Gene flow, effective population size and selection at major histocompatibility complex genes: brown trout in the Hardanger Fjord, Norway
Brown trout populations in the Hardanger Fjord, Norway, have declined drastically due to increased exposure to salmon lice from salmonid aquaculture. We studied contemporary samples from seven populations and historical samples (1972 and 1983) from the two largest populations, one of which has decli...
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Published in | Molecular ecology Vol. 16; no. 7; pp. 1413 - 1425 |
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Main Authors | , , , , |
Format | Journal Article |
Language | English |
Published |
Oxford, UK
Blackwell Publishing Ltd
01.04.2007
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Subjects | |
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Abstract | Brown trout populations in the Hardanger Fjord, Norway, have declined drastically due to increased exposure to salmon lice from salmonid aquaculture. We studied contemporary samples from seven populations and historical samples (1972 and 1983) from the two largest populations, one of which has declined drastically whereas the other remains stable. We analysed 11 microsatellite loci, including one tightly linked to the UBA gene of the major histocompatibility class I complex (MHC) and another locus linked to the TAP2A gene, also associated with MHC. The results revealed asymmetric gene flow from the two largest populations to the other, smaller populations. This has important conservation implications, and we predict that possible future population recoveries will be mediated primarily by the remaining large population. Tests for selection suggested diversifying selection at UBA, whereas evidence was inconclusive for TAP2A. There was no evidence for temporally fluctuating selection. We assessed the distribution of adaptive divergence among populations. The results showed the most pronounced footprints of selection between the two largest populations subject to the least immigration. We suggest that asymmetric gene flow has an important influence on adaptive divergence and constrains local adaptive responses in the smaller populations. Even though UBA alleles may not affect salmon louse resistance, the results bear evidence of adaptive divergence among populations at immune system genes. This suggests that similar genetic differences could exist at salmon louse resistance loci, thus rendering it a realistic scenario that differential population declines could reflect differences in adaptive variation. |
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AbstractList | Brown trout populations in the Hardanger Fjord, Norway, have declined drastically due to increased exposure to salmon lice from salmonid aquaculture. We studied contemporary samples from seven populations and historical samples (1972 and 1983) from the two largest populations, one of which has declined drastically whereas the other remains stable. We analysed 11 microsatellite loci, including one tightly linked to the UBA gene of the major histocompatibility class I complex (MHC) and another locus linked to the TAP2A gene, also associated with MHC. The results revealed asymmetric gene flow from the two largest populations to the other, smaller populations. This has important conservation implications, and we predict that possible future population recoveries will be mediated primarily by the remaining large population. Tests for selection suggested diversifying selection at UBA, whereas evidence was inconclusive for TAP2A. There was no evidence for temporally fluctuating selection. We assessed the distribution of adaptive divergence among populations. The results showed the most pronounced footprints of selection between the two largest populations subject to the least immigration. We suggest that asymmetric gene flow has an important influence on adaptive divergence and constrains local adaptive responses in the smaller populations. Even though UBA alleles may not affect salmon louse resistance, the results bear evidence of adaptive divergence among populations at immune system genes. This suggests that similar genetic differences could