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Social Interactions and Indirect Genetic Effects on Complex Juvenile and Adult Traits

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Book cover Systems Genetics

Part of the book series: Methods in Molecular Biology ((MIMB,volume 1488))

Abstract

Most animal species are social in one form or another, yet many studies in rodent model systems use either individually housed animals or ignore potential confounds caused by group housing. While such social interaction effects on developmental and behavioral traits are well established, the genetic basis of social interactions has not been researched in as much detail. Specifically, the effects of genetic variation in social partners on the phenotype of a focal individual have mostly been studied at the phenotypic level. Such indirect genetic effects (IGEs), where the genotype of one individual influences the phenotype of a second individual, can have important evolutionary and medically relevant consequences. In this chapter, we give a brief outline of social interaction effects, and how systems genetics approaches using recombinant inbred populations can be used to investigate indirect genetic effects specifically, including maternal genetic effects. We discuss experimental designs for the study of IGEs and show how indirect genetic loci can be identified that underlie social interaction effects, their mechanisms, and consequences for trait variation in focal individuals.

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References

  1. Arndt SS, Laarakker MC, van Lith HA et al (2009) Individual housing of mice—impact on behaviour and stress responses. Physiol Behav 97:385–393. doi:10.1016/j.physbeh.2009.03.008

    Article  CAS  PubMed  Google Scholar 

  2. Mashoodh R, Franks B, Curley JP, Champagne FA (2012) Paternal social enrichment effects on maternal behavior and offspring growth. Proc Natl Acad Sci U S A 109(Suppl):17232–17238. doi:10.1073/pnas.1121083109

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Hager R, Johnstone RA (2006) The influence of phenotypic and genetic effects on maternal provisioning and offspring weight gain in mice. Biol Lett 2:81–84. doi:10.1098/rsbl.2005.0403

    Article  PubMed  Google Scholar 

  4. Frank SA (2007) All of life is social. Curr Biol 17:R648–R650. doi:10.1016/j.cub.2007.06.005

    Article  CAS  PubMed  Google Scholar 

  5. Whitney G, Coble JR, Stockton MD, Tilson EF (1973) Ultrasonic emissions: do they facilitate courtship of mice? J Comp Physiol Psychol 84:445–452. doi:10.1037/h0034899

    Article  CAS  PubMed  Google Scholar 

  6. Doty RL (1974) A cry for the liberation of the female rodent: courtship and copulation in rodentia. Psychol Bull 81:159–172. doi:10.1037/h0035971

    Article  CAS  PubMed  Google Scholar 

  7. Neunuebel JP, Taylor AL, Arthur BJ, Egnor SR (2015) Female mice ultrasonically interact with males during courtship displays. Elife doi:10.7554/eLife.06203

    Google Scholar 

  8. Cox KH, Rissman EF (2011) Sex differences in juvenile mouse social behavior are influenced by sex chromosomes and social context. Genes Brain Behav 10:465–472. doi:10.1111/j.1601-183X.2011.00688.x

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Lukas M, Wöhr M (2015) Endogenous vasopressin, innate anxiety, and the emission of pro-social 50-kHz ultrasonic vocalizations during social play behavior in juvenile rats. Psychoneuroendocrinology 56:35–44. doi:10.1016/j.psyneuen.2015.03.005

    Article  CAS  PubMed  Google Scholar 

  10. Anholt RRH, Mackay TFC (2012) Genetics of aggression. Annu Rev Genet 46:145–164. doi:10.1146/annurev-genet-110711-155514

    Article  CAS  PubMed  Google Scholar 

  11. Wilson AJ, Gelin U, Perron M-C, Reale D (2009) Indirect genetic effects and the evolution of aggression in a vertebrate system. Proc R Soc B Biol Sci 276:533–541. doi:10.1098/rspb.2008.1193

    Article  Google Scholar 

  12. Smiseth PT, Kölliker M, Royle NJ (2012) What is parental care? In: Royle NJ, Smiseth PT, Kölliker M (eds) Evolution of parent care, 1st edn. Oxford University Press, Oxford, pp 1–18

    Chapter  Google Scholar 

  13. Hunt J, Simmons LW (2002) The genetics of maternal care: direct and indirect genetic effects on phenotype in the dung beetle Onthophagus taurus. Proc Natl Acad Sci U S A 99:6828–6832. doi:10.1073/pnas.092676199

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Kölliker M, Richner H (2001) Parent–offspring conflict and the genetics of offspring solicitation and parental response. Anim Behav 62:395–407. doi:10.1006/anbe.2001.1792

    Article  Google Scholar 

  15. Kölliker M, Brinkhof MWG, Heeb P et al (2000) The quantitative genetic basis of offspring solicitation and parental response in a passerine bird with biparental care. Proc R Soc B Biol Sci 267:2127–2132. doi:10.1098/rspb.2000.1259

    Article  Google Scholar 

  16. Moore AJ, Brodie ED III, Wolf JB (1997) Interacting phenotypes and the evolutionary process: I. Direct and indirect genetic effects of social interactions. Evolution 51:1352–1362. doi:10.2307/2411187

    Article  Google Scholar 

  17. Moore AJ, Haynes KF, Preziosi RF, Moore PJ (2002) The evolution of interacting phenotypes: genetics and evolution of social dominance. Am Nat 160(Suppl):S186–S197. doi:10.1086/342899

