Hostname: page-component-78c5997874-94fs2 Total loading time: 0 Render date: 2024-11-18T03:00:15.025Z Has data issue: false hasContentIssue false

Quality of early family relationships and the timing and tempo of puberty: Effects depend on biological sensitivity to context

Published online by Cambridge University Press:  24 January 2011

Bruce J. Ellis*
Affiliation:
University of Arizona
Elizabeth A. Shirtcliff
Affiliation:
University of New Orleans
W. Thomas Boyce
Affiliation:
University of British Columbia
Julianna Deardorff
Affiliation:
University of California
Marilyn J. Essex
Affiliation:
University of Wisconsin
*
Address correspondence and reprint requests to: Bruce J. Ellis, John and Doris Norton School of Family and Consumer Sciences, University of Arizona, McClelland Park, 650 North Park Avenue, Tucson, AZ 85721-0078; E-mail: [email protected].

Abstract

Guided by evolutionary–developmental theories of biological sensitivity to context and reproductive development, the current research examined the interactive effects of early family environments and psychobiologic reactivity to stress on the subsequent timing and tempo of puberty. As predicted by the theory, among children displaying heightened biological sensitivity to context (i.e., higher stress reactivity), higher quality parent–child relationships forecast slower initial pubertal tempo and later pubertal timing, whereas lower quality parent–child relationships forecast the opposite pattern. No such effects emerged among less context-sensitive children. Whereas sympathetic nervous system reactivity moderated the effects of parent–child relationships on both breast/genital and pubic hair development, adrenocortical activation only moderated the effect on pubic hair development. The current results build on previous research documenting what family contexts predict variation in pubertal timing by demonstrating for whom those contexts matter. In addition, the authors advance a new methodological approach for assessing pubertal tempo using piecewise growth curve analysis.

Type
Special Section Articles
Copyright
Copyright © Cambridge University Press 2011

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Abidin, R. R. (1986). Parenting Stress Index. Charlottesville, VA: Pediatric Psychology Press.Google Scholar
Alkon, A., Goldstein, L. H., Smider, N., Essex, M., Kupfer, D., & Boyce, W. T. (2003). Developmental and contextual influences on autonomic reactivity in young children. Developmental Psychobiology, 42, 6478.CrossRefGoogle ScholarPubMed
Azziz, R., Fox, L. M., Zacur, H. A., Parker, C. R. Jr., & Boots, L. R. (2001). Adrenocortical secretion of dehydroepiandrosterone in healthy women: Highly variable response to adrenocorticotropin. Journal of Clinical Endocrinology and Metabolism, 86, 25132517.Google ScholarPubMed
Barnett, R. C., & Marshall, N. L. (1989). Preliminary manual for the Role-Quality Scales. Wellesley, MA: Wellesley College, Center for Research on Women.Google Scholar
Belsky, J. (2000). Conditional and alternative reproductive strategies: Individual differences in susceptibility to rearing experience. In Rodgers, J.Rowe, D., & Miller, W. (Eds.), Genetic influences on human fertility and sexuality: Theoretical and empirical contributions from the biological and behavioral sciences (pp. 127146). Boston: Kluwer.CrossRefGoogle Scholar
Belsky, J. (2005). Differential susceptibility to rearing influences: An evolutionary hypothesis and some evidence. In Ellis, B., & Bjorklund, D. (Eds.), Origins of the social mind: Evolutionary psychology and child development (pp. 139163). New York: Guilford Press.Google Scholar
Belsky, J., & Pluess, M. (2009). Beyond diathesis–stress: Differential susceptibility to environmental influence. Psychological Bulletin, 135, 885908.CrossRefGoogle Scholar
