Diagnostic SNPs reveal widespread introgressive hybridization between introduced bighead and silver carp in the Mississippi River Basin

Molecular Ecology

Volumn 24, Issue 15, 2015, Pages 3931-3943

  Lamer, James T ^a,b   Ruebush, Blake C ^c   Arbieva, Zarema H ^d   McClelland, Michael A ^c   Epifanio, John M ^e   Sass, Greg G ^f  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^b WESTERN ILLINOIS UNIVERSITY   (United States)

^c ILLINOIS DEPARTMENT OF NATURAL RESOURCES   (United States)

^d UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

^e UNIVERSITY OF ILLINOIS   (United States)

^f WISCONSIN DEPARTMENT OF NATURAL RESOURCES   (United States)

Author keywords

bighead carp; hybridization; introgression; invasive species; silver carp; SNP

Indexed keywords

HYPOPHTHALMICHTHYS; HYPOPHTHALMICHTHYS NOBILIS;

MITOCHONDRIAL DNA;

ANIMAL; CARP; CYPRINIDAE; DNA SEQUENCE; ECOSYSTEM; GENE FLOW; GENETICS; GENOTYPE; HYBRIDIZATION; INTRODUCED SPECIES; RIVER; SINGLE NUCLEOTIDE POLYMORPHISM; UNITED STATES;

ANIMALS; CARPS; CYPRINIDAE; DNA, MITOCHONDRIAL; ECOSYSTEM; GENE FLOW; GENOTYPE; HYBRIDIZATION, GENETIC; INTRODUCED SPECIES; POLYMORPHISM, SINGLE NUCLEOTIDE; RIVERS; SEQUENCE ANALYSIS, DNA; UNITED STATES;

EID: 84937727623     PISSN: 09621083     EISSN: 1365294X     Source Type: Journal    
DOI: 10.1111/mec.13285     Document Type: Article

References (63)