    Article  PubMed  Google Scholar 

  18. Wolf JB, Brodie ED III, Moore AJ (1999) Interacting phenotypes and the evolutionary process. II. Selection resulting from social interactions. Am Nat 153:254–266. doi:10.1086/303168

    Article  Google Scholar 

  19. Trivers RL (1974) Parent-offspring conflict. Am Zool 14:249–264. doi:10.1093/icb/14.1.249

    Article  Google Scholar 

  20. Wolf JB, Brodie ED III, Cheverud JM et al (1998) Evolutionary consequences of indirect genetic effects. Trends Ecol Evol 13:64–69. doi:10.1016/S0169-5347(97)01233-0

    Article  CAS  PubMed  Google Scholar 

  21. Cheverud JM (2003) Evolution in a genetically heritable social environment. Proc Natl Acad Sci 100:4357–4359. doi:10.1073/pnas.0931311100

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Kölliker M, Brodie ED III, Moore AJ (2005) The coadaptation of parental supply and offspring demand. Am Nat 166:506–516. doi:10.1086/491687

    Article  PubMed  Google Scholar 

  23. West-Eberhard MJ (1983) Sexual selection, social competition, and speciation. Q Rev Biol 58:155–183. doi:10.2307/2828804

    Article  Google Scholar 

  24. Trubenová B, Hager R (2014) Social selection and indirect genetic effects in structured populations. Evol Biol 41:123–133. doi:10.1007/s11692-013-9252-5

    PubMed  Google Scholar 

  25. Agrawal AF, Brodie ED III, Wade MJ (2001) On indirect genetic effects in structured populations. Am Nat 158:308–323. doi:10.1086/321324

    Article  CAS  PubMed  Google Scholar 

  26. McGlothlin JW, Brodie ED III (2009) How to measure indirect genetic effects: the congruence of trait-based and variance-partitioning approaches. Evolution 63:1785–1795. doi:10.1111/j.1558-5646.2009.00676.x

    Article  PubMed  Google Scholar 

  27. Bijma P (2010) Multilevel selection 4: modeling the relationship of indirect genetic effects and group size. Genetics 186:1029–1031. doi:10.1534/genetics.110.120485

    Article  PubMed  PubMed Central  Google Scholar 

  28. Teplitsky C, Mills JA, Yarrall JW, Merilä J (2010) Indirect genetic effects in a sex-limited trait: the case of breeding time in red-billed gulls. J Evol Biol 23:935–944. doi:10.1111/j.1420-9101.2010.01959.x

    Article  CAS  PubMed  Google Scholar 

  29. Wolf JB (2003) Genetic architecture and evolutionary constraint when the environment contains genes. Proc Natl Acad Sci U S A 100:4655–4660. doi:10.1073/pnas.0635741100

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Mutic JJ, Wolf JB (2007) Indirect genetic effects from ecological interactions in Arabidopsis thaliana. Mol Ecol 16:2371–2381. doi:10.1111/j.1365-294X.2007.03259.x

    Article  CAS  PubMed  Google Scholar 

  31. Kirkpatrick M, Lande R (1989) The evolution of maternal characters. Evolution 43:485. doi:10.2307/2409054

    Article  Google Scholar 

  32. Wolf JB, Wade MJ (2009) What are maternal effects (and what are they not)? Philos Trans R Soc B Biol Sci 364:1107–1115. doi:10.1098/rstb.2008.0238

    Article  Google Scholar 

  33. Wolf J, Cheverud JM (2012) Detecting maternal-effect loci by statistical cross-fostering. Genetics 191:261–277. doi:10.1534/genetics.111.136440

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Dickerson GE (1947) Composition of hog carcasses as influenced by heritable differences in rate and economy of gain. Res Bull Iowa Agric Exp Stn 354:489–524

    Google Scholar 

  35. Willham RL (1963) The covariance between relatives for characters composed of components contributed by related individuals. Biometrics 19:18–27. doi:10.2307/2527570

    Article  Google Scholar 

  36. Willham RL (1972) The role of maternal effects in animal breeding. 3. Biometrical aspects of maternal effects in animals. J Anim Sci 35:1288–1293

    Article  CAS  PubMed  Google Scholar 

  37. Hanrahan JP, Eisen EJ (1973) Sexual dimorphism and direct and maternal genetic effects on body weight in mice. Theor Appl Genet 43:39–45. doi:10.1007/BF00277832

    Article  CAS  PubMed  Google Scholar 

  38. Hanrahan JP (1976) Maternal effects and selection response with an application to sheep data. Anim Prod 22:359–369. doi:10.1017/S0003356100035637

    Article  Google Scholar 

  39. Ellen ED, Rodenburg TB, Albers GAA et al (2014) The prospects of selection for social genetic effects to improve welfare and productivity in livestock. Front Genet 5:377. doi:10.3389/fgene.2014.00377

    Article  PubMed  PubMed Central  Google Scholar 

  40. Falconer DS, Mackay TFC (1996) Introduction to quantitative genetics, 4th edn. Longman, Burnt Mill

    Google Scholar 

  41. Harris WE, Hager R (2009) On the evolution of reproductive skew: a genetical view. In: Hager R, Jones CB (eds) Reproductive skew in vertebrates. Cambridge University Press, Cambridge, pp 467–479

