1932

Abstract

Nervous systems allow animals to acutely respond and behaviorally adapt to changes and recurring patterns in their environment at multiple timescales—from milliseconds to years. Behavior is further shaped at intergenerational timescales by genetic variation, drift, and selection. This sophistication and flexibility of behavior makes it challenging to measure behavior consistently in individual subjects and to compare it across individuals. In spite of these challenges, careful behavioral observations in nature and controlled measurements in the laboratory, combined with modern technologies and powerful genetic approaches, have led to important discoveries about the way genetic variation shapes behavior. A critical mass of genes whose variation is known to modulate behavior in nature is finally accumulating, allowing us to recognize emerging patterns. In this review, we first discuss genetic mapping approaches useful for studying behavior. We then survey how variation acts at different levels—in environmental sensation, in internal neuronal circuits, and outside the nervous system altogether—and then discuss the sources and types of molecular variation linked to behavior and the mechanisms that shape such variation. We end by discussing remaining questions in the field.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-genom-111219-080427
2020-08-31
2024-05-21
Loading full text...

Full text loading...

/deliver/fulltext/genom/21/1/annurev-genom-111219-080427.html?itemId=/content/journals/10.1146/annurev-genom-111219-080427&mimeType=html&fmt=ahah

Literature Cited

  1. 1. 
    Albert FW, Carlborg Ö, Plyusnina I, Besnier F, Hedwig D et al. 2009. Genetic architecture of tameness in a rat model of animal domestication. Genetics 182:541–54
    [Google Scholar]
  2. 2. 
    Andersson LS, Larhammar M, Memic F, Wootz H, Schwochow D et al. 2012. Mutations in DMRT3 affect locomotion in horses and spinal circuit function in mice. Nature 488:642–46
    [Google Scholar]
  3. 3. 
    Auer TO, Khallaf MA, Silbering AF, Zappia G, Ellis K et al. 2020. Olfactory receptor and circuit evolution promote host specialization. Nature 579:4028
    [Google Scholar]
  4. 4. 
    Baldwin MW, Toda Y, Nakagita T, O'Connell MJ, Klasing KC et al. 2014. Evolution of sweet taste perception in hummingbirds by transformation of the ancestral umami receptor. Science 345:929–33
    [Google Scholar]
  5. 5. 
    Baselmans BML, Jansen R, Ip HF, van Dongen J, Abdellaoui A et al. 2019. Multivariate genome-wide analyses of the well-being spectrum. Nat. Genet. 51:445–51a
    [Google Scholar]
  6. 6. 
    Bendesky A, Bargmann CI. 2011. Genetic contributions to behavioural diversity at the gene-environment interface. Nat. Rev. Genet. 12:809–20
    [Google Scholar]
  7. 7. 
    Bendesky A, Kwon Y-M, Lassance J-M, Lewarch CL, Yao S et al. 2017. The genetic basis of parental care evolution in monogamous mice. Nature 544:434–39
    [Google Scholar]
  8. 8. 
    Bendesky A, Pitts J, Rockman MV, Chen WC, Tan MW et al. 2012. Long-range regulatory polymorphisms affecting a GABA receptor constitute a quantitative trait locus (QTL) for social behavior in Caenorhabditis elegans. PLOS Genet 8:e1003157
    [Google Scholar]
  9. 9. 
    Bendesky A, Tsunozaki M, Rockman MV, Kruglyak L, Bargmann CI 2011. Catecholamine receptor polymorphisms affect decision-making in C. elegans. Nature 472:313–18
    [Google Scholar]
  10. 10. 
    Berrettini W, Yuan X, Tozzi F, Song K, Francks C et al. 2008. α-5/α-3 nicotinic receptor subunit alleles increase risk for heavy smoking. Mol. Psychiatry 13:368–73
    [Google Scholar]
  11. 11. 
    Bersaglieri T, Sabeti PC, Patterson N, Vanderploeg T, Schaffner SF et al. 2004. Genetic signatures of strong recent positive selection at the lactase gene. Am. J. Hum. Genet. 74:1111–20
    [Google Scholar]
  12. 12. 
    Bierut LJ, Goate AM, Breslau N, Johnson EO, Bertelsen S et al. 2012. ADH1B is associated with alcohol dependence and alcohol consumption in populations of European and African ancestry. Mol. Psychiatry 17:445–50
    [Google Scholar]
  13. 13. 
    Bigham A, Bauchet M, Pinto D, Mao X, Akey JM et al. 2010. Identifying signatures of natural selection in Tibetan and Andean populations using dense genome scan data. PLOS Genet 6:e1001116
    [Google Scholar]
  14. 14. 
    Blankers T, Oh KP, Shaw KL 2019. Parallel genomic architecture underlies repeated sexual signal divergence in Hawaiian Laupala crickets. Proc. Biol. Sci. 286:20191479
    [Google Scholar]
  15. 15. 
    Blomberg SP, Garland T, Ives AR 2003. Testing for phylogenetic signal in comparative data: Behavioral traits are more labile. Evolution 57:717–45
    [Google Scholar]
  16. 16. 
