Developmental responses to early-life adversity: Evolutionary and mechanistic perspectives

Adverse ecological and social conditions during early life are known to influence development, with rippling effects that may explain variation in adult health and fitness. The adaptive function of such developmental plasticity, however, remains relatively untested in long-lived animals, resulting i...

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Published in:Evolutionary Anthropology: Issues, News, and Reviews
Main Authors: Lu, Amy, Petrullo, Lauren, Carrera, Sofia, Feder, Jacob, Schneider‐crease, India, Snyder‐mackler, Noah
Format: Article in Journal/Newspaper
Language:unknown
Published: John Wiley & Sons, Inc. 2019
Subjects:
Online Access:https://hdl.handle.net/2027.42/152003
https://doi.org/10.1002/evan.21791
id ftumdeepblue:oai:deepblue.lib.umich.edu:2027.42/152003
record_format openpolar
institution Open Polar
collection University of Michigan: Deep Blue
op_collection_id ftumdeepblue
language unknown
topic predictive adaptive responses
developmental constraints
developmental plasticity
glucocorticoids
maternal capital
microbiome
Anthropology
Social Sciences
spellingShingle predictive adaptive responses
developmental constraints
developmental plasticity
glucocorticoids
maternal capital
microbiome
Anthropology
Social Sciences
Lu, Amy
Petrullo, Lauren
Carrera, Sofia
Feder, Jacob
Schneider‐crease, India
Snyder‐mackler, Noah
Developmental responses to early-life adversity: Evolutionary and mechanistic perspectives
topic_facet predictive adaptive responses
developmental constraints
developmental plasticity
glucocorticoids
maternal capital
microbiome
Anthropology
Social Sciences
description Adverse ecological and social conditions during early life are known to influence development, with rippling effects that may explain variation in adult health and fitness. The adaptive function of such developmental plasticity, however, remains relatively untested in long-lived animals, resulting in much debate over which evolutionary models are most applicable. Furthermore, despite the promise of clinical interventions that might alleviate the health consequences of early-life adversity, research on the proximate mechanisms governing phenotypic responses to adversity have been largely limited to studies on glucocorticoids. Here, we synthesize the current state of research on developmental plasticity, discussing both ultimate and proximate mechanisms. First, we evaluate the utility of adaptive models proposed to explain developmental responses to early-life adversity, particularly for long-lived mammals such as humans. In doing so, we highlight how parent-offspring conflict complicates our understanding of whether mothers or offspring benefit from these responses. Second, we discuss the role of glucocorticoids and a second physiological system-the gut microbiome-that has emerged as an additional, clinically relevant mechanism by which early-life adversity can influence development. Finally, we suggest ways in which nonhuman primates can serve as models to study the effects of early-life adversity, both from evolutionary and clinical perspectives. Peer Reviewed https://deepblue.lib.umich.edu/bitstream/2027.42/152003/1/evan21791_am.pdf https://deepblue.lib.umich.edu/bitstream/2027.42/152003/2/evan21791.pdf
format Article in Journal/Newspaper
author Lu, Amy
Petrullo, Lauren
Carrera, Sofia
Feder, Jacob
Schneider‐crease, India
Snyder‐mackler, Noah
author_facet Lu, Amy
Petrullo, Lauren
Carrera, Sofia
Feder, Jacob
Schneider‐crease, India
Snyder‐mackler, Noah
author_sort Lu, Amy
title Developmental responses to early-life adversity: Evolutionary and mechanistic perspectives
title_short Developmental responses to early-life adversity: Evolutionary and mechanistic perspectives
title_full Developmental responses to early-life adversity: Evolutionary and mechanistic perspectives
title_fullStr Developmental responses to early-life adversity: Evolutionary and mechanistic perspectives
title_full_unstemmed Developmental responses to early-life adversity: Evolutionary and mechanistic perspectives
title_sort developmental responses to early-life adversity: evolutionary and mechanistic perspectives
publisher John Wiley & Sons, Inc.
publishDate 2019
url https://hdl.handle.net/2027.42/152003
https://doi.org/10.1002/evan.21791
genre Arctic
genre_facet Arctic
op_relation Lu, Amy; Petrullo, Lauren; Carrera, Sofia; Feder, Jacob; Schneider‐crease, India
Snyder‐mackler, Noah (2019). "Developmental responses to early-life adversity: Evolutionary and mechanistic perspectives." Evolutionary Anthropology: Issues, News, and Reviews 28(5): 249-266.
