Skip to main content
SpringerLink
Log in

Some Differences in Thymus Morphology in Immature Insectivorous Mammals: Sorex araneus, Sorex caecutiens, Neomys fodiens, and Erinaceus roumanicus

  • Published:
Biology Bulletin Aims and scope Submit manuscript

Abstract

The thymus structure of four species of immature insectivorous mammals belonging to the families Soricidae and Erinaceidae (Eulipotyphla) has been studied. Representatives of the studied families are characterized by contrary surviving strategies, significantly differing in the intensity of metabolism and the activity of the animal. As these differences are presumably reflected in the morphological parameters of the thymus, this work aimed at a comparative study of these parameters of the thymus in representatives of the above two families. A light microscopy technique has been applied. Sections of thymus lobes 5 µm thick have been stained with hematoxylin and eosin, as well as picrofuchsin, according to van Gieson’s method, and with azure-eosin, according to Romanovskii–Giemsa. During the processing of the material, the mass index and the cortical-medullar index of the thymus have been determined. The area of the connective and lymphoid tissues on the thymus section has been identified. The number of thymocytes, as well as the number and area of the vessels of the microvasculature of both the thymus cortex and the medulla have been counted within the conventional unit area. The percentage of thymocytes in mitosis has been calculated. The results of the study show that the shrews have a higher thymus mass index than the northern white-breasted hedgehog. This leads to significant changes in the syntopy of the thymic lobules. In comparison to the northern white-breasted hedgehog, the thymus of shrews is characterized by an increased cortical-medullar index, a higher density of the arrangement of thymocytes per unit area, and a higher number and relative area of the vessels of the microvasculature. At the same time, all studied immature representatives of insectivorous mammalian species have equally high relative areas of lymphoid tissue. This indicates an active functional state of the thymus at this life stage in all Eulipotyphla representatives. The relative area of the thymus connective tissue is directly related to the absolute dimensions of the organ, which is necessary for the implementation of the frame function. The values of the mitotic index of the thymus medulla in Eulipotyphla representatives are higher than expected and may indicate the need for increasing the pool of thymocytes at a very late stage of differentiation. The patterns revealed indicate that the morphology of the thymus depends on the biological characteristics of representatives of different families of Eulipotyphla, has a certain adaptive value, and deserves further study.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1.
Fig. 2.

Similar content being viewed by others

REFERENCES

  1. Abrams, E.T. and Miller, E.M., The roles of the immune system in women’s reproduction: evolutionary constraints and life history trade-offs, Am. J. Phys. Anthropol., 2011, vol. 146, suppl. 53, pp. 134–154.https://doi.org/10.1002/ajpa.2162122101690

  2. Andersson, U. and Tracey, K.J., Reflex principles of immunological homeostasis, Annu. Rev. Immunol., 2012, vol. 30, no. 1, pp. 313–335.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Balu, J.N., A comparative study of the microcirculation in the guinea-pig thymus, lymph nodes and Peyer’s patches, Clin. Exp. Immunol., 1977, vol. 27, no. 2, pp. 340–347. PMID: 849659; PMCID: PMC1540799.

    CAS  PubMed  PubMed Central  Google Scholar 

  4. Bhandoola, A., von Boehmer, H., Petrie, H.T., and Zúñiga-Pflücker, J.C., Commitment and developmental potential of extrathymic and intrathymic T cell precursors: plenty to choose from, Immunity, 2007, vol. 26, no. 6, pp. 678–689.

    Article  CAS  PubMed  Google Scholar 

  5. Le Campion, A., Vasseur, F., and Pénit, C., Regulation and kinetics of premigrant thymocyte expansion, Eur. J. Immunol., 2000, vol. 30, no. 3, pp. 738–746. PMID: 10741388.https://doi.org/10.1002/1521-4141(200003)30:3<738::AID-IMMU738>3.0.CO;2-Y

    Article  CAS  PubMed  Google Scholar 

  6. Chen, W., The late stage of t cell development within mouse thymus, Cell. Mol. Immunol., 2004, vol. 1, no. 1, pp. 3–11.

    CAS  PubMed  Google Scholar 

  7. Chernova, O.F., Origin and evolution of the hair cover, in Evolyutsionnye faktory formirovaniya raznoobraziya zhivotnogo mira (Evolutionary Factors in the Formation of the Diversity of the Animal World), Vorob’ev, E.I. and Striganov, B.R., Eds., Moscow: KMK, 2005, pp. 135–149.

  8. Dudakov, J.A., Khong, D.M., Boyd, R.L., and Chidgey, A.P., Feeding the fire: the role of defective bone marrow function in exacerbating thymic involution, Trends Immunol., 2010, vol. 31, no. 5, pp. 191–198.