    Bogert CM. 1949. Thermoregulation in reptiles, a factor in evolution. Evolution 3:195–211
    [Google Scholar]
  17. 17. 
    Bult CJ, Blake JA, Smith CL, Kadin JA, Richardson JE 2019. Mouse Genome Database (MGD) 2019. Nucleic Acids Res 47:D801–6
    [Google Scholar]
  18. 18. 
    Buniello A, MacArthur JAL, Cerezo M, Harris LW, Hayhurst J et al. 2019. The NHGRI-EBI GWAS Catalog of published genome-wide association studies, targeted arrays and summary statistics 2019. Nucleic Acids Res 47:D1005–12
    [Google Scholar]
  19. 19. 
    Burger J, Kirchner M, Bramanti B, Haak W, Thomas MG 2007. Absence of the lactase-persistence-associated allele in early Neolithic Europeans. PNAS 104:3736–41
    [Google Scholar]
  20. 20. 
    Bycroft C, Freeman C, Petkova D, Band G, Elliott LT et al. 2018. The UK Biobank resource with deep phenotyping and genomic data. Nature 562:203–9
    [Google Scholar]
  21. 21. 
    Campbell DD, Parra MV, Duque C, Gallego N, Franco L et al. 2012. Amerind ancestry, socioeconomic status and the genetics of type 2 diabetes in a Colombian population. PLOS ONE 7:e33570
    [Google Scholar]
  22. 22. 
    Chang AJ, Bargmann CI. 2008. Hypoxia and the HIF-1 transcriptional pathway reorganize a neuronal circuit for oxygen-dependent behavior in Caenorhabditis elegans. PNAS 105:7321–26
    [Google Scholar]
  23. 23. 
    Clarke TK, Adams MJ, Davies G, Howard DM, Hall LS et al. 2017. Genome-wide association study of alcohol consumption and genetic overlap with other health-related traits in UK biobank (N = 112117). Mol. Psychiatry 22:1376–84
    [Google Scholar]
  24. 24. 
    Colosimo PF, Hosemann KE, Balabhadra S, Villarreal G Jr., Dickson M, et al. 2005. Widespread parallel evolution in sticklebacks by repeated fixation of ectodysplasin alleles. Science 307:1928–33
    [Google Scholar]
  25. 25. 
    Comeron JM. 2014. Background selection as baseline for nucleotide variation across the Drosophila genome. PLOS Genet 10:e1004434
    [Google Scholar]
  26. 26. 
    Coop G. 2019. Reading tea leaves? Polygenic scores and differences in traits among groups. arXiv:1909.00892 [q-bio.GN]
    [Google Scholar]
  27. 27. 
    Cornelis MC, Byrne EM, Esko T, Nalls MA, Ganna A et al. 2015. Genome-wide meta-analysis identifies six novel loci associated with habitual coffee consumption. Mol. Psychiatry 20:647–56
    [Google Scholar]
  28. 28. 
    Cornelis MC, Monda KL, Yu K, Paynter N, Azzato EM et al. 2011. Genome-wide meta-analysis identifies regions on 7p21 (AHR) and 15q24 (CYP1A2) as determinants of habitual caffeine consumption. PLOS Genet 7:e1002033
    [Google Scholar]
  29. 29. 
    Crabbe JC, Wahlsten D, Dudek BC 1999. Genetics of mouse behavior: interactions with laboratory environment. Science 284:1670–72
    [Google Scholar]
  30. 30. 
    Croze M, Wollstein A, Božičević V, Živković D, Stephan W, Hutter S 2017. A genome-wide scan for genes under balancing selection in Drosophila melanogaster. BMC Evol. Biol 17:15
    [Google Scholar]
  31. 31. 
    Dannemann M, Kelso J. 2017. The contribution of Neanderthals to phenotypic variation in modern humans. Am. J. Hum. Genet. 101:578–89
    [Google Scholar]
  32. 32. 
    de Bono M, Bargmann CI 1998. Natural variation in a neuropeptide Y receptor homolog modifies social behavior and food response in C. elegans. Cell 94:679–89
    [Google Scholar]
  33. 33. 
    de la Torre-Ubieta L, Stein JL, Won H, Opland CK, Liang D et al. 2018. The dynamic landscape of open chromatin during human cortical neurogenesis. Cell 172:289–304
    [Google Scholar]
  34. 34. 
    De Wijk RA, Prinz JF, Engelen L, Weenen H 2004. The role of α-amylase in the perception of oral texture and flavour in custards. Physiol. Behav. 83:81–91
    [Google Scholar]
  35. 35. 
    Dierick HA, Greenspan RJ. 2006. Molecular analysis of flies selected for aggressive behavior. Nat. Genet. 38:1023–31
    [Google Scholar]
  36. 36. 
    Ding Y, Berrocal A, Morita T, Longden KD, Stern DL 2016. Natural courtship song variation caused by an intronic retroelement in an ion channel gene. Nature 536:329–32
    [Google Scholar]
  37. 37. 
    Dunn LC, Gluecksohn-Schoenheimer S. 1950. Repeated mutations in one area of a mouse chromosome. PNAS 36:233–37
    [Google Scholar]
  38. 38. 