1060-1538
1520-6505
https://hdl.handle.net/2027.42/152003
doi:10.1002/evan.21791
Evolutionary Anthropology: Issues, News, and Reviews
Round JL, Mazmanian SK. 2009. The gut microbiota shapes intestinal immune responses during health and disease. Nat Rev Immunol 9: 313 - 323.
JaÅ¡areviÄ E, Howard CD, Misic AM, Beiting DP, Bale TL. 2017. Stress during pregnancy alters temporal and spatial dynamics of the maternal and offspring microbiome in a sex-specific manner. Sci Rep 7: 44182.
Bruce-Keller AJ, Fernandez-Kim S-O, Townsend RL, et al. 2017. Maternal obese-type gut microbiota differentially impact cognition, anxiety and compulsive behavior in male and female offspring in mice. PLoS One 12: e0175577.
Meyer KM, Mohammad M, Ma J, Chu D, Haymond M, Aagaard K. 2016. 66: Maternal diet alters the breast milk microbiome and microbial gene content. Am J Obstet Gynecol 214: S47 - S48.
Jiménez E, de Andrés J, Manrique M, et al. 2015. Metagenomic analysis of milk of healthy and mastitis-suffering women. J Hum Lact 31: 406 - 415.
Gomez-Gallego C, Garcia-Mantrana I, Salminen S, Collado MC. 2016. The human milk microbiome and factors influencing its composition and activity. Semin Fetal Neonatal Med 21: 400 - 405.
Davis JCC, Lewis ZT, Krishnan S, et al. 2017. Growth and morbidity of Gambian infants are influenced by maternal milk oligosaccharides and infant gut microbiota. Sci Rep 7: 40466.
Doherty AM, Lodge CJ, Dharmage SC, Dai X, Bode L, Lowe AJ. 2018. Human milk oligosaccharides and associations with immune-mediated disease and infection in childhood: A systematic review. Front Pediatr 6: 91.
Charbonneau MR, O’Donnell D, Blanton LV, et al. 2016. Sialylated milk oligosaccharides promote microbiota-dependent growth in models of infant undernutrition. Cell 164: 859 - 871.
Cryan JF, O’Mahony SM. 2011. The microbiome-gut-brain axis: From bowel to behavior. Neurogastroenterol Motil 23: 187 - 192.
Bravo JA, Forsythe P, Chew MV, et al. 2011. Ingestion of Lactobacillus strain regulates emotional behavior and central GABA receptor expression in a mouse via the vagus nerve. Proc Natl Acad Sci U S A National Acad Sciences. 108: 16050 - 16055.
Zivkovic AM, German JB, Lebrilla CB, Mills DA. 2011. Human milk glycobiome and its impact on the infant gastrointestinal microbiota. Proc Natl Acad Sci U S A 108 ( Suppl 1 ): 4653 - 4658.
Wiles TJ, Jemielita M, Baker RP, et al. 2016. Host gut motility promotes competitive exclusion within a model intestinal microbiota. PLoS Biol 14: e1002517.
Costello EK, Stagaman K, Dethlefsen L, Bohannan BJM, Relman DA. 2012. The application of ecological theory toward an understanding of the human microbiome. Science 336: 1255 - 1262.
Maynard CL, Elson CO, Hatton RD, Weaver CT. 2012. Reciprocal interactions of the intestinal microbiota and immune system. Nature 489: 231 - 241.
Korpela K, Costea P, Coelho LP, et al. 2018. Selective maternal seeding and environment shape the human gut microbiome. Genome Res 28: 561 - 568.