    Article  CAS  PubMed  Google Scholar 

  9. Eckrich, C.A., Flaherty, E.A., and Ben-David, M., Functional and numerical responses of shrews to competition vary with mouse density, PLoS One, 2018, vol. 13, no. 1, pp. 1–21.

    Article  Google Scholar 

  10. Francini, A. and Ottaviani, E., Thymus: conservation in evolution, Gen. Comp. Endocrinol., 2017, vol. 246, no. 15, pp. 46–50.

    Article  Google Scholar 

  11. Galagudza, M.M., Sonin, D.L., Vlasov, T.D., Kurapeev, D.I., and Shlyakhto, E.V., Remote vs. local ischaemic preconditioning in the rat heart: infarct limitation, suppression of ischaemic arrhythmia and the role of reactive oxygen species, Int. J. Clin. Exp. Pathol., 2016, vol. 97, no. 1, pp. 66–74.

    Article  CAS  Google Scholar 

  12. Gennen, V., The appearance of the thymus and the integrated evolution of adaptive immune and neuroendocrine systems, Acta Clin. Belg., 2012, vol. 67, no. 3, pp. 209–213.

    Google Scholar 

  13. Haigh, A., O’Riordan, R., and Butler, F., Nesting behavior and seasonal body mass changes in a rural Irish population of the Western hedgehog (Erinaceus europaeus), Acta Theriol., 2012, vol. 57, no. 4, pp. 321–331.

    Article  Google Scholar 

  14. Käkelä, R. and Hyvarinen, H., Fatty acids in the triglycerides and phospholipids of the common shrew (Sorex araneus) and the water shrew (Neomys fodiens), Comp. Biochem. Physiol., Part B: Biochem. Mol. Biol., 1995, vol. 112, no. 1, pp. 71–81.

    Article  Google Scholar 

  15. Kiselev, S.V., Physiological response of the even-toothed shrew (Sorex isodon) to starvation and refeeding, Zh. Evol. Biokhim. Fiziol., 2017, vol. 53, no. 4, pp. 288–294.

    Google Scholar 

  16. Klein, L., Hinterberger, M., Wirnsberger, G., and Kyewski, B., Antigen presentation in the thymus for positive selection and central tolerance induction, Nat. Rev. Immunol., 2009, vol. 9, no. 12, pp. 33–44. PMID: 19935803.https://doi.org/10.1038/nri2669

  17. Klevezal’, G.A., Printsipy i metody opredeleniya vozrasta mlekopitayushchikh (Principles and Methods for Determining the Age of Mammals), Moscow: KMK, 2007.

  18. Kondo, K., Ohigashi, I., and Takahama, Y., Thymus machinery for T-cell selection, Int. Immunol., 2019, vol. 31, no. 3, pp. 119–125. PMID: 30476234; PMCID: PMC6400048.https://doi.org/10.1093/intimm/dxy081

  19. Kowalski, K., Marciniak, P., Rosiński, G., and Rychlik, L., Evaluation of the physiological activity of venom from the Eurasian water shrew Neomys fodiens, Front. Zool., 2017, vol. 14, p. 46. www.ncbi.nlm.nih.gov/pmc/articles/PMC5622582. Updated September 30, 2017. https://doi.org/10.1186/s12983-017-0230-0

  20. Kupriyanov, V.V., Puti mikrotsirkulyatsii (Ways of Microcirculation), Chisinau: Kartya Moldovenske, 1969.

  21. Kvetnoi, I.M., Yarilin, A.A., Polyakova, V.O., and Knyaz’kin, I.V., Neiroimmunoendokrinologiya timusa (Thymus Neuroimmunoendocrinology), St. Petersburg: DEAN, 2005.

  22. Lazaro, J., Hertel, M., Muturi, M., and Dechmann, D.K., Seasonal reversible size changes in the braincase and mass of common shrews are flexibly modified by environmental conditions, Sci. Rep., 2019, vol. 9, p. 2489. www.nature.com/articles/s41598-019-38884-1. Updated March 21, 2019. https://doi.org/10.1038/s41598-019-38884-1

  23. Long, K.Z. and Nanthakumar, N., Energetic and nutritional regulation of the adaptive immune response and trade-offs in ecological immunology, Am. J. Hum. Biol., 2004, vol. 16, pp. 499–507.

    Article  PubMed  Google Scholar 

  24. Luc, S., Buza-Vidas, N., and Jacobsen, S.E.W., Biological and molecular evidence for existence of lymphoid-primed multipotent progenitors, Ann. N.Y. Acad. Sci., 2007, vol. 1106, pp. 89–94.

    Article  CAS  PubMed  Google Scholar 

  25. McDade, T.W., Life history theory and the immune system: steps toward a human ecological immunology, Am. J. Phys. Anthropol., 2003, suppl. 37, pp. 100–125.

