Behavior Genetics

, Volume 44, Issue 1, pp 77–88 | Cite as

QTL Analysis of Behavior in Nine-Spined Sticklebacks (Pungitius pungitius)

  • Veronika N. LaineEmail author
  • Gábor Herczeg
  • Takahito Shikano
  • Johanna Vilkki
  • Juha Merilä
Original Research


The genetic architecture of behavioral traits is yet relatively poorly understood in most non-model organisms. Using an F2-intercross (n = 283 offspring) between behaviorally divergent nine-spined stickleback (Pungitius pungitius) populations, we tested for and explored the genetic basis of different behavioral traits with the aid of quantitative trait locus (QTL) analyses based on 226 microsatellite markers. The behaviors were analyzed both separately (viz. feeding activity, risk-taking and exploration) and combined in order to map composite behavioral type. Two significant QTL—explaining on average 6 % of the phenotypic variance—were detected for composite behavioral type on the experiment-wide level, located on linkage groups 3 and 8. In addition, several suggestive QTL located on six other linkage groups were detected on the chromosome-wide level. Apart from providing evidence for the genetic basis of behavioral variation, the results provide a good starting point for finer-scale analyses of genetic factors influencing behavioral variation in the nine-spined stickleback.


Behavior Fish Microsatellite Personality QTL Stickleback 



We thank Abigel Gonda, Mirva Turtianen and Pirkko Siikamäki (the Oulanka Research Station; University of Oulu) for help in obtaining the fish, Kirsi Kähkönen for help in genotyping, Jacquelin De Faveri for comments that improved an earlier version of this manuscript and DJ de Koning for suggestions regarding treating of the trait data. Our research was supported by Academy of Finland (grant numbers 34728, 250435 and 265211to J.M. and 128716 to G.H.) and the Biological Interactions Graduate School (to V.N.L). G.H. was also supported by the Hungarian Scientific Research Fund (G.H. # OTKA-K 105517) and the János Bólyai Research Scholarship of the Hungarian Academy of Sciences. The experiments carried out in this study were conducted under license from the Finnish National Animal Experiment Board (license no. STH211A), and the fish from Kuusamo were obtained with license from Metsähallitus (permit given for G.H.).


  1. Ab Ghani NI, Herczeg G, Merilä J (2012) Body size divergence in nine-spined sticklebacks: disentangling additive genetic and maternal effects. Biol J Linn Soc 107:521–528CrossRefGoogle Scholar
  2. Ab Ghani NI, Herczeg G, Leinonen T, Merilä J (2013) Evidence for genetic differentiation in timing of maturation among nine-spined stickleback populations. J Evol Biol 26:775–782CrossRefGoogle Scholar
  3. Beavis WD (1994) The power and deceit of QTL experiments: lessons from comparative QTL studies. In: Proceedings of the Forty-Ninth Annual Corn, Sorghum Industry Research Conference. pp. 250–266Google Scholar
  4. Beavis WD (1998) QTL analyses: power, precision, and accuracy. In: Paterson AH (ed) Molecular dissection of complex traits. CRC Press, New York, pp 145–162Google Scholar
  5. Bell AM (2007) Future directions in behavioural syndromes research. Proc R Soc Lond B 274:755–761CrossRefGoogle Scholar