Shukri NHM, Wells J, Mukhtar F, Lee MHS, Fewtrell M. 2017. Study protocol: An investigation of mother-infant signalling during breastfeeding using a randomised trial to test the effectiveness of breastfeeding relaxation therapy on maternal psychological state, breast milk production and infant behaviour and growth. Int Breastfeed J 12: 33.
Arrieta M-C, Walter J, Finlay BB. 2016. Human microbiota-associated mice: A model with challenges. Cell Host Microbe 19: 575 - 578.
West-Eberhard MJ. 2005. Developmental plasticity and the origin of species differences. Proc Natl Acad Sci U S A 102 ( Suppl 1 ): 6543 - 6549.
Costantini D, Metcalfe NB, Monaghan P. 2010. Ecological processes in a hormetic framework. Ecol Lett 13: 1435 - 1447.
Masten AS, Obradovic J. 2006. Competence and resilience in development. Ann N Y Acad Sci 1094: 13 - 27.
Rutter M. 1993. Resilience: some conceptual considerations. J Adolesc Health 14: 626 - 631. 690-696.
Boyce WT, Chesterman E. 1990. Life events, social support, and cardiovascular reactivity in adolescence. J Dev Behav Pediatr 11: 105 - 111.
Hales CN, Barker DJ. 1992. Type 2 (non-insulin-dependent) diabetes mellitus: The thrifty phenotype hypothesis. Diabetologia 35: 595 - 601.
Douhard M, Loe LE, Stien A, et al. 2016. The influence of weather conditions during gestation on life histories in a wild Arctic ungulate. Proc Biol Sci 283: 20161760.
Del Giudice M, Ellis BJ, Shirtcliff EA. 2011. The adaptive calibration model of stress responsivity. Neurosci Biobehav Rev 35: 1562 - 1592.
Vickers MH, Gluckman PD, Coveny AH, et al. 2005. Neonatal leptin treatment reverses developmental programming. Endocrinology 146: 4211 - 4216.
Godfrey K. 2006. The -developmental origins- hypothesis: Epidemiology. In: Gluckman P et al., editors. Developmental origins of health and disease, Cambridge: Cambridge University Press. p 6 - 32.
Lea AJ, Altmann J, Alberts SC, Tung J. 2015. Developmental constraints in a wild primate. Am Nat 185: 809 - 821.
Tung J, Archie EA, Altmann J, Alberts SC. 2016. Cumulative early life adversity predicts longevity in wild baboons. Nat Commun 7: 11181.
French JA, Carp SB. 2016. Early-life social adversity and developmental processes in nonhuman primates. Curr Opin Behav Sci 7: 40 - 46.
Zipple MN, Roberts EK, Alberts SC, Beehner JC. 2019. Male-mediated prenatal loss: Functions and mechanisms. Evol Anthropol 28: 114 - 125.
Petrullo LA, Mandalaywala TM, Parker KJ, Maestripieri D, Higham JP. 2016. Effects of early life adversity on cortisol/salivary alpha-amylase symmetry in free-ranging juvenile rhesus macaques. Horm Behav 86: 78 - 84.
Altmann SA. 1998. Foraging for survival: Yearling baboons in Africa, Chicago: University of Chicago Press.
Gluckman PD, Hanson MA, Bateson P, et al. 2009. Towards a new developmental synthesis: Adaptive developmental plasticity and human disease. Lancet 373: 1654 - 1657.
Sapolsky RM, Romero LM, Munck AU. 2000. How do glucocorticoids influence stress responses? Integrating permissive, suppressive, stimulatory, and preparative actions. Endocr Rev 21: 55 - 89.
Sheriff MJ, Bell A, Boonstra R, et al. 2017. Integrating ecological and evolutionary context in the study of maternal stress. Integr Comp Biol 57: 437 - 449.
Seckl JR. 2001. Glucocorticoid programming of the fetus: Adult phenotypes and molecular mechanisms. Mol Cell Endocrinol 185: 61 - 71.
Hinde K. 2013. Lactational programming of infant behavioral phenotype. In: Clancy KBH, Hinde K, Rutherford JN, editors. Building babies: Primate development in proximate and ultimate perspective, Springer New York: New York, NY. p 187 - 207.
