Specificity of the female's local cellular immune response in genital plug producing scorpion species.

Mariela A Oviedo-Diego, Camilo I Mattoni, Alfredo V Peretti
Author Information
  1. Mariela A Oviedo-Diego: Universidad Nacional de Córdoba, Facultad de Ciencias Exactas, Físicas y Naturales, Departamento de Diversidad Biológica y Ecología, Córdoba Capital, Córdoba, Argentina. ORCID
  2. Camilo I Mattoni: Universidad Nacional de Córdoba, Facultad de Ciencias Exactas, Físicas y Naturales, Departamento de Diversidad Biológica y Ecología, Córdoba Capital, Córdoba, Argentina. ORCID
  3. Alfredo V Peretti: Universidad Nacional de Córdoba, Facultad de Ciencias Exactas, Físicas y Naturales, Departamento de Diversidad Biológica y Ecología, Córdoba Capital, Córdoba, Argentina.

Abstract

Immune defense is a key feature in the life history of organisms, expensive to maintain, highly regulated by individuals and exposed to physiological and evolutionary trade-offs. In chelicerates, relatively scarce are the studies that relate postcopulatory mechanisms and immune response parameters. This work makes an approximation to the female's immunological consequences produced after the placement of a foreign body in the genitalia of three scorpions species, two species that normally receive genital plugs during mating (Urophonius brachycentrus and U. achalensis) and one that does not (Zabius fuscus). Here we performed the first morphological description of the natural plugs of the two Urophonius species. We described complex three zoned structure anchored to the female genital atrium and based on this information we placed implants in the genitalia (for eliciting the local immune response) of virgin females of the three species and measured the immune encapsulation response to this foreign body. We found a greater and heterogeneous response in different zones of the implants in the plug producing species. To corroborate the specificity of this immune response, we compared the local genital reaction with the triggered response at a systemic level by inserting implants into the female body cavity of U. brachycentrus and Zabius fuscus. We found that the systemic response did not differ between species and that only in the plug producing species the local response in the genitalia was higher than the systemic one. We also compared the total hemocyte load before and after the genital implantation to see if this parameter was compromised by the immunological challenge. We confirmed that in Urophonius species the presence of a strange body in the genitalia caused a decrease in the hemocyte load. Besides, we find correlations between the body weight and the immunological parameters, as well as between different immunological parameters with each other. Complementarily, we characterized the hemocytes of the three scorpion species for the first time. This comparative study can help to provide a wider framework of the immunological characteristics of the species, their differences and their relationship with the particular postcopulatory mechanism such as the genital plugs.

