Genetically based population divergence in overwintering energy mobilization in brook charr (Salvelinus fontinalis)

Genetica

Volumn 141, Issue 1-3, 2013, Pages 51-64

  Crespel, Amélie ^a   Bernatchez, Louis ^b   Garant, Dany ^c   Audet, Céline ^a  

^a INSTITUT DES SCIENCES DE LA MER DE RIMOUSKI   (Canada)

^b UNIVERSITÉ LAVAL   (Canada)

^c UNIVERSITÉ DE SHERBROOKE   (Canada)

Author keywords

Energy mobilization strategy; Fish physiology; Genetic and phenotypic correlation; Heritability; Local adaptation; Non additive effects

Indexed keywords

SALVELINUS FONTINALIS;

EID: 84875639068     PISSN: 00166707     EISSN: None     Source Type: Journal    
DOI: 10.1007/s10709-013-9705-x     Document Type: Article

References (81)

1. Altwegg R, Dummermuth S, Anholt BR, Flatt T (2005) Winter weather affects asp viper Vipera aspis population dynamics through susceptible juveniles. Oikos 110: 55-66.
2. Bieri J, Kawecki TJ (2003) Genetic architecture of differences between populations of cowpea weevil (Callosobruchus maculatus) evolved in the same environment. Evolution 57: 274-287.
3. Billerbeck JM, Lankford TE, Conover DO (2001) Evolution of intrinsic growth and energy acquisition rates. I. Trade-offs with swimming performance in Menidia menidia. Evolution 55: 1863-1872.
4. Bjorklund M, Ranta E, Kaitala V, Bach LA, Lunderberg P et al (2009) Quantitative trait evolution and environmental change. PLoS ONE 4: e4521. doi: 10. 1371.
5. Bougas B, Granier S, Audet C, Bernatchez L (2010) The transcriptional landscape of cross-specific hybrids and its possible link with growth in brook charr (Salvelinus fontinalis Mitchill). Genetics 186: 97-107. doi: 10. 1534/genetics. 110. 118158.
6. Boutilier RG, Donohoe PH, Tattersall GJ, West TG (1997) Hypometabolic homeostasis in overwintering aquatic amphibians. J Exp Biol 200: 387-400.
7. Box J, Lill A, Baldwin J (2010) Is there seasonal variation in stored energy reserves and catabolic enzyme activities in Superb fairy-wrens? Avian Biol Res 3: 107-114.
8. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein dye binding. Anal Biochem 72: 248-254.
9. Bryden CA, Heath JW, Heath DD (2004) Performance and heterosis in farmed and wild Chinook salmon (Oncorhynchus tshawyacha) hybrid and purebred crosses. Aquaculture 235: 249-261. doi: 10. 1016/j. aquaculture. 2004. 01. 027.
10. Cargnelli LM, Gross MR (1997) Fish energetics: larger individuals emerge from winter in better condition. Trans Am Fish Soc 126: 153-156.
11. Carr RS, Neff JM (1984) Quantitative semi-automated enzymatic assay for tissue glycogen. Comp Biochem Physiol 77B: 447-449.
12. Charmantier A, Kruuk LEB, Blondel J, Lambrechts MM (2004) Testing for microevolution in body size in three blue tit populations. J Evol Biol 17: 732-743. doi: 10. 1111/j. 1420-9101. 2004. 00734. x.
13. Child AR, Laing I (1998) Comparative low temperature tolerance of small juvenile European, Ostrea edulis L., and Pacific oysters, Crassostrea gigas Thunberg. Aquac Res 29: 103-113.
14. Collins AL, Anderson TA (1995) The regulation of endogeneous energy stores during starvation and refeeding in the somatic tissues of the golden perch. J Fish Biol 47: 1004-1015.
15. Cooke SJ, Kassler TW, Phillipp DP (2001) Physiological performance of largemouth bass related to local adaptation and interstock hybridization: implications for conservation and management. J Fish Biol 59: 248-268. doi: 10. 1111/j. 1095-8649. 2001. tb01389. x.
16. Crespel A, Bernatchez L, Audet C, Garant D (2013) Population specific gene-environment interactions and evolutionary potential for growth in brook charr (Salvelinus fontinalis). G3 Genes Genomes Genet 3. doi: 10. 1534/g3. 112. 005017.
17. Crespel A, Bernatchez L, Garant D, Audet C (2011) Quantitative genetic analysis of the physiological stress response in three strains of brook charr Salvelinus fontinalis and their hybrids. J Fish Biol 79: 2019-2033. doi: 10. 1111/j. 1095-8649. 2011. 03149. x.
18. Eckmann R (2004) Overwinter changes in mass and lipid content of Perca fluviatilis and Gymnocephalus cernuus. J Fish Biol 65: 1498-1511. doi: 10. 1111/j. 1095-8649. 2004. 00553. x.
