Human disturbance causes the formation of a hybrid swarm between two naturally sympatric fish species

Molecular Ecology

Volumn 23, Issue 5, 2014, Pages 1137-1152

  Hasselman, Daniel J ^a   Argo, Emily E ^a   McBride, Meghan C ^b   Bentzen, Paul ^b   Schultz, Thomas F ^c   Perez Umphrey, Anna A ^c   Palkovacs, Eric P ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b DALHOUSIE UNIVERSITY   (Canada)

^c DUKE UNIVERSITY MARINE LABORATORY   (United States)

Author keywords

Alosa; anadromous; hybrid swarm; hybridization; introgression; landlocked

Indexed keywords

ALOSA; ALOSA AESTIVALIS; ALOSA PSEUDOHARENGUS; CLUPEIDAE;

MICROSATELLITE DNA;

ALOSA; ANADROMOUS; ANIMAL; ARTICLE; BAYES THEOREM; BIOLOGICAL MODEL; CLUSTER ANALYSIS; DNA SEQUENCE; ECOSYSTEM; FISH; GENETICS; GENOTYPING TECHNIQUE; HUMAN; HYBRID; HYBRIDIZATION; INTROGRESSION; LANDLOCKED; NORTH AMERICA; POPULATION GENETICS; SYMPATRY;

ALOSA; ANADROMOUS; HYBRID SWARM; HYBRIDIZATION; INTROGRESSION; LANDLOCKED;

ANIMALS; BAYES THEOREM; CLUSTER ANALYSIS; ECOSYSTEM; FISHES; GENETICS, POPULATION; GENOTYPING TECHNIQUES; HUMANS; HYBRIDIZATION, GENETIC; MICROSATELLITE REPEATS; MODELS, GENETIC; NORTH AMERICA; SEQUENCE ANALYSIS, DNA; SYMPATRY;

EID: 84896699539     PISSN: 09621083     EISSN: 1365294X     Source Type: Journal    
DOI: 10.1111/mec.12674     Document Type: Article

References (87)