  6. Bell AM, Backström T, Huntingford FA, Pottinger TG, Winberg S (2007) Variable neuroendocrine responses to ecologically-relevant challenges in sticklebacks. Physiol Behav 91:15–25PubMedCrossRefGoogle Scholar
  7. Bell AM, Hankison SJ, Laskowski KL (2009) The repeatability of behaviour: a meta-analysis. Anim Behav 77:771–783CrossRefGoogle Scholar
  8. Berger M, Gray JA, Roth BL (2009) The expanded biology of serotonin. Annu Rev Med 60:355–366PubMedCrossRefGoogle Scholar
  9. Blanchet S, Bernatchez L, Dodson JJ (2009) Does interspecific competition influence relationships between heterozygosity and fitness-related behaviors in juvenile Atlantic salmon (Salmo salar)? Behav Ecol Sociobiol 63:605–615CrossRefGoogle Scholar
  10. Boake CRB (1989) Repeatability: its role in evolutionary studies of mating behavior. Evol Ecol 3:173–182CrossRefGoogle Scholar
  11. Boake CRB, Arnold SJ, Breden F, Meffert LM, Ritchie MG, Taylor BJ, Wolf JB, Moore AJ (2002) Genetic tools for studying adaptation and the evolution of behavior. Am Nat 160:S143–S159PubMedCrossRefGoogle Scholar
  12. Bookstein FL (1991) Morphometric tools for landmark data: geometry and biology. Cambridge University Press, CambridgeGoogle Scholar
  13. Bouchard TJ, Loehlin JC (2001) Genes, evolution, and personality. Behav Genet 31:243–273PubMedCrossRefGoogle Scholar
  14. Burmeister SS, Kailasanath V, Fernald RD (2007) Social dominance regulates androgen and estrogen receptor gene expression. Horm Behav 51:164–170PubMedCentralPubMedCrossRefGoogle Scholar
  15. Chan YF, Marks ME, Jones FC et al (2010) Adaptive evolution of pelvic reduction in sticklebacks by recurrent deletion of a Pitx1 enhancer. Science 327:302–305PubMedCentralPubMedCrossRefGoogle Scholar
  16. Churchill GA, Doerge RW (1994) Empirical threshold values for quantitative trait mapping. Genetics 138:963–971PubMedGoogle Scholar
  17. Cole NJ, Tanaka M, Prescott A, Tickle CA (2003) Expression of limb initiation genes and clues to the basis of morphological diversification in threespine sticklebacks. Curr Biol 13:R951–R952PubMedCrossRefGoogle Scholar
  18. Colosimo PF, Peichel CL, Nereng K, Blackman BK, Shapiro MD, Schluter D, Kingsley DM (2004) The genetic architecture of parallel armor plate reduction in threespine sticklebacks. PLoS Biol 2:635–641CrossRefGoogle Scholar
  19. Coyle SM, Huntingford FA, Peichel CL (2007) Parallel evolution of Pitx1 underlies pelvic reduction in Scottish threespine stickleback (Gasterosteus aculeatus). J Hered 98:581–586PubMedCrossRefGoogle Scholar
  20. Cresko WA, Amores A, Wilson C, Murphy J, Currey M, Phillips P, Bell MA, Kimmel CB, Postlethwait JH (2004) Parallel genetic basis for repeated evolution of armor loss in Alaskan threespine stickleback populations. Proc Natl Acad Sci USA 101:6050–6055PubMedCrossRefGoogle Scholar
  21. David M, Auclair Y, Cézilly F (2011) Personality predicts social dominance in female zebra finches, Taeniopygia guttata, in a feeding context. Anim Behav 81:219–224CrossRefGoogle Scholar
  22. Dingemanse NJ, Both C, Drent PJ, van Oers K, van Noordwijk AJ (2002) Repeatability and heritability of exploratory behaviour in great tits from the wild. Anim Behav 64:929–938CrossRefGoogle Scholar
  23. Dingemanse NJ, Van der Plas F, Wright J, Réale D, Schrama M, Roff DA, Van der Zee E, Barber I (2009) Individual experience and evolutionary history of predation affect expression of heritable variation in fish personality and morphology. Proc R Soc Lond B 276:1285–1293CrossRefGoogle Scholar