Belsky, J., Steinberg, L., & Draper, P. (1991). Childhood experience, interpersonal development and reproductive strategy: An evolutionary theory of socialization. Child Development, 62, 647670.CrossRefGoogle ScholarPubMed
Belsky, J., Steinberg, L., Houts, R. M., Friedman, S. L., DeHart, G., Cauffman, E., et al. (2007). Family rearing antecedents of pubertal timing. Child Development, 78, 13021321.CrossRefGoogle ScholarPubMed
Bernstein, L. (2002). Epidemiology of endocrine-related risk factors for breast cancer. Journal of Mammary Gland Biology and Neoplasia, 7, 315.CrossRefGoogle ScholarPubMed
Biro, F. M., Huang, G., Crawford, P. B., Lucky, A. W., Striegel-Moore, R., Barton, B. A., et al. (2006). Pubertal correlates in black and white girls. Journal of Pediatrics, 148, 234240.CrossRefGoogle ScholarPubMed
Block, J. H. (1965). The Child-Rearing Practices Report (CRPR): A set of Q items for the description of parental socialization attitudes and values. Berkeley, CA: Institute of Human Development.Google Scholar
Boyce, W. T., & Ellis, B. J. (2005). Biological sensitivity to context: I. An evolutionary–developmental theory of the origins and functions of stress reactivity. Development and Psychopathology, 17, 271301.CrossRefGoogle ScholarPubMed
Boyce, W. T., Essex, M. J., Alkon, A., Goldsmith, H. H., Kraemer, H. C., & Kupfer, D. J. (2006). Early father involvement moderates biobehavioral susceptibility to mental health problems in middle childhood. Journal of the American Academy of Child & Adolescent Psychiatry, 45, 15101520.CrossRefGoogle ScholarPubMed
Boyce, W. T., Essex, M., Woodward, H. R., Measelle, J. R., Ablow, J. C., & Kupfer, D. J. (2002). The confluence of mental, physical, social and academic difficulties in middle childhood: I. Exploring the “headwaters” of early life morbidities. Journal of the American Academy of Child & Adolescent Psychiatry, 41, 580587.CrossRefGoogle Scholar
Boyce, W. T., Quas, J., Alkon, A., Smider, N., Essex, M., & Kupfer, D. J. (2001). Autonomic reactivity and psychopathology in middle childhood. British Journal of Psychiatry, 179, 144150.CrossRefGoogle ScholarPubMed
Bratberg, G. H., Nilsen, T. I., Holmen, T. L., & Vatten, L. J. (2007). Early sexual maturation, central adiposity and subsequent overweight in late adolescence. A four-year follow-up of 1,605 adolescent Norwegian boys and girls: The Young HUNT study. BMC Public Health, 12, 54.Google Scholar
Brumbach, B. H., Figueredo, A. J., & Ellis, B. J. (2009). Effects of harsh and unpredictable environments in adolescence on the development of life history strategies: A longitudinal test of an evolutionary model. Human Nature, 20, 2551.CrossRefGoogle ScholarPubMed
Buchanan, C. M., Eccles, J. S., & Becker, J. B. (1992). Are adolescents the victims of raging hormones: Evidence for activational effects of hormones on moods and behavior at adolescence. Psychological Bulletin, 111, 62107.CrossRefGoogle ScholarPubMed
Bundak, R., Darendeliler, F., Gunoz, H., Bas, F., Saka, N., & Neyzi, O. (2007). Analysis of puberty and pubertal growth in healthy boys. European Journal of Pediatrics, 166, 595600.CrossRefGoogle ScholarPubMed
Cacioppo, J. T., Berntson, G. G., Binkley, P. F., Quigley, K. S., Uchino, B. N., & Fieldstone, A. (1994). Autonomic cardiac control. II. Noninvasive indices and basal response as revealed by autonomic blockades. Psychophysiology, 31, 586598.CrossRefGoogle ScholarPubMed
Cacioppo, J. T., Berntson, G. G., Malarkey, W. B., Kiecolt-Glaser, J. K., Sheridan, J. F., Poehlmann, K. M., et al. (1998). Autonomic, neuroendocrine, and immune responses to psychological stress: The reactivity hypothesis. Annals of the New York Academy of Science, 840, 664673.CrossRefGoogle ScholarPubMed
Cacioppo, J. T., Uchino, B. N., & Berntson, G. G. (1994). Individual differences in the autonomic origins of heart rate reactivity: The psychometrics of respiratory sinus arrhythmia and preejection period. Psychophysiology, 31, 412419.CrossRefGoogle ScholarPubMed
