Biological Invasions

, Volume 17, Issue 3, pp 951–971

Genetic studies of aquatic biological invasions: closing the gap between research and management

Molecular Tools

Abstract

Recent years have seen a dramatic rise in the application of genetic methods to understand aquatic biological invasions. In part these methods have been adopted to address fundamental questions in biogeography, evolutionary biology, population ecology, and other fields. But it is also commonly suggested that genetic information has the potential to directly inform the management of aquatic invasions. Here I explore the potential promise of genetic approaches for informing management of aquatic invasive species, the degree to which that promise has been realized in terms of utilization of genetic information by managers and other decision-makers, and the likely limitations to the value of genetic methods (both in principle and in practice) and ways in which these limitations might be overcome. I consider a range of possible applications of genetic tools for management, including molecular detection and identification of cryptic invaders, source tracking and reconstruction of invasion history, and inference of population demographics. Retrospective assessment of the utility of such applications is based on both literature review and solicitation of expert opinion, and suggests that a number of hurdles likely often prevent genetic information from effectively informing decision-making. These include (1) limitations or misunderstandings of the resolution and certainty afforded by genetic analysis; (2) failure to engage decision-makers in problem formulation, research design and research implementation; and (3) complex relationships between basic research and management actions. While some of the obstacles considered are rooted in theoretical and practical limitations of genetic analysis, others are clearly associated with poor communication and insufficient engagement of potential end-users of genetic information. I consider possible avenues for overcoming these obstacles and for improving the applicability of genetic information for supporting management decisions.

Keywords

Aquatic invasive species Genetics eDNA Marine Management Policy 

Supplementary material

10530_2014_726_MOESM1_ESM.pdf (147 kb)
Supplementary material 1 (PDF 147 kb)

