfaces. Nucleic Acids Res 40:e115

    Article  Google Scholar 

  • Vavrek MJ (2011) Fossil: palaeoecological and palaeogeographical analysis tools. Palaeontol Electron 14:1T

    Google Scholar 

  • 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 229–258

    Google Scholar 

  • Young W (1971) Ecological studies of Entocytheridae (Ostracoda). Am Midl Nat 85:399–409

    Article  Google Scholar 

  • 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 12:2697–2706

    Article  Google Scholar 

  • Zhang Z, Schwartz S, Wagner L, Miller W (2000) A greedy algorithm for aligning DNA sequences. J Comput Biol 7:203–214

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We thank Josep Antoni Aguilar-Alberola, Maria Antón, Marco Arruej, Andreu Castillo, Andreu Escrivà, Jose Antonio Gil-Delgado, Cristina Molina, Adrian Ponz, Josep R. Roca, Olivier Schmit, Luis Valls, Laia Zamora, Noel Novelo, Jonathan L. West, Will Sheftal, Julie Delabbio, Taren Manley, Mike Kennedy, Shirley and Shai for their help in the fieldwork; Andy Kruppa, Gavin Horsburgh and Barbara Morrissey for their assistance in the lab; Laurent Excoffier and Ivan Scotti for their help in coalescent simulation analyses. This research was funded by the Spanish Ministry of Science and Innovation Project ECOINVADER (CGL2008-01296/BOS) and the University of Valencia (“V-Segles” predoctoral grant to A. Mestre).

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Authors and Affiliations

  1. Department of Microbiology and Ecology, Cavanilles Institute of Biodiversity and Evolutionary Biology, University of Valencia, Dr. Moliner 50, 46100, Burjassot, Valencia, Spain

    Alexandre Mestre, Juan S. Monrós & Francesc Mesquita-Joanes

  2. Department of Animal and Plant Sciences, University of Sheffield, Sheffield, UK

    Roger K. Butlin

  3. School of Renewable Natural Resources, Louisiana State University, Baton Rouge, LA, USA

    William E. Kelso

  4. Aquaculture Research Station, Louisiana State University Agricultural Center, Baton Rouge, LA, USA

    Robert Romaire

  5. Department of Biological Sciences, Nicholls State University, Thibodaux, LA, USA

    Christopher P. Bonvillain

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  1. Alexandre Mestre
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Correspondence to Alexandre Mestre.

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Mestre, A., Butlin, R.K., Kelso, W.E. et al. Contrasting patterns of genetic diversity and spatial structure in an invasive symbiont-host association. Biol Invasions 18, 3175–3191 (2016). https://doi.org/10.1007/s10530-016-1207-1

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