References

  1. Curr Biol. 2000 Jun 29;10(13):781-4 [PMID: 10898983]
  2. Proc Biol Sci. 2007 May 7;274(1614):1211-7 [PMID: 17311779]
  3. Mol Immunol. 2007 Jul;44(13):3338-44 [PMID: 17391764]
  4. Curr Opin Microbiol. 2002 Feb;5(1):102-10 [PMID: 11834378]
  5. Curr Biol. 2004 Feb 3;14(3):R100-2 [PMID: 14986632]
  6. Proc Biol Sci. 2003 Feb 22;270(1513):357-66 [PMID: 12639314]
  7. Theriogenology. 2008 Nov;70(8):1174-81 [PMID: 18757083]
  8. Immunol Rev. 2004 Apr;198:116-26 [PMID: 15199959]
  9. Immunol Rev. 2005 Aug;206:306-35 [PMID: 16048557]
  10. Philos Trans R Soc Lond B Biol Sci. 2013 Jan 21;368(1613):20120335 [PMID: 23339245]
  11. Naturwissenschaften. 2017 Aug;104(7-8):53 [PMID: 28620738]
  12. Heredity (Edinb). 2001 Nov;87(Pt 5):511-21 [PMID: 11869341]
  13. Nature. 2001 Nov 29;414(6863):506 [PMID: 11734840]
  14. Proc Natl Acad Sci U S A. 2000 Mar 28;97(7):3376-81 [PMID: 10725405]
  15. Zoology (Jena). 2007;110(5):398-408 [PMID: 17869076]
  16. Curr Biol. 2006 Jun 20;16(12):1206-10 [PMID: 16782011]
  17. Naturwissenschaften. 2011 Jul;98(7):605-13 [PMID: 21607653]
  18. Curr Biol. 2005 Sep 20;15(18):1690-4 [PMID: 16169493]
  19. J Morphol. 2010 Apr;271(4):383-93 [PMID: 20101728]
  20. Insect Biochem Mol Biol. 2002 Oct;32(10):1295-309 [PMID: 12225920]
  21. Mol Phylogenet Evol. 2018 May;122:37-45 [PMID: 29366829]
  22. Immunity. 2000 Nov;13(5):737-48 [PMID: 11114385]
  23. J Reprod Immunol. 2002 Oct-Nov;57(1-2):61-79 [PMID: 12385834]
  24. Dev Comp Immunol. 1983 Spring;7(2):229-39 [PMID: 6409683]
  25. BMC Biol. 2013 Apr 30;11:55 [PMID: 23631603]
  26. Annu Rev Entomol. 1995;40:31-56 [PMID: 7810989]
  27. Trends Ecol Evol. 2007 Jan;22(1):48-55 [PMID: 17028056]
  28. Curr Biol. 2015 Mar 16;25(6):790-797 [PMID: 25702579]
  29. Annu Rev Entomol. 1998;43:153-74 [PMID: 15012387]
  30. Cold Spring Harb Perspect Biol. 2014 Sep 11;6(11):a017731 [PMID: 25213095]
  31. Proc Biol Sci. 2003 Dec 7;270(1532):2475-80 [PMID: 14667338]
  32. Evolution. 2004 Nov;58(11):2478-85 [PMID: 15612291]
  33. Proc Biol Sci. 2000 Jun 22;267(1449):1171-5 [PMID: 10902682]
  34. Zoology (Jena). 2011 Oct;114(5):272-5 [PMID: 21907554]
  35. Annu Rev Entomol. 1997;42:611-43 [PMID: 9017902]
  36. Proc Biol Sci. 2010 Dec 7;277(1700):3649-57 [PMID: 20573620]
  37. Genome. 2004 Oct;47(5):900-10 [PMID: 15499404]
  38. Arthropod Struct Dev. 2010 Mar-May;39(2-3):124-42 [PMID: 20093195]
  39. Proc Biol Sci. 2001 Feb 7;268(1464):259-61 [PMID: 11217895]
  40. PLoS One. 2015 Apr 20;10(4):e0123964 [PMID: 25893243]
  41. Dev Comp Immunol. 2014 Mar;43(1):59-67 [PMID: 24183821]
  42. Annu Rev Entomol. 2011;56:21-40 [PMID: 20868282]
  43. J Insect Physiol. 2001 Apr;47(4-5):325-31 [PMID: 11166296]
  44. Trends Ecol Evol. 1996 Aug;11(8):317-21 [PMID: 21237861]
  45. J Biol Chem. 2000 Oct 27;275(43):33464-70 [PMID: 10942757]
  46. Dev Comp Immunol. 1989 Winter;13(1):17-23 [PMID: 2767305]
  47. Mol Biol Evol. 2014 Nov;31(11):2963-84 [PMID: 25107551]
  48. Integr Comp Biol. 2006 Dec;46(6):1000-15 [PMID: 21672803]
  49. Proc Natl Acad Sci U S A. 2002 Jul 23;99(15):9916-8 [PMID: 12097648]
  50. Trends Genet. 2007 Jul;23(7):342-9 [PMID: 17532525]
  51. Science. 1982 Oct 22;218(4570):384-7 [PMID: 7123238]
  52. Cell Mol Life Sci. 2004 Jun;61(12):1507-19 [PMID: 15197474]
  53. Fish Shellfish Immunol. 2014 Aug;39(2):415-22 [PMID: 24929244]
  54. Anim Behav. 1999 Oct;58(4):743-749 [PMID: 10512647]
  55. J Invertebr Pathol. 2011 Oct;108(2):126-30 [PMID: 21843526]
  56. Proc Biol Sci. 2001 Jul 22;268(1475):1449-54 [PMID: 11454287]
  57. BMC Genomics. 2011 Jun 10;12:306 [PMID: 21663664]
  58. Biochem Biophys Res Commun. 1993 Jul 15;194(1):17-22 [PMID: 8333834]
  59. Evolution. 1988 Sep;42(5):1097-1101 [PMID: 28581170]
  60. EMBO J. 1998 Aug 10;17(5):1217-27 [PMID: 9482719]
  61. Genetica. 2010 Jan;138(1):75-104 [PMID: 19705286]
  62. J Evol Biol. 2004 Mar;17(2):421-9 [PMID: 15009275]
  63. J Insect Physiol. 1974 Sep;20(9):1713-28 [PMID: 4412626]
  64. J Morphol. 1974 Sep;144(1):1-10 [PMID: 4137978]
  65. Immunol Rev. 2004 Apr;198:97-105 [PMID: 15199957]
  66. Nat Methods. 2012 Jul;9(7):671-5 [PMID: 22930834]
  67. Science. 2000 Apr 7;288(5463):146-9 [PMID: 10753120]
  68. Fish Shellfish Immunol. 2002 Jul;13(1):27-45 [PMID: 12201651]
  69. Proc Biol Sci. 2005 Jun 7;272(1568):1139-44 [PMID: 16024375]
  70. EMBO Rep. 2001 Mar;2(3):239-43 [PMID: 11266367]
  71. Zookeys. 2017 Aug 29;(694):41-70 [PMID: 29133999]
  72. Cell Tissue Res. 1994 Mar;275(3):467-79 [PMID: 8137397]
  73. Riv Malariol. 1963 Dec;42:149-76 [PMID: 14118422]
  74. Proc Natl Acad Sci U S A. 2001 Jul 3;98(14):7904-9 [PMID: 11416162]

MeSH Term

Animals
Biological Evolution
Copulation
Female
Genitalia
Immunity, Cellular
Reproduction
Scorpions
Sexual Behavior, Animal

Word Cloud

Created with Highcharts 10.0.0speciesresponsegenitalimmuneimmunologicalbodygenitaliathreelocalparametersplugsUrophoniusimplantsplugproducingsystemicpostcopulatoryfemale'sforeigntwobrachycentrusUoneZabiusfuscusfirstfemalefounddifferentcomparedhemocyteloadscorpionImmunedefensekeyfeaturelifehistoryorganismsexpensivemaintainhighlyregulatedindividualsexposedphysiologicalevolutionarytrade-offscheliceratesrelativelyscarcestudiesrelatemechanismsworkmakesapproximationconsequencesproducedplacementscorpionsnormallyreceivematingachalensisperformedmorphologicaldescriptionnaturaldescribedcomplexzonedstructureanchoredatriumbasedinformationplacedelicitingvirginfemalesmeasuredencapsulationgreaterheterogeneouszonescorroboratespecificityreactiontriggeredlevelinsertingcavitydifferhigheralsototalimplantationseeparametercompromisedchallengeconfirmedpresencestrangecauseddecreaseBesidesfindcorrelationsweightwellComplementarilycharacterizedhemocytestimecomparativestudycanhelpprovidewiderframeworkcharacteristicsdifferencesrelationshipparticularmechanismSpecificitycellular

Similar Articles

Cited By