exist at salmon louse resistance loci, thus rendering it a realistic scenario that differential population declines could reflect differences in adaptive variation.Brown trout populations in the Hardanger Fjord, Norway, have declined drastically due to increased exposure to salmon lice from salmonid aquaculture. We studied contemporary samples from seven populations and historical samples (1972 and 1983) from the two largest populations, one of which has declined drastically whereas the other remains stable. We analysed 11 microsatellite loci, including one tightly linked to the UBA gene of the major histocompatibility class I complex (MHC) and another locus linked to the TAP2A gene, also associated with MHC. The results revealed asymmetric gene flow from the two largest populations to the other, smaller populations. This has important conservation implications, and we predict that possible future population recoveries will be mediated primarily by the remaining large population. Tests for selection suggested diversifying selection at UBA, whereas evidence was inconclusive for TAP2A. There was no evidence for temporally fluctuating selection. We assessed the distribution of adaptive divergence among populations. The results showed the most pronounced footprints of selection between the two largest populations subject to the least immigration. We suggest that asymmetric gene flow has an important influence on adaptive divergence and constrains local adaptive responses in the smaller populations. Even though UBA alleles may not affect salmon louse resistance, the results bear evidence of adaptive divergence among populations at immune system genes. This suggests that similar genetic differences could exist at salmon louse resistance loci, thus rendering it a realistic scenario that differential population declines could reflect differences in adaptive variation. Brown trout populations in the Hardanger Fjord, Norway, have declined drastically due to increased exposure to salmon lice from salmonid aquaculture. We studied contemporary samples from seven populations and historical samples (1972 and 1983) from the two largest populations, one of which has declined drastically whereas the other remains stable. We analysed 11 microsatellite loci, including one tightly linked to the UBA gene of the major histocompatibility class I complex (MHC) and another locus linked to the TAP2A gene, also associated with MHC. The results revealed asymmetric gene flow from the two largest populations to the other, smaller populations. This has important conservation implications, and we predict that possible future population recoveries will be mediated primarily by the remaining large population. Tests for selection suggested diversifying selection at UBA, whereas evidence was inconclusive for TAP2A. There was no evidence for temporally fluctuating selection. We assessed the distribution of adaptive divergence among populations. The results showed the most pronounced footprints of selection between the two largest populations subject to the least immigration. We suggest that asymmetric gene flow has an important influence on adaptive divergence and constrains local adaptive responses in the smaller populations. Even though UBA alleles may not affect salmon louse resistance, the results bear evidence of adaptive divergence among populations at immune system genes. This suggests that similar genetic differences could exist at salmon louse resistance loci, thus rendering it a realistic scenario that differential population declines could reflect differences in adaptive variation. Brown trout populations in the Hardanger Fjord, Norway, have declined drastically due to increased exposure to salmon lice from salmonid aquaculture. We studied contemporary samples from seven populations and historical samples (1972 and 1983) from the two largest populations, one of which has declined drastically whereas the other remains stable. We analysed 11 microsatellite loci, including one tightly linked to the UBA gene of the major histocompatibility class I complex (MHC) and another locus linked to the TAP2A gene, also associated with MHC. The results revealed asymmetric gene flow from the two