JaÅ¡areviÄ E, Howard CD, Morrison K, et al. 2018. The maternal vaginal microbiome partially mediates the effects of prenatal stress on offspring gut and hypothalamus. Nat Neurosci 21: 1061 - 1071.
JaÅ¡areviÄ E, Howerton CL, Howard CD, Bale TL. 2015. Alterations in the vaginal microbiome by maternal stress are associated with metabolic reprogramming of the offspring gut and brain. Endocrinology 156: 3265 - 3276.
Bailey MT, Lubach GR, Coe CL. 2004. Prenatal stress alters bacterial colonization of the gut in infant monkeys. J Pediatr Gastroenterol Nutr 38: 414 - 421.
Allen-Blevins CR, Sela DA, Hinde K. 2015. Milk bioactives may manipulate microbes to mediate parent-offspring conflict. Evol Med Public Health 2015: 106 - 121.
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spelling ftumdeepblue:oai:deepblue.lib.umich.edu:2027.42/152003 2023-08-20T04:03:11+02:00 Developmental responses to early-life adversity: Evolutionary and mechanistic perspectives Lu, Amy Petrullo, Lauren Carrera, Sofia Feder, Jacob Schneider‐crease, India Snyder‐mackler, Noah 2019-09 application/pdf https://hdl.handle.net/2027.42/152003 https://doi.org/10.1002/evan.21791 unknown John Wiley & Sons, Inc. Lu, Amy; Petrullo, Lauren; Carrera, Sofia; Feder, Jacob; Schneider‐crease, India Snyder‐mackler, Noah (2019). "Developmental responses to early-life adversity: Evolutionary and mechanistic perspectives." Evolutionary Anthropology: Issues, News, and Reviews 28(5): 249-266. 1060-1538 1520-6505 https://hdl.handle.net/2027.42/152003 doi:10.1002/evan.21791 Evolutionary Anthropology: Issues, News, and Reviews Round JL, Mazmanian SK. 2009. The gut microbiota shapes intestinal immune responses during health and disease. Nat Rev Immunol 9: 313 - 323. JaÅ¡areviÄ E, Howard CD, Misic AM, Beiting DP, Bale TL. 2017. Stress during pregnancy alters temporal and spatial dynamics of the maternal and offspring microbiome in a sex-specific manner. Sci Rep 7: 44182. Bruce-Keller AJ, Fernandez-Kim S-O, Townsend RL, et al. 2017. Maternal obese-type gut microbiota differentially impact cognition, anxiety and compulsive behavior in male and female offspring in mice. PLoS One 12: e0175577. Meyer KM, Mohammad M, Ma J, Chu D, Haymond M, Aagaard K. 2016. 66: Maternal diet alters the breast milk microbiome and microbial gene content. Am J Obstet Gynecol 214: S47 - S48. Jiménez E, de Andrés J, Manrique M, et al. 2015. Metagenomic analysis of milk of healthy and mastitis-suffering women. J Hum Lact 31: 406 - 415. Gomez-Gallego C, Garcia-Mantrana I, Salminen S, Collado MC. 2016. The human milk microbiome and factors influencing its composition and activity. Semin Fetal Neonatal Med 21: 400 - 405. Davis JCC, Lewis ZT, Krishnan S, et al. 2017. Growth and morbidity of Gambian infants are influenced by maternal milk oligosaccharides and infant gut microbiota. Sci Rep 7: 40466. Doherty AM, Lodge CJ, Dharmage SC, Dai X, Bode L, Lowe AJ. 2018. Human milk oligosaccharides and associations with immune-mediated disease and infection in childhood: A systematic review. Front Pediatr 6: 91. Charbonneau MR, O’Donnell D, Blanton LV, et al. 2016. Sialylated milk oligosaccharides promote microbiota-dependent growth in models of infant undernutrition. Cell 164: 859 - 871. Cryan JF, O’Mahony SM. 2011. The microbiome-gut-brain axis: From bowel to behavior. Neurogastroenterol Motil 23: 187 - 192. Bravo JA, Forsythe P, Chew MV, et al. 2011. Ingestion of Lactobacillus strain regulates emotional behavior and central GABA receptor expression in a mouse via the vagus nerve. Proc Natl Acad Sci U S A National Acad Sciences. 