References

  1. Arlettaz R, Schaub M, Fournier J et al (2010) From publications to public actions: when conservation biologists bridge the gap between research and implementation. Bioscience 60:835–842CrossRefGoogle Scholar
  2. Bagley MJ, Geller JB (2000) Microsatellite analysis of native and invading populations of European green crabs. In: Pederson J (ed) Marine bioinvasions: proceedings of the first national conference. MIT Seagrant, pp 241–243Google Scholar
  3. Barun A, Niemiller ML, Fitzpatrick BM et al (2013) Can genetic data confirm or refute historical records? The island invasion of the small Indian mongoose (Herpestes auropunctatus). Biol Invasions 15:2243–2251CrossRefGoogle Scholar
  4. Bayliss HR, Wilcox A, Stewart GB et al (2012) Does research information meet the needs of stakeholders? Exploring evidence selection in the global management of invasive species. Evid Policy 8:37–56CrossRefGoogle Scholar
  5. Bean DW, Kazmer DJ, Gardner K et al (2013) Molecular genetic and hybridization studies of Diorhabda spp. Released for biological control of Tamarix. Invasive Plant Sci Manag 6:1–15CrossRefGoogle Scholar
  6. Belzile F, Labbé J, LeBlanc M-C et al (2009) Seeds contribute strongly to the spread of the invasive genotype of the common reed (Phragmites australis). Biol Invasions 12:2243–2250CrossRefGoogle Scholar
  7. Bickford D, Lohman DJ, Sodhi NS et al (2007) Cryptic species as a window on diversity and conservation. Trends Ecol Evol 22:148–155CrossRefPubMedGoogle Scholar
  8. Blackburn TM, Pyšek P, Bacher S et al (2011) A proposed unified framework for biological invasions. Trends Ecol Evol 26:333–339CrossRefPubMedGoogle Scholar
  9. Blakeslee A, McKenzie C, Darling J et al (2010) A hitchhiker’s guide to the Maritimes: anthropogenic transport facilitates long-distance dispersal of an invasive marine crab to Newfoundland. Divers Distrib 16:879–891CrossRefGoogle Scholar
  10. Blanchet S (2012) The use of molecular tools in invasion biology: an emphasis on freshwater ecosystems. Fish Manag Ecol 19:120–132Google Scholar
  11. Bott N, Ophel-Keller K, Sierp M et al (2010) Toward routine, DNA-based detection methods for marine pests. Biotechnol Adv 28:706–714CrossRefPubMedGoogle Scholar
  12. Bronnenhuber JE, Dufour BA, Higgs DM et al (2011) Dispersal strategies, secondary range expansion and invasion genetics of the nonindigenous round goby, Neogobius melanostomus, in Great Lakes tributaries. Mol Ecol 20:1845–1859CrossRefPubMedGoogle Scholar
  13. Budescu DV, Broomell S, Por HH (2009) Improving communication of uncertainty in the reports of the intergovernmental panel on climate change. Psychol Sci 20:299–308CrossRefPubMedGoogle Scholar
  14. Carlton JT (2009) Deep Invasion Ecology and the Assembly of Communities in Historical Time. In: Rilov G, Crooks JA (eds) Biological invasions in marine ecosystems. Springer-Verlag, Berlin, pp 13–56Google Scholar
  15. Chapple DG, Whitaker AH, Chapple SNJ et al (2012) Biosecurity interceptions of an invasive lizard: origin of stowaways and human-assisted spread within New Zealand. Evol Appl 6:324–339CrossRefPubMedCentralPubMedGoogle Scholar
  16. Cohen AN, Weinstein A, Emmett MA et al (2001) Investigations into the introduction of non-indigenous marine organisms via the cross-continental trade in marine baitworms. U.S. Fish and Wildlife Service San Francisco Bay programGoogle Scholar
  17. Committee ACRC (2013) Fiscal year 2013 Asian carp control strategy framework. Council on environmental qualityGoogle Scholar
  18. Costello MJ, Coll M, Danovaro R et al (2010) A census of marine biodiversity knowledge, resources, and future challenges. Plos One 5:e12110Google Scholar
  19. Darling JA, Blum M (2007) DNA-based methods for monitoring invasive species: a review and prospectus. Biol Invasions 9:751–765CrossRefGoogle Scholar
  20. Darling JA, Mahon A (2011) From molecules to management: adopting DNA-based methods for monitoring biological invasions in aquatic environments. Environ Res 111:1–11Google Scholar