largest populations to the other, smaller populations. This has important conservation implications, and we predict that possible future population recoveries will be mediated primarily by the remaining large population. Tests for selection suggested diversifying selection at UBA, whereas evidence was inconclusive for TAP2A. There was no evidence for temporally fluctuating selection. We assessed the distribution of adaptive divergence among populations. The results showed the most pronounced footprints of selection between the two largest populations subject to the least immigration. We suggest that asymmetric gene flow has an important influence on adaptive divergence and constrains local adaptive responses in the smaller populations. Even though UBA alleles may not affect salmon louse resistance, the results bear evidence of adaptive divergence among populations at immune system genes. This suggests that similar genetic differences could exist at salmon louse resistance loci, thus rendering it a realistic scenario that differential population declines could reflect differences in adaptive variation. [PUBLICATION ABSTRACT] |
Author | HANSEN, MICHAEL M. JENSEN, LASSE FAST SKAALA, ØYSTEIN BEKKEVOLD, DORTE MENSBERG, KAREN-LISE D. |
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BackLink | https://www.ncbi.nlm.nih.gov/pubmed/17391266$$D View this record in MEDLINE/PubMed |
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Molecular Ecology, 13, 67-80. Slettan A, Olsaker I, Lie Ø (1996) Atlantic salmon, Salmo salar, microsatellites at the SSOSL438, SSOSL439 and SSOSL444 loci. Animal Genetics, 27, 57-64. Palm S, Laikre L, Jorde PE, Ryman N (2003) Effective population size and temporal genetic change in stream resident brown trout (Salmo trutta L.). Conservation Genetics, 4, 249-264. 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. Laikre L, Järvi T, Johansson L, Palm S, Rubin J-F, Glimsäter CE, Landergren P, Ryman N (2002) Spatial and temporal population structure of sea trout (Salmo trutta) at the island of Gotland, Sweden, delineated from mitochondrial DNA. Journal of Fish Biology, 60, 49-71. Guo SW, Thompson EA (1992) Performing the exact test for Hardy-Weinberg proportion for multiple alleles. Biometrics, 48, 361-372. 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Otterå H, Skilbrei O, Skaala Ø, Boxaspen K, Aure J, Taranger GL, Ervik A, Borgstrøm R (2004) The Hardanger Fjord - Salmonid Aquaculture and Effects on Wild Salmonid Populations. Report from the Institute of Marine Research, Bergen, Norway. (In Norwegian.) Nielsen EE, Hansen MM, Meldrup D (2006) Evidence of microsatellite hitch-hiking selection in Atlantic cod (Gadus morhua L.): implications for inferring population structure in nonmodel organisms. Molecular Ecology, 15, 3219-3229. Abdo ZAID, Crandall KA, Joyce PAUL (2004) Evaluating the performance of likelihood methods for detecting population structure and migration. Molecular Ecology, 13, 837-851. Miller KM, Kaukinen KH, Beacham TD, Withler RE (2001) Geographic heterogeneity in natural selection on an MHC locus in sockeye salmon. Genetica, 111, 237-257. Taylor EB (1991) A review of local adaptation in Salmonidae, with particular reference to Pacific and Atlantic salmon. Aquaculture, 98, 185-207. Schlötterer C (2002) A microsatellite-based multilocus screen for the identification of local selective sweeps. Genetics, 160, 753-763. Beerli P, Felsenstein J (2001) Maximum likelihood estimation of a migration matrix and effective population size in n subpopulations by using a coalescent approach. Proceedings of the National Academy of Sciences, USA, 98, 4563-4568. Manier MK, Arnold SJ (2005) Population genetic analysis identifies source-sink dynamics for two sympatric garter snake species (Thamnophis elegans and Thamnophis sirtalis). Molecular Ecology, 14, 3965-3976. Dias PC (1996) Sources and sinks in population biology. Trends in Ecology & Evolution, 11, 326-330. Vasemägi A, Nilsson J, Primmer CR (2005a) Expressed sequence tag-linked microsatellites as a source of gene-associated polymorphisms for detecting signatures of divergent selection in Atlantic salmon (Salmo salar L.). Molecular Biology and Evolution, 22, 1067-1076. Goudet