Skip to main content
SpringerLink
Log in

X-linked and lineage-dependent inheritance of coping responses to stress

  • Published:
Mammalian Genome Aims and scope Submit manuscript

Abstract

Coping—or how one routinely deals with stress—is a complex behavioral trait with bearing on chronic disease and susceptibility to psychiatric disorders. This complexity is a result of not only underlying multigenic factors, but also important non-genetic ones. The defensive burying (DB) test, although originally developed as a test of anxiety, can accurately measure differences in coping strategies by assaying an animal’s behavioral response to an immediate threat with ethological validity. Using offspring derived from reciprocal crosses of two inbred rat strains differing in DB behaviors, we provide convergent phenotypic and genotypic evidence that coping styles are inherited in an X-linked fashion. We find that first-generation (F1) males, but not females, show maternally derived coping styles, and second-generation (F2) females, but not males, show significant differences in coping styles when separated by grandmaternal lineage. By using a linear modeling approach to account for covariate effects (sex and lineage) in QTL analysis, we map three quantitative trait loci (QTL) on the X Chromosome (Chr) (Coping-1, Approach-1, and Approach-2) associated with coping behaviors in the DB paradigm. Distinct loci were associated with different aspects of coping, and their effects were modulated by both the sex and lineage of the animals, demonstrating the power of the general linear modeling approach and the important interplay of allelic and non-allelic factors in the inheritance of coping behaviors.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Figure 1
Figure 2
Figure 3
Figure 4
Figure 5
Figure 6

Similar content being viewed by others

References

  1. JC Alcolado K Laji R Gill-Randall (2002) ArticleTitleMaternal transmission of diabetes. Diabet Med 1 89–98 Occurrence Handle10.1046/j.1464-5491.2002.00675.x

    Article  Google Scholar 

  2. KW Broman H Wu S Sen GA Churchill (2003) ArticleTitleR/qtl: an extensible QTL mapping environment. Bioinformatics 19 1–2 Occurrence Handle10.1093/bioinformatics/btg112

    Article  Google Scholar 

  3. A Busjahn HD Faulhaber K Freier FC Luft (1999) ArticleTitleGenetic and environmental influences on coping styles: a twin study. Psychosom Med 61 469–475 Occurrence Handle1:STN:280:DyaK1MzntFemtw%3D%3D Occurrence Handle10443755

    CAS  PubMed  Google Scholar 

  4. GA Churchill RW Doerge (1994) ArticleTitleEmpirical threshold values for quantitative trait mapping. Genetics 138 963–971 Occurrence Handle1:STN:280:ByqC2MvntFw%3D Occurrence Handle7851788

    CAS  PubMed  Google Scholar 

  5. P Costa R McCrae (1989) . K Markides C Cooper (Eds) Aging, Stress, and Health, Wiley New York 269–285

    Google Scholar 

  6. DD Francis C Caldji F Champagne PM Plotsky MJ Meaney (1999) ArticleTitleThe role of corticotropin-releasing factor—norepinephrine systems in mediating the effects of early experience on the development of behavioral and endocrine responses to stress. Biol Psyrchiatry 46 1153–1166 Occurrence Handle10.1016/S0006-3223(99)00237-1 Occurrence Handle1:CAS:528:DyaK1MXotVOktr8%3D

    Article  CAS  Google Scholar 

  7. G Huether (1996) ArticleTitleThe central adaptation syndrome: psychosocial stress as a trigger for adaptive modifications of brain structure and brain function. Prog Neurobiol 48 569–612 Occurrence Handle10.1016/0301-0082(96)00003-2 Occurrence Handle1:STN:280:BymH3crnvVQ%3D Occurrence Handle8809909

    Article  CAS  PubMed  Google Scholar 

  8. JM Koolhaas SM Korte SF De Boer BJ Van Der Vegt CG Van Reenen et al. (1999) ArticleTitleCoping styles in animals: current status in behavior and stress-physiology. Neurosci Biobehav Rev 23 925–935 Occurrence Handle1:STN:280:DC%2BD3c%2Fks1amsA%3D%3D Occurrence Handle10580307