  21. Darling JA, Herborg LM, Davidson IC (2012) Intracoastal shipping drives patterns of regional population expansion by an invasive marine invertebrate. Ecol Evol 2:2557–2566CrossRefPubMedCentralPubMedGoogle Scholar
  22. 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
  23. Engineers UACo (2013) Environmental DNA calibration study (ECALS), interim technical review reportGoogle Scholar
  24. Esler KJ, Prozesky H, Sharma GP et al (2010) How wide is the “knowing-doing” gap in invasion biology? Biol Invasions 12:4065–4075CrossRefGoogle Scholar
  25. Estoup A, Guillemaud T (2010) Reconstructing routes of invasion using genetic data: why, how and so what? Mol Ecol 19:4113–4130CrossRefPubMedGoogle Scholar
  26. Estoup A, Baird SJE, Ray N et al (2010) Combining genetic, historical and geographical data to reconstruct the dynamics of bioinvasions: application to the cane toad Bufo marinus. Mol Ecol Resour 10:886–901CrossRefPubMedGoogle Scholar
  27. Etchegary H, Green J, Parfrey P et al (2013) Community engagement with genetics: public perceptions and expectations about genetics research. Health Expect. doi:10.1111/hex.12122 PubMedGoogle Scholar
  28. Excoffier L, Foll M, Petit RJ (2009) Genetic consequences of range expansions. Annu Rev Ecol Evol Syst 40:481–501CrossRefGoogle Scholar
  29. Facon B, Jarne P, Pointier JP et al (2005) Hybridization and invasiveness in the freshwater snail Melanoides tuberculata: hybrid vigour is more important than increase in genetic variance. J Evol Biol 18:524–535CrossRefPubMedGoogle Scholar
  30. Finnoff D, Shogren JF, Leung B et al (2007) Take a risk: preferring prevention over control of biological invaders. Ecol Econ 62:216–222CrossRefGoogle Scholar
  31. Fitzpatrick BM, Fordyce JA, Niemiller ML et al (2012) What can DNA tell us about biological invasions? Biol Invasions 14:245–253CrossRefGoogle Scholar
  32. Fontaine B, Perrard A, Bouchet P (2012) 21 years of shelf life between discovery and description of new species. Curr Biol 22:R943–R944CrossRefPubMedGoogle Scholar
  33. Frischer ME, Kelly KL, Nierzwicki-Bauer SA (2012) Accuracy and reliability of Dreissena spp. larvae detection by cross-polarized light microscopy, imaging flow cytometry, and polymerase chain reaction assays. Lake Reserv Manag 28:265–276CrossRefGoogle Scholar
  34. Gaither MR, Toonen RJ, Bowen BW (2012) Coming out of the starting blocks: extended lag time rearranges genetic diversity in introduced marine fishes of Hawai’i. Proc R Soc B Biol Sci 279:3948–3957CrossRefGoogle Scholar
  35. Gaskin JF, Bon M-C, Cock MJW et al (2011) Applying molecular-based approaches to classical biological control of weeds. Biol Control 58:1–21CrossRefGoogle Scholar
  36. Geller JB, Walton E, Grosholz E et al (1997) Cryptic invasions of the crab Carcinus detected by molecular phylogeography. Mol Ecol 6:901–906CrossRefPubMedGoogle Scholar
  37. Geller JB, Darling JA, Carlton JT (2010) Genetic perspectives on marine biological invasions. Annu Rev Mar Sci 2:367–393CrossRefGoogle Scholar
  38. Ghabooli S, ZHAN A, Sardiña P et al (2013) Genetic diversity in introduced golden mussel populations corresponds to vector activity. PLoS One 8:e59328CrossRefPubMedCentralPubMedGoogle Scholar
  39. Goldstien SJ, Inglis GJ, Schiel DR et al (2013) Using temporal sampling to improve attribution of source populations for invasive species. PLoS One 8:e65656CrossRefPubMedCentralPubMedGoogle Scholar
  40. Goolsby JA, de Barro PJ, Makinson JR et al (2005) Matching the origin of an invasive weed for selection of a herbivore haplotype for a biological control programme. Mol Ecol 15:287–297CrossRefGoogle Scholar
  41. Grosholz ED, Ruiz GM, Dean CA et al (2000) The impacts of a nonindigenous marine predator in a California bay. Ecology 81:1206–1224CrossRefGoogle Scholar
  42. Grosholz E, Lovell S, Besedin E et al (2011) Modeling the impacts of the European green crab on commercial shellfisheries. Ecol Appl 21:915–924CrossRefPubMedGoogle Scholar