Chisholm, J. S. (1996). The evolutionary ecology of attachment organization. Human Nature, 7, 138.CrossRefGoogle ScholarPubMed
Colditz, G. A., & Frazier, A. L. (1995). Models of breast cancer show that risk is set by events of early life: Prevention efforts must shift focus. Cancer Epidemiology, Biomarkers and Prevention, 4, 567571.Google ScholarPubMed
Cohen, S., Hamrick, N., Rodriguez, M. S., Feldman, P. J., Rabin, B. S., & Manuck, S. B. (2000). The stability of and intercorrelations among cardiovascular, immune, endocrine, and psychological reactivity. Annals of Behavioral Medicine, 22, 171179.CrossRefGoogle ScholarPubMed
Costello, E. J., Sung, M., Worthman, C., & Angold, A. (2007). Pubertal maturation and the development of alcohol use and abuse. Drug and Alcohol Dependence, 88(Suppl. 1), S50S59.CrossRefGoogle ScholarPubMed
Deardorff, J., Gonzales, N. A., Christopher, F. S., Roosa, M. W., & Millsap, R. (2005). Early puberty and adolescent pregnancy: The influence of alcohol use. Pediatrics, 116, 14511456.CrossRefGoogle ScholarPubMed
Deardorff, J., Hayward, C., Wilson, K. A., Bryson, S., Hammer, L. D., & Agras, S. (2007). Puberty and gender interact to predict social anxiety symptoms in early adolescence. Journal of Adolescent Health, 41, 102104.CrossRefGoogle ScholarPubMed
Dedovic, K., Duchesne, A., Andrews, J., Engert, V., & Pruessner, J. C. (2009). The brain and the stress axis: The neural correlates of cortisol regulation in response to stress. NeuroImage, 47, 864871.CrossRefGoogle ScholarPubMed
Dick, D. M., Rose, R. J., Viken, R. J., & Kaprio, J. (2000). Pubertal timing and substance use: Associations between and within families across late adolescence. Developmental Psychology, 36, 180189.CrossRefGoogle ScholarPubMed
Dickerson, S. S., & Kemeny, M. E. (2004). Acute stressors and cortisol responses: A theoretical integration and synthesis of laboratory research. Psychological Bulletin, 130, 355391.CrossRefGoogle ScholarPubMed
Dorn, L. D., Dahl, R. E., Woodward, H. R., & Biro, F. (2006). Defining the boundaries of early adolescence: A user's guide to assessing pubertal status and pubertal timing in research with adolescents. Applied Developmental Science, 10, 3056.CrossRefGoogle Scholar
Ellis, B. J. (2004). Timing of pubertal maturation in girls: An integrated life history approach. Psychological Bulletin, 130, 920958.CrossRefGoogle ScholarPubMed
Ellis, B. J., Boyce, W. T., Belsky, J., Bakermans-Kranenburg, M. J., & van IJzendoorn, M. H. (2011). Differential susceptibility to the environment: An evolutionary–neurodevelopmental theory. Development and Psychopathology, 23, 728.CrossRefGoogle Scholar
Ellis, B. J., & Essex, M. J. (2007). Family environments, adrenarche, and sexual maturation: A longitudinal test of a life history model. Child Development, 78, 17991817.CrossRefGoogle ScholarPubMed
Ellis, B. J., Essex, M. J., & Boyce, W. T. (2005). Biological sensitivity to context: II. Empirical explorations of an evolutionary–developmental theory. Development and Psychopathology, 17, 303328.CrossRefGoogle ScholarPubMed
Ellis, B. J., Figueredo, A. J., Brumbach, B. H., & Schlomer, G. L. (2009). Fundamental dimensions of environmental risk: The impact of harsh versus unpredictable environments on the evolution and development of life history strategies. Human Nature, 20, 204268.CrossRefGoogle ScholarPubMed
Ellis, B. J., Jackson, J. J., & Boyce, W. T. (2006). The stress response systems: Universality and adaptive individual differences. Developmental Review, 26, 175212.CrossRefGoogle Scholar
Ellis, B. J., McFadyen-Ketchum, S., Dodge, K. A., Pettit, G. S., & Bates, J. E. (1999). Quality of early family relationships and individual differences in the timing of pubertal maturation in girls: A longitudinal test of an evolutionary model. Journal of Personality and Social Psychology, 77, 387401.CrossRefGoogle ScholarPubMed