    CAS  PubMed  Google Scholar 

  9. SM Korte GAH Bouws JM Koolhaas B Bohus (1992) ArticleTitleNeuroendocrine and behavioral responses during conditioned active and passive behavior in the defensive burying/probe avoidance paradigm: effects of ipsapirone. Physiol Behav 52 355–361 Occurrence Handle1:CAS:528:DyaK38XlsVegtLk%3D Occurrence Handle1355919

    CAS  PubMed  Google Scholar 

  10. ES Lander D Botstein (1989) ArticleTitleMapping Mendelian factors underlying quanititative traits using RFLP linkage maps. Genetics 121 185–199 Occurrence Handle1:STN:280:BiaC3sjpsVw%3D Occurrence Handle2563713

    CAS  PubMed  Google Scholar 

  11. R Lazarus S Folkman (1984) Stress, Appraisal and Coping. Springer New York

    Google Scholar 

  12. CA Mellins M Gatz L Baker (1996) ArticleTitleChildren’s methods of coping with stress: a twin study of genetic and environmental influences. J Child Psychol Psyrchiatry Allied Discip 37 721–730 Occurrence Handle1:STN:280:ByiD2M%2Fit1E%3D

    CAS  Google Scholar 

  13. IY Millwood MT Bihoreau D Gauguier G Hyne ER Levy et al. (1997) ArticleTitleA gene-based genetic linkage and comparative map of the rat X chromosome. Genomics 40 253–261 Occurrence Handle10.1006/geno.1996.4555 Occurrence Handle1:CAS:528:DyaK2sXhvVOnt74%3D Occurrence Handle9119392

    Article  CAS  PubMed  Google Scholar 

  14. RJ Oakey CV Beechey (2002) ArticleTitleImprinted genes: identification by chromosome rearrangements and post-genomic strategies. Trends Genet 18 359–366 Occurrence Handle10.1016/S0168-9525(02)02708-7 Occurrence Handle1:CAS:528:DC%2BD38XlsVOlsrk%3D Occurrence Handle12127776

    Article  CAS  PubMed  Google Scholar 

  15. WP Pare (1994) ArticleTitleOpen field, learned helplessness, conditioned defensive burying, and forced-swim tests in WKY rats. Physiol Behav 55 433–439 Occurrence Handle1:STN:280:ByuB2cfhvVQ%3D Occurrence Handle8190758

    CAS  PubMed  Google Scholar 

  16. RJ Rodgers (1997) ArticleTitleAnimal models of ‘anxiety’: where next? Behav Pharmacol 8 477–504 Occurrence Handle1:CAS:528:DyaK2sXnvFCqt7Y%3D Occurrence Handle9832964

    CAS  PubMed  Google Scholar 

  17. M Rostrup A Westheim SE Kjeldsen I Eide (1993) ArticleTitleCardiovascular reactivity, coronary risk factors, and sympathetic activity in young men. Hypertension 22 891–899 Occurrence Handle1:STN:280:ByuD28vhtVQ%3D Occurrence Handle8244522

    CAS  PubMed  Google Scholar 

  18. M Rutter (1985) ArticleTitleResilience in the face of adversity: protective factors and resistance to psyrchiatric disorder. Br J Psyrchiatry 147 598–611 Occurrence Handle1:STN:280:BimC28%2FmtVw%3D

    CAS  Google Scholar 

  19. S Sen GA Churchill (2001) ArticleTitleA statistical framework for quantitative trait mapping. Genetics 159 371–387 Occurrence Handle1:STN:280:DC%2BD3MrhtlShsA%3D%3D Occurrence Handle11560912

    CAS  PubMed  Google Scholar 

  20. K Shimomura SS Low-Zeddies DP King TD Steeves A Whiteley et al. (2001) ArticleTitleGenome-wide epistatic interaction analysis reveals complex genetic determinants of circadian behavior in mice. Genome Res 11 959–980 Occurrence Handle10.1101/gr.171601 Occurrence Handle1:CAS:528:DC%2BD3MXkt12rur0%3D Occurrence Handle11381025

    Article  CAS  PubMed  Google Scholar 

  21. F Sluyter SM Korte B Bohus GA Van Oortmerssen (1996) ArticleTitleBehavioral stress response of genetically selected aggressive and nonagressive wild house mice in the shock-probe/defensive burying test. Pharmacol Biochem Behav 54 113–116 Occurrence Handle10.1016/0091-3057(95)02164-7 Occurrence Handle1:CAS:528:DyaK28XisVOis7k%3D Occurrence Handle8728547