  43. Guillemaud T, Beaumont MA, Ciosi M et al (2010) Inferring introduction routes of invasive species using approximate Bayesian computation on microsatellite data. Heredity 104:88–99CrossRefPubMedGoogle Scholar
  44. Haydar D (2012) What is natural? The scale of cryptogenesis in the North Atlantic Ocean. Divers Distrib 18:101–110CrossRefGoogle Scholar
  45. Hegger D, Lamers M, Van Zeijl-Rozema A et al (2012) Conceptualising joint knowledge production in regional climate change adaptation projects: success conditions and levers for action. Environ Sci Policy 18:52–65CrossRefGoogle Scholar
  46. Hoban SM, Hauffe HC, Pérez-Espona S et al (2013) Bringing genetic diversity to the forefront of conservation policy and management. Conserv Genet Resour 5:593–598CrossRefGoogle Scholar
  47. Holland BS (2000) Genetics of marine bioinvasions. Hydrobiologia 420:63–71CrossRefGoogle Scholar
  48. Holm P, Goodsite ME, Cloetingh S et al (2013) Collaboration between the natural, social and human sciences in global change research. Environ Sci Policy 28:25–35CrossRefGoogle Scholar
  49. Hopkins GW, Freckleton RP (2002) Declines in the numbers of amateur and professional taxonomists: implications for conservation. Anim Conserv 5:245–249CrossRefGoogle Scholar
  50. Hulme PE (2003) Biological invasions: winning the science battles but losing the conservation war? Oryx 37:178–193CrossRefGoogle Scholar
  51. Jentoft S, Chuenpagdee R (2009) Fisheries and coastal governance as a wicked problem. Mar Policy 33:553–560CrossRefGoogle Scholar
  52. Jerde CL, Mahon AR, Chadderton WL et al (2011) “Sight-unseen” detection of rare aquatic species using environmental DNA. Conserv Lett 4:150–157CrossRefGoogle Scholar
  53. Jerde CL, Chadderton WL, Mahon AR et al (2013) Detection of Asian carp DNA as part of a Great Lakes basin-wide surveillance program. Can J Fish Aquat Sci 70:522–526CrossRefGoogle Scholar
  54. Jolibert C, Wesselink A (2012) Research impacts and impact on research in biodiversity conservation: the influence of stakeholder engagement. Environ Sci Policy 22:100–111CrossRefGoogle Scholar
  55. Jones WJ, Preston CM, Marin R et al (2008) A robotic molecular method for in situ detection of marine invertebrate larvae. Mol Ecol Resour 8:540–550CrossRefPubMedGoogle Scholar
  56. Kalinowski ST, Muhlfeld CC, Guy CS et al (2010) Founding population size of an aquatic invasive species. Conserv Genet 11:2049–2053CrossRefGoogle Scholar
  57. Kandlikar M, Risbey J, Dessai S (2005) Representing and communicating deep uncertainty in climate-change assessments. C R Geosci 337:443–455CrossRefGoogle Scholar
  58. Kueffer C, Hadorn GH, Bammer G et al (2007) Towards a publication culture in transdisciplinary research. Gaia 16:22–26Google Scholar
  59. Lacoursiere-Roussel A, Bock DG, Cristescu ME et al (2012) Disentangling invasion processes in a dynamic shipping–boating network. Mol Ecol 21:4227–4241CrossRefPubMedGoogle Scholar
  60. Lawson Handley LJ, Estoup A, Evans DM et al (2011) Ecological genetics of invasive alien species. Biocontrol 56:409–428CrossRefGoogle Scholar
  61. Lee CE (2002) Evolutionary genetics of invasive species. Trends Ecol Evol 17:386–391CrossRefGoogle Scholar
  62. Lodge DM, Turner CR, Jerde CL et al (2012) Conservation in a cup of water: estimating biodiversity and population abundance from environmental DNA. Mol Ecol 21:2555–2558CrossRefPubMedCentralPubMedGoogle Scholar
  63. Lombaert E, Guillemaud T, Thomas C et al (2011) Inferring the origin of populations introduced from a genetically structured native range by approximate Bayesian computation: case study of the invasive ladybird Harmonia axyridis. Mol Ecol 20:4654–4670CrossRefPubMedGoogle Scholar
  64. Mackie JA, Geller J (2010) Experimental parameters affecting quantitative PCR of Artemia franciscana: a model for a marine zooplanktonic target in natural plankton samples. Limnol Oceanogr Methods 8:337–347CrossRefGoogle Scholar