    Eigenbrod O, Debus KY, Reznick J, Bennett NC, Sánchez-Carranza O et al. 2019. Rapid molecular evolution of pain insensitivity in multiple African rodents. Science 364:852–59
    [Google Scholar]
  39. 39. 
    Eriksson N, Wu S, Do CB, Kiefer AK, Tung JY et al. 2012. A genetic variant near olfactory receptor genes influences cilantro preference. Flavour 1:22
    [Google Scholar]
  40. 40. 
    Farallo VR, Wier R, Miles DB 2018. The Bogert effect revisited: Salamander regulatory behaviors are differently constrained by time and space. Ecol. Evol. 8:11522–32
    [Google Scholar]
  41. 41. 
    Feng P, Zheng J, Rossiter SJ, Wang D, Zhao H 2014. Massive losses of taste receptor genes in toothed and baleen whales. Genome Biol. Evol. 6:1254–65
    [Google Scholar]
  42. 42. 
    Flint J. 2003. Analysis of quantitative trait loci that influence animal behavior. J. Neurobiol. 54:46–77
    [Google Scholar]
  43. 43. 
    Gallego Romero I, Basu Mallick C, Liebert A, Crivellaro F, Chaubey G et al. 2011. Herders of Indian and European cattle share their predominant allele for lactase persistence. Mol. Biol. Evol. 29:249–60
    [Google Scholar]
  44. 44. 
    Gilad Y, Bustamante CD, Lancet D, Pääbo S 2003. Natural selection on the olfactory receptor gene family in humans and chimpanzees. Am. J. Hum. Genet. 73:489–501
    [Google Scholar]
  45. 45. 
    Gracheva EO, Cordero-Morales JF, González-Carcacía JA, Ingolia NT, Manno C et al. 2011. Ganglion-specific splicing of TRPV1 underlies infrared sensation in vampire bats. Nature 476:88–92
    [Google Scholar]
  46. 46. 
    Gracheva EO, Ingolia NT, Kelly YM, Cordero-Morales JF, Hollopeter G et al. 2010. Molecular basis of infrared detection by snakes. Nature 464:1006–11
    [Google Scholar]
  47. 47. 
    Graham AM, McCracken KG. 2019. Convergent evolution on the hypoxia-inducible factor (HIF) pathway genes EGLN1 and EPAS1 in high-altitude ducks. Heredity 122:819–32
    [Google Scholar]
  48. 48. 
    Gray JM, Karow DS, Lu H, Chang AJ, Chang JS et al. 2004. Oxygen sensation and social feeding mediated by a C. elegans guanylate cyclase homologue. Nature 430:317–22
    [Google Scholar]
  49. 49. 
    Greene JS, Brown M, Dobosiewicz M, Ishida IG, Macosko EZ et al. 2016. Balancing selection shapes density-dependent foraging behaviour. Nature 539:254–58
    [Google Scholar]
  50. 50. 
    Greene JS, Dobosiewicz M, Butcher RA, McGrath PT, Bargmann CI 2016. Regulatory changes in two chemoreceptor genes contribute to a Caenorhabditis elegans QTL for foraging behavior. eLife 5:e21454
    [Google Scholar]
  51. 51. 
    Greenwood AK, Mills MG, Wark AR, Archambeault SL, Peichel CL 2016. Evolution of schooling behavior in threespine sticklebacks is shaped by the Eda gene. Genetics 203:677–81
    [Google Scholar]
  52. 52. 
    Greenwood AK, Wark AR, Yoshida K, Peichel CL 2013. Genetic and neural modularity underlie the evolution of schooling behavior in threespine sticklebacks. Curr. Biol. 23:1884–88
    [Google Scholar]
  53. 53. 
    Hernandez RD, Uricchio LH, Hartman K, Ye C, Dahl A, Zaitlen N 2019. Ultrarare variants drive substantial cis heritability of human gene expression. Nat. Genet. 51:1349–55
    [Google Scholar]
  54. 54. 
    Herrmann M, Mayer WE, Sommer RJ 2006. Nematodes of the genus Pristionchus are closely associated with scarab beetles and the Colorado potato beetle in western Europe. Zoology 109:96–108
    [Google Scholar]
  55. 55. 
    Heyne HO, Lautenschläger S, Nelson R, Besnier F, Rotival M et al. 2014. Genetic influences on brain gene expression in rats selected for tameness and aggression. Genetics 198:1277–90
    [Google Scholar]
  56. 56. 
    Higham T, Douka K, Wood R, Ramsey CB, Brock F et al. 2014. The timing and spatiotemporal patterning of Neanderthal disappearance. Nature 512:306–9
    [Google Scholar]
  57. 57. 
    Hodgkin J, Doniach T. 1997. Natural variation and copulatory plug formation in Caenorhabditis elegans. Genetics 146:149–64
    [Google Scholar]
  58. 58. 
    Hong RL, Witte H, Sommer RJ 2008. Natural variation in Pristionchus pacificus insect pheromone attraction involves the protein kinase EGL-4. PNAS 105:7779–84
    [Google Scholar]
  59. 59. 
