Trade-offs between immunity and competitive ability in fighting ant males
Tóm tắt
Fighting disease while fighting rivals exposes males to constraints and trade-offs during male-male competition. We here tested how both the stage and intensity of infection with the fungal pathogen Metarhizium robertsii interfere with fighting success in Cardiocondyla obscurior ant males. Males of this species have evolved long lifespans during which they can gain many matings with the young queens of the colony, if successful in male-male competition. Since male fights occur inside the colony, the outcome of male-male competition can further be biased by interference of the colony’s worker force. We found that severe, but not yet mild, infection strongly impaired male fighting success. In late-stage infection, this could be attributed to worker aggression directed towards the infected rather than the healthy male and an already very high male morbidity even in the absence of fighting. Shortly after pathogen exposure, however, male mortality was particularly increased during combat. Since these males mounted a strong immune response, their reduced fighting success suggests a trade-off between immune investment and competitive ability already early in the infection. Even if the males themselves showed no difference in the number of attacks they raised against their healthy rivals across infection stages and levels, severely infected males were thus losing in male-male competition from an early stage of infection on. Males of the ant C. obscurior have a well-developed immune system that raises a strong immune response very fast after fungal exposure. This allows them to cope with mild pathogen exposures without compromising their success in male-male competition, and hence to gain multiple mating opportunities with the emerging virgin queens of the colony. Under severe infection, however, they are weak fighters and rarely survive a combat already at early infection when raising an immune response, as well as at progressed infection, when they are morbid and preferentially targeted by worker aggression. Workers thereby remove males that pose a future disease threat by biasing male-male competition. Our study thus reveals a novel social immunity mechanism how social insect workers protect the colony against disease risk.
Tài liệu tham khảo
Clutton-Brock TH, Albon SD, Gibson RM, Guinness FE. The logical stag: adaptive aspects of fighting in red deer (Cervus elaphus L). Anim Behav. 1979;27(PART 1):211–25.
Schnell AK, Smith CL, Hanlon RT, Harcourt R. Giant australian cuttlefish use mutual assessment to resolve male-male contests. Anim Behav. 2015;107:31–40.
Kemp DJ, Wiklund C. Fighting without weaponry: a review of male-male contest competition in butterflies. Behav Ecol Sociobiol. 2001;49(6):429–42.
West SA, Murray MG, Machado CA, Griffin AS, Herre EA. Testing Hamilton’s rule with competition between relatives. Nature. 2001;409(6819):510–3.
Abe J, Kamimura Y, Shimada M. Individual sex ratios and offspring emergence patterns in a parasitoid wasp, Melittobia australica (Eulophidae), with superparasitism and lethal combat among sons. Behav Ecol Sociobiol. 2005;57(4):366–73.
Heinze J, Hölldobler B, Yamauchi K. Male competition in Cardiocondyla ants. Behav Ecol Sociobiol. 1998;42(4):239–46.
Kinomura K, Yamauchi K. Fighting and mating behaviors of dimorphic males in the ant - Cardiocondyla wroughtoni. J Ethol. 1987;5(1):75–81.
Heinze J, Hölldobler B. Fighting for a harem of queens: physiology of reproduction in Cardiocondyla male ants. Proc Natl Acad Sci U S A. 1993;90(18):8412–4.
Hölldobler B, Wilson EO. The ants. Harvard University Press; 1990.
Yamauchi K, Kimura Y, Corbara B, Kinomura K, Tsuji K. Dimorphic ergatoid males and their reproductive behavior in the ponerine ant Hypoponera bondroiti. Ins Soc. 1996;43:119–30.
Hamilton WD. Wingless and fighting males in fig wasps and other insects. In: Eds Blum MS, Blum NA, editors. Sexual selection and reproductive competition in insects. New York: Academic Press; 1979. pp. 167–220.
Boomsma JJ, Baer B, Heinze J. The evolution of male traits in social insects. Annu Rev Entomol. 2005;50:395–420.
Sheldon BC, Verhulst S. Ecological immunology: costly parasite defences and trade-offs in evolutionary ecology. Trends Ecol Evol. 1996;11(8):317–21.
Schwenke RA, Lazzaro BP, Wolfner MF. Reproduction-Immunity Trade-Offs in Insects. Annu Rev Entomol. 2016;61:239–56.
Barribeau SM, Otti O. Sexual Reproduction and Immunity. eLS. 2020;1–10.
Mazur A, Booth A. Testosterone and dominance in men. Behav Brain Sci. 1998;21(3):353–97.
Eisenegger C, Haushofer J, Fehr E. The role of testosterone in social interaction. Trends Cogn Sci. 2011;15(6):263–71.
Alexander J, Stimson WH. Sex hormones and the course of parasitic infection. Parasitol Today. 1988;4(7):189–93.
Zuk M, Thornhill R, Ligon JD, Johnson K. Parasites and mate choice in red jungle fowl. Integr Comp Biol. 1990;30(2):235–44.