1. A'Hara SW, Amouroux P, Argo EE, et al,. (2012) Permanent genetic resources added to Molecular Ecology Resources Database 1(August), pp. 2011-30, September 2011. Molecular Ecology Resources, 12, 185-189.
2. Alexandrino P, Faria R, Linhares D, et al,. (2006) Interspecific differentiation and intraspecific substructure in to closely related clupeids with extensive hybridization. Journal of Fish Biology, 69 (Supplement B), 242-259.
3. Allendorf FW, Leary RF, Spruell P, Wenburg JK, (2001) The problems with hybrids: setting conservation guidelines. Trends in Ecology & Evolution, 16, 613-622.
4. Anderson E, (1948) Hybridization of the habitat. Evolution, 2, 1-9.
5. Anderson EC, Thompson EA, (2002) A model-based method for identifying species hybrids using multilocus genetic data. Genetics, 160, 1217-1229.
6. Atlantic States Marine Fisheries Commission (2012) River herring benchmark stock assessment. Volume 1. Stock Assessment Report No. 12-02 of the Atlantic States Marine Fisheries Commission. Washington, DC.
7. Barton NH, (2001) The role of hybridization in evolution. Molecular Ecology, 10, 551-568.
8. Behm JE, Ives AR, Boughman JW, (2010) Breakdown in postmating isolation and the collapse of a species pair through hybridization. The American Naturalist, 175, 11-26.
9. Belkhir K, Borsa P, Chikhi L, Raufaste N, Bonhomme F, (2004) GENETIX 4.05, logiciel sous Windows TM pour la genetique des populations.
10. Benjamini Y, Hochberg Y, (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. Journal of the Royal Statistical Society Series B, 57, 289-300.
11. Bentzen P, Paterson IG, (2005) Genetic analyses of freshwater and anadromous alewife (Alosa pseudoharengus) populations from the St. Croix River, Maine/New Brunswick. Final Report to Maine Rivers, 3 Wade Street, Augusta, ME 04330.
12. Bentzen P, Leggett WC, Brown GG, (1993) Genetic relationships among the shads (Alosa) revealed by mitochondrial DNA analysis. Journal of Fish Biology, 43, 909-917.
13. Boisneau P, Mennesson-Boisneau C, Guyomard R, (1992) Electrophoretic identity between allis shad, Alosa alosa (L.), and twaite shad, A. fallax (Lacepede). Journal of Fish Biology, 40, 731-738.
14. Buerkle CA, Morris RJ, Asmussen MA, Rieseberg LH, (2000) The likelihood of homoploid hybrid speciation. Heredity, 84 (Pt 4), 441-451.
15. Burgarella C, Lorenzo Z, Jabbour-Zahab R, et al,. (2009) Detection of hybrids in nature: application to oaks (Quercus suber and Q. ilex). Heredity, 102, 442-452.
16. Carnes WC, (1965) Survey and Classification of the Roanoke River Watershed North Carolina. North Carolina Wildlife Resources Commission, Raleigh, North Carolina, 17 p.
17. Chapman R, Patton J, Eleby B, (1994) Comparison of mitochondrial DNA variation in four alosid species as revealed by the total genome, the NADH dehydrogenase I and cytochrome b regions. In: Genetics and Evolution of Aquatic Organisms (ed., Beaumont A,), pp. 29-263. Chapman and Hall, London, UK.
18. Coscia I, Rountree V, King JJ, et al,. (2010) A highly permeable species boundary between two anadromous fishes. Journal of Fish Biology, 77, 1137-1149.
19. Coyne JA, Orr HA, (2004) Speciation. Sinauer Associates, Sunderland, Massachusetts.
20. De León LF, Raeymaekers JAM, Bermingham E, et al,. (2011) Exploring possible human influences on the evolution of Darwin's finches. Evolution, 65, 2258-2272.
21. Echelle AA, Connor PJ, (1989) Geographically extensive genetic introgression after secondary contact between two pupfish species (Cyprinodon, cyprinodontidae). Evolution, 43, 717-727.
22. Ellis D, Vokoun JC, (2009) Earlier spring warming of coastal streams and implications for alewife migration timing. North American Journal of Fisheries Management, 29, 1584-1589.
23. Falush D, Stephens M, Pritchard JK, (2003) Inference of population structure using multilocus genotype data: Linked loci and correlated allele frequencies. Genetics, 164, 1567-1587.
24. Faria R, Weiss S, Alexandrino P, (2006) A molecular phylogenetic perspective on the evolutionary history of Alosa spp. (Clupeidae). Molecular Phylogenetics and Evolution, 40, 298-304.
25. Gilk SE, Wang IA, Hoover CL, et al,. (2004) Outbreeding depression in hybrids between spatially separated pink salmon, Oncorhynchus gorbuscha, populations: marine survival, homing ability, and variability in family size. Environmental Biology of Fishes, 69, 287-297.
26. Gompert Z, Buerkle CA, (2009) A powerful regression-based method for admixture mapping of isolation across the genome of hybrids. Molecular Ecology, 18, 1207-1224.
27. Gompert Z, Buerkle CA, (2010) Introgress: a software package for mapping components of isolation in hybrids. Molecular Ecology Resources, 10, 378-384.
28. Goudet J, (2001) FSTAT, a program to estimate and test gene diversities and fixation indices (version 2.9.3).