108: 16050 - 16055. Zivkovic AM, German JB, Lebrilla CB, Mills DA. 2011. Human milk glycobiome and its impact on the infant gastrointestinal microbiota. Proc Natl Acad Sci U S A 108 ( Suppl 1 ): 4653 - 4658. Wiles TJ, Jemielita M, Baker RP, et al. 2016. Host gut motility promotes competitive exclusion within a model intestinal microbiota. PLoS Biol 14: e1002517. Costello EK, Stagaman K, Dethlefsen L, Bohannan BJM, Relman DA. 2012. The application of ecological theory toward an understanding of the human microbiome. Science 336: 1255 - 1262. Maynard CL, Elson CO, Hatton RD, Weaver CT. 2012. Reciprocal interactions of the intestinal microbiota and immune system. Nature 489: 231 - 241. Korpela K, Costea P, Coelho LP, et al. 2018. Selective maternal seeding and environment shape the human gut microbiome. Genome Res 28: 561 - 568. Shukri NHM, Wells J, Mukhtar F, Lee MHS, Fewtrell M. 2017. Study protocol: An investigation of mother-infant signalling during breastfeeding using a randomised trial to test the effectiveness of breastfeeding relaxation therapy on maternal psychological state, breast milk production and infant behaviour and growth. Int Breastfeed J 12: 33. Arrieta M-C, Walter J, Finlay BB. 2016. Human microbiota-associated mice: A model with challenges. Cell Host Microbe 19: 575 - 578. West-Eberhard MJ. 2005. Developmental plasticity and the origin of species differences. Proc Natl Acad Sci U S A 102 ( Suppl 1 ): 6543 - 6549. Costantini D, Metcalfe NB, Monaghan P. 2010. Ecological processes in a hormetic framework. Ecol Lett 13: 1435 - 1447. Masten AS, Obradovic J. 2006. Competence and resilience in development. Ann N Y Acad Sci 1094: 13 - 27. Rutter M. 1993. Resilience: some conceptual considerations. J Adolesc Health 14: 626 - 631. 690-696. Boyce WT, Chesterman E. 1990. Life events, social support, and cardiovascular reactivity in adolescence. J Dev Behav Pediatr 11: 105 - 111. Hales CN, Barker DJ. 1992. Type 2 (non-insulin-dependent) diabetes mellitus: The thrifty phenotype hypothesis. Diabetologia 35: 595 - 601. Douhard M, Loe LE, Stien A, et al. 2016. The influence of weather conditions during gestation on life histories in a wild Arctic ungulate. Proc Biol Sci 283: 20161760. Del Giudice M, Ellis BJ, Shirtcliff EA. 2011. The adaptive calibration model of stress responsivity. Neurosci Biobehav Rev 35: 1562 - 1592. Vickers MH, Gluckman PD, Coveny AH, et al. 2005. Neonatal leptin treatment reverses developmental programming. Endocrinology 146: 4211 - 4216. Godfrey K. 2006. The -developmental origins- hypothesis: Epidemiology. In: Gluckman P et al., editors. Developmental origins of health and disease, Cambridge: Cambridge University Press. p 6 - 32. Lea AJ, Altmann J, Alberts SC, Tung J. 2015. Developmental constraints in a wild primate. Am Nat 185: 809 - 821. Tung J, Archie EA, Altmann J, Alberts SC. 2016. Cumulative early life adversity predicts longevity in wild baboons. Nat Commun 7: 11181. French JA, Carp SB. 2016. Early-life social adversity and developmental processes in nonhuman primates. Curr Opin Behav Sci 7: 40 - 46. Zipple MN, Roberts EK, Alberts SC, Beehner JC. 2019. Male-mediated prenatal loss: Functions and mechanisms. Evol Anthropol 28: 114 - 125. Petrullo LA, Mandalaywala TM, Parker KJ, Maestripieri D, Higham JP. 2016. Effects of early life adversity on cortisol/salivary alpha-amylase symmetry in free-ranging juvenile rhesus macaques. Horm Behav 86: 78 - 84. Altmann SA. 1998. Foraging for survival: Yearling baboons in Africa, Chicago: University of Chicago Press. Gluckman PD, Hanson MA, Bateson P, et al. 2009. Towards