Hillgarth N, Wingfield JC. Testosterone and immunosuppression in vertebrates: implications for parasite-mediated sexual selection. Parasites Pathog. 1997;143–55.
Hart BL. Biological basis of the behavior of sick animals. Neurosci Biobehav Rev. 1988;12(2):123–37.
Kent S, Bluthé RM, Kelley KW, Dantzer R. Sickness behavior as a new target for drug development. Trends Pharmacol Sci. 1992;13:24–8.
Konsman JP, Parnet P, Dantzer R. Cytokine-induced sickness behavior: mechanisms and implications. Trends Neurosci. 2002;25(3):154–9.
Shakhar K, Shakhar G. Why do we feel sick when infected—can Altruism play a role? PLoS Biol. 2015;13(10).
Liu PC, Wei JR, Tian S, Hao D. Male-male lethal combat in the quasi-gregarious parasitoid Anastatus disparis (Hymenoptera: Eupelmidae). Sci Rep. 2017;7:1–8.
Clutton-Brock TH. Reproductive effort and terminal investment in iteroparous animals. Am Nat. 1984;123(2):212–29.
Loehle C. Social barriers to pathogen transmission in wild animal populations. Ecology. 1995;76(2):326–35.
Konrad M, Pull CD, Metzler S, Seif K, Naderlinger E, Grasse AV, et al. Ants avoid superinfections by performing risk-adjusted sanitary care. Proc Natl Acad Sci U S A. 2018;115(11):2782–7.
Heinze J, Cremer S, Eckl N, Schrempf A. Stealthy invaders: the biology of Cardiocondyla tramp ants. Insectes Soc. 2006;53(1):1–7.
Sunamura E, Hoshizaki S, Sakamoto H, Fujii T, Nishisue K, Suzuki S, et al. Workers select mates for queens: a possible mechanism of gene flow restriction between supercolonies of the invasive Argentine ant. Naturwissenschaften. 2011;98(5):361–8.
Helft F, Monnin T, Doums C. First evidence of inclusive sexual selection in the ant Cataglyphis cursor: worker aggressions differentially affect male access to virgin queens. Ethology. 2015;121(7):641–50.
Vidal M, Königseder F, Giehr J, Schrempf A, Lucas C, Heinze J. Worker ants promote outbreeding by transporting young queens to alien nests. Commun Biol. 2021;4(1):1–8.
Cremer S, Armitage SAO, Schmid-Hempel P. Social immunity. Curr Biol. 2007;17(16):R693–702.
Hamilton WD, Zuk M. Heritable true fitness and bright birds: a role for parasites? Science. 1982;218(4570):384–7.
Holway DA, Lach L, Suarez AV, Tsutsui ND, Case TJ. The causes and consequences of ant invasions. Annu Rev Ecol Syst. 2002;33:181–233.
Cremer S, Ugelvig LV, Drijfhout FP, Schlick-Steiner BC, Florian M, Seifert B, et al. The evolution of invasiveness in Garden Ants. PLoS ONE. 2008;3(12):e3838.
Kenis M, Auger-Rozenberg MA, Roques A, Timms L, Péré C, Cock MJW, et al. Ecological effects of invasive alien insects. Biol Invasions. 2009;11(1):21–45.
Heinze J. Life-history evolution in ants: the case of Cardiocondyla. Proc R Soc B. 2017;284(1850).
Yamauchi K, Kawase N. Pheromonal manipulation of workers by a fighting male to kill his rival males in the ant Cardiocondyla wroughtonii. Naturwissenschaften. 1992;79(6):274–6.
Cremer S, Suefuji M, Schrempf A, Heinze J. The dynamics of male-male competition in Cardiocondyla obscurior ants. BMC Ecol. 2012;12(7):11–5.
Metzler S, Heinze J, Schrempf A. Mating and longevity in ant males. Ecol Evol. 2016;6(24):8903–6.
Schrempf A, Moser A, Delabie J, Heinze J. Sperm traits differ between winged and wingless males of the ant Cardiocondyla obscurior. Integr Zool. 2016;11(6):427–32.
Boomsma JJ. Beyond promiscuity: mate-choice commitments in social breeding. Philos Trans R Soc B. 2013;368:1613.
Baer B, Krug A, Boomsma JJ, Hughes WOH. Examination of the immune responses of males and workers of the leaf-cutting ant Acromyrmex echinatior and the effect of infection. Insectes Soc. 2005;52:298–303.
Vainio L, Hakkarainen H, Rantala MJ, Sorvari J. Individual variation in immune function in the ant Formica exsecta; effects of the nest, body size and sex. Evol Ecol. 2004;18(1):75–84.
Gerloff CU, Ottmer BK, Schmid-Hempel P. Effects of inbreeding on immune response and body size in a social insect, Bombus terrestris. Func Ecol. 2003;17(5):582–9.
Angelone S, Bidochka MJ. Diversity and abundance of entomopathogenic fungi at ant colonies. J Invertebr Pathol. 2018;156:73–6.