    Chapter  Google Scholar 

  42. Cheverud JM, Moore AJ (1994) Quantitative genetics and the role of the environment provided by relatives in behavioral evolution. In: Boake CRB (ed) Quantitative genetic studies of behavioral evolution. University of Chicago Press, Chicago, IL, pp 67–100

    Google Scholar 

  43. Wolf JB, Brodie ED III (1998) The coadaptation of parental and offspring characters. Evolution 52:299–308. doi:10.2307/2411068

    Article  Google Scholar 

  44. Bijma P, Wade MJ (2008) The joint effects of kin, multilevel selection and indirect genetic effects on response to genetic selection. J Evol Biol 21:1175–1188. doi:10.1111/j.1420-9101.2008.01550.x

    Article  CAS  PubMed  Google Scholar 

  45. McGlothlin JW, Moore AJ, Wolf JB, Brodie ED III (2010) Interacting phenotypes and the evolutionary process. III. Social evolution. Evolution 64:2558–2574. doi:10.1111/j.1558-5646.2010.01012.x

    Article  PubMed  Google Scholar 

  46. Hager R, Lu L, Rosen GD, Williams RW (2012) Genetic architecture supports mosaic brain evolution and independent brain-body size regulation. Nat Commun 3:1079. doi:10.1038/ncomms2086

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  47. Trubenová B, Hager R (2012) Phenotypic and evolutionary consequences of social behaviours: interactions among individuals affect direct genetic effects. PLoS One 7:e46273. doi:10.1371/journal.pone.0046273

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  48. Cheverud JM (1984) Evolution by kin selection: a quantitative genetic model illustrated by maternal performance in mice. Evolution (NY) 38:766. doi:10.2307/2408388

    Article  Google Scholar 

  49. Wolf JB, Vaughn TT, Pletscher LS, Cheverud JM (2002) Contribution of maternal effect QTL to genetic architecture of early growth in mice. Heredity (Edinb) 89:300–310. doi:10.1038/sj.hdy.6800140

    Article  CAS  Google Scholar 

  50. Petfield D, Chenoweth SF, Rundle HD, Blows MW (2005) Genetic variance in female condition predicts indirect genetic variance in male sexual display traits. Proc Natl Acad Sci U S A 102:6045–6050. doi:10.1073/pnas.0409378102

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Camerlink I, Turner SP, Bijma P, Bolhuis JE (2013) Indirect genetic effects and housing conditions in relation to aggressive behaviour in pigs. PLoS One 8:e65136. doi:10.1371/journal.pone.0065136

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Bailey NW, Hoskins JL (2014) Detecting cryptic indirect genetic effects. Evolution 68:1871–1882. doi:10.1111/evo.12401

    Article  PubMed  PubMed Central  Google Scholar 

  53. Donohue K (2003) Setting the stage: phenotypic plasticity as habitat selection. Int J Plant Sci 164:S79–S92. doi:10.1086/368397

    Article  Google Scholar 

  54. Haley CS, Knott SA (1992) A simple regression method for mapping quantitative trait loci in line crosses using flanking markers. Heredity (Edinb) 69:315–324. doi:10.1038/hdy.1992.131

    Article  CAS  Google Scholar 

  55. McAdam AG, Boutin S, Réale D, Berteaux D (2002) Maternal effects and the potential for evolution in a natural population of animals. Evolution 56:846–851

    Article  PubMed  Google Scholar 

  56. Neser FWC, Erasmus GJ, van Wyk JB (2001) Genetic parameter estimates for pre-weaning weight traits in Dorper sheep. Small Rumin Res 40:197–202. doi:10.1016/S0921-4488(01)00172-9

    Article  PubMed  Google Scholar 

  57. Aggrey SE, Cheng KM (1993) Genetic and posthatch parental influences on growth in pigeon squabs. J Hered 84:184–187

    Google Scholar 

  58. Smith HG, Wettermark KJ (1995) Heritability of nestling growth in cross-fostered European Starlings Sturnus vulgaris. Genetics 141:657–665

    CAS  PubMed  PubMed Central  Google Scholar 

  59. Rauter CM, Moore AJ (2002) Evolutionary importance of parental care performance, food resources, and direct and indirect genetic effects in a burying beetle. J Evol Biol 15:407–417. doi:10.1046/j.1420-9101.2002.00412.x

    Article  Google Scholar 

  60. Rauter CM, Moore AJ (2002) Quantitative genetics of growth and development time in the burying beetle Nicrophorus pustulatus in the presence and absence of post-hatching parental care. Evolution 56:96–110. doi:10.1554/0014-3820(2002)056[0096:QGOGAD]2.0.CO;2

    Article  PubMed  Google Scholar 

  61. Head ML, Berry LK, Royle NJ, Moore AJ (2012) Paternal care: direct and indirect genetic effects of fathers on offspring performance. Evolution 66:3570–3581. doi:10.1111/j.1558-5646.2012.01699.x

    Article  PubMed  Google Scholar 

  62. Cheverud JM, Leamy LJ, Atchley WR, Rutledge JJ (1983) Quantitative genetics and the evolution of ontogeny: I. Ontogenetic changes in quantitative genetic variance components in randombred mice. Genet Res 42:65. doi:10.1017/S0016672300021492

    Article  Google Scholar 

  63. Riska B, Rutledge JJ, Atchley WR (1985) Covariance between direct and maternal genetic effects in mice, with a model of persistent environmental influences. Genet Res 45:287–297. doi:10.1017/S0016672300022278