  24. Doerge RW, Churchill GA (1996) Permutation tests for multiple loci affecting a quantitative character. Genetics 142:285–294PubMedGoogle Scholar
  25. Ducci F, Enoch M-A, Yuan Q, Shen PH, White KV, Hodgkinson C, Albaugh B, Virkkunen M, Goldman D (2009) HTR3B is associated with alcoholism with antisocial behavior and alpha EEG power—an intermediate phenotype for alcoholism and co-morbid behaviors. Alcohol 43:73–84PubMedCentralPubMedCrossRefGoogle Scholar
  26. Ellegren H, Sheldon BC (2008) Genetic basis of fitness differences in natural populations. Nature 452:169–175PubMedCrossRefGoogle Scholar
  27. Elphinstone MS, Hinten GN, Anderson MJ, Nock CJ (2003) An inexpensive and high-throughput procedure to extract and purify total genomic DNA for population studies. Mol Ecol Notes 3:317–320CrossRefGoogle Scholar
  28. Falconer DS, Mackay TFC (1996) Introduction to quantitative genetics. Longman, New YorkGoogle Scholar
  29. Fidler AE, van Oers K, Drent PJ, Kuhn S, Mueller JC, Kempenaers B (2007) Drd4 gene polymorphisms are associated with personality variation in a passerine bird. Proc R Soc Lond B 274:1685–1691CrossRefGoogle Scholar
  30. Fitzpatrick MJ, Ben-Shahar Y, Smid HM, Vet LEM, Robinson GE, Sokolowski MB (2005) Candidate genes for behavioural ecology. Trends Ecol Evol 20:96–104PubMedCrossRefGoogle Scholar
  31. Flint J, Corley R (1996) Do animal models have a place in the genetic analysis of quantitative human behavioural traits? J Mol Med 74:515–521PubMedCrossRefGoogle Scholar
  32. Flint J, Munafo M (2013) Herit-ability. Science 340:1416–1417PubMedCrossRefGoogle Scholar
  33. Green P, Falls K, Crooks S (1990) Documentation for CRI-MAP (version 2.4). Washington University School of Medicine, St. Louis, Missouri.
  34. Heckel G, Zbinden M, Mazzi D, Kohler A, Reckeweg G, Bakker TCM, Largiadér CR (2002) Microsatellite markers for the three-spined stickleback (Gasterosteus aculeatus L.) and their applicability in a freshwater and an anadromous population. Conserv Genet 3:79–81CrossRefGoogle Scholar
  35. Henderson ND, Turri MG, DeFries JC, Flint J (2004) QTL analysis of multiple behavioral measures of anxiety in mice. Behav Genet 34:267–293PubMedCrossRefGoogle Scholar
  36. Herczeg G, Välimäki K (2011) Intraspecific variation in behaviour: effects of evolutionary history, ontogenetic experience and sex. J Evol Biol 24:2434–2444PubMedCrossRefGoogle Scholar
  37. Herczeg G, Gonda A, Merilä J (2009a) Evolution of gigantism in nine-spined sticklebacks. Evolution 63:3190–3200PubMedCrossRefGoogle Scholar
  38. Herczeg G, Gonda A, Merilä J (2009b) Predation mediated population divergence in complex behaviour of nine-spined stickleback (Pungitius pungitius). J Evol Biol 22:544–552PubMedCrossRefGoogle Scholar
  39. Herczeg G, Turtiainen M, Merilä J (2010) Morphological divergence of North-European nine-spined sticklebacks (Pungitius pungitius): signatures of parallel evolution. Biol J Linn Soc 101:403–416CrossRefGoogle Scholar
  40. Herczeg G, Gonda A, Kuparinen A, Merilä J (2012) Contrasting growth strategies of pond versus marine populations of nine-spined stickleback (Pungitius pungitius): a combined effect of predation and competition? Evol Ecol 26:109–122CrossRefGoogle Scholar
