Quantitative genetic analysis of brain size variation in sticklebacks: Support for the mosaic model of brain evolution

Proceedings of the Royal Society B: Biological Sciences

Volumn 282, Issue 1810, 2015, Pages

  Noreikiene, Kristina ^a   Herczeg, Gábor ^a,b   Gonda, Abigél ^a   Balázs, Gergely ^b   Husby, Arild ^a   Merilä, Juha ^a  

^a UNIVERSITY OF HELSINKI   (Finland)

^b EÖTVÖS LORÁND UNIVERSITY   (Hungary)

Author keywords

Brain size; Evolvability; Genetic correlation; Heritability; Integration

Indexed keywords

BODY SIZE; BRAIN; CORRELATION; FISH; GENETIC ANALYSIS; HERITABILITY; NATIVE SPECIES; PHENOTYPIC PLASTICITY;

GASTEROSTEUS ACULEATUS;

ANATOMY AND HISTOLOGY; ANIMAL; BRAIN; EVOLUTION; FEMALE; GENETIC VARIATION; GENETICS; MALE; ORGAN SIZE; SMEGMAMORPHA;

ANIMALS; BIOLOGICAL EVOLUTION; BRAIN; FEMALE; GENETIC VARIATION; MALE; ORGAN SIZE; SMEGMAMORPHA;

EID: 84933055016     PISSN: 09628452     EISSN: 14712954     Source Type: Journal    
DOI: 10.1098/rspb.2015.1008     Document Type: Article

References (60)