Euling, S. Y., Herman-Giddens, M. E., Lee, P. A., Selevan, S. G., Juul, A., Sorenson, T., et al. (2008). Examination of US puberty-timing data from 1940 to 1994 for secular trends: Panel findings. Pediatrics, 121, S172S191.CrossRefGoogle ScholarPubMed
Ge, X., Kim, I. J., Brody, G. H., Conger, R. D., Simons, R. L., Gibbons, F. X., et al. (2003). It's about timing and change: Pubertal transition effects on symptoms of major depression among African American youths. Developmental Psychology, 39, 430439.CrossRefGoogle ScholarPubMed
Goldstein, D. S., & Kopin, I. J. (2008). Adrenomedullary, adrenocortical, and sympathoneural responses to stressors: A meta-analysis. Endocrine Regulations, 42, 111119.Google ScholarPubMed
Golub, M. S., Collman, G. W., Foster, P. D., Kiimmel, C. A., Rajpert-De Meyts, E., Reiter, E. O., et al. (2008). Public health implications of altered pubertal timing. Pediatrics, 121, S218230.CrossRefGoogle Scholar
Gordis, E. B., Granger, D. A., Susman, E. J., & Trickett, P. K. (2006). Asymmetry between salivary cortisol and alpha-amylase reactivity to stress: Relation to aggressive behavior in adolescents. Psychoneuroendocrinology, 31, 976987.CrossRefGoogle ScholarPubMed
Graber, J. A., Brooks-Gunn, J., & Warren, M. P. (1995). The antecedents of menarcheal age: Heredity, family environment, and stressful life events. Child Development, 66, 346359.CrossRefGoogle ScholarPubMed
Granger, D. A., Kivlighan, K. T., el-Sheikh, M., Gordis, E. B., & Stroud, L. R. (2007). Salivary alpha-amylase in biobehavioral research: Recent developments and applications. Annals of the New York Academy of Science, 1098, 122144.CrossRefGoogle ScholarPubMed
Grumbach, M. M. (2002). The neuroendocrinology of human puberty revisited. Hormone Research, 57(Suppl. 2), 214.CrossRefGoogle ScholarPubMed
Grumbach, M. M., Bin-Abbas, B. S., & Kaplan, S. L. (1998). The growth hormone cascade: Progress and long-term results of growth hormone treatment in growth hormone deficiency. Hormone Research, 49(Suppl. 2), 4157.CrossRefGoogle ScholarPubMed
Gunnar, M. R., Talge, N. M., & Herrera, A. (2009). Stressor paradigms in developmental studies: What does and does not work to produce mean increases in salivary cortisol. Psychoneuroendocrinology, 34, 953967.CrossRefGoogle Scholar
Halberstadt, A. G. (1986). Family socialization of emotional expression and nonverabal communication styles and skills. Journal of Personality and Social Psychology, 51, 827836.CrossRefGoogle Scholar
Halberstadt, A. G. (1991). Studies in emotion and social interaction. In Feldman, R. S. & Rime, B. (Eds.), Fundamentals of nonverbal behavior (pp. 106160). New York: Cambridge University Press.Google Scholar
Hox, J. (2002). Multilevel analysis techniques and applications. Mahwah, NJ: Erlbaum.CrossRefGoogle Scholar
Hyde, J. S., Klein, M. H., Essex, M. J., & Clark, R. (1995). Maternity leave and women's mental health. Psychology of Women Quarterly, 19, 257285.CrossRefGoogle Scholar
Jacobsen, B. K., Oda, K., Knutsen, S. F., & Fraser, G. E. (2009). Age at menarche, total mortality and mortality from ischaemic heart disease and stroke: The Adventist Health Study, 1976–1988. International Journal of Epidemiology, 38, 245252.CrossRefGoogle Scholar
Kelsey, J. L., Gammon, M. D., & John, E. M. (1993). Reproductive factors and breast cancer. Epidemiologic Reviews, 15, 3647.CrossRefGoogle ScholarPubMed
Kim, K., & Smith, P. K. (1998). Retrospective survey of parental marital relations and child reproductive development. International Journal of Behavioral Development, 22, 729751.CrossRefGoogle Scholar
Kim, K., Smith, P. K., & Palermiti, A. L. (1997). Conflict in childhood and reproductive development. Evolution and Human Behavior, 18, 109142.CrossRefGoogle Scholar
Kirschbaum, C., & Hellhammer, D. H. (1994). Salivary cortisol in psychoneuroendocrine research: Recent developments and applications. Psychoneuroendocrinology, 19, 313333.CrossRefGoogle ScholarPubMed