  41. Herczeg G, Ab Ghani NI, Merilä J (2013) Evolution of stickleback feeding behaviour: genetics of population divergence at different ontogenetic stages. J Evol Biol 26:955–962PubMedCrossRefGoogle Scholar
  42. Hettinger JA, Liu X, Schwartz CE, Michaelis RC, Holden JJA (2008) A DRD1 haplotype is associated with risk for autism spectrum disorders in male-only affected sib-pair families. Am J Med Genet Part B 147B:628–636PubMedCrossRefGoogle Scholar
  43. Hoffmann AA (2002) Laboratory and field heritabilites: some lessons from Drosophila. In: Mousseau TA, Sinervo B, Endler JA (eds) Adaptive genetic variation in the wild. Oxford University Press, Oxford, pp 200–218Google Scholar
  44. Inoue-Murayama M (2009) Genetic polymorphism as a background of animal behavior. Anim Sci J 80:113–120PubMedCrossRefGoogle Scholar
  45. Johnston SE, Beraldi D, McRae AF, Pemberton JM, Slate J (2010) Horn type and horn length genes map to the same chromosomal region in soay sheep. Heredity 104:196–205PubMedCrossRefGoogle Scholar
  46. Kukekova AV, Trut LN, Chase K, Kharlamova AV, Johnson JL, Temnykh SV, Oskina IN, Gulevich RG, Vladimirova AV, Klebanov S, Shepeleva DV, Shikhevich SG, Acland GM, Lark KG (2011) Mapping loci for fox domestication: deconstruction/reconstruction of a behavioral phenotype. Behav Genet 41:593–606PubMedCentralPubMedCrossRefGoogle Scholar
  47. Laine VN, Herczeg G, Shikano T, Primmer CR (2012a) Heterozygosity-behaviour correlations in nine-spined stickleback (Pungitius pungitius) populations: contrasting effects at random and functional loci. Mol Ecol 21:4872–4884PubMedCrossRefGoogle Scholar
  48. Laine VN, Primmer CR, Herczeg G, Merilä J, Shikano T (2012b) Isolation and characterization of 13 new nine-spined stickleback, Pungitius pungitius, microsatellites located nearby candidate genes for behavioural variation. Ann Zool Fenn 49:123–128CrossRefGoogle Scholar
  49. Laine VN, Shikano T, Herczeg G, Vilkki J, Merilä J (2013) Quantitative trait loci for growth and body size in the nine-spined stickleback Pungitius pungitius L. Mol Ecol. doi: 10.1111/mec.12526
  50. Lamonerie T, Tremblay JJ, Lanctôt C, Therrien M, Gauthier Y, Drouin J (1996) Ptx1, a bicoid-related homeo box transcription factor involved in transcription of the pro-opiomelanocortin gene. Genes Dev 10:1284–1295PubMedCrossRefGoogle Scholar
  51. Lander E, Kruglyak L (1995) Genetic dissection of complex traits: guidelines for interpreting and reporting linkage results. Nat Genet 11:241–247PubMedCrossRefGoogle Scholar
  52. Largiadèr CR, Fries V, Kobler B, Bakker TCM (1999) Isolation and characterization of microsatellite loci from the three-spined stickleback (Gasterosteus aculeatus L.). Mol Ecol 8:342–344PubMedGoogle Scholar
  53. Lynch M, Walsh B (1998) Genetics and Analysis of Quantitative Traits, Sinauer AssociatesGoogle Scholar
  54. Mackay TFC, Stone EA, Ayroles JF (2009) The genetics of quantitative traits: challenges and prospects. Nat Rev Genet 10:565–577PubMedCrossRefGoogle Scholar
  55. Mäkinen HS, Cano JM, Merilä J (2008) Identifying footprints of directional and balancing selection in marine and freshwater three-spined stickleback (Gasterosteus aculeatus) populations. Mol Ecol 17:3565–3582PubMedCrossRefGoogle Scholar