1. Falconer DS, Mackay TFC. 1996 Introduction to quantitative genetics. London, UK: Pearson Education Limited.
2. Lynch M, Walsh B. 1998 Genetics and analysis of quantitative traits. Sunderland, MA: Sinauer Assoc.
3. Lande R, Arnold SJ. 1983 The measurement of selection on correlated characters. Evolution 37, 1210–1226. (doi:10.2307/2408842)
4. Blows MW, Hoffmann AA. 2005 A reassessment of genetic limits to evolutionary change. Ecology 86, 1371–1384. (doi:10.1890/04-1209)
5. Walsh B, Blows MW. 2009 Abundant genetic variationþ strong selection¼ multivariate genetic constraints: a geometric view of adaptation. Annu. Rev. Ecol. Evol. Syst. 40, 41–59. (doi:10.1146/annurev.ecolsys.110308.120232)
6. Teplitsky C, Robinsson M, Merilä J. 2014 Evolutionary potential and constraints in wild populations. In Quantitative genetics in the wild (eds A Charmantier, D Garant, LEB Kruuk), pp. 190–208. Oxford, UK: Oxford University Press.
7. Lande R. 1979 Quantitative genetic analysis of multivariate evolution, applied to brain: body size allometry. Evolution 33, 402–416. (doi:10.2307/2407630)
8. Pagel MD, Harvey PH. 1989 Taxonomic differences in the scaling of brain on body weight among mammals. Science 244, 1589–1593. (doi:10.1126/science.2740904)
9. Striedter GF. 2005 Principles of brain evolution. Sunderland, MA: Sinauer Assoc. Inc.
10. de Winter W, Oxnard CE. 2001 Evolutionary radiations and convergences in the structural organization of mammalian brains. Nature 409, 710–714. (doi:10.1038/35055547)
11. Gómez-Robles A, Hopkins WD, Sherwood CC. 2014 Modular structure facilitates mosaic evolution of the brain in chimpanzees and humans. Nat. Comm. 5, 2041–2723. (doi:10.1038/ncomms5469)
12. Gonda A, Herczeg G, Merilä J. 2013 Evolutionary ecology of intraspecific brain size variation: a review. Ecol. Evol. 3, 2751–2764. (doi:10.1002/ece3.627)
13. Mahaney MC, Williams-Blangero S, Blangero J, Leland MM. 1993 Quantitative genetics of organ weight variation in captive baboons. Hum. Biol. 65, 991–1003.
14. Baaré WF, Pol HEH, Boomsma DI, Posthuma D, de Geus EJ, Schnack HG, van Haren EM, van Oel CJ, Kahn RS. 2001 Quantitative genetic modeling of variation in human brain morphology. Cerebral Cortex 11, 816–824. (doi:10.1093/cercor/11.9.816)
15. Toga AW, Thompson PM. 2005 Genetic of brain structure and intelligence. Annu. Rev. Neurosci. 28, 1–23. (doi:10.1146/annurev.neuro.28.061604.135655)
16. Hulshoff Pol HEH et al. 2006 Genetic contributions to human brain morphology and intelligence. J. Neurosci. 26, 10235–10242. (doi:10.1523/JNEUROSCI.1312-06.2006)
17. Peper JS, Brouwer RM, Boomsma DI, Kahn RS, Hulshoff Pol HE. 2007 Genetic influences on human brain structure: a review of brain imaging studies in twins. Hum. Brain Mapping 28, 464–473. (doi:10.1002/hbm.20398)
18. Roderick TH, Wimer RE, Wimer CC, Schwartzkroin PA. 1973 Genetic and phenotypic variation in weight of brain and spinal cord between inbred strains of mice. Brain Res. 64, 345–353. (doi:10.1016/0006-8993(73) 90188-1)
19. Atchley WR, Riska B, Kohn LA, Plummer AA, Rutledge JJ. 1984 A quantitative genetic analysis of brain and body size associations, their origin and ontogeny: data from mice. Evolution 38, 1165–1179. (doi:10.2307/2408625)
20. Riska B, Atchley W. 1985 Genetics of growth predict patterns of brain-size evolution. Science 229, 668–671. (doi:10.1126/science.229.4714.668)
21. Airey DG, Castialla-Juare H, Casella G, Pollak EJ, DeVoogd TJ. 2000 Variation in the volume of zebra finch song control nuclei is heritable: developmental and evolutionary implications. Proc. R. Soc. Lond. B 267, 2099–2104. (doi:10.1098/rspb.2000.1255)
22. Kotrschal A, Rogell B, Bundsen A, Svensson B, Zajitschek S, Brännström I, Kolm N. 2013 Artificial selection on relative brain size in the guppy reveals costs and benefits of evolving a larger brain. Curr. Biol. 23, 168–171. (doi:10.1016/j.cub.2012.11.058)
23. Barton RA, Harvey RH. 2000 Mosaic evolution of brain structure in mammals. Nature 405, 1055–1058. (doi:10.1038/35016580)
24. Finlay BL, Darlington RB. 1995 Linked regularities in the development and evolution of mammalian brains. Science 268, 1578–1584. (doi:10.1126/science.7777856)
25. Finlay BL, Darlington RB, Nicastro N. 2001 Developmental structure in brain evolution. Behav. Brain Sci. 24, 263–278. (doi:10.1017/S0140525X01003958)
26. Yopak KE, Lisney TJ, Darlington RB, Collin SP, Montgomery JC, Finlay BL. 2010 A conserved pattern of brain scaling from sharks to primates. Proc. Natl Acad. Sci. USA 107, 12946–12951. (doi:10.1073/pnas.1002195107)
27. Hager R, Lu L, Rosen GD, William RD. 2012 Genetic architecture supports mosaic brain evolution and independent brain–body size regulation. Nat. Comm. 3, 1079. (doi:10.1038/ncomms2086)
28. Kihslinger RL, Nevitt GA. 2006 Early rearing environment impacts cerebellar growth in juvenile salmon. J. Exp. Biol. 209, 504–509. (doi:10.1242/jeb.02019)
29. Gonda A, Herczeg G, Merilä J. 2009 Habitat-dependent and -independent plastic responses to social environment in the nine-spined stickleback (Pungitius pungitius) brain. Proc. R. Soc. B 276, 2085–2092. (doi:10.1098/rspb.2009.0026)
30. Gonda A, Herczeg G, Merilä J. 2011 Population variation in brain size of nine-spined sticklebacks (Pungitius pungitius)—local adaptation or environmentally induced variation? BMC Evol. Biol. 11, 75. (doi:10.1186/1471-2148-11-75)