    Horton BM, Hudson WH, Ortlund EA, Shirk S, Thomas JW et al. 2014. Estrogen receptor α polymorphism in a species with alternative behavioral phenotypes. PNAS 111:1443–48
    [Google Scholar]
  60. 60. 
    Hu Y, Wu Q, Ma S, Ma T, Shan L et al. 2017. Comparative genomics reveals convergent evolution between the bamboo-eating giant and red pandas. PNAS 114:1081–86
    [Google Scholar]
  61. 61. 
    Huerta-Sánchez E, Jin X, Asan Bianba Z, Peter BM et al. 2014. Altitude adaptation in Tibetans caused by introgression of Denisovan-like DNA. Nature 512:194–97
    [Google Scholar]
  62. 62. 
    Hughes GM, Boston ESM, Finarelli JA, Murphy WJ, Higgins DG, Teeling EC 2018. The birth and death of olfactory receptor gene families in mammalian niche adaptation. Mol. Biol. Evol. 35:1390–406
    [Google Scholar]
  63. 63. 
    Ilardo MA, Moltke I, Korneliussen TS, Cheng J, Stern AJ et al. 2018. Physiological and genetic adaptations to diving in Sea Nomads. Cell 173:569–80
    [Google Scholar]
  64. 64. 
    Insel TR. 2010. The challenge of translation in social neuroscience: a review of oxytocin, vasopressin, and affiliative behavior. Neuron 65:768–79
    [Google Scholar]
  65. 65. 
    Ishikawa Y, Takanashi T, Kim C, Hoshizaki S, Tatsuki S, Huang Y 1999. Ostrinia spp. in Japan: their host plants and sex pheromones. Entomol. Exp. Appl. 91:237–44
    [Google Scholar]
  66. 66. 
    Itoigawa A, Hayakawa T, Suzuki-Hashido N, Imai H 2019. A natural point mutation in the bitter taste receptor TAS2R16 causes inverse agonism of arbutin in lemur gustation. Proc. Biol. Sci. 296:2861904
    [Google Scholar]
  67. 67. 
    Jiang P, Josue J, Li X, Glaser D, Li W et al. 2012. Major taste loss in carnivorous mammals. PNAS 109:4956–61
    [Google Scholar]
  68. 68. 
    Kamilar JM, Cooper N. 2013. Phylogenetic signal in primate behaviour, ecology and life history. Philos. Trans. R. Soc. B 368:20120341
    [Google Scholar]
  69. 69. 
    Karageorgi M, Groen SC, Sumbul F, Pelaez JN, Verster KI et al. 2019. Genome editing retraces the evolution of toxin resistance in the monarch butterfly. Nature 574:409–12
    [Google Scholar]
  70. 70. 
    Karlsson Linnér R, Biroli P, Kong E, Meddens SFW, Wedow R et al. 2019. Genome-wide association analyses of risk tolerance and risky behaviors in over 1 million individuals identify hundreds of loci and shared genetic influences. Nat. Genet. 51:245–57
    [Google Scholar]
  71. 71. 
    Kawamura S. 2016. Color vision diversity and significance in primates inferred from genetic and field studies. Genes Genom 38:779–91
    [Google Scholar]
  72. 72. 
    Keller L, Parker JD. 2002. Behavioral genetics: a gene for supersociality. Curr. Biol. 12:180–81
    [Google Scholar]
  73. 73. 
    Khan I, Yang Z, Maldonado E, Li C, Zhang G et al. 2015. Olfactory receptor subgenomes linked with broad ecological adaptations in Sauropsida. Mol. Biol. Evol. 32:2832–43
    [Google Scholar]
  74. 74. 
    Kimchi T, Xu J, Dulac C 2007. A functional circuit underlying male sexual behaviour in the female mouse brain. Nature 448:1009–14
    [Google Scholar]
  75. 75. 
    Kiontke K, Fitch DHA. 2005. The phylogenetic relationships of Caenorhabditis and other rhabditids. WormBook C. elegans Res. Commun. https://doi.org/10.1895/wormbook.1.11.1
    [Crossref] [Google Scholar]
  76. 76. 
    Kishida T, Kubota S, Shirayama Y, Fukami H 2007. The olfactory receptor gene repertoires in secondary-adapted marine vertebrates: evidence for reduction of the functional proportions in cetaceans. Biol. Lett. 3:428–30
    [Google Scholar]
  77. 77. 
    Kocher SD, Mallarino R, Rubin BER, Yu DW, Hoekstra HE, Pierce NE 2018. The genetic basis of a social polymorphism in halictid bees. Nat. Commun. 9:4338
    [Google Scholar]
  78. 78. 
    Kong A, Thorleifsson G, Frigge ML, Vilhjalmsson BJ, Young AI et al. 2018. The nature of nurture: effects of parental genotypes. Science 359:424–28
    [Google Scholar]
  79. 79. 
    Kukekova AV, Johnson JL, Xiang X, Feng S, Liu S et al. 2018. Red fox genome assembly identifies genomic regions associated with tame and aggressive behaviours. Nat. Ecol. Evol. 2:1479–91
    [Google Scholar]
  80. 80. 