  56. Mather K, Jinks JL (1982) Biometrical genetics. The study of continuous variation. Chapman and Hall, LondonCrossRefGoogle Scholar
  57. Merilä J (2013) Nine-spined stickleback (Pungitius pungitius): an emerging model for evolutionary biology research. Ann N Y Acad Sci 1289:18–35PubMedCrossRefGoogle Scholar
  58. Miller CT, Beleza S, Pollen AA, Schluter D, Kittles RA, Shriver MD, Kingsley DM (2007) cis-Regulatory changes in kit ligand expression and parallel evolution of pigmentation in sticklebacks and humans. Cell 131:1179–1189PubMedCentralPubMedCrossRefGoogle Scholar
  59. Misener VL, Luca P, Azeke O, Crosbie J, Waldman I, Tannock R, Roberts W, Malone M, Schachar R, Ickowicz A, Kennedy JL, Barr CL (2004) Linkage of the dopamine receptor D1 gene to attention-deficit/hyperactivity disorder. Mol Psychiatry 9:500–509PubMedCrossRefGoogle Scholar
  60. Mousseau TA, Roff DA (1987) Natural selection and the heritability of fitness components. Heredity 59:181–197PubMedCrossRefGoogle Scholar
  61. Noblett KL, Coccaro EF (2005) Molecular genetics of personality. Curr Psychiatry Rep 7:73–80PubMedCrossRefGoogle Scholar
  62. Peichel CL, Nereng K, Ohgi KA, Cole BLE, Colosimo PF, Buerkle CA, Schluter D, Kingsley DM (2001) The genetic architecture of divergence between threespine stickleback species. Nature 414:901–905PubMedCrossRefGoogle Scholar
  63. Philippi A, Tores F, Carayol J, Rousseau F, Letexier M, Roschmann E, Lindenbaum P, Benajjou A, Fontaine K, Vazart C, Gesnouin P, Brooks P, Hager J (2007) Association of autism with polymorphisms in the paired-like homeodomain transcription factor 1 (PITX1) on chromosome 5q31: a candidate gene analysis. BMC Med Genet 8:74PubMedCentralPubMedCrossRefGoogle Scholar
  64. Rebai A, Goffinet B, Mangin B (1995) Comparing power of different methods for QTL detection. Biometrics 51:87–99PubMedCrossRefGoogle Scholar
  65. Reif A, Lesch K-P (2003) Toward a molecular architecture of personality. Behav Brain Res 139:1–20PubMedCrossRefGoogle Scholar
  66. Roth B (1994) Multiple serotonin receptors: clinical and experimental aspects. Ann Clin Psychiatry 6:67–78PubMedCrossRefGoogle Scholar
  67. Schütz KE, Kerje S, Jacobsson L, Forkman B, Carlborg O, Andersson L, Jensen P (2004) Major growth QTLs in fowl are related to fearful behavior: possible genetic links between fear responses and production traits in a red junglefowl x white leghorn intercross. Behav Genet 34:121–130PubMedCrossRefGoogle Scholar
  68. Shapiro MD, Marks ME, Peichel CL, Blackman BK, Nereng KS, Jónsson B, Schluter D, Kingsley DM (2004) Genetic and developmental basis of evolutionary pelvic reduction in threespine sticklebacks. Nature 428:717–723PubMedCrossRefGoogle Scholar
  69. Shapiro MD, Summers BR, Balabhadra S, Aldenhoven JT, Miller AL, Cunningham CB, Bell MA, Kingsley DM (2009) The genetic architecture of skeletal convergence and sex determination in ninespine sticklebacks. Curr Biol 19:1140–1145PubMedCentralPubMedCrossRefGoogle Scholar
  70. Shikano T, Ramadevi J, Shimada Y, Merilä J (2010) Utility of sequenced genomes for microsatellite marker development in non-model organisms: a case study of functionally important genes in nine-spined sticklebacks (Pungitius pungitius). BMC Genomics 11:334PubMedCentralPubMedCrossRefGoogle Scholar