1. Abbott R, Albach D, Ansell S, et al,. (2013) Hybridization and speciation. Journal of Evolutionary Biology, 26, 229-246.
2. Aboim MA, MaváRez J, Bernatchez L, Coelho MM, (2010) Introgressive hybridization between two Iberian endemic cyprinid fish: A comparison between two independent hybrid zones. Journal of Evolutionary Biology, 23, 817-828.
3. Allendorf FW, Luikart G, (2007) Conservation and the genetics of populations. Blackwell Pub, Malden, MA, Oxford.
4. Amberg JJ, Schreier TM, Gaikowski MP, (2012) Molecular responses differ between sensitive silver carp and tolerant bighead carp and bigmouth buffalo exposed to rotenone. Fish Physiology and Biochemistry, 38, 1379-1391.
5. Anderson EC, Thompson EA, (2002) A model-based method for identifying species hybrids using multilocus genetic data. Genetics, 160, 1217-1229.
6. Arnold ML, Martin NH, (2010) Hybrid fitness across time and habitats. Trends in Ecology & Evolution, 25, 530-536.
7. Arnold ML, Sapir Y, Martin NH, (2008) Genetic exchange and the origin of adaptations: prokaryotes to primates. Philosophical Transactions of the Royal Society B: Biological Sciences, 363, 2813-2820.
8. Baskett ML, Gomulkiewicz R, (2011) Introgressive hybridization as a mechanism for species rescue. Theoretical Ecology, 4, 223-239.
9. Bierne N, David P, Langlade A, Bonhomme F, (2002) Can habitat specialisation maintain a mosaic hybrid zone in marine bivalves? Marine Ecology Progress Series, 245, 157-170.
10. Broughton RE, Vedala KC, Crowl TM, Ritterhouse LL, (2011) Current and historical hybridization with differential introgression among three species of cyprinid fishes (genus Cyprinella). Genetica, 139, 699-707.
11. Brummett RE, Smitherman RO, Dunham RA, (1988) Isozyme expression in bighead carp, silver carp and their reciprocal hybrids. Aquaculture, 70, 21-28.
12. Burke JM, Arnold ML, (2001) Genetics and the fitness of hybrids. Annual Review of Genetics, 35, 31-52.
13. Costedoat C, Pech N, Chappaz R, Gilles A, (2007) Novelties in hybrid zones: crossroads between population genomic and ecological approaches. PLoS ONE, 2, e357.
14. Crespin L, Berrebi P, Lebreton J-D, (2002) Spatially varying natural selection in a fish hybrid zone. Journal of Fish Biology, 61, 696-711.
15. DeGrandchamp KL, Garvey JE, Colombo RE, (2008) Movement and habitat selection by invasive Asian carps in a large river. Transactions of the American Fisheries Society, 137, 45-56.
16. Deredec A, Courchamp F, (2007) Importance of the Allee effect for reintroductions. Ecoscience, 14, 440-451.
17. Dowling TE, Secor CL, (1997) The role of hybridization and introgression in the diversification of animals. Annual Review of Ecology and Systematics, 28, 593-619.
18. Ellstrand NC, Schierenbeck KA, (2000) Hybridization as a stimulus for the evolution of invasiveness in plants? Proceedings of the National Academy of Sciences, 97, 7043-7050.
19. Farrington HL, Edwards CE, Guan X, Carr MR, Baerwaldt K, Lance RF, (2015) Mitochondrial Genome Sequencing and Development of Genetic Markers for the Detection of DNA of Invasive Bighead and Silver Carp (Hypophthalmichthys nobilis and H. molitrix) in Environmental Water Samples from the United States. PLoS ONE, 10, e0117803.
20. Freeze M, Henderson S, (1982) Distribution and status of the bighead carp and silver carp in Arkansas. North American journal of fisheries management, 2, 197-200.
21. Green BW, Smitherman RO, (1984) Relative growth, survival and harvestability of bighead carp, silver carp, and their reciprocal hybrids. Aquaculture, 37, 87-95.
22. Harrison RG, (ed.) (1993) Hybrid zones and the evolutionary process. Oxford University Press, New York.
23. Hasselman DJ, Argo EE, McBride MC, et al,. (2014) Human disturbance causes the formation of a hybrid swarm between two naturally sympatric fish species. Molecular Ecology, 23, 1137-1152.
24. Haynes GD, Gongora J, Gilligan DM, et al,. (2012) Cryptic hybridization and introgression between invasive Cyprinid species Cyprinus carpio and Carassius auratus in Australia: implications for invasive species management: hybridization between Cyprinid species (D Reed, Ed,). Animal Conservation, 15, 83-94.
25. Hubbs CL, (1955) Hybridization between fish species in nature. Systematic Zoology, 4, 1-20.
26. Hulata G, (2001) Genetic manipulations in aquaculture: A review of stock improvement by classical and modern technologies. Genetica, 111, 155-173.
27. Irons KS, Sass GG, McClelland MA, Stafford JD, (2007) Reduced condition factor of two native fish species coincident with invasion of non-native Asian carps in the Illinois River, U.S.A. Is this evidence for competition and reduced fitness? Journal of Fish Biology, 71, 258-273.
28. Issa MA, Horvath L, Kosba MA, Sharvabi M, (1986) A note on the survival, growth, feed conversion and some morphological characters of the reciprocal hybrids of silver carp (Hypophthalmichthys molitrix Val.) and bighead carp (Aristichthys nobilis Rich.) raised in polyculture. Aquacultura Hungarica, 5, 7-14.
29. Jerde CL, Mahon AR, Chadderton WL, Lodge DM, (2011) "Sight-unseen" detection of rare aquatic species using environmental DNA. Conservation Letters, 4, 150-157.
30. Jerde CL, Chadderton WL, Mahon AR, et al,. (2013) Detection of Asian carp DNA as part of a Great Lakes basin-wide surveillance program. Canadian Journal of Fisheries and Aquatic Sciences, 70, 522-526.
31. Jiggins CD, Mallet J, (2000) Bimodal hybrid zones and speciation. Trends in Ecology & Evolution, 15, 250-255.
32. Junk WJ, Bayley PB, Sparks RE, (1989) The flood pulse concept in river-floodplain systems. Canadian Special Publication of Fisheries and Aquatic Sciences, 106, 110-127.