    Article  CAS  PubMed  Google Scholar 

  64. Nagai J, Bakker H, Eisen EJ (1976) Partitioning average and heterotic components of direct and maternal genetic effects on growth in mice using crossfostering techniques. Genetics 84:113–124

    CAS  PubMed  PubMed Central  Google Scholar 

  65. Williams WR, Eisen EJ, Nagai J, Bakker H (1978) Direct and maternal genetic effects on body weight maturing patterns in mice. Theor Appl Genet 51:249–260. doi:10.1007/BF00273772

    Article  CAS  PubMed  Google Scholar 

  66. Cheverud JM, Leamy LJ (1985) Quantitative genetics and the evolution of ontogeny. III. Ontogenetic changes in correlation structure among live-body traits in randombred mice. Genet Res 46:325–335. doi:10.1017/S0016672300022813

    Article  CAS  PubMed  Google Scholar 

  67. Cheverud JM, Routman EJ, Duarte FA et al (1996) Quantitative trait loci for murine growth. Genetics 142:1305–1319

    CAS  PubMed  PubMed Central  Google Scholar 

  68. Vaughn TT, Pletscher LS, Peripato A et al (1999) Mapping quantitative trait loci for murine growth: a closer look at genetic architecture. Genet Res 74:313–322

    Article  CAS  PubMed  Google Scholar 

  69. Cowley DE, Pomp D, Atchley WR et al (1989) The impact of maternal uterine genotype on postnatal growth and adult body size in mice. Genetics 122:193–203

    CAS  PubMed  PubMed Central  Google Scholar 

  70. Casellas J, Farber CR, Gularte RJ et al (2009) Evidence of maternal QTL affecting growth and obesity in adult mice. Mamm Genome 20:269–280. doi:10.1007/s00335-009-9182-9

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  71. Wolf JB, Leamy LJ, Roseman CC, Cheverud JM (2011) Disentangling prenatal and postnatal maternal genetic effects reveals persistent prenatal effects on offspring growth in mice. Genetics 189:1069–1082. doi:10.1534/genetics.111.130591

    Article  PubMed  PubMed Central  Google Scholar 

  72. Drews C (1993) The concept and definition of dominance in animal behaviour. Behaviour 125:283–313. doi:10.1163/156853993X00290

    Article  Google Scholar 

  73. Herberholz J, McCurdy C, Edwards DH (2007) Direct benefits of social dominance in juvenile crayfish. Biol Bull 213:21–27

    Article  PubMed  Google Scholar 

  74. Willisch CS, Neuhaus P (2010) Social dominance and conflict reduction in rutting male Alpine ibex, Capra ibex. Behav Ecol 21:372–380. doi:10.1093/beheco/arp200

    Article  Google Scholar 

  75. Franck D, Ribowski A (1993) Dominance hierarchies of male green swordtails (Xiphophorus helleri) in nature. J Fish Biol 43:497–499. doi:10.1111/j.1095-8649.1993.tb00586.x

    Article  Google Scholar 

  76. Wilson AJ, Morrissey MB, Adams MJ et al (2011) Indirect genetics effects and evolutionary constraint: an analysis of social dominance in red deer, Cervus elaphus. J Evol Biol 24:772–783. doi:10.1111/j.1420-9101.2010.02212.x

    Article  CAS  PubMed  Google Scholar 

  77. Sartori C, Mantovani R (2013) Indirect genetic effects and the genetic bases of social dominance: evidence from cattle. Heredity (Edinb) 110:3–9. doi:10.1038/hdy.2012.56

    Article  CAS  Google Scholar 

  78. Moore AJ (2013) Genetic influences on social dominance: cow wars. Heredity (Edinb) 110:1–2. doi:10.1038/hdy.2012.85

    Article  CAS  Google Scholar 

  79. Bechstein P, Rehbach N-J, Yuhasingham G et al (2014) The clock gene Period1 regulates innate routine behaviour in mice. Proc Biol Sci 281:20140034. doi:10.1098/rspb.2014.0034

    Article  PubMed  PubMed Central  Google Scholar 

  80. Zakany J, Duboule D (2012) A genetic basis for altered sexual behavior in mutant female mice. Curr Biol 22:1676–1680. doi:10.1016/j.cub.2012.06.067

    Article  CAS  PubMed  Google Scholar 

  81. Kent C, Azanchi R, Smith B et al (2008) Social context influences chemical communication in D. melanogaster males. Curr Biol 18:1384–1389. doi:10.1016/j.cub.2008.07.088

    Article  CAS  PubMed  Google Scholar 

  82. Bleakley BH, Brodie ED III (2009) Indirect genetic effects influence antipredator behavior in guppies: estimates of the coefficient of interaction psi and the inheritance of reciprocity. Evolution 63:1796–1806. doi:10.1111/j.1558-5646.2009.00672.x

    Article  PubMed  Google Scholar 

  83. Miller CW, Moore AJ (2007) A potential resolution to the lek paradox through indirect genetic effects. Proc R Soc B Biol Sci 274:1279–1286. doi:10.1098/rspb.2006.0413

    Article  Google Scholar 

  84. Bijma P, Muir WM, Ellen ED et al (2007) Multilevel selection 2: estimating the genetic parameters determining inheritance and response to selection. Genetics 175:289–299. doi:10.1534/genetics.106.062729