  65. Mahon AR, Barnes MA, Senapati S et al (2011) Molecular detection of invasive species in heterogeneous mixtures using a microfluidic carbon nanotube platform. PLoS One 6:e17280CrossRefPubMedCentralPubMedGoogle Scholar
  66. Mahon AR, Barnes MA, Li F et al (2013a) DNA-based species detection capabilities using laser transmission spectroscopy. J R Soc Interface 10:20120637CrossRefPubMedCentralGoogle Scholar
  67. Mahon AR, Jerde CL, Galaska M et al (2013b) Validation of eDNA surveillance sensitivity for detection of Asian carps in controlled and field experiments. PLoS One 8:e58316CrossRefPubMedCentralPubMedGoogle Scholar
  68. Matzek V, Covino J, Funk JL et al (2013) Closing the knowing-doing gap in invasive plant management: accessibility and interdisciplinarity of scientific research. Conserv Lett 0:1–8Google Scholar
  69. McGlashan DJ, Ponniah M, Cassey P et al (2008) Clarifying marine invasions with molecular markers: an illustration based on mtDNA from mistaken calyptraeid gastropod identifications. Biol Invasions 10:51–57CrossRefGoogle Scholar
  70. Muirhead JR, Gray DK, Kelly DW et al (2008) Identifying the source of species invasions: sampling intensity vs. genetic diversity. Mol Ecol 17:1020–1035CrossRefPubMedGoogle Scholar
  71. Neiva J, Pearson GA, Valero M et al (2010) Surfing the wave on a borrowed board: range expansion and spread of introgressed organellar genomes in the seaweed Fucus ceranoides L. Mol Ecol 19:4812–4822CrossRefPubMedGoogle Scholar
  72. Nielsen EE, Cariani A, Mac Aoidh E et al (2012) Gene-associated markers provide tools for tackling illegal fishing and false eco-certification. Nat Commun 3:851CrossRefPubMedGoogle Scholar
  73. Ojaveer H, Galil BS, Minchin D et al (2013) Ten recommendations for advancing the assessment and management of non-indigenous species in marine ecosystems. Mar Policy 44:1–6Google Scholar
  74. Paterson B, Isaacs M, Hara M et al (2010) Transdisciplinary co-operation for an ecosystem approach to fisheries: a case study from the South African sardine fishery. Mar Policy 34:782–794CrossRefGoogle Scholar
  75. Perez-Portela R, Arranz V, Rius M et al (2013) Cryptic speciation or global spread? The case of a cosmopolitan marine invertebrate with limited dispersal capabilities. Sci Rep 3:3197Google Scholar
  76. Pilgrim EM, Darling JA (2010) Genetic diversity in two introduced biofouling amphipods (Ampithoe valida and Jassa marmorata) along the Pacific North American coast: investigation into molecular identification and cryptic diversity. Divers Distrib 16:827–839CrossRefGoogle Scholar
  77. Piraino S, Aglieri G, Martell L et al (2014) Pelagian benovici sp. nov. (Cnidaria, Scyphozoa): a new jellyfish in the Mediterranean Sea. Zootaxa 3794:455–468Google Scholar
  78. Pluess T, Cannon R, Jarošík V et al (2012a) When are eradication campaigns successful? A test of common assumptions. Biol Invasions 14:1365–1378CrossRefGoogle Scholar
  79. Pluess T, Jarosik V, Pysek P et al (2012b) Which factors affect the success or failure of eradication campaigns against alien species? PLoS One 7:e48157CrossRefPubMedCentralPubMedGoogle Scholar
  80. Pochon X, Bott NJ, Smith KF et al (2013) Evaluating detection limits of next-generation sequencing for the surveillance and monitoring of international marine pests. PLoS One 8:e73935CrossRefPubMedCentralPubMedGoogle Scholar
  81. Pohl C (2008) From science to policy through transdisciplinary research. Environ Sci Policy 11:46–53CrossRefGoogle Scholar
  82. Pringle JM, Blakeslee AMH, Byers JE et al (2011) Asymmetric dispersal allows an upstream region to control population structure throughout a species’ range. Proc Natl Acad Sci USA 108:15288–15293CrossRefPubMedCentralPubMedGoogle Scholar
  83. Purcell KM, Ling N, Stockwell CA (2012) Evaluation of the introduction history and genetic diversity of a serially introduced fish population in New Zealand. Biol Invasions 14:2057–2065CrossRefGoogle Scholar