19. Edmands S (1999) Heterosis and outbreeding depression in interpopulation crosses spanning a wide range of divergence. Evolution 53: 1757-1768.
20. Emlen JM (1991) Heterosis and outbreeding depression-a multilocus model and an application to salmon production. Fish Res 12: 187-212.
21. Falconer DS, Mackay TFC (1996) Introduction to quantitative genetics. Longman Group, Essex.
22. Finstad AG, Ugedal O, Forseth T, Naesje TF (2004) Energy-related juvenile winter mortality in a northern population of Atlantic salmon (Salmo salar). Can J Fish Aquat Sci 61: 2358-2368. doi: 10. 1139/F04-213.
23. Finstad AG, Berg OK, Forseth T, Ugedal O, Naesje TF (2010) Adaptive winter survival strategies: defended energy levels in juvenile Atlantic salmon along a latitudinal gradient. Proc R Soc B Biol Sci 277: 1113-1120.
24. Frings CS, Fendley TW, Dunn RT, Queen CA (1972) Improved determination of total serum lipids by the sulfo-phospho-vanillin reaction. Clin Chem 18: 673-674.
25. Gienapp P, Teplitsky C, Alho JS, Mills JA, Merila J (2008) Climate change and evolution: disentangling environmental and genetic responses. Mol Ecol 17: 167-178. doi: 10. 1111/j. 1365-294X. 2007. 03413. x.
26. Gilmour AR, Gogel BJ, Cullis BR, Thompson R (2006) ASReml user guide release 2. 0. VSN International Ltd, Hemel Hempstead.
27. Goto SG, Yoshida T, Beppu K, Kimura MT (1999) Evolution of overwinter strategies in Eurasian species of the Drosophila obscura species group. Biol J Linn Soc 68: 429-441.
28. Granier S, Audet C, Bernatchez L (2011) Evidence for both heterosis and outbreeding depression in growth of young-of-the year brook charr (Salvelinus fontinalis). Can J Zool 89: 190-198.
29. Heermann L, Eriksson LO, Magnhagen C, Borcherding J (2009) Size-dependent energy storage and winter mortality of perch. Ecol Freshw Fish 18: 560-571. doi: 10. 1111/j. 1600-0633. 2009. 00371. x.
30. Hermida M, Fernandes C, Amaro R, San Miguel E (2002) Heritability and "evolvability" of meristic characters in a natural population of Gasterosteus aculeatus. Can J Zool 80: 532-541.
31. Hickey JM, Keane MG, Kenny DA, Cromie AR, Veerkamp RF (2007) Genetic parameters for EUROP carcass traits within different groups of cattle in Ireland. J Anim Sci 85: 314-321. doi: 10. 2527/jas. 2006-263.
32. Hodges KE, Boonstra R, Krebs CJ (2006) Overwinter mass loss of snowshoe hares in the Yukon: stravation, stress, adaptation or artefact? J Anim Ecol 75: 1-13. doi: 10. 1111/j. 1365-2656. 2005. 01018. x.
33. Hoffmann AA, Merilä J (1999) Heritable variation and evolution under favourable and unfavourable conditions. Trends Ecol Evol 14: 96-101.
34. Hoffmann AA, Sgro CM (2011) Climate change and evolutionary adaptation. Nature 470: 479-485.
35. Hotz H, Semlitsch RD, Gutmann E, Guex GD, Beerli P (1999) Spontaneous heterosis in larval life-history traits of hemiclonal frog hybrids. Proc Natl Acad Sci USA 96: 2171-2176.
36. Houle D (1992) Comparing evolvability and variability of quantitative traits. Genetics 130: 195-204.
37. Hurst TP (2007) Causes and consequences of winter mortality in fishes. J Fish Biol 71: 315-345. doi: 10. 1111/j. 1095-8649. 2007. 01596. x.
38. Huss M, Bystrom P, Strand A, Eriksson LO, Persson L (2008) Influence of growth history on the accumulation of energy reserves and winter mortality in young fish. Can J Fish Aquat Sci 65: 2149-2156. doi: 10. 1139/F08-115.
39. Hutchings JA, Pickle A, McGregor-Shaw CR, Poirier L (1999) Influence of sex, body size, and reproduction on overwinter lipid depletion in brook trout. J Fish Biol 55: 1020-1028.
40. Ibarz A, Blasco J, Gallardo MA, Fernandez-Borras J (2010) Energy reserves and metabolic status affect the acclimation of gilthead sea bream (Sparus aurata) to cold. Comp Biochem Phys A 155: 319-326. doi: 10. 1016/j. cbpa. 2009. 11. 012.
41. Jensen H, Saether BE, Ringsby TH, Tufto J, Griffith SC et al (2003) Sexual variation in heritability and genetic correlations of morphological traits in house sparrow (Passer domesticus). J Evol Biol 16: 1296-1307. doi: 10. 1046/j. 1420-9101. 2003. 00614. x.