    Küpper C, Stocks M, Risse JE, Dos Remedios N, Farrell LL et al. 2015. A supergene determines highly divergent male reproductive morphs in the ruff. Nat. Genet. 48:79–83
    [Google Scholar]
  81. 81. 
    Lamichhaney S, Fan G, Widemo F, Gunnarsson U, Thalmann DS et al. 2015. Structural genomic changes underlie alternative reproductive strategies in the ruff (Philomachus pugnax). Nat. Genet. 48:84–88
    [Google Scholar]
  82. 82. 
    Lander ES, Schork NJ. 1994. Genetic dissection of complex traits. Science 265:2037–48
    [Google Scholar]
  83. 83. 
    Lappalainen T, Scott AJ, Brandt M, Hall IM 2019. Genomic analysis in the age of human genome sequencing. Cell 177:70–84
    [Google Scholar]
  84. 84. 
    Lassance JM, Groot AT, Liénard MA, Antony B, Borgwardt C et al. 2010. Allelic variation in a fatty-acyl reductase gene causes divergence in moth sex pheromones. Nature 466:486–89
    [Google Scholar]
  85. 85. 
    Leary GP, Allen JE, Bunger PL, Luginbill JB, Linn CE et al. 2012. Single mutation to a sex pheromone receptor provides adaptive specificity between closely related moth species. PNAS 109:14081–86
    [Google Scholar]
  86. 86. 
    Lee D, Zdraljevic S, Cook DE, Frézal L, Hsu J et al. 2019. Selection and gene flow shape niche-associated variation in pheromone response. Nat. Ecol. Evol. 3:1455–63
    [Google Scholar]
  87. 87. 
    L'Etoile ND, Coburn CM, Eastham J, Kistler A, Gallegos G, Bargmann CI 2002. The cyclic GMP-dependent protein kinase EGL-4 regulates olfactory adaptation in C. elegans. Neuron 36:1079–89
    [Google Scholar]
  88. 88. 
    Levene H. 1953. Genetic equilibrium when more than one ecological niche is available. Am. Nat. 87:331–33
    [Google Scholar]
  89. 89. 
    Li R, Fan W, Tian G, Zhu H, He L et al. 2010. The sequence and de novo assembly of the giant panda genome. Nature 463:311–17
    [Google Scholar]
  90. 90. 
    Li X, Li W, Wang H, Cao J, Maehashi K et al. 2005. Pseudogenization of a sweet-receptor gene accounts for cats’ indifference toward sugar. PLOS Genet 1:e3
    [Google Scholar]
  91. 91. 
    Lin JJ, Wang FY, Li WH, Wang TY 2017. The rises and falls of opsin genes in 59 ray-finned fish genomes and their implications for environmental adaptation. Sci. Rep. 7:15568
    [Google Scholar]
  92. 92. 
    Liu M, Jiang Y, Wedow R, Li Y, Brazel DM et al. 2019. Association studies of up to 1.2 million individuals yield new insights into the genetic etiology of tobacco and alcohol use. Nat. Genet. 51:237–44
    [Google Scholar]
  93. 93. 
    Long T, Hicks M, Yu H-C, Biggs WH, Kirkness EF et al. 2017. Whole-genome sequencing identifies common-to-rare variants associated with human blood metabolites. Nat. Genet. 49:568–78
    [Google Scholar]
  94. 94. 
    Lonn E, Koskela E, Mappes T, Mokkonen M, Sims AM, Watts PC 2017. Balancing selection maintains polymorphisms at neurogenetic loci in field experiments. PNAS 114:3690–95
    [Google Scholar]
  95. 95. 
    Louis J, David JR. 1985. Ecological specialization in the Drosophila melanogaster species subgroup: a case study of D. sechellia. Acta Oecol 7:215–29
    [Google Scholar]
  96. 96. 
    Luczak S, Glatt SJ, Wall TJ 2006. Meta-analyses of ALDH2 and ADH1B with alcohol dependence in Asians. Psychol. Bull. 132:607–21
    [Google Scholar]
  97. 97. 
    Lyon MF. 2003. Transmission ratio distortion in mice. Annu. Rev. Genet. 37:393–408
    [Google Scholar]
  98. 98. 
    Macosko EZ, Pokala N, Feinberg EH, Chalasani SH, Butcher RA et al. 2009. A hub-and-spoke circuit drives pheromone attraction and social behaviour in C. elegans. Nature 458:1171–75
    [Google Scholar]
  99. 99. 
    Mandel AL, Peyrot des Gachons C, Plank KL, Alarcon S, Breslin PAS 2010. Individual differences in AMY1 gene copy number, salivary α-amylase levels, and the perception of oral starch. PLOS ONE 5:e13352
    [Google Scholar]
  100. 100. 
    Mayr E. 1963. Animal Species and Evolution Cambridge, MA: Harvard Univ. Press
  101. 101. 
    McBride CS, Baier F, Omondi AB, Spitzer SA, Lutomiah J et al. 2014. Evolution of mosquito preference for humans linked to an odorant receptor. Nature 515:222–27
    [Google Scholar]
  102. 102. 