    Article  CAS  PubMed  Google Scholar 

  22. D Treit (1991) Defensive burying: a pharmacolgocial animal model for specific fears? P Soubrie D Widlocker (Eds) Anxiety, Depression, and Mania: Animal Models of Psyrchiatric Disorders. Karger New York, Basel 1–19

    Google Scholar 

  23. D Treit J Menard (1994) ArticleTitleThe shock-probe burying test. Neurosci Protocols . 9–17

    Google Scholar 

  24. D Treit JP Pinel HC Fibiger (1981) ArticleTitleConditioned defensive burying: a new paradigm for the study of anxiolytic agents. Pharmacol Biochem Behav 15 619–626 Occurrence Handle1:CAS:528:DyaL3MXmtFGjur8%3D Occurrence Handle6117086

    CAS  PubMed  Google Scholar 

  25. D Treit VM Lolordo DE Armstrong (1986) ArticleTitleThe effects of diazepam on “fear” reactions in rats are modulated by environmental constraints on the rat’s defensive repertoire. Pharmacol Biochem Behav 25 561–556 Occurrence Handle10.1016/0091-3057(86)90141-3 Occurrence Handle1:CAS:528:DyaL28Xls1Cqsbw%3D Occurrence Handle3774820

    Article  CAS  PubMed  Google Scholar 

  26. C Vogele A Steptoe (1992) ArticleTitleEmotional coping and tonic blood pressure as determinants of cardiovascular responses to mental stress. J Hypertens 10 1079–1087 Occurrence Handle1:STN:280:ByyD3MjotlM%3D Occurrence Handle1328368

    CAS  PubMed  Google Scholar 

  27. B Wechsler (1995) ArticleTitleCoping and coping strategies: a behavioural view. Appl Anim Behav Sci 43 123–134 Occurrence Handle10.1016/0168-1591(95)00557-9

    Article  Google Scholar 

  28. EE Werner (1989) ArticleTitleHigh-risk rchildren in young adulthood: a longitudinal study from birth to 32 years. Am J Orthopsyrchiatry 59 72–81 Occurrence Handle1:STN:280:BiaC1M%2Fps1Q%3D

    CAS  Google Scholar 

  29. SL Whatley AC Foreman S Richards (1998) ArticleTitleThe relationship of coping style to dysphoria, anxiety, and anger. Psychol Rep 83 783–791 Occurrence Handle1:STN:280:DyaK1M7itF2jtQ%3D%3D Occurrence Handle9923152

    CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We thank Amber E. Baum for assistance with DNA isolation, and Hoda Mahmoudi for assistance with initial phenotype characterization and DNA isolation. Photographs used in Fig. 1 were kindly provided by William P. Pare. This study was supported by NIH grant MH60789. J.S. Takahashi is an Investigator in the Howard Hughes Medical Institute.

Author information

Authors and Affiliations

  1. Department of Psychiatry and Behavioral Sciences, Northwestern University Feinberg School of Medicine, 303 E. Chicago Ave., Ward 9-190 Chicago, Illinois 60611, USA

    Nasim Ahmadiyeh, Leah C. Solberg & Eva E. Redei

  2. Howard Hughes Medical Institute, Northwestern University, Evanston, Illinois 60208, USA

    Nasim Ahmadiyeh, Kazuhiro Shimomura & Joseph S. Takahashi

  3. Department of Neurobiology and Physiology, Northwestern University, Evanston, Illinois 60208, USA

    Nasim Ahmadiyeh, Kazuhiro Shimomura, Leah C. Solberg & Joseph S. Takahashi

  4. The Jackson Laboratory, Bar Harbor, Maine 04609, USA

    Gary A. Churchill

Authors
  1. Nasim Ahmadiyeh
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Gary A. Churchill
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Kazuhiro Shimomura
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Leah C. Solberg
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Joseph S. Takahashi
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Eva E. Redei
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Nasim Ahmadiyeh.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Ahmadiyeh, N., Churchill, G.A., Shimomura, K. et al. X-linked and lineage-dependent inheritance of coping responses to stress . Mamm Genome 14, 748–757 (2003). https://doi.org/10.1007/s00335-003-2292-x

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00335-003-2292-x

Keywords

Search

Navigation