42. Jobling M (1993) Bioenergetics: feed intake and energy partitioning. In: Ranking JC, Jensen FB (eds) Fish ecophysiology, 1st edn. Chapman & Hall, London, pp 1-44.
43. Jones LD, Nielsen MK, Britton RA (1992) Genetic variation in liver mass, body mass, and liver-body mass in mice. J Anim Sci 70: 2999-3006.
44. Jumbo-Lucioni P, Ayroles JF, Chambers MM, Jordan KW, Leips J et al (2010) Systems genetics analysis of body weight and energy metabolism traits in Drosophila melanogaster. BMC Genomics 11: 297.
45. Kause A, Ritola O, Paananen T, Mantysaari EA, Eskelinen U (2002) Coupling body weight and its composition: a quantitative genetic analysis in rainbow trout. Aquaculture 211: 65-79.
46. Kellermann VM, van Heerwaarden B, Hoffmann AA, Sgro CM (2006) Very low additive genetic variance and evolutionary potential in multiple populations of two rainforest Drosophila species. Evolution 60: 1104-1108. doi: 10. 1554/05-710. 1.
47. Lo LL, McLaren DG, McKeith FK, Fernando RL, Novakofski J (1992) Genetic analyses of growth, real-time ultrasound, carcass, and pork quality in Duroc and Landrace pigs: II heritabilities and correlations. J Anim Sci 70: 2387-2396.
48. Lynch M, Walsh JB (1998) Genetics and analysis of quantitative traits. Sinauer Associates, Sunderland.
49. Martin S, Savaria J-Y, Audet C, Bernatchez L (1997) Microsatellites reveal no evidence for inbreeding effects but low inter-stock genetic diversity among brook charr stocks used for production in Quebec. Bull Aquac Assoc Can 97: 21-23.
50. Morinville GR, Rasmussen JB (2008) Distinguishing between juvenile anadromous and resident brook trout (Salvelinus fontinalis) using morphology. Environ Biol Fishes 81: 171-184. doi: 10. 1007/s10641-007-9186-9.
51. Navarro A, Zamorano MJ, Hildebrandt S, Gines R, Aguilera C et al (2009) Estimates of heritabilities and genetic correlation for body composition traits and GXE interactions, in gilthead seabream (Sparus auratus L.). Aquaculture 295: 183-187. doi: 10. 1016/j. aquaculture. 2009. 07. 012.
52. Neira R, Lhorente JP, Araneda C, Diaz N, Bustos E et al (2004) Studies on carcass quality traits in two populations of Coho salmon (Oncorhynchus kisutch): phenotypic and genetic parameters. Aquaculture 241: 117-131. doi: 10. 1016/j. aquaculture. 2004. 08. 009.
53. Nespolo RF, Bacigalupe LD, Bozinovic F (2003) Heritability of energetics in a wild mammal, the leaf-eared mouse (Phyllotis darwini). Evolution 57: 1679-1688.
54. Pelletier F, Reale D, Garant D, Coltman DW, Festa-Bianchet M (2007) Selection on heritable seasonal phenotypic plasticity of body mass. Evolution 61: 1969-1979. doi: 10. 1111/j. 1558-5646. 2007. 00160. x.
55. Perry GML, Audet C, Laplatte B, Bernatchez L (2004) Shifting patterns in genetic control at the embryo-alevin boundary in brook charr. Evolution 58: 2002-2012.
56. Polo V, Carrascal LM, Metcalfe NB (2007) The effects of latitude and day length on fattening strategies of wintering coal tits Periparus ater (L.): a field study and aviary experiment. J Anim Ecol 76: 866-872. doi: 10. 1111/j. 1365-2656. 2007. 01270. x.
57. Rieserberg LH, Archer MA, Wayne RK (1999) Transgressive segregation, adaptation and speciation. Heredity 83: 363-372.
58. Rios FS, Moraes G, Oba ET, Fernandes MN, Donatti L et al (2006) Mobilization and recovery of energy stores in traira, Hoplias malabaricus Bloch (Teleostei, Erythrinidae) during long-term starvation and after re-feeding. J Comp Physiol B 176: 721-728. doi: 10. 1007/s00360-006-0098-3.
59. Robinson MR, Wilson AJ, Pilkington JG, Clutton-Brock TH, Pemberton JM et al (2009) The impact of environmental heterogeneity on genetic architecture in a wild population of Soay sheep. Genetics 181: 1639-1648. doi: 10. 1534/genetics. 108. 086801.
60. Robles H, Ciudad C, Vera R, Baglione V (2007) No effect of habitat fragmentation on post-fledging, first-year and adult survival in the middle spotted woodpecker. Ecography 30: 685-694. doi: 10. 1111/j. 2007. 0906-7590. 05179. x.