    Article  PubMed  PubMed Central  Google Scholar 

  85. Carlier M, Roubertoux P, Cohen-Salmon C (1982) Differences in patterns of pup care in Mus musculus domesticus I—comparisons between eleven inbred strains. Behav Neural Biol 35:205–210. doi:10.1016/S0163-1047(82)91213-4

    Article  CAS  PubMed  Google Scholar 

  86. Klug H, Bonsall MB (2014) What are the benefits of parental care? The importance of parental effects on developmental rate. Ecol Evol 4:2330–2351. doi:10.1002/ece3.1083

    Article  PubMed  PubMed Central  Google Scholar 

  87. McIver AH, Jeffrey WE (1967) Strain differences in maternal behavior in rats. Behaviour 28:210–216. doi:10.1163/156853967X00244

    Article  CAS  PubMed  Google Scholar 

  88. Myers MM, Brunelli SA, Shair HN et al (1989) Relationships between maternal behavior of SHR and WKY dams and adult blood pressures of cross-fostered F1 pups. Dev Psychobiol 22:55–67. doi:10.1002/dev.420220105

    Article  CAS  PubMed  Google Scholar 

  89. Champagne FA, Curley JP, Keverne EB, Bateson PPG (2007) Natural variations in postpartum maternal care in inbred and outbred mice. Physiol Behav 91:325–334. doi:10.1016/j.physbeh.2007.03.014

    Article  CAS  PubMed  Google Scholar 

  90. Chourbaji S, Hoyer C, Richter SH et al (2011) Differences in mouse maternal care behavior – is there a genetic impact of the glucocorticoid receptor? PLoS One 6:e19218. doi:10.1371/journal.pone.0019218

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  91. Peripato AC, Cheverud JM (2002) Genetic influences on maternal care. Am Nat 160(Suppl):S173–S185. doi:10.1086/342900

    Article  PubMed  Google Scholar 

  92. Peripato AC, De Brito RA, Vaughn TT et al (2002) Quantitative trait loci for maternal performance for offspring survival in mice. Genetics 162:1341–1353

    CAS  PubMed  PubMed Central  Google Scholar 

  93. Anisman H, Zaharia MD, Meaney MJ, Merali Z (1998) Do early-life events permanently alter behavioral and hormonal responses to stressors? Int J Dev Neurosci 16:149–164. doi:10.1016/S0736-5748(98)00025-2

    Article  CAS  PubMed  Google Scholar 

  94. Akers KG, Nakazawa M, Romeo RD et al (2006) Early life modulators and predictors of adult synaptic plasticity. Eur J Neurosci 24:547–554. doi:10.1111/j.1460-9568.2006.04921.x

    Article  PubMed  Google Scholar 

  95. Branchi I, Cirulli F (2014) Early experiences: building up the tools to face the challenges of adult life. Dev Psychobiol 56:1661–1674. doi:10.1002/dev.21235

    Article  PubMed  Google Scholar 

  96. Lerch S, Brandwein C, Dormann C et al (2014) What makes a good mother? Implication of inter-, and intrastrain strain “cross fostering” for emotional changes in mouse offspring. Behav Brain Res 274:270–281. doi:10.1016/j.bbr.2014.08.021

    Article  PubMed  Google Scholar 

  97. Priebe K, Brake WG, Romeo RD et al (2005) Maternal influences on adult stress and anxiety-like behavior in C57BL/6J and BALB/cJ mice: a cross-fostering study. Dev Psychobiol 47:398–407. doi:10.1002/dev.20098

    Article  CAS  PubMed  Google Scholar 

  98. Holmes A, le Guisquet AM, Vogel E et al (2005) Early life genetic, epigenetic and environmental factors shaping emotionality in rodents. Neurosci Biobehav Rev 29:1335–1346. doi:10.1016/j.neubiorev.2005.04.012

    Article  PubMed  Google Scholar 

  99. Francis DD, Champagne FA, Liu D, Meaney MJ (1999) Maternal care, gene expression, and the development of individual differences in stress reactivity. Ann N Y Acad Sci 896:66–84. doi:10.1111/j.1749-6632.1999.tb08106.x

    Article  CAS  PubMed  Google Scholar 

  100. Liu D, Diorio J, Tannenbaum B et al (1997) Maternal care, hippocampal glucocorticoid receptors, and hypothalamic-pituitary-adrenal responses to stress. Science 277:1659–1662. doi:10.1126/science.277.5332.1659

    Article  CAS  PubMed  Google Scholar 

  101. Caldji C, Diorio J, Anisman H, Meaney MJ (2004) Maternal behavior regulates benzodiazepine/GABAA receptor subunit expression in brain regions associated with fear in BALB/c and C57BL/6 mice. Neuropsychopharmacology 29:1344–1352. doi:10.1038/sj.npp.1300436

    Article  CAS  PubMed  Google Scholar 

  102. Francis DD, Champagne FC, Meaney MJ (2000) Variations in maternal behaviour are associated with differences in oxytocin receptor levels in the rat. J Neuroendocrinol 12:1145–1148. doi:10.1046/j.1365-2826.2000.00599.x

    Article  CAS  PubMed  Google Scholar 

  103. Boccia ML, Pedersen CA (2001) Brief vs. long maternal separations in infancy: contrasting relationships with adult maternal behavior and lactation levels of aggression and anxiety. Psychoneuroendocrinology 26:657–672. doi:10.1016/S0306-4530(01)00019-1