31. Gonda A, Välimäki K, Herczeg G, Merilä J. 2012 Brain development and predation: plastic responses depend on evolutionary history. Biol. Lett. 8, 249–252. (doi:10.1098/rsbl.2011.0837)
32. Huber R, Staaden MJ, van Kaufman LS, Liem KF. 1997 Microhabitat use, trophic patterns, and the evolution of brain structure in African cichlids. Brain Behav. Evol. 50, 167–182. (doi:10.1159/000113330)
33. Pollen AA, Dobberfuhl AP, Scace J, Igulu MM, Renn SCP, Shumway CA, Hofmann HA. 2007 Environmental complexity and social organization sculpt the brain in Lake Tanganyikan cichlid fish. Brain Behav. Evol. 70, 21–39. (doi:10.1159/000101067)
34. Gonda A, Herczeg G, Merila¨ J. 2009 Adaptive brain size divergence in nine-spined sticklebacks (Pungitius pungitius)? J. Evol. Biol. 22, 1721–1726. (doi:10.1111/j.1420-9101.2009.01782.x)
35. Rohlf FJ. 2002 tpsDig, digitize landmarks and outlines, ver. 1.37. Stony Brook, NY: Department of Ecology and Evolution, State University of New York.
36. Becker WA. 1992 A manual of quantitative genetics, 5th edn. Pullman, WA: Academic Enterprises.
37. Van Oosterhout C, Hutchinson WF, Wills DP, Shipley P. 2004 MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Mol. Ecol. Notes 4, 535–538. (doi:10.1111/j.1471-8286.2004.00684.x)
38. Kalinowski ST, Taper ML, Marshall TC. 2007 Revising how the computer program CERVUS accommodates genotyping error increases success in paternity assignment. Mol. Ecol. 16, 1099–1106. (doi:10.1111/j.1365-294X.2007.03089.x)
39. Peichel K et al. 2004 The master sex determination locus in threespine sticklebacks in a nascent Y chromosome. Curr. Biol. 14, 1416–1424. (doi:10.1016/j.cub.2004.08.030)
40. Hadfield JD. 2009 MCMC methods for multi-response generalised linear mixed models: the MCMCglmm R package. J. Stat. Software 33, 1–22.
41. R Development Core Team 2011 R: a language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing.
42. Oksanen J et al. 2011 vegan: community ecology package. R package version 2.0–2. See http://CRAN.R-project.org/package=vegan.
43. Schaefer J, Opgen-Rhein R, Zuber V, Duarte Silva AP, Strimmer K. 2012 corpcor: efficient estimation of covariance and (partial) correlation. R package version 1.6.2. See http://CRAN.R-project.org/package=corpcor.
44. Garcia-Gonzalez F, Simmons LW, Tomkins JL, Kotiaho JS, Evans JP. 2012 Comparing evolvabilities: common errors surrounding the calculation and use of coefficients of additive genetic variation. Evolution 66, 2341–2349. (doi:10.1111/j.1558-5646.2011.01565.x)
45. Hansen TF, Pelabon C, Houle D. 2011 Heritability is not evolvability. Evol. Biol. 38, 258–277. (doi:10.1007/s11692-011-9127-6)
46. Iwaniuk AN, Dean KM, Nelson JE. 2004 A mosaic pattern characterizes the evolution of the avian brain. Proc. R. Soc. Lond. B 271, S148–S151. (doi:10.1098/rsbl.2003.0127)
47. Gonzalez-Voyer A, Winberg S, Kolm N. 2009 Distinct evolutionary patterns of brain and body size during adaptive radiation. Evolution 63, 2266–2274. (doi:10.1111/j.1558-5646.2009.00705.x)
48. Falconer DS. 1960 Introduction to quantitative genetics. Glasgow, UK: Robert MacLehose and Co.
49. Bartley AJ, Jones DW, Weinberger DR. 1997 Genetic variability of human brain size and cortical gyral patterns. Brain 120, 257–269. (doi:10.1093/brain/120.2.257)
50. Cheverud JM, Falk D, Vannier M, Konigsberg L, Helmkamp RC, Hildebolt C. 1990 Heritability of brain size and surface features in rhesus macaques (Macaca mulatta). J. Hered. 81, 51–57.
51. Rogers J, Kochunov P, Lancaster J, Shelledy W, Glahn D, Blangero J, Fox P. 2007 Heritability of brain volume, surface area and shape: an MRI study in an extended pedigree of baboons. Hum. Brain Mapping 28, 576–583. (doi:10.1002/hbm.20407)
52. Zupanc GKH, Horschke I, Ott R, Rascher GB. 1996 Postembryonic development of the cerebellum in gymnotiform fish. J. Comp. Neurol. 370, 443–464. (doi:10.1002/(SICI)1096-9861(19960708)370:4,443:: AID-CNE3.3.0.CO;2-4)
53. Ebbesson LOE, Braithwaite VA. 2012 Environmental effects on fish neural plasticity and cognition. J. Fish Biol. 81, 2151–2174. (doi:10.1111/j.1095-8649.2012.03486.x)
54. Kotrschal A, Rogell B, Maklakov AA, Kolm N. 2012 Sex-specific plasticity in brain morphology depends on social environment of the guppy, Poecilia reticulata. Behav. Ecol. Sociobiol. 66, 1485–1492. (doi:10.1007/s00265-012-1403-7)
55. Eifert C et al. 2015 Brain size variation in extremophile fish: local adaptation versus phenotypic plasticity. J. Zool. 295, 143–153. (doi:10.1111/jzo.12190)
56. Park PJ, Chase I, Bell MA. 2012 Phenotypic plasticity of the threespine stickleback Gasterosteus aculeatus telencephalon in response to experience in captivity. Curr. Zool. 58, 189–210.
57. Houle D. 1992 Comparing evolvability and variability of quantitative traits. Genetics 130, 195–204.
58. Miller GF, Penke L. 2007 The evolution of human intelligence and the coefficient of additive genetic variance in human brain size. Intelligence 35, 97–114. (doi:10.1016/j.intell.2006.08.008)
59. Quinn JL, Charmantier A, Garant D, Sheldon BC. 2006 Data depth, data completeness, and their influence on quantitative genetic estimation in two contrasting bird populations. J. Evol. Biol. 19, 994–1002. (doi:10.1111/j.1420-9101.2006.01081.x)
60. Guidelines for the treatment of animals in behavioural research and teaching. Anim. Behav. 83, 301–309. (doi:10.1016/j.anbehav.2011.10.031)