  26. Merkulov, G.A., Kurs patologicheskoi tekhniki (Pathological Technique Course), Moscow: Meditsina, 1969.

  27. Meyer, P.A.R., Re-orchestration of blood flow by micro-circulations, Eye (London), 2018, vol. 32, no. 2, pp. 222–229. www.nature.com/articles/eye2017315. Updated January 19, 2018. https://doi.org/10.1038/eye.2017.315

  28. Mori, K., Itoi, M., Tsukamoto, N., Kubo, H., and Amagai, T., The perivascular space as a path of hematopoietic progenitor cells and mature t cells between the blood circulation and thymic parenchyma, Int. Immunol., 2007, vol. 19, no. 6, pp. 745–753.

    Article  CAS  PubMed  Google Scholar 

  29. Panov, V.V. and Karpenko, S.V., Population dynamics of the common water shrew Neomus fodiens (Mammalia: Soricidae) and its helminth fauna in Northern Barbara, Parazitologiya, 2004, vol. 38, no. 5, pp. 448–456.

    CAS  Google Scholar 

  30. Pearse, G., Normal structure, function and histology of the thymus, Toxicol. Pathol., 2006, vol. 34, no. 5, pp. 504–514.

    Article  PubMed  Google Scholar 

  31. Prendergast, B.J., Freeman, D.A., Zucker, I., and Nelson, R.J., Periodic arousal from hibernation is necessary for initiation of immune responses in ground squirrels, Am. J. Physiol., Regul., Integr. Comp. Physiol., 2002, vol. 282, pp. 1054–1062.

    Article  Google Scholar 

  32. Rutovskaya, M.V., Diatroptov, M.E., Kuznetsova, E.V., Anufriev, A.I., Feoktistova, N.Yu., and Surov, A.V., The dynamics of body temperature of the Eastern European hedgehog (Erinaceus roumanicus) during winter hibernation, Biol. Bull. (Moscow), 2019, vol. 46, no. 9, pp. 1136–1145.

    Article  Google Scholar 

  33. Sapin, M.R. and Etingen, L.E., Immunnaya sistema cheloveka (Human Immune System), Moscow: Meditsina, 1996.

  34. Schaeffer, P.J., O’Mara, M.T., Breiholz, J., Keicher, L., Lázaro, J., et al., Metabolic rate in common shrews is unaffected by temperature, leading to lower energetic costs through seasonal size reduction, R. Soc. Open Sci., 2020, vol. 7, no. 4, p. 191989. https://royalsocietypublishing.org/doi/pdf/https://doi.org/10.1098/rsos.191989. Updated May 8, 2020. 10.1098/rsos.191989

  35. Sundel, J., Church, C., and Ovaskainen, O., Spatio-temporal patterns of habitat use in voles and shrews modified by density, season and predators, J. Anim. Ecol., 2012, vol. 81, no. 4, pp. 747–755.

    Article  Google Scholar 

  36. Wang, A.Z., Husak, J.F., and Lovern, M., Leptin ameliorates the immunity, but not reproduction, trade-off with endurance in lizards, J. Comp. Physiol., B, 2019, vol. 189, no. 2, pp. 261–269. PMID: 30666396.https://doi.org/10.1007/s00360-019-01202-2

    Article  CAS  PubMed  Google Scholar 

  37. Whiting, J.R., Magalhaes, I.S., R Singkam, A.R., Robertson, S., D’Agostino, D., et al., A genetics-based approach confirms immune associations with life history across multiple populations of an aquatic vertebrate (Gasterosteus aculeatus), Mol. Ecol., 2018, vol. 27, no. 15, pp. 3174–3191. https://doi.org/10.1111/mec.14772

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Yurchinskii, V.Ya. and Erofeeva, L.M., Comparative characteristics of age-related changes in the lymphoid and fibrous connective tissue component of the thymus of vertebrates (Chordata: Vertebrata), Zh. Obshch. Biol., 2020, vol. 81, no. 1, pp. 20–30.

    Google Scholar 

Download references

Funding

This work was supported by the Russian Foundation for Basic Research, project no. 11-04-97530 r-center-a.

Author information

Authors and Affiliations

  1. Smolensk State University, 21400, Smolensk, Russia

    V. Ya. Yurchinsky

  2. Smolensk State Medical University, 214019, Smolensk, Russia

    V. Ya. Yurchinsky

Authors
  1. V. Ya. Yurchinsky
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to V. Ya. Yurchinsky.

Ethics declarations

Conflict of interest. The author declares that he has no conflicts of interest.

Statement on the welfare of animals. All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.

Additional information

Translated by T. Kuznetsova

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Yurchinsky, V.Y. Some Differences in Thymus Morphology in Immature Insectivorous Mammals: Sorex araneus, Sorex caecutiens, Neomys fodiens, and Erinaceus roumanicus. Biol Bull Russ Acad Sci 50, 1503–1510 (2023). https://doi.org/10.1134/S1062359023070312

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S1062359023070312

Keywords:

Search

Navigation