J, Raymond M, DeMeeus T, Rousset F (1996) Testing differentiation in diploid populations. Genetics, 144, 1933-1940. Grimholt U, Drablos F, Jorgensen SM, Hoyheim B, Stet RJM (2002) The major histocompatibility class I locus in Atlantic salmon (Salmo salar L.): polymorphism, linkage analysis and protein modelling. Immunogenetics, 54, 570-581. Estoup A, Largiader CR, Perrot E, Chourrout D (1996) Rapid one-tube DNA extraction for reliable PCR detection of fish polymorphic markers and transgenes. Molecular Marine Biology and Biotechnology, 5, 295-298. Beaumont MA, Nichols RA (1996) Evaluating loci for use in the genetic analysis of population structure. Proceedings of the Royal Society of London. Series B, Biological Sciences, 263, 1619-1626. Grimholt U (1997) Transport-associated proteins in Atlantic salmon (Salmo salar). Immunogenetics, 46, 213-221. Bernatchez L, Landry C (2003) MHC studies in nonmodel vertebrates: what have we learned about natural selection in 15 years? Journal of Evolutionary Biology, 16, 363-377. El Mousadik A, Petit RJ (1996) High level of genetic differentiation for allelic richness among populations of the argan tree [Argania spinosa (L.) Skeels] endemic to Morocco. Theoretical and Applied Genetics, 92, 832-839. Wright (1931) Evolution in Mendelian populations. Genetics, 16, 97-159. Langefors AH (2005) Adaptive and neutral genetic variation and colonization history of 1931; 16 2004; 61 1989; 43 1991; 98 2002; 56 1997; 46 2002; 54 2002; 11 2004; 4 2003; 16 1996; 144 2005b; 6 2002; 60 1996; 263 1997; 6 2003; 12 2006; 60 2001 2006; 21 1993; 71 1995; 26 1997; 145 2005; 74 1999; 173 2003; 4 1999; 53 1992; 48 1996; 5 1996; 27 1998; 55 2003; 165 2001; 98 2001; 10 2003; 163 1995; 52 2006; 96 2006; 15 1996 2004 1996; 92 2006; 313 1996; 53 1996; 11 1995; 86 2001; 111 2002; 160 2005a; 22 1977; 58 1984; 38 2004; 17 2004; 58 2004; 13 2005; 95 2005; 6 1998; 7 2005; 59 2003; 60 1999; 119 2005; 14 e_1_2_7_5_1 e_1_2_7_3_1 e_1_2_7_9_1 e_1_2_7_7_1 e_1_2_7_19_1 e_1_2_7_60_1 e_1_2_7_17_1 e_1_2_7_62_1 e_1_2_7_15_1 e_1_2_7_41_1 e_1_2_7_64_1 e_1_2_7_13_1 e_1_2_7_43_1 e_1_2_7_66_1 e_1_2_7_11_1 e_1_2_7_45_1 e_1_2_7_68_1 e_1_2_7_47_1 e_1_2_7_26_1 e_1_2_7_49_1 e_1_2_7_28_1 Young FW (e_1_2_7_69_1) 1996 e_1_2_7_50_1 e_1_2_7_25_1 e_1_2_7_31_1 e_1_2_7_52_1 e_1_2_7_23_1 e_1_2_7_33_1 e_1_2_7_54_1 e_1_2_7_21_1 e_1_2_7_35_1 e_1_2_7_56_1 e_1_2_7_37_1 e_1_2_7_58_1 e_1_2_7_39_1 e_1_2_7_4_1 e_1_2_7_8_1 e_1_2_7_16_1 e_1_2_7_40_1 e_1_2_7_61_1 e_1_2_7_2_1 e_1_2_7_14_1 e_1_2_7_42_1 e_1_2_7_63_1 Fraser DJ (e_1_2_7_20_1) 2005; 59 e_1_2_7_12_1 e_1_2_7_44_1 e_1_2_7_65_1 e_1_2_7_10_1 e_1_2_7_67_1 e_1_2_7_48_1 e_1_2_7_27_1 Hendry AP (e_1_2_7_32_1) 2004 e_1_2_7_29_1 Otterå H (e_1_2_7_46_1) 2004 Kauer MO (e_1_2_7_36_1) 2003; 165 e_1_2_7_51_1 e_1_2_7_70_1 e_1_2_7_30_1 e_1_2_7_53_1 Skurdal J (e_1_2_7_55_1) 2001 Estoup A (e_1_2_7_18_1) 1996; 5 e_1_2_7_24_1 Bakke TA (e_1_2_7_6_1) 1998; 55 e_1_2_7_22_1 e_1_2_7_34_1 e_1_2_7_57_1 e_1_2_7_59_1 e_1_2_7_38_1 |
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Snippet | Brown trout populations in the Hardanger Fjord, Norway, have declined drastically due to increased exposure to salmon lice from salmonid aquaculture. We... |
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SubjectTerms | Adaptation alleles Animal populations Animals Aquaculture Aquatic ecosystems asymmetric gene flow Bayes Theorem Conservation of Natural Resources Deoxyribonucleic acid DNA Fish populations Fjords Freshwater Gene flow Gene Flow - genetics Gene loci Genetic Variation genetics Genetics, Population history Immune system immunology Lepeophtheirus salmonis local adaptation loci major histocompatibility complex Major Histocompatibility Complex - genetics MHC microsatellite DNA microsatellite repeats Microsatellite Repeats - genetics Norway Population decline Population Density population dynamics Population number population size prediction rescue effects Salmo trutta Salmon Salmonidae selection tests Selection, Genetic Trout Trout - genetics Trout - immunology Ursidae |
Title | Gene flow, effective population size and selection at major histocompatibility complex genes: brown trout in the Hardanger Fjord, Norway |
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