    McGrath PT, Rockman MV, Zimmer M, Jang H, Macosko EZ et al. 2009. Quantitative mapping of a digenic behavioral trait implicates globin variation in C. elegans sensory behaviors. Neuron 61:692–99
    [Google Scholar]
  103. 103. 
    McGrath PT, Xu Y, Ailion M, Garrison JL, Butcher RA, Bargmann CI 2011. Parallel evolution of domesticated Caenorhabditis species targets pheromone receptor genes. Nature 477:321–25
    [Google Scholar]
  104. 104. 
    Merritt JR, Grogan KE, Zinzow-Kramer WM, Sun D, Ortlund EA 2020. A behavioral polymorphism caused by a single gene inside a supergene. bioRxiv 2020.01.13.897637. https://doi.org/10.1101/2020.01.13.897637
    [Crossref] [Google Scholar]
  105. 105. 
    Muñoz MM, Losos JB. 2018. Thermoregulatory behavior simultaneously promotes and forestalls evolution in a tropical lizard. Am. Nat. 191:E15–26
    [Google Scholar]
  106. 106. 
    Muralidhar P. 2019. Mating preferences of selfish sex chromosomes. Nature 570:376–79
    [Google Scholar]
  107. 107. 
    Musilova Z, Cortesi F, Matschiner M, Davies WIL, Patel JS et al. 2019. Vision using multiple distinct rod opsins in deep-sea fishes. Science 364:588–92
    [Google Scholar]
  108. 108. 
    Nakka P, Pattillo Smith S, O'Donnell-Luria AH, McManus KF, Agee M et al. 2019. Characterization of prevalence and health consequences of uniparental disomy in four million individuals from the general population. Am. J. Hum. Genet. 105:921–32
    [Google Scholar]
  109. 109. 
    Nei M, Niimura Y, Nozawa M 2008. The evolution of animal chemosensory receptor gene repertoires: roles of chance and necessity. Nat. Rev. Genet. 9:951–63
    [Google Scholar]
  110. 110. 
    Niimura Y, Nei M. 2007. Extensive gains and losses of olfactory receptor genes in mammalian evolution. PLOS ONE 2:e708
    [Google Scholar]
  111. 111. 
    Nikaido M, Suzuki H, Toyoda A, Fujiyama A, Hagino-Yamagishi K et al. 2013. Lineage-specific expansion of vomeronasal type 2 receptor-like (OlfC) genes in cichlids may contribute to diversification of amino acid detection systems. Genome Biol. Evol. 5:711–22
    [Google Scholar]
  112. 112. 
    Noble LM, Chang AS, McNelis D, Kramer M, Yen M et al. 2015. Natural variation in plep-1 causes male-male copulatory behavior in C. elegans. Curr. Biol 25:2730–37
    [Google Scholar]
  113. 113. 
    Okhovat M, Berrio A, Wallace G, Ophir AG, Phelps SM 2015. Sexual fidelity trade-offs promote regulatory variation in the prairie vole brain. Science 350:1371–74
    [Google Scholar]
  114. 114. 
    Ophir AG, Phelps SM, Sorin AB, Wolff JO 2008. Social but not genetic monogamy is associated with greater breeding success in prairie voles. Anim. Behav. 75:1143–54
    [Google Scholar]
  115. 115. 
    Paaby AB, Rockman M V 2014. Cryptic genetic variation: evolution's hidden substrate. Nat. Rev. Genet. 15:247–58
    [Google Scholar]
  116. 116. 
    Pajic P, Pavlidis P, Dean K, Neznanova L, Romano RA et al. 2019. Independent amylase gene copy number bursts correlate with dietary preferences in mammals. eLife 8:e44628
    [Google Scholar]
  117. 117. 
    Polderman TJC, Benyamin B, De Leeuw CA, Sullivan PF, Van Bochoven A et al. 2015. Meta-analysis of the heritability of human traits based on fifty years of twin studies. Nat. Genet. 47:702–9
    [Google Scholar]
  118. 118. 
    Prieto-Godino LL, Rytz R, Bargeton B, Abuin L, Arguello JR et al. 2016. Olfactory receptor pseudo-pseudogenes. Nature 539:93–97
    [Google Scholar]
  119. 119. 
    Prieto-Godino LL, Rytz R, Cruchet S, Bargeton B, Abuin L et al. 2017. Evolution of acid-sensing olfactory circuits in drosophilids. Neuron 93:661–76
    [Google Scholar]
  120. 120. 
    Ray R, Tyndale RF, Lerman C 2009. Nicotine dependence pharmacogenetics: role of genetic variation in nicotine-metabolizing enzymes. J. Neurogenet. 23:252–61
    [Google Scholar]
  121. 121. 
    Ripke S, Neale BM, Corvin A, Walters JTR, Farh K-H et al. 2014. Biological insights from 108 schizophrenia-associated genetic loci. Nature 511:421–27
    [Google Scholar]
  122. 122. 
    Robinson GE, Fernald RD, Clayton DF 2008. Genes and social behavior. Science 322:896–900
    [Google Scholar]
  123. 123. 
