Maternal stress has divergent effects on gene expression patterns in the brains of male and female threespine stickleback.
Maternal stress can have long-term effects on neurodevelopment that can influence offspring performance and population evolutionary trajectories. To examine the mechanistic basis for these neurodevelopmental effects of maternal stress, we used RNA-seq to assess differential gene expression across the brain transcriptome of adult male and female threespine stickleback (Gasterosteus aculeatus) from stressed and unstressed mothers. We identified sexually divergent effects of maternal stress on the brain transcriptome. In males, genes that were upregulated by maternal stress were enriched for processes involved in synaptic function and organization and steroid hormone-mediated signalling pathways, whereas in females genes that were upregulated by maternal stress were enriched for processes involved in protein translation and metabolic functions. The expression of several genes involved in the hypothalamic-pituitary-interrenal response to stress and epigenetic processes such as the regulation of DNA methylation patterns and miRNAs increased in males and not in females. These data suggest that maternal stress has markedly different effects on cellular pathways in the brains of male and female offspring of mothers that are exposed to stress, which could have important implications when assessing the long-term ecological and evolutionary impacts of stress across generations.
Department of Zoology, 6270 University Boulevard, University of British Columbia, Vancouver, BC, Canada V6T 1Z4 dmetzger@zoology.ubc.ca.
David C H
http://orcid.org/0000-0001-7552-1204
DC
Metzger
Department of Zoology, 6270 University Boulevard, University of British Columbia, Vancouver, BC, Canada V6T 1Z4.
Patricia M
http://orcid.org/0000-0002-5237-8836
PM
Schulte
Gasterosteus aculeatus; RNA-seq; maternal effect; sex-dependent; sexual dimorphism; transcriptome
Genome Biol. 2010;11(2):R14
20132535
Am Nat. 2010 Mar;175(3):382-90
20109061
J Neurosci. 2012 Feb 15;32(7):2241-7
22396398
Genome Biol. 2010;11(10):R106
20979621
Science. 1999 Nov 5;286(5442):1155-8
10550053
Glob Chang Biol. 2015 Dec;21(12):4387-400
26183221
Front Zool. 2015 Dec 24;12:38
26705404
Gene. 2016 Sep 30;590(2):307-16
27259666
Nat Rev Neurosci. 2010 Jan;11(1):9-17
20019686
Physiol Behav. 2013 Oct 2;122:222-7
23628383
RNA. 2014 Nov;20(11):1684-96
25246651
Gen Comp Endocrinol. 2017 Feb 1;242:30-37
26718080
Epigenetics. 2008 Mar-Apr;3(2):97-106
18536531
Proc Biol Sci. 2011 Jun 7;278(1712):1753-9
21068041
Bioinformatics. 2015 Jan 15;31(2):233-41
25273110
Comp Biochem Physiol A Mol Integr Physiol. 2008 Mar;149(3):314-24
18289901
Philos Trans R Soc Lond B Biol Sci. 2008 Jan 12;363(1489):101-22
17282988
Comp Biochem Physiol Part D Genomics Proteomics. 2016 Jun;18:10-20
26922644
Trends Genet. 2005 May;21(5):298-305
15851067
Evolution. 1984 Jul;38(4):735-742
28555827
Mol Ecol. 2013 Jun;22(12):3216-41
23763602
Nat Neurosci. 2009 Dec;12(12):1559-66
19898468
Genome Biol Evol. 2015 Jan 23;7(2):581-90
25618140
Nat Neurosci. 2001 Feb;4(2):170-5
11175878
BMC Genomics. 2014 Aug 06;15:655
25099474
J Evol Biol. 2014 Aug;27(8):1604-12
24898271
Br Med Bull. 2001;60:5-20
11809615
PLoS One. 2008 Mar 12;3(3):e1791
18335061
Neurochem Res. 2007 Oct;32(10):1730-40
17406975
Mol Biol Evol. 2015 Aug;32(8):1981-95
25818858
Trends Ecol Evol. 1996 Feb;11(2):82-6
21237767
Proc Biol Sci. 2009 Jun 7;276(1664):2085-92
19324759
Proc Biol Sci. 2015 Jul 7;282(1810):
26108633
Mar Biotechnol (NY). 2015 Oct;17(5):613-23
26242754
PLoS One. 2012;7(1):e30055
22276144
Nucleic Acids Res. 2014 Jun;42(11):e91
24753412
J Evol Biol. 2014 Nov;27(11):2297-307
25264208
J Evol Biol. 2010 Jun 1;23(6):1261-77
20406344
Mol Ecol Resour. 2016 Nov;16(6):1389-1400
27238091
Curr Opin Behav Sci. 2016 Feb 1;7:28-32
26858970
J Neurosci Methods. 2004 Sep 30;138(1-2):199-206
15325128
Front Neuroendocrinol. 1998 Oct;19(4):323-62
9799588
Nat Rev Neurosci. 2015 Jun;16(6):332-44
25921815
Science. 1997 Sep 12;277(5332):1659-62
9287218
Gen Comp Endocrinol. 2014 Jan 15;196:72-80
24291303
Ecol Lett. 2013 Feb;16(2):271-80
23205937
BMC Genomics. 2014 May 26;15:400
24886435
Biochim Biophys Acta. 1999 Feb 9;1410(2):159-70
10076024
Nat Neurosci. 2004 Aug;7(8):847-54
15220929
J Evol Biol. 2009 Dec;22(12):2524-31
19878498
Nat Rev Genet. 2007 Sep;8(9):689-98
17680007
Proc Biol Sci. 2016 Sep 28;283(1839):
27683372
Evol Appl. 2016 Feb 28;9(9):1096-1111
27695518
Annu Rev Psychol. 1998;49:43-64
9496621
BMC Genomics. 2016 Jan 05;17:28
26732976
Ecol Evol. 2014 Aug;4(16):3236-43
25473476
Ann N Y Acad Sci. 2008;1133:151-61
18559819
Mol Biol Evol. 2010 Jul;27(7):1495-503
20142438
Nat Biotechnol. 2014 Sep;32(9):896-902
25150836
Front Neuroendocrinol. 2015 Oct;39:28-37
26368654
Biochim Biophys Acta. 1998 Aug 10;1366(1-2):211-23
9714810
Neurosci Biobehav Rev. 2015 Jan;48:70-91
25464029
Neurosci Biobehav Rev. 2015 Aug;55:520-35
26073068