    Article  CAS  PubMed  Google Scholar 

  104. Champagne FA, Weaver ICG, Diorio J et al (2003) Natural variations in maternal care are associated with estrogen receptor alpha expression and estrogen sensitivity in the medial preoptic area. Endocrinology 144:4720–4724. doi:10.1210/en.2003-0564

    Article  CAS  PubMed  Google Scholar 

  105. Champagne FA, Francis DD, Mar A, Meaney MJ (2003) Variations in maternal care in the rat as a mediating influence for the effects of environment on development. Physiol Behav 79:359–371. doi:10.1016/S0031-9384(03)00149-5

    Article  CAS  PubMed  Google Scholar 

  106. Weaver ICG, Diorio J, Seckl JR et al (2004) Early environmental regulation of hippocampal glucocorticoid receptor gene expression: characterization of intracellular mediators and potential genomic target sites. Ann N Y Acad Sci 1024:182–212. doi:10.1196/annals.1321.099

    Article  CAS  PubMed  Google Scholar 

  107. Weaver ICG, Cervoni N, Champagne FA et al (2004) Epigenetic programming by maternal behavior. Nat Neurosci 7:847–854. doi:10.1038/nn1276

    Article  CAS  PubMed  Google Scholar 

  108. Veenema AH, Blume A, Niederle D et al (2006) Effects of early life stress on adult male aggression and hypothalamic vasopressin and serotonin. Eur J Neurosci 24:1711–1720. doi:10.1111/j.1460-9568.2006.05045.x

    Article  PubMed  Google Scholar 

  109. Veenema AH, Bredewold R, Neumann ID (2007) Opposite effects of maternal separation on intermale and maternal aggression in C57BL/6 mice: link to hypothalamic vasopressin and oxytocin immunoreactivity. Psychoneuroendocrinology 32:437–450. doi:10.1016/j.psyneuen.2007.02.008

    Article  CAS  PubMed  Google Scholar 

  110. Murgatroyd C, Patchev AV, Wu Y et al (2010) Dynamic DNA methylation programs persistent adverse effects of early-life stress. Nat Neurosci 13:649. doi:10.1038/nn0510-649e

    Article  CAS  Google Scholar 

  111. Curley JP, Rock V, Moynihan AM et al (2010) Developmental shifts in the behavioral phenotypes of inbred mice: the role of postnatal and juvenile social experiences. Behav Genet 40:220–232. doi:10.1007/s10519-010-9334-4

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  112. Gudsnuk KMA, Champagne FA (2011) Epigenetic effects of early developmental experiences. Clin Perinatol 38:703–717. doi:10.1016/j.clp.2011.08.005

    Article  PubMed  Google Scholar 

  113. Curley JP, Jensen CL, Mashoodh R, Champagne FA (2011) Social influences on neurobiology and behavior: epigenetic effects during development. Psychoneuroendocrinology 36:352–371. doi:10.1016/j.psyneuen.2010.06.005

    Article  CAS  PubMed  Google Scholar 

  114. Veenema AH (2012) Toward understanding how early-life social experiences alter oxytocin- and vasopressin-regulated social behaviors. Horm Behav 61:304–312. doi:10.1016/j.yhbeh.2011.12.002

    Article  CAS  PubMed  Google Scholar 

  115. Franks B, Champagne FA, Curley JP (2015) Postnatal maternal care predicts divergent weaning strategies and the development of social behavior. Dev Psychobiol 57(7):809–817. doi:10.1002/dev.21326

    Article  CAS  PubMed  Google Scholar 

  116. Wells JCK (2007) The thrifty phenotype as an adaptive maternal effect. Biol Rev 82:143–172. doi:10.1111/j.1469-185X.2006.00007.x

    Article  PubMed  Google Scholar 

  117. Lunde A, Melve KK, Gjessing HK et al (2007) Genetic and environmental influences on birth weight, birth length, head circumference, and gestational age by use of population-based parent-offspring data. Am J Epidemiol 165:734–741. doi:10.1093/aje/kwk107

    Article  PubMed  Google Scholar 

  118. Barker DJP, Eriksson JG, Forsén T, Osmond C (2002) Fetal origins of adult disease: strength of effects and biological basis. Int J Epidemiol 31:1235–1239. doi:10.1093/ije/31.6.1235

    Article  CAS  PubMed  Google Scholar 

  119. Ressler RH (1962) Parental handling in two strains of mice reared by foster parents. Science 137:129–130. doi:10.1126/science.137.3524.129

    Article  CAS  PubMed  Google Scholar 

  120. Bester-Meredith JK, Marler CA (2001) Vasopressin and aggression in cross-fostered California Mice (Peromyscus californicus) and White-Footed Mice (Peromyscus leucopus). Horm Behav 40:51–64. doi:10.1006/hbeh.2001.1666

    Article  CAS  PubMed  Google Scholar 

  121. Champagne FA, Weaver ICG, Diorio J et al (2006) Maternal care associated with methylation of the estrogen receptor-α1b promoter and estrogen receptor-α expression in the medial preoptic area of female offspring. Endocrinology 147:2909–2915. doi:10.1210/en.2005-1119

    Article  CAS  PubMed  Google Scholar 

  122. Hager R, Cheverud JM, Wolf JB (2009) Change in maternal environment induced by cross-fostering alters genetic and epigenetic effects on complex traits in mice. Proc Biol Sci 276:2949–2954. doi:10.1098/rspb.2009.0515

