Abstract
The prenatal social environment affects offspring development in most studied taxa with potentially lifelong consequences. To understand the adaptive significance of such maternal influences on offspring development, it is important to study their effects on fitness. In guinea pigs, social instability during pregnancy leads to delayed development of male offspring. This has been interpreted as an adaptation to high social densities, where young males need to queue for reproductive opportunities since they cannot out-compete older dominant males. The consequences for male reproductive success are, however, so far unknown. To study the effects of different prenatal social densities on offspring reproductive performance, we housed females individually or in small groups during late pregnancy. Offspring from both treatments were reared together in large groups until independence and thereafter housed in same-sex pairs of the same treatment. We then observed courtship, aggressive behavior, and reproductive success in a low-density context with one male from each treatment competing over access to two females. Sons born to individually housed females initiated more fights, had more social contacts, courted females more, and had a higher reproductive success than sons of group-housed females. Sons born to mothers experiencing low social densities before birth therefore perform better at low social group sizes, suggesting that male development may be adaptively adjusted to anticipated social densities, although performance under high densities still needs to be compared.
Similar content being viewed by others
References
Asher M, de Oliveira ES, Sachser N (2004) Social system and spatial organization of wild guinea pigs (Cavia aperea) in a natural population. J Mammal 85:788–796
Asher M, Lippmann T, Epplen JT, Kraus C, Trillmich F, Sachser N (2008) Large males dominate: ecology, social organization, and mating system of wild cavies, the ancestors of the guinea pig. Behav Ecol Sociobiol 62:1509–1521
Badyaev AV (2005) Stress-induced variation in evolution: from behavioural plasticity to genetic assimilation. Proc R Soc Lond B 272:877–886
Bateson P, Barker D, Clutton-Brock T (2004) Developmental plasticity and human health. Nature 419–421
Bauer B, Womastek I, Dittami J, Huber S (2008) The effects of early environmental conditions on the reproductive and somatic development of juvenile guinea pigs (Cavia aperea f. porcellus). Gen Comp Endocrinol 155:680–685
Belsky J, Steinberg L, Draper P (1991) Childhood experience, interpersonal development, and reproductive strategy: an evolutionary theory of socialization. Child Dev 62:647–670
Brain P (1975) What does individual housing mean to a mouse? Life Sciences 16:187–200
Champagne FA, Meaney MJ (2007) Trans generational effects of social environment on variations in maternal care and behavioral response to novelty. Behav Neurosci 121:1353–1363
Christian JJ (1961) Phenomena associated with population density. Proc Natl Acad Sci U S A 47:428–449
Crump CJ, Chevins PF (1989) Prenatal stress reduces fertility of male offspring in mice, without affecting their adult testosterone levels. Horm Behav 23:333–343
Dahlöf L, Hård E, Larsson K (1978) Influence of maternal stress on the development of the fetal genital system. Physiol Behav 20:193–195
De Catanzaro D, Gorzalka BB (1979) Isolation-induced facilitation of male sexual behavior in mice. J Comp Physiol Psychol 93:211–222
Deitchman R, Sanders RE, Burkholder J, Newman I (1977) Effects of prenatal crowding on behavior of rodent mothers and offspring. Psychol Rev 40:327–338
Del Giudice M (2012) Fetal programming by maternal stress: insights from a conflict perspective. Psychoneuroendocrinology 37:1614–1629
Dloniak SM, French JA, Holekamp KE (2006) Rank-related maternal effects of androgens on behaviour in wild spotted hyaenas. Nature 440:1190–1193
Dufty A (2002) Hormones, developmental plasticity and adaptation. Trends Ecol Evol 17:190–196
Harvey P, Chevins P (1985) Crowding pregnant mice affects attack and threat behavior of male offspring. Horm Behav 19:86–97
Hennessy MB (2003) Enduring maternal influences in a precocial rodent. Dev Psychobiol 42:225–236
Hennessy MB, Kaiser S, Sachser N (2009) Social buffering of the stress response: diversity, mechanisms, and functions. Front Neuroendocrinol 30:470–482
Horton T (2005) Fetal origins of developmental plasticity: animal models of induced life history variation. Am J Hum Biol 17:34–43
Jablonka E, Lamb MJ (2005) Evolution in four dimensions: genetic, epigenetic, behavioral, and symbolic variation in the history of life. The MIT Press, Cambridge
Kaiser S, Sachser N (1998) The social environment during pregnancy and lactation affects the female offsprings’ endocrine status and behaviour in guinea pigs. Physiol Behav 63:361–366
Kaiser S, Sachser N (2001) Social stress during pregnancy and lactation affects in guinea pigs the male offsprings’ endocrine status and infantilizes their behaviour. Psychoneuroendocrinology 26:503–519
Kaiser S, Sachser N (2005) The effects of prenatal social stress on behaviour: mechanisms and function. Neurosci Biobehav Rev 29:283–294
Kaiser S, Sachser N (2009) Effects of prenatal social stress on offspring development: pathology or adaptation? Curr Dir Psychol Sci 18:118–121
Kaiser S, Heemann K, Straub RH, Sachser N (2003a) The social environment affects behaviour and androgens, but not cortisol in pregnant female guinea pigs. Psychoneuroendocrinology 28:67–83