61. Roff DA, Mousseau TA (1999) Does natural selection alter genetic architecture? An evaluation of quantitative genetic variation among populations of Allonemobius socius and A. fasciatus. J Evol Biol 12: 361-369.
62. Ronning B, Jensen H, Moe B, Bech C (2007) Basal metabolic rate: heritability and genetic correlations with morphological traits in the zebra finch. J Evol Biol 20: 1815-1822.
63. Saillant E, Dupont-Nivet M, Sabourault M, Haffray P, Laureau S et al (2009) Genetic variation for carcass quality traits in cultured sea bass (Dicentrarchus labrax). Aquat Living Resour 22: 105-112. doi: 10. 1051/Alr/2009010.
64. Schultz ET, Conover DO (1997) Latitudinal differences in somatic energy storage: adaptive responses to seasonality in an estuarine fish (Atherinidae: Menidia menidia). Oecologia 109: 516-529.
65. Schultz ET, Conover DO (1999) The allometry of energy reserve depletion: test of a mechanism for size-dependent winter mortality. Oecologia 119: 474-483.
66. Schultz ET, Conover DO, Ehtisham A (1998) The dead of winter: size dependent variation and genetic differences in seasonal mortality among Atlantic silverside (Atherinidae: Menidia menidia) from different latitudes. Can J Fish Aquat Sci 55: 1149-1157.
67. Serbezov D, Bernatchez L, Olsen EM, Vollestad LA (2010) Quantitative genetic parameters for wild stream-living brown trout: heritability and parental effects. J Evol Biol 23: 1631-1641.
68. Sogard SM (1997) Size-selective mortality in the juvenile stage of teleost fishes: a review. Bull Mar Sci 60: 1129-1157.
69. Stelkens RB, Schmid C, Selz O, Seehausen O (2009) Phenotypic novelty in experimental hybrids is predicted by the genetic distance between species of cichlid fish. BMC Evol Biol 9: 283. doi: 10. 1186/1471-2148-9-283.
70. Suttie JM, Webster JR (1995) Extreme seasonal growth in arctic deer: comparisons and control mechanisms. Am Zool 35: 215-221.
71. Tattersall GJ, Ultsch GR (2008) Physiological ecology of aquatic overwintering in ranid frogs. Biol Rev 83: 119-140. doi: 10. 1111/j. 1469-185X. 2008. 00035. x.
72. Teplitsky C, Mills JA, Yarrall JW, Merila J (2009) Heritability of fitness components in a wild bird population. Evolution 63: 716-726. doi: 10. 1111/j. 1558-5646. 2008. 00581. x.
73. Tieleman BI, Versteegh MA, Helm B, Dingemanse NJ (2009) Quantitative genetics parameters show partial independent evolutionary potential for body mass and metabolism in stonechats from different populations. J Zool 279: 129-136. doi: 10. 1111/j. 1469-7998. 2009. 00597. x.
74. Tobin D, Kause A, Mantysaari EA, Martin SAM, Houlihan DF et al (2006) Fat or lean? The quantitative genetic basis for selection strategies of muscle and body composition traits in breeding schemes of rainbow trout (Oncorhynchus mykiss). Aquaculture 261: 510-521. doi: 10. 1016/j. aquaculture. 2006. 07. 023.
75. Tymchuk WE, Sundstrom LF, Devlin RH (2007) Growth and survival trade-offs and outbreeding depression in rainbow trout (Oncorhynchus mykiss). Evolution 61: 1225-1237. doi: 10. 1111/j. 1558-5646. 2007. 00102. x.
76. Uller T, Olsson M, Stahlberg F (2002) Variation in heritability of tadpole growth: an experimental analysis. Heredity 88: 480-484. doi: 10. 1038/sj/hdy/6800088.
77. Visscher PM, Hill WG, Wray NR (2008) Heritability in the genomics era-concepts and misconceptions. Nat Genet 9: 255-266. doi: 10. 1038/Nrg2322.
78. Visser ME (2008) Keeping up with a warming world; assessing the rate of adaptation to climate change. Proc R Soc B Biol Sci 275: 649-659. doi: 10. 1098/rspb. 2007. 0997.
79. Vollenweider JJ, Heintz RA, Schaufler L, Bradshaw R (2011) Seasonal cycles in whole-body proximate composition and energy content of forage fish vary with water depth. Mar Biol 158: 413-427.
80. Xiang J, Peichao W (1990) Annual cycles of lipid contents and caloric values of carcass and some organs of the gecko, Gekko japonicus. Comp Biochem Physiol 96A: 267-271.
81. Zamer WE, McManus MG, Rowell CB (1999) Physiological variation in clonal anemones: energy balance and quantitative genetics. Am Zool 39: 412-421.