  71. Shikano T, Natri HM, Shimada Y, Merilä J (2011) High degree of sex chromosome differentiation in stickleback fishes. BMC Genomics 12:474PubMedCentralPubMedCrossRefGoogle Scholar
  72. Shikano T, Laine VN, Herczeg G, Vilkki J, Merilä J (2013) Genetic architecture of parallel pelvic reduction in ninespine sticklebacks. G3: Genes, Genomics. Genetics. 3:1833–1842Google Scholar
  73. Shimada Y, Shikano T, Kuparinen A, Gonda A, Leinonen T, Merilä J (2011a) Quantitative genetics of body size and timing of maturation in two nine-spined stickleback (Pungitius pungitius) populations. PLoS One 6:e28859PubMedCentralPubMedCrossRefGoogle Scholar
  74. Shimada Y, Shikano T, Merilä J (2011b) A high incidence of selection on physiologically important genes in the three-spined stickleback, Gasterosteus aculeatus. Mol Biol Evol 28:181–193PubMedCrossRefGoogle Scholar
  75. Slate J (2005) Quantitative trait locus mapping in natural populations: progress, caveats and future directions. Mol Ecol 14:363–379PubMedCrossRefGoogle Scholar
  76. Slate J (2013) From beavis to beak colour: a simulation study to examine how much QTL mapping can reveal about the genetic architecture of quantitative traits. Evolution 67:1251–1262PubMedGoogle Scholar
  77. Slate J, Pemberton JM, Visscher PM (1999) Power to detect QTL in a free-living polygynous population. Heredity 83:327–336PubMedCrossRefGoogle Scholar
  78. Slate J, Gratten J, Beraldi D, Stapley J, Hale M, Pemberton JM (2009) Gene mapping in the wild with SNPs: guidelines and future directions. Genetica 136:97–107PubMedCrossRefGoogle Scholar
  79. Sokolowski MB (2001) Drosophila: genetics meets behaviour. Nat Rev Genet 2:879–890PubMedCrossRefGoogle Scholar
  80. Stinchcombe JR, Hoekstra HE (2008) Combining population genomics and quantitative genetics: finding the genes underlying ecologically important traits. Heredity 100:158–170PubMedCrossRefGoogle Scholar
  81. Takeuchi Y, Hashizume C, Arata S, Inoue-Murayama M, Maki T, Hart BL, Mori Y (2009) An approach to canine behavioural genetics employing guide dogs for the blind. Anim Genet 40:217–224PubMedCrossRefGoogle Scholar
  82. Tarka M, Akesson M, Beraldi D, Hernández-Sánchez J, Hasselquist D, Bensch S, Hansson B (2010) A strong quantitative trait locus for wing length on chromosome 2 in a wild population of great reed warblers. Proc R Soc Lond B 277:2361–2369CrossRefGoogle Scholar
  83. Tiira K, Laurila A, Peuhkuri N, Piironen J, Ranta E, Primmer CR (2003) Aggressiveness is associated with genetic diversity in landlocked salmon (Salmo salar). Mol Ecol 12:2399–2407PubMedCrossRefGoogle Scholar
  84. Tiira K, Laurila A, Enberg K et al (2006) Do dominants have higher heterozygosity? Social status and genetic variation in brown trout, Salmo trutta. Behav Ecol Sociobiol 59:657–665CrossRefGoogle Scholar
  85. Tschirren B, Bensch S (2010) Genetics of personalities: no simple answers for complex traits. Mol Ecol 19:624–626PubMedCrossRefGoogle Scholar
  86. Våge J, Wade C, Biagi T, Fatjó J, Amat M, Lindblad-Toh K, Lingaas F (2010) Association of dopamine- and serotonin-related genes with canine aggression. Genes Brain Behav 9:372–378PubMedCrossRefGoogle Scholar
  87. Välimäki K, Herczeg G (2012) Ontogenetic and evolutionary effects of predation and competition on nine-spined stickleback (Pungitius pungitius) body size. J Anim Ecol 81:859–867PubMedCrossRefGoogle Scholar