33. King TL, Eackles MS, Chapman DC, (2011) Tools for assessing kinship, population structure, phylogeography, and interspecific hybridization in Asian carps invasive to the Mississippi River, USA: isolation and characterization of novel tetranucleotide microsatellite DNA loci in silver carp Hypophthalmichthys molitrix. Conservation Genetics Resources, 3, 397-401.
34. Kolar CS, Chapman DC, Courtenay WR Jr, et al. (eds.) (2007) Bigheaded carps: A biological synopsis and environmental risk assessment. American Fisheries Society, Bethesda, Maryland.
35. Lamer JT, Dolan CR, Petersen JL, Chick JH, Epifanio JM, (2010) Introgressive hybridization between bighead carp and silver carp in the Mississippi and Illinois rivers. North American Journal of Fisheries Management, 30, 1452-1461.
36. Lamer JT, Sass GG, Boone JQ, et al,. (2014) Restriction site-associated DNA sequencing generates high-quality single nucleotide polymorphisms for assessing hybridization between bighead and silver carp in the United States and China. Molecular Ecology Resources, 14, 79-86.
37. Leary RF, Allendorf FW, Sage GK, (1995) Hybridization and introgression between introduced and native fish. American Fisheries Society symposium, 15, 91-101.
38. Maheshwari S, Barbash DA, (2011) The genetics of hybrid incompatibilities. Annual Review of Genetics, 45, 331-355.
39. Mallet J, (2005) Hybridization as an invasion of the genome. Trends in Ecology & Evolution, 20, 229-237.
40. Marian T, Krasznai Z, Olah J, (1986) Characteristic karyological, biochemical and morphological markers of silver carp (Hypophthalmichthys molitrix Val.), bighead carp (Aristichthys nobilis Rich.) and their hybrids. Aquacultura Hungarica, 5, 15-30.
41. Mia MY, Taggart JB, Gilmour AE, et al,. (2005) Detection of hybridization between Chinese carp species (Hypophthalmichthys molitrix and Aristichthys nobilis) in hatchery broodstock in Bangladesh, using DNA microsatellite loci. Aquaculture, 247, 267-273.
42. Palumbi SR, (2009) Speciation and the evolution of gamete recognition genes: pattern and process. Heredity, 102, 66-76.
43. Pegg MA, Chick JH, (2001) Invasive carp in the Mississippi River Basin. Science, 492, 2250-2251.
44. Peters LM, Pegg MA, Reinhardt UG, (2006) Movements of adult radio-tagged bighead carp in the Illinois River. Transactions of the American Fisheries Society, 135, 1205-1212.
45. Prentis PJ, Wilson JRU, Dormontt EE, Richardson DM, Lowe AJ, (2008) Adaptive evolution in invasive species. Trends in Plant Science, 13, 288-294.
46. Rahel FJ, (2002) Homogenization of freshwater faunas. Annual Review of Ecology & Systematics, 33, 291.
47. Rogers SM, Bernatchez L, (2006) The genetic basis of intrinsic and extrinsic post-zygotic reproductive isolation jointly promoting speciation in the lake whitefish species complex (Coregonus clupeaformis). Journal of Evolutionary Biology, 19, 1979-1994.
48. Ryan MT, Hoogenraad NJ, (2007) Mitochondrial-nuclear communications. Annual Review of Biochemistry, 76, 701-722.
49. Sampson SJ, Chick JH, Pegg MA, (2009) Diet overlap among two Asian carp and three native fishes in backwater lakes on the Illinois and Mississippi rivers. Biological Invasions, 11, 483-496.
50. Sass GG, Cook TR, Irons KS, et al,. (2010) A mark-recapture population estimate for invasive silver carp (Hypophthalmichthys molitrix) in the La Grange Reach, Illinois River. Biological Invasions, 12, 433-436.
51. Sass GG, Hinz C, Erickson AC, et al,. (2014) Invasive bighead and silver carp effects on zooplankton communities in the Illinois River, Illinois, USA. Journal of Great Lakes Research, 40, 911-921.
52. Schrank SJ, Guy CS, (2002) Age, growth, and gonadal characteristics of adult bighead carp, Hypophthalmichthys nobilis, in the Lower Missouri River. Environmental Biology of Fishes, 64, 443-450.
53. Schwenk K, Brede N, Streit B, (2008) Introduction. Extent, processes and evolutionary impact of interspecific hybridization in animals. Philosophical Transactions of the Royal Society B: Biological Sciences, 363, 2805-2811.
54. Scribner KT, Page KS, Bartron ML, (2001) Hybridization in freshwater fishes: A review of case studies and cytonuclear methods of biological inference. Reviews in Fish Biology and Fisheries, 10, 293-323.
55. Seehausen O, (2004) Hybridization and adaptive radiation. Trends in Ecology & Evolution, 19, 198-207.
56. Seehausen O, Takimoto G, Roy D, Jokela J, (2008) Speciation reversal and biodiversity dynamics with hybridization in changing environments. Molecular Ecology, 17, 30-44.
57. Stephens MR, Clipperton NW, May B, (2009) Subspecies-informative SNP assays for evaluating introgression between native golden trout and introduced rainbow trout. Molecular Ecology Resources, 9, 339-343.
58. Twyford AD, Ennos RA, (2012) Next-generation hybridization and introgression. Heredity, 108, 179-189.
59. Vignal A, Milan D, SanCristobal M, Eggen A, (2002) A review on SNP and other types of molecular markers and their use in animal genetics. Genetics Selection Evolution, 34, 275-305.
60. Voropaev HV, (1978) Biology and Fishery Importance of Hybrids Between Bighead and Silver Carp. Szarvas Fishery Research Institute, Szarvas, Hungary.
61. Wiley C, Qvarnström A, Andersson G, Borge T, Saetre G-P, (2009) Postzygotic isolation over multiple generations of hybrid descendants in a natural hybrid zone: how well do single-generation estimates reflect reproductive isolation? Evolution, 63, 1731-1739.
62. Yan A, (1994) Reproduction. In: Developments in Aquaculture and Fisheries Science; Freshwater fish culture in China: Principles and practice (eds, Li S, Mathias J,), pp. 51-78. Huazhong Agricultural University, Wuhan, Hubei Province, China.
63. Zhang X, (1994) Genetics and breeding. In: Developments in Aquaculture and Fisheries Science; Freshwater fish Culture in China: Principles and Practice (eds, Li S, Mathias J,), pp. 129-162. Changjiang Fisheries Research Institute, Shashi, Hubei Province, China.