    Robson SKA, Kohout RJ, Beckenbach AT, Moreau CS 2015. Evolutionary transitions of complex labile traits: silk weaving and arboreal nesting in Polyrhachis ants. Behav. Ecol. Sociobiol. 69:449–58
    [Google Scholar]
  124. 124. 
    Rockman MV, Kruglyak L. 2009. Recombinational landscape and population genomics of Caenorhabditis elegans. PLOS Genet 5:e1000419
    [Google Scholar]
  125. 125. 
    Ross KG, Keller L. 1998. Genetic control of social organization in an ant. PNAS 95:14232–37
    [Google Scholar]
  126. 126. 
    Runge JN, Lindholm AK. 2018. Carrying a selfish genetic element predicts increased migration propensity in free-living wild house mice. Proc. Biol. Sci. 285:20181333
    [Google Scholar]
  127. 127. 
    Schrider DR, Kern AD. 2017. Soft sweeps are the dominant mode of adaptation in the human genome. Mol. Biol. Evol. 34:1863–77
    [Google Scholar]
  128. 128. 
    Schweizer RM, Velotta JP, Ivy CM, Jones MR, Muir SM et al. 2019. Physiological and genomic evidence that selection on the transcription factor Epas1 has altered cardiovascular function in high-altitude deer mice. PLOS Genet 15:e1008420
    [Google Scholar]
  129. 129. 
    Seeholzer LF, Seppo M, Stern DL, Ruta V 2018. Evolution of a central neural circuit underlies Drosophila mate preferences. Nature 559:564–69
    [Google Scholar]
  130. 130. 
    Shi P, Zhang J. 2006. Contrasting modes of evolution between vertebrate sweet/umami receptor genes and bitter receptor genes. Mol. Biol. Evol. 23:292–300
    [Google Scholar]
  131. 131. 
    Silver LM. 1985. Mouse t haplotypes. Annu. Rev. Genet. 19:179–208
    [Google Scholar]
  132. 132. 
    Stacey D, Fauman EB, Ziemek D, Sun BB, Harshfield EL et al. 2019. ProGeM: a framework for the prioritization of candidate causal genes at molecular quantitative trait loci. Nucleic Acids Res 47:e3
    [Google Scholar]
  133. 133. 
    Staiger EA, Almén MS, Promerová M, Brooks S, Cothran EG et al. 2017. The evolutionary history of the DMRT3 ‘Gait keeper’ haplotype. Anim. Genet. 48:551–59
    [Google Scholar]
  134. 134. 
    Stern DL. 2014. Identification of loci that cause phenotypic variation in diverse species with the reciprocal hemizygosity test. Trends Genet 30:547–54
    [Google Scholar]
  135. 135. 
    Stirling DG, Réale D, Roff DA 2002. Selection, structure and the heritability of behaviour. J. Evol. Biol. 15:277–89
    [Google Scholar]
  136. 136. 
    Sutter A, Lindholm AK. 2015. Detrimental effects of an autosomal selfish genetic element on sperm competitiveness in house mice. Proc. R. Soc. B 282:20150974
    [Google Scholar]
  137. 137. 
    Swallow DM. 2003. Genetics of lactase persistence and lactose intolerance. Annu. Rev. Genet. 37:197–219
    [Google Scholar]
  138. 138. 
    Taverner AM, Yang L, Barile ZJ, Lin B, Peng J et al. 2019. Adaptive substitutions underlying cardiac glycoside insensitivity in insects exhibit epistasis in vivo. eLife 8:e48224
    [Google Scholar]
  139. 139. 
    Thomas JW, Caceres M, Lowman JJ, Morehouse CB, Short ME et al. 2008. The chromosomal polymorphism linked to variation in social behavior in the white-throated sparrow (Zonotrichia albicollis) is a complex rearrangement and suppressor of recombination. Genetics 179:1455–68
    [Google Scholar]
  140. 140. 
    Thorgeirsson TE, Gudbjartsson DF, Surakka I, Vink JM, Amin N et al. 2010. Sequence variants at CHRNB3-CHRNA6 and CYP2A6 affect smoking behavior. Nat. Genet. 42:448–53
    [Google Scholar]
  141. 141. 
    Thorneycroft HB. 1975. A cytogenetic study of the white-throated sparrow, Zonotrichia albicollis (Gmelin). Int. J. Org. Evol. 29:611–21
    [Google Scholar]
  142. 142. 
    Tishkoff SA, Reed FA, Ranciaro A, Voight BF, Babbitt CC et al. 2007. Convergent adaptation of human lactase persistence in Africa and Europe. Nat. Genet. 39:31–40
    [Google Scholar]
  143. 143. 
    Toews DPL, Taylor SA, Streby HM, Kramer GR, Lovette IJ 2019. Selection on VPS13A linked to migration in a songbird. PNAS 116:18272–74
    [Google Scholar]
  144. 144. 
    Torgerson DG, Boyko AR, Hernandez RD, Indap A, Hu X et al. 2009. Evolutionary processes acting on candidate cis-regulatory regions in humans inferred from patterns of polymorphism and divergence. PLOS Genet 5:e1000592
    [Google Scholar]
  145. 145. 