Kreft, I., & De Leeuw, J. (1998). Introducing multilevel modeling. Thousand Oaks, CA: Sage.CrossRefGoogle Scholar
Laitinen-Krispijn, S., Van der Ende, J., Hazebroek-Kampschreur, A. A., & Verhulst, F. C. (1999). Pubertal maturation and the development of behavioural and emotional problems in early adolescence. Acta Psychiatrica Scandinavica, 99, 1625.CrossRefGoogle ScholarPubMed
Lakshman, R., Forouhi, N. G., sharp, S. J., Luben, R., Bingham, S. A., Khaw, K-T., et al. (2009). Early age at menarche associated with cardiovascular disease and mortality. Journal of Clinical Endocrinology and Metabolism, 94, 49535960.CrossRefGoogle ScholarPubMed
Llop-Viñolas, D., Vizmanos, B., Closa Monasterolo, R., Escribano Subías, J., Fernández-Ballart, J. D., & Martí-Henneberg, C. (2004). Onset of puberty at eight years of age in girls determines a specific tempo of puberty but does not affect adult height. Acta Paediatrica, 93, 874879.CrossRefGoogle Scholar
Manuck, S. B., Craig, A. E., Flory, J. D., Halder, I., & Ferrell, R. E. (2011). Reported early family environment covaries with menarcheal age as a function of polymorphic variation in estrogen receptor-α. Development and Psychopathology, 23, 6983.CrossRefGoogle ScholarPubMed
Marshall, W. A., & Tanner, J. M. (1969). Variations in pattern of pubertal changes in girls. Archives of Disease in Childhood, 44, 291303.CrossRefGoogle ScholarPubMed
Marshall, W. A., & Tanner, J. M. (1970). Variations in the pattern of pubertal changes in boys. Archives of Disease in Childhood, 45, 1323.CrossRefGoogle ScholarPubMed
Miller, W. B., & Pasta, D. J. (2000). Early family environment, reproductive strategy, and contraceptive behavior: Testing a genetic hypothesis. In Rodgers, J. L., Rowe, D. C., & Miller, W. B. (Eds.), Genetic influences on human fertility and sexuality (pp. 183230). Boston: Kluwer Academic.CrossRefGoogle Scholar
Morris, N. M., & Udry, R. J. (1980). Validation of a self-administered instrument to assess stage of adolescent development. Journal of Youth and Adolescence, 9, 271280.CrossRefGoogle ScholarPubMed
Mustanski, B. S., Viken, R. J., Kaprio, J., Pulkkinen, L., & Rose, R. J. (2004). Genetic and environmental influences on pubertal development: Longitudinal data from Finnish twins at ages 11 and 14. Developmental Psychology, 40, 11881198.CrossRefGoogle ScholarPubMed
Nater, U. M., & Rohleder, N. (2009). Salivary alpha-amylase as a non-invasive biomarker for the sympathetic nervous system: Current state of research. Psychoneuroendocrinology, 34, 486496.CrossRefGoogle ScholarPubMed
Obradović, J., & Boyce, W. T. (2009). Individual differences in behavioral, physiological, and genetic sensitivities to contexts: Implications for development and adaptation. Developmental Neuroscience, 31, 300308.CrossRefGoogle ScholarPubMed
Obradović, J., Bush, N. R., Stamperdahl, J., Adler, N. E., & Boyce, W. T. (2010). Biological sensitivity to context: The interactive effects of stress reactivity and family adversity on socio-emotional behavior and school readiness. Child Development, 81, 270289.CrossRefGoogle Scholar
Pantsiotou, S., Papadimitriou, A., Douros, K., Priftis, K., Nicolaidou, P., & Fretzayas, A. (2008). Maturational tempo differences in relation to the timing of the onset of puberty in girls. Acta Paediatrica, 97, 217220.CrossRefGoogle Scholar
Parker, L. N. (1991). Adrenarche. Endocrinology Metabolism Clinics of North America, 20, 7183.CrossRefGoogle ScholarPubMed
Parry, B. L., & Newton, R. P. (2001). Chronobiological basis of female-specific mood disorders. Neuropsychopharmacology, 25(Suppl. 5), S102S108.CrossRefGoogle ScholarPubMed
Petersen, A., Crockett, L., Richards, M., & Boxer, A. (1988). A self-report measure of pubertal status: Reliability, validity, and initial norms. Journal of Youth and Adolescence, 17, 117133.CrossRefGoogle ScholarPubMed