29. Gow JL, Peichel CL, Taylor EB, (2006) Contrasting hybridization rates between sympatric three-spined sticklebacks highlight the fragility of reproductive barriers between evolutionarily young species. Molecular Ecology, 15, 739-752.
30. Gow JL, Piechel CL, Taylor EB, (2007) Ecological selection against hybrids in natural populations of sympatric threespine sticklebacks. Journal of Evolutionary Biology, 20, 2173-2180.
31. Guest WC, Drenner R, (1991) Relationship between feeding of blueback herring and the zooplankton community of a Texas reservoir. Hydrobiologia, 209, 1-6.
32. Hall CJ, Jordaan A, Frisk MG, (2011) The historic influence of dams on diadromous fish habitat with a focus on river herring and hydrologic longitudinal connectivity. Landscape Ecology, 26, 95-107.
33. Hall CJ, Jordaan A, Frisk MG, (2012) Centuries of anadromous forage fish loss: consequences for ecosystem connectivity and productivity. BioScience, 62, 723-731.
34. Hasselman DJ, Limburg KE, (2012) Alosine restoration in the 21st century: challenging the status quo. Marine and Coast Fisheries: Dynamics, Management, and Ecosystem Science, 4, 174-187.
35. Hendry AP, Grant PR, Rosemary Grant B, et al,. (2006) Possible human impacts on adaptive radiation: beak size bimodality in Darwin's finches. Proceedings of the Royal Society B-Biological Sciences, 273, 1887-1894.
36. Holm S, (1979) A simple sequentially rejective multiple test procedure. Scandinavian Journal of Statistics, 6, 65-70.
37. Hubbs C, (1955) Hybridization between fish species in nature. Systematic Zoology, 4, 1-20.
38. Jakobsson M, Rosenberg NA, (2007) CLUMPP: a cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinformatics, 23, 1801-1806.
39. Jolly MT, Maitland PS, Genner MJ, (2011) Genetic monitoring of two decades of hybridization between allis shad (Alosa alosa) and twaite shad (Alosa fallax). Conservation Genetics, 12, 1087-1100.
40. Jolly MT, Aprahamian MW, Hawkins SJ, et al,. (2012) Population genetic structure of protected allis shad (Alosa alosa) and twaite shad (Alosa fallax). Marine Biology, 159, 675-687.
41. Jordan DS, Evermann BW, (1896) The fishes of North and Middle America. Bulletin of the US National Museum, 47, 1-1240.
42. Julian SE, Bartron ML, (2007) Microsatellite DNA markers for American shad (Alosa sapidissima) and cross-species amplification within the family Clupeidae. Molecular Ecology Notes, 7, 805-807.
43. Kullback S, Leibler RA, (1951) On information and sufficiency. The Annals of Mathematical Statistics, 22, 79-86.
44. Labbe EM, (2012) Influence of stocking history and geography on the population genetics of alewife (Alosa pseudoharengus) in Maine rivers. M.Sc. Thesis. University of Southern Maine. Portland, ME.
45. Lehman N, Eisenhawer A, Hansen K, et al,. (1991) Introgression of coyote mitochondrial DNA into sympatric North American gray wolf populations. Evolution, 45, 104-119.
46. Lexer C, Welch ME, Durphy JL, Rieseberg LH, (2003) Natural selection for salt tolerance quantitative trait loci (QTLs) in wild sunflower hybrids: implications for the origin of Helianthus paradoxus, a diploid hybrid species. Molecular Ecology, 12, 1225-1235.
47. Limburg KE, Waldman JR, (2009) Dramatic declines in North Atlantic diadromous fishes. BioScience, 59, 955-965.
48. Locke A, Hanson JM, Klassen GJ, et al,. (2003) The damming of the Petitcodiac River: species, populations, and habitats lost. Northeastern Naturalist, 10, 39-54.
49. Loesch JG, (1987) Overview of life history aspects of anadromous alewife and blueback herring in freshwater habitats. American Fisheries Society Symposium, 1, 89-103.
50. Maitland PS, Lyle AA, (2005) Ecology of Allis Shad Alosa alosa and Twaite Shad Alosa fallax in the Solway Firth, Scotland. Hydrobiologia, 534, 205-221.
51. McBride M, (2013) Population structure of river herring (alewife, Alosa pseudoharengus and blueback herring, A. aestivalis) examined using neutral genetic markers. M.Sc. Thesis, Dalhousie University, Halifax, Nova Scotia.
52. McDevitt AD, Mariani S, Hebblewhite M, et al,. (2009) Survival in the Rockies of an endangered hybrid swarm from diverged caribou (Rangifer tarandus) lineages. Molecular Ecology, 18, 665-679.
53. Messieh S, (1977) Population structure and biology of alewife (Alosa pseudoharengus) and blueback herring (A. aestivalis) in the St. John River, NB. Environmental Biology of Fishes, 2, 195-210.
54. Nielsen EE, Bach LA, Kotlicki P, (2006) Hybridlab (version 1.0): a program for generating simulated hybrids from population samples. Molecular Ecology Notes, 6, 971-973.
55. Nolte AW, Gompert Z, Buerkle CA, (2009) Variable patterns of introgression in two sculpin hybrid zones suggest that genomic isolation differs among populations. Molecular Ecology, 18, 2615-2627.