    Article  PubMed  PubMed Central  Google Scholar 

  123. Cox KH, So NLT, Rissman EF (2013) Foster dams rear fighters: strain-specific effects of within-strain fostering on aggressive behavior in male mice. PLoS One 8:e75037. doi:10.1371/journal.pone.0075037

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  124. Peña CJ, Neugut YD, Champagne FA (2013) Developmental timing of the effects of maternal care on gene expression and epigenetic regulation of hormone receptor levels in female rats. Endocrinology 154:4340–4351. doi:10.1210/en.2013-1595

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  125. Gouldsborough I, Black V, Johnson IT, Ashton N (1998) Maternal nursing behaviour and the delivery of milk to the neonatal spontaneously hypertensive rat. Acta Physiol Scand 162:107–114. doi:10.1046/j.1365-201X.1998.0273f.x

    Article  CAS  PubMed  Google Scholar 

  126. Caldji C, Diorio J, Meaney MJ (2000) Variations in maternal care in infancy regulate the development of stress reactivity. Biol Psychiatry 48:1164–1174. doi:10.1016/S0006-3223(00)01084-2

    Article  CAS  PubMed  Google Scholar 

  127. Cameron NM, Fish EW, Meaney MJ (2008) Maternal influences on the sexual behavior and reproductive success of the female rat. Horm Behav 54:178–184. doi:10.1016/j.yhbeh.2008.02.013

    Article  PubMed  Google Scholar 

  128. Lande R, Kirkpatrick M (1990) Selection response in traits with maternal inheritance. Genet Res 55:189–197

    Article  CAS  PubMed  Google Scholar 

  129. Wilson AJ, Coltman DW, Pemberton JM et al (2004) Maternal genetic effects set the potential for evolution in a free-living vertebrate population. J Evol Biol 18:405–414. doi:10.1111/j.1420-9101.2004.00824.x

    Article  Google Scholar 

  130. Nephew B, Murgatroyd C (2013) The role of maternal care in shaping CNS function. Neuropeptides 47:371–378. doi:10.1016/j.npep.2013.10.013

    Article  CAS  PubMed  Google Scholar 

  131. Kruuk LEB, Hadfield JD (2007) How to separate genetic and environmental causes of similarity between relatives. J Evol Biol 20:1890–1903. doi:10.1111/j.1420-9101.2007.01377.x

    Article  CAS  PubMed  Google Scholar 

  132. Lock JE, Smiseth PT, Moore AJ (2004) Selection, inheritance, and the evolution of parent-offspring interactions. Am Nat 164:13–24. doi:10.1086/421444

    Article  PubMed  Google Scholar 

  133. Aldhous P (1989) The effects of individual cross-fostering on the development of intrasexual kin discrimination in male laboratory mice, Mus musculus. Anim Behav 37:741–750. doi:10.1016/0003-3472(89)90060-2

    Article  Google Scholar 

  134. Penn D, Potts W (1998) MHC-disassortative mating preferences reversed by cross-fostering. Proc Biol Sci 265:1299–1306. doi:10.1098/rspb.1998.0433

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  135. Matthews PA, Samuelsson A-M, Seed P et al (2011) Fostering in mice induces cardiovascular and metabolic dysfunction in adulthood. J Physiol 589:3969–3981. doi:10.1113/jphysiol.2011.212324

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  136. Wattez J-S, Delahaye F, Barella LF et al (2014) Short- and long-term effects of maternal perinatal undernutrition are lowered by cross-fostering during lactation in the male rat. J Dev Orig Health Dis 5:109–120. doi:10.1017/S2040174413000548

    Article  CAS  PubMed  Google Scholar 

  137. van Vugt RWM, Meyer F, van Hulten JA et al (2014) Maternal care affects the phenotype of a rat model for schizophrenia. Front Behav Neurosci 8:268. doi:10.3389/fnbeh.2014.00268

    PubMed  PubMed Central  Google Scholar 

  138. Hager R, Johnstone RA (2003) The genetic basis of family conflict resolution in mice. Nature 421:533–535. doi:10.1038/nature01239

    Article  CAS  PubMed  Google Scholar 

  139. Hager R, Johnstone RA (2005) Differential growth of own and alien young in mixed litters of mice: a role for genomic imprinting? Ethology 111:705–714. doi:10.1111/j.1439-0310.2005.01097.x

    Article  Google Scholar 

  140. Macnair MR, Parker GA (1979) Models of parent-offspring conflict. III. Intra-brood conflict. Anim Behav 27:1202–1209. doi:10.1016/0003-3472(79)90067-8

    Article  Google Scholar 

  141. Kilner RM, Hinde CA (2012) Parent-offspring conflict. In: Smiseth PT, Kölliker M, Royle N (eds) Evolution of parent care. Oxford University Press, Oxford, pp 119–132

    Google Scholar 

  142. Svare B, Kinsley CH, Mann MA, Broida J (1984) Infanticide: accounting for genetic variation in mice. Physiol Behav 33:137–152

    Article  CAS  PubMed  Google Scholar 

  143. Perrigo G, Belvin L, Quindry P et al (1993) Genetic mediation of infanticide and parental behavior in male and female domestic and wild stock house mice. Behav Genet 23:525–531