  88. Välimäki K, Herczeg G, Merilä J (2012) Morphological anti-predator defences in the nine-spined sticklebacks: constitutive, induced or both? Biol J Linn Soc 107:854–866CrossRefGoogle Scholar
  89. Van Oers K, Mueller JC (2010) Evolutionary genomics of animal personality. Proc R Soc Lond B 365:3991–4000Google Scholar
  90. van Oers K, de Jong G, van Noordwijk A, Drent P (2005) Contribution of genetics to the study of animal personalities: a review of case studies. Behaviour 142:1185–1206CrossRefGoogle Scholar
  91. Vilhunen S, Tiira K, Laurila A, Hirvonen H (2008) The bold and the variable: fish with high heterozygosity act recklessly in the vicinity of predators. Ethology 114:7–15CrossRefGoogle Scholar
  92. Visscher PM, Goddard ME, Derks EM, Wray NR (2012) Evidence-based psychiatric genetics, AKA the false dichotomy between common and rare variant hypotheses. Mol Psychiatry 17:474–485PubMedCrossRefGoogle Scholar
  93. Voorrips RE (2002) MapChart: software for the graphical presentation of linkage maps and QTLs. J Hered 93:77–78PubMedCrossRefGoogle Scholar
  94. Weber JN, Peterson BK, Hoekstra HE (2013) Discrete genetic modules are responsible for complex burrow evolution in Peromyscus mice. Nature 493:402–405PubMedCrossRefGoogle Scholar
  95. Weiss A, King JE, Figueredo AJ (2000) The heritability of personality factors in chimpanzees (Pan troglodytes). Behav Genet 30:213–221PubMedCrossRefGoogle Scholar
  96. Winberg S, Nilsson A, Hylland P, Söderström V, Nilsson GE (1997) Serotonin as a regulator of hypothalamic-pituitary-interrenal activity in teleost fish. Neurosci Lett 230:113–116PubMedCrossRefGoogle Scholar
  97. Wright D, Butlin RK, Carlborg O (2006a) Epistatic regulation of behavioural and morphological traits in the zebrafish (Danio rerio). Behav Genet 36:914–922PubMedCrossRefGoogle Scholar
  98. Wright D, Nakamichi R, Krause J, Butlin RK (2006b) QTL analysis of behavioral and morphological differentiation between wild and laboratory zebrafish (Danio rerio). Behav Genet 36:271–284PubMedCrossRefGoogle Scholar
  99. Xu S (2003) Theoretical basis of the Beavis effect. Genetics 165:2259–2268PubMedGoogle Scholar
  100. Xu H, Shen X, Zhou M, Fang M, Zeng H, Nie Q, Zhang X (2010) The genetic effects of the dopamine D1 receptor gene on chicken egg production and broodiness traits. BMC Genet 11:17PubMedCentralPubMedCrossRefGoogle Scholar
  101. Zhou H, Deeb N, Evock-Clover CM, Ashwell CM, Lamont SJ (2006) Genome-wide linkage analysis to identify chromosomal regions affecting phenotypic traits in the chicken. I. Growth and average daily gain. Poult Sci 85:1700–1711PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2013

Authors and Affiliations

  • Veronika N. Laine
    • 1
    Email author
  • Gábor Herczeg
    • 2
    • 4
  • Takahito Shikano
    • 2
  • Johanna Vilkki
    • 3
  • Juha Merilä
    • 2
  1. 1.Division of Genetics and Physiology, Department of BiologyUniversity of TurkuTurkuFinland
  2. 2.Ecological Genetics Research Unit, Department of BiosciencesUniversity of HelsinkiHelsinkiFinland
  3. 3.MTT Agrifood Research FinlandJokioinenFinland
  4. 4.Behavioural Ecology Group, Department of Systematic Zoology and EcologyEötvös Loránd UniversityBudapestHungary

Personalised recommendations