56. Palkovacs EP, Dion KB, Post DM, Caccone A, (2008) Independent evolutionary origins of landlocked alewife populations and rapid parallel evolution of phenotypic traits. Molecular Ecology, 17, 582-597.
57. Palkovacs EP, Hasselman DJ, Argo EE, et al,. (2013) Combining genetic and demographic information to prioritize recovery efforts for anadromous alewife and blueback herring. Evolutionary Applications, 7, 212-226.
58. Prince ED, Barwick DH, (1981) Landlocked blueback herring in two South Carolina reservoirs: reproduction and suitability as stocked prey. North American Journal of Fisheries Management, 1, 41-45.
59. Pritchard JK, Stephens M, Donnelly P, (2000) Inference of population structure using multilocus genotype data. Genetics, 155, 945-959.
60. R Development Core Team (2010) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0, URL http://www.R-project.org.
61. Reyer HU, (2008) Mating with the wrong species can be right. Trends in Ecology & Evolution, 23, 289-292.
62. Rhymer M, Simberloff D, (1996) Extinction by hybridization and introgression. Annual Reviews of Ecology and Systematics, 27, 83-109.
63. Rice WR, (1989) Analyzing tables of statistical tests. Evolution, 43, 223-225.
64. Roca AL, Georgiadis N, O'Brien SJ, (2005) Cytonuclear genomic dissociation in African elephant species. Nature Genetics, 37, 96-100.
65. Rosenberg NA, (2004) DISTRUCT: a program for the graphical display of population structure. Molecular Ecology Notes, 4, 137-138.
66. Rosenfield JA, Todd T, Greil R, (2000) Asymmetric hybridization and introgression between pink salmon and Chinook salmon in the Laurentian Great Lakes. Transactions of the American Fisheries Society, 129, 670-679.
67. Rousset F, (2007) Genepop'007: a complete re-implementation of the genepop software for Windows and Linux. Molecular Ecology Notes, 8, 103-106.
68. Rundle HD, Nosil P, (2005) Ecological speciation. Ecology Letters, 8, 336-352.
69. Rundle HD, Schluter D, (1998) Reinforcement of stickleback mate preferences: sympatry breeds contempt. Evolution, 52, 200-208.
70. Scott WB, Crossman ED, (1973) Freshwater fishes of Canada. J. Fish. Res. Bd. Can. No. 184.
71. Scribner KT, Page KS, Bartron ML, (2001) Hybridization in freshwater fishes: a review and case studies and cytonuclear methods of biological inference. Reviews in Fish Biology and Fisheries, 10, 293-323.
72. Seehausen O, (2006) Conservation: losing biodiversity by reverse speciation. Current Biology, 16, 334-337.
73. Seehausen O, van Alphen J, Witte F, (1997) Cichlid fish diversity threatened by eutrophication that curbs sexual selection. Science, 277, 1808-1811.
74. Seehausen O, Takimoto G, Roy D, Jokela J, (2008) Speciation reversal and biodiversity dynamics with hybridization in changing environments. Molecular Ecology, 17, 30-44.
75. Servedio MR, Noor MAF, (2003) The role of reinforcement in speciation: theory and data. Annual Review of Ecology, Evolution, and Systematics, 34, 339-364.
76. SPSS, Inc. (2004) SYSTAT version 11.0. SPSS, Inc., Chicago, Illinois.
77. Strasburg JL, Rieseberg LH, (2008) Molecular demographic history of the annual sunflowers Helianthus annuus and H. petiolaris-large effective population sizes and rates of long-term gene flow. Evolution, 62, 1936-1950.
78. Taylor EB, Boughman JW, Groenenboom M, et al,. (2006) Speciation in reverse: morphological and genetic evidence of the collapse of a three-spined stickleback (Gasterosteus aculeatus) species pair. Molecular Ecology, 15, 343-355.
79. Todd N, Stedman RM, (1989) Hybridization of ciscoes (Coregonus spp.) in Lake Huron. Canadian Journal of Zoology, 67, 1679-1685.
80. Utter F, (2001) Patterns of subspecific anthropogenic introgression in two salmonid genera. Reviews in Fish Biology and Fisheries, 10, 265-279.
81. Vähä JP, Primmer CR, (2006) Efficiency of model-based Bayesian methods for detecting hybrid individuals under different hybridization scenarios and with different numbers of loci. Molecular Ecology, 15, 63-72.
82. Van Oosterhout C, Hutchinson WF, Wills DPM, Shipley P, (2004) MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Molecular Ecology Notes, 4, 535-538.
83. Vonlanthen P, Bittner D, Hudson AG, et al,. (2012) Eutrophication causes speciation reversal in whitefish adaptive radiations. Nature, 482, 357-362.
84. Walters DM, Blum MJ, Rashleigh B, et al,. (2008) Red shiner invasion and hybridization with blacktail shiner in the upper Coosa River, USA. Biological Invasions, 10, 1229-1242.
85. Waters JM, Epifanio JM, Gunter T, Brown BL, (2000) Homing behaviour facilitates subtle genetic differentiation among river populations of Alosa sapidissima: microsatellites and mtDNA. Journal of Fish Biology, 56, 622-636.
86. Weir BS, Cockerham CC, (1984) Estimating F-statistics for the analysis of population structure. Evolution, 38, 1358-1370.
87. Wiegand K, (1935) A taxonomist's experience with hybrids in the wild. Science, 81, 161-166.