    Article  CAS  PubMed  Google Scholar 

  144. Sayler A, Salmon M (1969) Communal nursing in mice: influence of multiple mothers on the growth of the young. Science 164:1309–1310. doi:10.1126/science.164.3885.1309

    Article  CAS  PubMed  Google Scholar 

  145. König B (1997) Cooperative care of young in mammals. Naturwissenschaften 84:95–104. doi:10.1007/s001140050356

    Article  PubMed  Google Scholar 

  146. Weidt A, Lindholm AK, König B (2014) Communal nursing in wild house mice is not a by-product of group living: females choose. Naturwissenschaften 101:73–76. doi:10.1007/s00114-013-1130-6

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  147. Heiderstadt KM, Vandenbergh DJ, Gyekis JP, Blizard DA (2014) Communal nesting increases pup growth but has limited effects on adult behavior and neurophysiology in inbred mice. J Am Assoc Lab Anim Sci 53:152–160

    CAS  PubMed  PubMed Central  Google Scholar 

  148. Calamandrei G, Wilkinson LS, Keverne EB (1992) Olfactory recognition of infants in laboratory mice: role of noradrenergic mechanisms. Physiol Behav 52:901–907

    Article  CAS  PubMed  Google Scholar 

  149. Malenfant SA, Barry M, Fleming AS (1991) Effects of cycloheximide on the retention of olfactory learning and maternal experience effects in postpartum rats. Physiol Behav 49:289–294

    Article  CAS  PubMed  Google Scholar 

  150. Mock DW, Parker GA (1997) The evolution of sibling rivalry. Oxford University Press, Oxford

    Google Scholar 

  151. Hager R, Johnstone RA (2007) Maternal and offspring effects influence provisioning to mixed litters of own and alien young in mice. Anim Behav 74:1039–1045. doi:10.1016/j.anbehav.2007.01.021

    Article  Google Scholar 

  152. Martin P, Bateson PPG (2007) Measuring behaviour: an introductory guide, 3rd edn. Cambridge University Press, Cambridge

    Book  Google Scholar 

  153. Miles CM, Wayne M (2008) Quantitative trait locus (QTL) analysis. Nat Educ 1:208

    Google Scholar 

  154. Broman KW, Wu H, Sen S, Churchill GA (2003) R/qtl: QTL mapping in experimental crosses. Bioinformatics 19:889–890. doi:10.1093/bioinformatics/btg112

    Article  CAS  PubMed  Google Scholar 

  155. Wang J, Williams RW, Manly KF (2003) WebQTL: web-based complex trait analysis. Neuroinformatics 1:299–308. doi:10.1385/NI:1:4:299

    Article  PubMed  Google Scholar 

  156. Gene Ontology Consortium (2015) Gene Ontology Consortium: going forward. Nucleic Acids Res 43:D1049–D1056. doi:10.1093/nar/gku1179

    Article  Google Scholar 

  157. Mulligan MK, Dubose C, Yue J et al (2013) Expression, covariation, and genetic regulation of miRNA biogenesis genes in brain supports their role in addiction, psychiatric disorders, and disease. Front Genet 4:126. doi:10.3389/fgene.2013.00126

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  158. Andreux PA, Williams EG, Koutnikova H et al (2012) Systems genetics of metabolism: the use of the BXD murine reference panel for multiscalar integration of traits. Cell 150:1287–1299. doi:10.1016/j.cell.2012.08.012

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  159. Alberts R, Schughart K (2010) QTLminer: identifying genes regulating quantitative traits. BMC Bioinformatics 11:516. doi:10.1186/1471-2105-11-516

    Article  PubMed  PubMed Central  Google Scholar 

  160. Ashbrook DG, Delprato A, Grellmann C et al (2014) Transcript co-variance with Nestin in two mouse genetic reference populations identifies Lef1 as a novel candidate regulator of neural precursor cell proliferation in the adult hippocampus. Front Neurosci 8:418. doi:10.3389/fnins.2014.00418

    Article  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

We would like to thank Beatrice Gini and Sophie Lyst for help with data collection and colony management. This research is supported by NERC grants NE/I001395/1 and NE/F013418/1.

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Authors and Affiliations

  1. Dept. of Biological Sciences University of Toronto Scarborough Science Wing, SW3261265 Military Trail, Toronto, ON, M1C, UK

    David G. Ashbrook

  2. Department of Computational and Evolutionary Biology, Faculty of Life Sciences, University of Manchester, C1.261 Michael Smith Bldg., Oxford Road, Manchester, M13 9PT, UK

    Reinmar Hager

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  1. David G. Ashbrook
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  2. Reinmar Hager
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Correspondence to Reinmar Hager .

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  1. Department of Infection Genetics, Helmholtz Centre for Infection Research & University of Veterinary Medicine Hannover, Braunschweig, Niedersachsen, Germany

    Klaus Schughart

  2. Department of Microbiology, Immunology and Biochemistry, University of Tennessee Health Science Center, Memphis, Tennessee, USA

    Robert W. Williams

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Ashbrook, D.G., Hager, R. (2017). Social Interactions and Indirect Genetic Effects on Complex Juvenile and Adult Traits. In: Schughart, K., Williams, R. (eds) Systems Genetics. Methods in Molecular Biology, vol 1488. Humana Press, New York, NY. https://doi.org/10.1007/978-1-4939-6427-7_24

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