Kaiser S, Kruijver FPM, Straub RH, Sachser N, Swaab DF (2003b) Early social stress in male Guinea-pigs changes social behaviour, and autonomic and neuroendocrine functions. J Neuroendocrinol 15:761–769
Kanitz R, Trillmich F, Bonatto SL (2009) Characterization of new microsatellite loci for the South-American rodents Cavia aperea and C. magna. Conserv Genet Resour 1:47–50
Karels T, Boonstra R (2000) Concurrent density dependence and independence in populations of arctic ground squirrels. Nature 408:460–463
Kemme K, Kaiser S, von Engelhardt N, Wewers D, Groothuis T, Sachser N (2009) An unstable social environment affects sex ratio in guinea pigs: an adaptive maternal effect? Behaviour 146:1513–1529
Koolhaas JM, de Boer SF, Buwalda B (2006) Stress and adaptation. Curr Dir Psychol Sci 15:109–112
Koolhaas JM, de Boer SF, Buwalda B, van Reenen K (2007) Individual variation in coping with stress: a multidimensional approach of ultimate and proximate mechanisms. Brain Behav Evol 70:218–226
Korpimäki E, Norrdahl K, Klemola T, Pettersen T, Stenseth NC (2002) Dynamic effects of predators on cyclic voles: field experimentation and model extrapolation. Proc R Soc Lond B 269:991–997
Korpimäki E, Brown PR, Jacob J, Pech RP (2004) The puzzles of population cycles and outbreaks of small mammals solved? Bioscience 54:1071–1079
Kraus C, Thomson DL, Künkele J, Trillmich F (2005). Living slow and dying young? Life-history strategy and age-specific survival rates in a precocial small mammal. J Anim Ecol 74:171–180
Künzl C, Sachser N (1999) The behavioral endocrinology of domestication: a comparison between the domestic guinea pig (Cavia aperea f. porcellus ) and its wild ancestor, the cavy (Cavia aperea). Horm Behav 37:28–37
Marshall DJ, Uller TO (2007) When is a maternal effect adaptive? Oikos 116:1957–1963
Oehler J, Jähkel M, Schmidt J (1987) Neuronal transmitter sensitivity after social isolation in rats. Physiol Behav 41:187–191
Phillips D (2002) Endocrine programming and fetal origins of adult disease. Trends Endocrinol Metab 13:363
Rood JP (1972) Ecological and behavioural comparisons of three genera of Argentine cavies. Anim Behav Monogr 5:1–83
Sachser N, Kaiser S (1996) Prenatal social stress masculinizes the females’ behaviour in guinea pigs. Physiol Behav 60:589–594
Sachser N, Dürschlag M, Hirzel D (1998) Social relationships and the management of stress. Psychoneuroendocrinology 23:891–904
Sachser N, Hennessy MB, Kaiser S (2011) Adaptive modulation of behavioural profiles by social stress during early phases of life and adolescence. Neurosci Biobehav Rev 35:1518–1533
Sánchez MM, Aguado F, Sánchez-Toscano F, Saphier D (1995) Effects of prolonged social isolation on responses of neurons in the bed nucleus of the stria terminalis, preoptic area, and hypothalamic paraventricular nucleus to stimulation of the medial amygdala. Psychoneuroendocrinology 20:525–541
Schiml PA, Hennessy MB (1990) Light-dark variation and changes across the lactational period in the behaviors of undisturbed mother and infant guinea pigs (Cavia porcellus). J Comp Psychol 104:283–288
Schmidt M, Kreutz M, Löffler G, Schölmerich J, Straub RH (2000) Conversion of dehydroepiandrosterone to downstream steroid hormones in macrophages. J Endocrinol 164:161–169
Siegeler K, Sachser N, Kaiser S (2011) The social environment during pregnancy and lactation shapes the behavioral and hormonal profile of male offspring in wild cavies. Dev Psychobiol 53:575–584
Sorrells AD, Eicher SD, Scott KA, Harris MJ, Pajor EA, Lay DC Jr, Richert BT (2006) Postnatal behavioral and physiological responses of piglets from gilts housed individually or in groups during gestation. J Anim Sci 84:757–766
Van den Hove DL, Steinbusch HWM, Scheepens A, Van de Berg WDJ, Kooiman LAM, Boosten BJG, Prickaert J, Blanco CE (2006) Prenatal stress and neonatal rat brain development. Neuroscience 137:145–155
von Holst D (1998) The concept of stress and its relevance for animal behavior. Adv Study Behav 27:1–131
Weinstock M (2006) The potential influence of maternal stress hormones on development and mental health of the offspring. Brain Behav Immun 19:296–308
Weinstock M, Poltyrev T, Schorer-Apelbaum D, Men D, McCarty R (1998) Effect of prenatal stress on plasma corticosterone and catecholamines in response to footshock in rats. Physiol Behav 64:439–444
West-Eberhard MJ (2003) Developmental plasticity and evolution. Oxford University Press, Oxford
Acknowledgments
We would like to thank Fritz Trillmich for valuable comments on the manuscript. We greatly appreciate the help of our animal caretakers.
Ethical note
The experimental procedures were in accordance with German animal protection laws. Animal facilities were approved (dated 18 April 2002) for keeping and breeding guinea pigs for research purposes by the local government authority responsible for health, veterinary, and food monitoring (Gesundheits-, Veterinär- und Lebensmittelüberwachungsamt).
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by E. Korpimäki
Rights and permissions
About this article
Cite this article
Guenther, A., Kowalski, G. & von Engelhardt, N. Prenatal social conditions shape offspring adult phenotype and reproductive success. Behav Ecol Sociobiol 68, 1661–1667 (2014). https://doi.org/10.1007/s00265-014-1774-z
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00265-014-1774-z