    Wada-Katsumata A, Silverman J, Schal C 2013. Changes in taste neurons support the emergence of an adaptive behavior in cockroaches. Science 340:972–75
    [Google Scholar]
  146. 146. 
    Wallberg A, Schoning C, Webster MT, Hasselmann M 2017. Two extended haplotype blocks are associated with adaptation to high altitude habitats in East African honey bees. PLOS Genet 13:e1006792
    [Google Scholar]
  147. 147. 
    Walters RK, Polimanti R, Johnson EC, McClintick JN, Adams MJ et al. 2018. Transancestral GWAS of alcohol dependence reveals common genetic underpinnings with psychiatric disorders. Nat. Neurosci. 21:1656–69
    [Google Scholar]
  148. 148. 
    Wang J, Wurm Y, Nipitwattanaphon M, Riba-Grognuz O, Huang YC et al. 2013. A Y-like social chromosome causes alternative colony organization in fire ants. Nature 493:664–68
    [Google Scholar]
  149. 149. 
    Weber JN, Peterson BK, Hoekstra HE 2013. Discrete genetic modules are responsible for complex burrow evolution in Peromyscus mice. Nature 493:402–5
    [Google Scholar]
  150. 150. 
    Won H, de la Torre-Ubieta L, Stein JL, Parikshak NN, Huang J et al. 2016. Chromosome conformation elucidates regulatory relationships in developing human brain. Nature 538:523–27
    [Google Scholar]
  151. 151. 
    Wooding S, Bufe B, Grassi C, Howard MT, Stone AC et al. 2006. Independent evolution of bitter-taste sensitivity in humans and chimpanzees. Nature 440:930–34
    [Google Scholar]
  152. 152. 
    Wu Z, Autry AE, Bergan JF, Watabe-Uchida M, Dulac CG 2014. Galanin neurons in the medial preoptic area govern parental behaviour. Nature 509:325–30
    [Google Scholar]
  153. 153. 
    Yassin A, Debat V, Bastide H, Gidaszewski N, David JR, Pool JE 2016. Recurrent specialization on a toxic fruit in an island Drosophila population. PNAS 113:4771–76
    [Google Scholar]
  154. 154. 
    Yi X, Liang Y, Huerta-Sanchez E, Jin X, Cuo ZXP et al. 2010. Sequencing of 50 human exomes reveals adaptation to high altitude. Science 329:75–78
    [Google Scholar]
  155. 155. 
    York RA, Patil C, Abdilleh K, Johnson ZV, Conte MA et al. 2018. Behavior-dependent cis regulation reveals genes and pathways associated with bower building in cichlid fishes. PNAS 115:E11081–90
    [Google Scholar]
  156. 156. 
    Young AI, Benonisdottir S, Przeworski M, Kong A 2019. Deconstructing the sources of genotype-phenotype associations in humans. Science 365:1396–400
    [Google Scholar]
  157. 157. 
    Young AI, Frigge ML, Gudbjartsson DF, Thorleifsson G, Bjornsdottir G et al. 2018. Relatedness disequilibrium regression estimates heritability without environmental bias. Nat. Genet. 50:1304–10
    [Google Scholar]
  158. 158. 
    Young JM, Massa HF, Hsu L, Trask BJ 2010. Extreme variability among mammalian V1R gene families. Genome Res 20:10–18
    [Google Scholar]
  159. 159. 
    Young JM, Trask BJ. 2007. V2R gene families degenerated in primates, dog and cow, but expanded in opossum. Trends Genet 23:212–15
    [Google Scholar]
  160. 160. 
    Young LJ, Wang Z, Insel TR 1998. Neuroendocrine bases of monogamy. Trends Neurosci 21:71–75
    [Google Scholar]
  161. 161. 
    Zhang J, Webb DM. 2003. Evolutionary deterioration of the vomeronasal pheromone transduction pathway in catarrhine primates. PNAS 100:8337–41
    [Google Scholar]
  162. 162. 
    Zhao H, Li J, Zhang J 2015. Molecular evidence for the loss of three basic tastes in penguins. Curr. Biol. 25:R141–42
    [Google Scholar]
  163. 163. 
    Zhao H, Xu D, Zhang S, Zhang J 2012. Genomic and genetic evidence for the loss of umami taste in bats. Genome Biol. Evol. 4:73–79
    [Google Scholar]
  164. 164. 
    Zhao H, Zhou Y, Pinto CM, Charles-Dominique P, Galindo-González J et al. 2010. Evolution of the sweet taste receptor gene Tas1r2 in bats. Mol. Biol. Evol. 27:2642–50
    [Google Scholar]
  165. 165. 
    Zhen Y, Aardema ML, Medina EM, Schumer M, Andolfatto P 2012. Parallel molecular evolution in an herbivore community. Science 337:1634–37
    [Google Scholar]
  166. 166. 
    Zinzow-Kramer WM, Horton BM, McKee CD, Michaud JM, Tharp GK et al. 2015. Genes located in a chromosomal inversion are correlated with territorial song in white-throated sparrows. Genes Brain Behav 14:641–54
    [Google Scholar]
/content/journals/10.1146/annurev-genom-111219-080427
Loading
/content/journals/10.1146/annurev-genom-111219-080427
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error