Porges, S. W. (1995). Orienting in a defensive world: Mammalian modifications of our evolutionary heritage. A polyvagal theory. Psychophysiology, 32, 301318.CrossRefGoogle Scholar
Pruessner, J. C., Dedovic, K., Pruessner, M., Lord, C., Buss, C., Collins, L., et al. (2010). Stress regulation in the central nervous system: Evidence from structural and functional neuroimaging studies in human populations. Psychoneuroendocrinology, 35, 179191.CrossRefGoogle ScholarPubMed
Quas, J. A., Bauer, A., & Boyce, W. T. (2004). Physiological reactivity, social support, and memory in early childhood. Child Development, 75, 797814.CrossRefGoogle ScholarPubMed
Radloff, L. S. (1977). The CES-D Scale: A self-report depression scale for research in the general population. Applied Psychological Measurement, 1, 385401.CrossRefGoogle Scholar
Romans, S. E., Martin, M., Gendall, K., & Herbison, G. P. (2003). Age of menarche: The role of some psychosocial factors. Psychological Medicine, 33, 933939.CrossRefGoogle ScholarPubMed
Rowe, D. C. (2000). Environmental and genetic influences on pubertal development: Evolutionary life history traits. In Rodgers, J. L., Rowe, D. C., & Miller, W. B. (Eds.), Genetic influences on human fertility and sexuality: Theoretical and empirical contributions from the biological and behavioral sciences (pp. 147168). Boston: Kluwer Academic.CrossRefGoogle Scholar
Sapolsky, R. M., Romero, L. M., & Munck, A. U. (2000). How do glucocorticoids influence stress responses? Integrating permissive, suppressive, stimulatory, and preparative actions. Endocrine Reviews, 21, 5589.Google ScholarPubMed
Shirtcliff, E., Zahn-Waxler, C., Klimes-Dougan, B., & Slattery, M. (2007). Salivary dehydroepiandrosterone responsiveness to social challenge in adolescents with internalizing problems. Journal of Child Psychology and Psychiatry, 48, 580591.CrossRefGoogle ScholarPubMed
Shirtcliff, E. A., Dahl, R. E., & Pollak, S. D. (2009). Pubertal development: Correspondence between hormonal and physical development. Child Development, 80, 327337.CrossRefGoogle ScholarPubMed
Slap, G. B., Khalid, N., Paikoff, R. L., & Brooks-Gunn, J. (1994). Evolving self-image, pubertal manifestations, and pubertal hormones: Preliminary findings in young adolescent girls. Journal of Adolescent Health, 15, 327335.CrossRefGoogle ScholarPubMed
Steinberg, L. (1988). Reciprocal relation between parent–child distance and pubertal maturation. Developmental Psychology, 24, 122128.CrossRefGoogle Scholar
Stoll, B. A., Vatten, L. J., & Kvinnsland, S. (1994). Does early physical maturity influence breast cancer risk? Acta Oncologica, 33, 171176.CrossRefGoogle ScholarPubMed
Styne, D. M., & Grumbach, M. M. (2002). Puberty in boys and girls. In Pfaff, D., Arnold, A., Etgen, A. M., Fahrbach, S., & Rubin, R. T. (Eds.), Hormones, brain and behavior (Vol. 4, pp. 661716). San Diego, CA: Elsevier Science.CrossRefGoogle Scholar
Tither, J. M., & Ellis, B. J. (2008). Impact of fathers on daughters' age of menarche: A genetically and environmentally controlled sibling study. Developmental Psychology, 44, 14091420.CrossRefGoogle ScholarPubMed
Vo, C., & Carney, M. (2007). Ovarian cancer hormonal and environmental risk effect. Obstetrics & Gynecological Clinics of North America, 34, 687700.CrossRefGoogle ScholarPubMed
Warren, M. P., & Brooks-Gunn, J. (1989). Mood and behavior at adolescence: Evidence for hormonal factors. Journal of Clinical Endocrinology and Metabolism, 69, 7782.CrossRefGoogle ScholarPubMed
West-Eberhard, M. J. (2003). Developmental plasticity and evolution. New York: Oxford University Press.CrossRefGoogle Scholar
Wolf, M., van Doorn, G. S., & Weissing, F. J. (2008). Evolutionary emergence of responsive and unresponsive personalities. Proceedings of the National Academy of Sciences of the United States of America, 105, 1582515830.CrossRefGoogle ScholarPubMed