Previous studies on arthropods showed that seasonality and parity in breeding considerably impact the direction of sex differences in immunocompetence, and it has been suggested that life span and the time window available for breeding play key roles in shaping sex-differences in immunity. One proposed mechanism behind this phenomenon is differential investment into life history traits in sexes. Here, we tested whether in a seasonally breeding semelparous arthropod sexes differ in their immunocompetence, predicting that females would show weaker immune response than males. We compared encapsulation efficiency (a well-established and widely used method for assessing immunocompetence) of freshly matured, virgin males and females of the lycosid spider Pardosa agrestis (Westring, 1861). On average, males mounted stronger immune response than females and the extent of encapsulation was positively associated with prosoma length in males, but not in females. Also, time until maturation was positively related to the extent of encapsulation in both sexes, but did not significantly affect adult prosoma length. We propose that sex-difference in encapsulation is likely shaped by combined effects of relatively higher costs of reproduction in females, narrow time window of reproductive activity, and the absence of trade-off between current and future reproduction.
This is a preview of subscription content, access via your institution.
Buy single article
Instant access to the full article PDF.
Price excludes VAT (USA)
Tax calculation will be finalised during checkout.
Ahtiainen JJ, Alatalo RV, Kortet R, Rantala MJ (2004) Sexual advertisement and immune function in an arachnid species (Lycosidae). Behav Ecol 15(4):602–606. https://doi.org/10.1093/beheco/arh062
Ahtiainen JJ, Alatalo RV, Kortet R, Rantala MJ (2005) A trade-off between sexual signalling and immune function in a natural population of the drumming wolf spider Hygrolycosa rubrofasciata. J Evol Biol 18(4):985–991. https://doi.org/10.1111/j.1420-9101.2005.00907.x
Aisenberg A, Peretti AV (2011) Sexual dimorphism in immune response, fat reserves and muscle mass in a sex role reversed spider. Zoology (Jena) 114(5):272–275. https://doi.org/10.1016/j.zool.2011.05.003
Bates D, Maechler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Soft 67(1):1–48. https://doi.org/10.18637/jss.v067.i01
Cappa F, Beani L, Cervo R, Grozinger C, Manfredini F (2015) Testing male immunocompetence in two hymenopterans with different levels of social organization:‘live hard, die young?’. Biol J Linn Soc 114(2):274–278. https://doi.org/10.1111/bij.12427
Fargallo JA, Laaksonen T, Pöyri V, Korpimäki E (2002) Inter-sexual differences in the immune response of Eurasian kestrel nestlings under food shortage. Ecol Lett 5(1):95–101. https://doi.org/10.1046/j.1461-0248.2002.00290.x
Foelix RF (2011) Biology of spiders. Oxford university press, Oxford
French SS, DeNardo DF, Moore MC (2007) Trade-offs between the reproductive and immune systems: facultative responses to resources or obligate responses to reproduction? Am Nat 170(1):79–89. https://doi.org/10.1086/518569
Gelman A (2008) Scaling regression inputs by dividing by two standard deviations. Stat Med 27(15):2865–2873. https://doi.org/10.1002/sim.3107
Hayward A, Gillooly JF (2011) The cost of sex: quantifying energetic investment in gamete production by males and females. PLoS One 6(1):e16557. https://doi.org/10.1371/journal.pone.0016557
Kelly CD (2016) Effect of nutritional stress and sex on melanotic encapsulation rate in the sexually size dimorphic Cook Strait giant weta. Can J Zool 94(11):787–792. https://doi.org/10.1139/cjz-2016-0108
Lackie AM (1980) Invertebrate immunity. Parasitology 80(2):393–412. https://doi.org/10.1017/S0031182000000846
Lin T, Zhang D, Liu X, Xiao D (2016) Parental care improves immunity in the seahorse (Hippocampus erectus). Fish Shellfish Immunol 58:554–562. https://doi.org/10.1016/j.fsi.2016.09.065
Maklakov AA, Bilde T, Lubin Y (2004) Sexual selection for increased male body size and protandry in a spider. Anim Behav 68(5):1041–1048. https://doi.org/10.1016/j.anbehav.2004.02.010
McKean KA, Nunney L (2005) Bateman's principle and immunity: phenotypically plastic reproductive strategies predict changes in immunological sex differences. Evolution 59(7):1510–1517. https://doi.org/10.1554/04-657
Niemelä PT, Dingemanse NJ, Alioravainen N, Vainikka A, Kortet R (2013) Personality pace-of-life hypothesis: testing genetic associations among personality and life history. Behav Ecol 24(4):935–941. https://doi.org/10.1093/beheco/art014
Ricklefs RE, Wikelski M (2002) The physiology/life-history nexus. TrEE 17(10):462–468. https://doi.org/10.1016/S0169-5347(02)02578-8
Schmid-Hempel P (2003) Variation in immune defence as a question of evolutionary ecology. Proc R Soc Lond B 270(1513):357–366. https://doi.org/10.1098/rspb.2002.2265
Schneider CA, Rasband WS, Eliceiri KW (2012) NIH image to ImageJ: 25 years of image analysis. Nat Methods 9(7):671–675. https://doi.org/10.1038/nmeth.2089
Schwarzenbach GA, Hosken DJ, Ward PI (2005) Sex and immunity in the yellow dung fly Scathophaga stercoraria. J Evol Biol 18(2):455–463. https://doi.org/10.1111/j.1420-9101.2004.00820.x
Söderhäll K, Cerenius L (1998) Role of the prophenoloxidase-activating system in invertebrate immunity. Curr Opin Immunol 10(1):23–28. https://doi.org/10.1016/S0952-7915(98)80026-5
Team RC (2014) R: A language and environment for statistical Computing. R Found Stat Comp, Vienna
Uetz GW, Papke R, Kilinc B (2002) Influence of feeding regime on body size, body condition and a male secondary sexual character in Schizocosa ocreata wolf spiders (Araneae, Lycosidae): condition-dependence in a visual signaling trait. J Arachnol 30(3):461–469. https://doi.org/10.1636/0161-8202(2002)030[0461:IOFROB]2.0.CO;2
Vincent CM, Gwynne DT (2014) Sex-biased immunity is driven by relative differences in reproductive investment. Proc R Soc B 281(1790):20140333. https://doi.org/10.1098/rspb.2014.0333
Zuk M, Simmons LW, Rotenberry JT, Stoehr AM (2004) Sex differences in immunity in two species of field crickets. Can J Zool 82(4):627–634. https://doi.org/10.1139/z04-032
We thank Orsolya Vincze, Melinda Babits, Ferenc Báthori and Szabolcs Ádám for helping in the presented study. We are indebted to Csongor I. Vágási and four anonymous reviewers for their valuable insights and constructive comments on the manuscript.
ZR was supported by National Talent Programme (NTP-EFÖ-P-15-0328-A) of Hungarian Human Resources Support Management. ZN was supported by the National Research, Development and Innovation Office of Hungary (NKFIH PD 121013, FK 124414). ZB was supported by NKFIH grant (no. K112527). The publication is supported by EFOP-3.6.1-16-2016-00022 project. The project is co-financed by the European Union and European Social Fund.
Communicated by: Sven Thatje
About this article
Cite this article
Rádai, Z., Németh, Z. & Barta, Z. Sex-dependent immune response in a semelparous spider. Sci Nat 105, 39 (2018). https://doi.org/10.1007/s00114-018-1568-7