  84. Radulovici AE, Archambault P, Dufresne F (2010) DNA barcodes for marine biodiversity: moving fast forward? Diversity 2:450–472CrossRefGoogle Scholar
  85. Reynolds RG, Fitzpatrick BM (2013) Tests of two methods for identifying founder effects in metapopulations reveal substantial type II error. Genetica 141:119–131CrossRefPubMedGoogle Scholar
  86. Rius M, Turon X, Ordóñez V et al (2012) Tracking invasion histories in the sea: facing complex scenarios using multilocus data. PLoS One 7:e35815CrossRefPubMedCentralPubMedGoogle Scholar
  87. Roman J (2006) Diluting the founder effect: cryptic invasions expand a marine invader’s range. Proc R Soc B Biol Sci 273:2453–2459CrossRefGoogle Scholar
  88. Roman J, Darling JA (2007) Paradox lost: genetic diversity and the success of aquatic invasions. Trends Ecol Evol 22:454–464CrossRefPubMedGoogle Scholar
  89. Shaw JD, Wilson JRU, Richardson DM (2010) Initiating dialogue between scientists and managers of biological invasions. Biol Invasions 12:4077–4083CrossRefGoogle Scholar
  90. Simberloff D (2003) How much information on population biology is needed to manage introduced species? Conserv Biol 17:83–92CrossRefGoogle Scholar
  91. Sunderland T, Sunderland-Groves J, Shanley P et al (2009) Bridging the gap: how can information access and exchange between conservation biologists and field practitioners be improved for better conservation outcomes? Biotropica 41:549–554CrossRefGoogle Scholar
  92. Taylor DR, Keller SR (2007) Historical range expansion determines the phylogenetic diversity introduced during contemporary species invasion. Evolution 61:334–345CrossRefPubMedGoogle Scholar
  93. Tepolt CK, Darling JA, Bagley MJ et al (2009) European green crabs (Carcinus maenas) in the northeastern Pacific: genetic evidence for high population connectivity and current-mediated expansion from a single introduced source population. Divers Distrib 15:997–1009CrossRefGoogle Scholar
  94. Teske PR, Rius M, McQuaid CD et al (2011) “Nested” cryptic diversity in a widespread marine ecosystem engineer: a challenge for detecting biological invasions. BMC Evol Biol 11:176CrossRefPubMedCentralPubMedGoogle Scholar
  95. Thibault I, Bernatchez L, Dodson JJ (2009) The contribution of newly established populations to the dynamics of range expansion in a one-dimensional fluvial-estuarine system: rainbow trout (Oncorhynchus mykiss) in Eastern Quebec. Divers Distrib 15:1060–1072CrossRefGoogle Scholar
  96. Vernesi C, Bruford MW, Bertorelle G et al (2008) Where’s the conservation in conservation genetics? Conserv Biol 22:802–804CrossRefPubMedGoogle Scholar
  97. von der Heydan S, Beger M, Toonen R et al (2014) The application of genetics to marine management and conservation: examples from the Indo-Pacific. Bull Mar Sci 90:123–158CrossRefGoogle Scholar
  98. Webster M (2003) Communicating climate change uncertainty to policy-makers and the public—an editorial comment. Clim Change 61:1–8CrossRefGoogle Scholar
  99. Weed DL (2005) Weight of evidence: a review of concept and methods. Risk Anal 25:1545–1557CrossRefPubMedGoogle Scholar
  100. Wickson F, Carew AL, Russell AW (2006) Transdisciplinary research: characteristics, quandaries and quality. Futures 38:1046–1059CrossRefGoogle Scholar
  101. Zehr SC (2000) Public representations of scientific uncertainty about global climate change. Public Underst Sci 9:85–103CrossRefGoogle Scholar
  102. Zhan AB, Hulak M, Sylvester F et al (2013) High sensitivity of 454 pyrosequencing for detection of rare species in aquatic communities. Methods Ecol Evol 4:558–565CrossRefGoogle Scholar
  103. Zhou X, Li Y, Liu S et al (2013) Ultra-deep sequencing enables high-fidelity recovery of biodiversity for bulk arthropod samples without PCR amplification. Gigascience 2:1–12CrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland (outside the USA) 2014

Authors and Affiliations

  1. 1.National Exposure Research LaboratoryUnited States Environmental Protection AgencyDurhamUSA

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