a new developmental synthesis: Adaptive developmental plasticity and human disease. Lancet 373: 1654 - 1657. Sapolsky RM, Romero LM, Munck AU. 2000. How do glucocorticoids influence stress responses? Integrating permissive, suppressive, stimulatory, and preparative actions. Endocr Rev 21: 55 - 89. Sheriff MJ, Bell A, Boonstra R, et al. 2017. Integrating ecological and evolutionary context in the study of maternal stress. Integr Comp Biol 57: 437 - 449. Seckl JR. 2001. Glucocorticoid programming of the fetus: Adult phenotypes and molecular mechanisms. Mol Cell Endocrinol 185: 61 - 71. Hinde K. 2013. Lactational programming of infant behavioral phenotype. In: Clancy KBH, Hinde K, Rutherford JN, editors. Building babies: Primate development in proximate and ultimate perspective, Springer New York: New York, NY. p 187 - 207. JaÅ¡areviÄ E, Howard CD, Morrison K, et al. 2018. The maternal vaginal microbiome partially mediates the effects of prenatal stress on offspring gut and hypothalamus. Nat Neurosci 21: 1061 - 1071. JaÅ¡areviÄ E, Howerton CL, Howard CD, Bale TL. 2015. Alterations in the vaginal microbiome by maternal stress are associated with metabolic reprogramming of the offspring gut and brain. Endocrinology 156: 3265 - 3276. Bailey MT, Lubach GR, Coe CL. 2004. Prenatal stress alters bacterial colonization of the gut in infant monkeys. J Pediatr Gastroenterol Nutr 38: 414 - 421. Allen-Blevins CR, Sela DA, Hinde K. 2015. Milk bioactives may manipulate microbes to mediate parent-offspring conflict. Evol Med Public Health 2015: 106 - 121. IndexNoFollow predictive adaptive responses developmental constraints developmental plasticity glucocorticoids maternal capital microbiome Anthropology Social Sciences Article 2019 ftumdeepblue https://doi.org/10.1002/evan.2179110.1002/ajpa.23315 2023-07-31T20:46:57Z Adverse ecological and social conditions during early life are known to influence development, with rippling effects that may explain variation in adult health and fitness. The adaptive function of such developmental plasticity, however, remains relatively untested in long-lived animals, resulting in much debate over which evolutionary models are most applicable. Furthermore, despite the promise of clinical interventions that might alleviate the health consequences of early-life adversity, research on the proximate mechanisms governing phenotypic responses to adversity have been largely limited to studies on glucocorticoids. Here, we synthesize the current state of research on developmental plasticity, discussing both ultimate and proximate mechanisms. First, we evaluate the utility of adaptive models proposed to explain developmental responses to early-life adversity, particularly for long-lived mammals such as humans. In doing so, we highlight how parent-offspring conflict complicates our understanding of whether mothers or offspring benefit from these responses. Second, we discuss the role of glucocorticoids and a second physiological system-the gut microbiome-that has emerged as an additional, clinically relevant mechanism by which early-life adversity can influence development. Finally, we suggest ways in which nonhuman primates can serve as models to study the effects of early-life adversity, both from evolutionary and clinical perspectives. Peer Reviewed https://deepblue.lib.umich.edu/bitstream/2027.42/152003/1/evan21791_am.pdf https://deepblue.lib.umich.edu/bitstream/2027.42/152003/2/evan21791.pdf Article in Journal/Newspaper Arctic University of Michigan: Deep Blue Evolutionary Anthropology: Issues, News, and Reviews 28 5 249 266