Casillas-Pérez B, Pull CD, Naiser F, Naderlinger E, Matas J, Cremer S. Early queen infection shapes developmental dynamics and induces long-term disease protection in incipient ant colonies. Ecol Lett. 2022;25(1):89–100.
Pull CD, Hughes WOH, Brown MJF. Tolerating an infection: an indirect benefit of co-founding queen associations in the ant Lasius niger. Naturwissenschaften. 2013;100(12):1125–36.
Konrad M, Vyleta ML, Theis FJ, Stock M, Tragust S, Klatt M, et al. Social transfer of pathogenic fungus promotes active immunisation in ant colonies. PLOS Biol. 2012;10(4):e1001300.
Hughes WOH, Eilenberg J, Boomsma JJ. Trade-offs in group living: transmission and disease resistance in leaf-cutting ants. Proc R Soc B. 2002;269:1811–9.
Vestergaard S, Butt TM, Bresciani J, Gillespie AT, Eilenberg J. Light and Electron Microscopy Studies of the infection of the Western Flower Thrips Frankliniella occidentalis (Thysanoptera: Thripidae) by the Entomopathogenic Fungus Metarhizium anisopliae. J Invertebr Pathol. 1999;73(1):25–33.
Myllymäki H, Valanne S, Rämet M. The Drosophila Imd Signaling Pathway. J Immunol. 2014;192(8):3455–62.
Sheehan G, Garvey A, Croke M, Kavanagh K. Innate humoral immune defences in mammals and insects: the same, with differences? Virulence. 2018;9(1):1625–39.
Gillespie JP, Kanost MR, Trenczek T. Biological mediators of insect immunity. Annu Rev Entomol. 1997;42:611–43.
Cerenius L, Lee BL, Söderhäll K. The proPO-system: pros and cons for its role in invertebrate immunity. Trends Immunol. 2008;29(6):263–71.
Cerenius L, Söderhäll K. The prophenoloxidase-activating system in invertebrates. Immunol Rev. 2004;198:116–26.
Viljakainen L, Pamilo P. Identification and molecular characterization of defensin gene from the ant Formica aquilonia. Insect Mol Biol. 2005;14(4):335–8.
Viljakainen L, Pamilo P. Selection on an antimicrobial peptide defensin in ants. J Mol Evol. 2008;67(6):643–52.
Bajgar A, Kucerova K, Jonatova L, Tomcala A, Schneedorferova I, Okrouhlik J, et al. Extracellular adenosine mediates a systemic metabolic switch during immune response. PloS Biol. 2015;13(4):e1002135.
Schlamp F, Delbare SYN, Early AM, Wells MT, Basu S, Clark AG. Dense time-course gene expression profiling of the Drosophila melanogaster innate immune response. BMC Genomics. 2021;22(1):304.
Dolezal T, Krejcova GK, Bajgar A, Nedbalova P, Strasser P. Molecular regulations of metabolism during immune response in insects. Insect Biochem Mol Biol. 2019;109:31–42.
Clark RI, Tan SWS, Péan CB, Roostalu U, Vivancos V, Bronda K, et al. MEF2 is an in vivo Immune-Metabolic switch. Cell. 2013;155(2):435–47.
Blacklock BJ, Ryan RO. Hemolymph lipid transport. Insect Biochem Mol Biol. 1994;24(9):885–73.
Dhawan R, Gupta K, Kajla M, Kakani P, Choudhury TP, Kumar S, et al. Apolipophorin-III acts as a positive regulator of Plasmodium development in Anopheles stephensi. Front Physiol. 2017;8:1–9.
Whitten MMA, Tew IF, Lee BL, Ratcliffe NA. A novel role for an insect apolipoprotein (apolipophorin III) in β-1,3-glucan pattern recognition and cellular encapsulation reactions. J Immunol. 2004;172(4):2177–85.
Yu HZ, Wang J, Zhang SZ, Toufeeq S, Li B, Li Z, et al. Molecular characterisation of Apolipophorin-III gene in Samia cynthia ricini and its roles in response to bacterial infection. J Invertebr Pathol. 2018;159:61–70.
Gray EM, Bradley TJ. Malarial infection in Aedes aegypti: effects on feeding, fecundity and metabolic rate. Parasitology. 2006;132(Pt 2):169–7.
Otti O, Gantenbein-Ritter I, Jacot A, Brinkhof MWG. Immune response increases predation risk. Evolution. 2012;66(3):732–9.
O’Donnell S, Beshers SN. The role of male disease susceptibility in the evolution of haplodiploid insect societies. Proc R Soc B. 2004;271(1542):979–83.
Ruiz-Gonzáles MX, Brown MJ. Males vs workers: testing the assumptions of the haploid susceptibility hypothesis in bumblebees. Behav Ecol Sociobiol. 2006;60:501–9.
Stürup M, Baer B, Boomsma JJ. Short independent lives and selection for maximal sperm survival make investment in immune defences unprofitable for leaf-cutting ant males. Behav Ecol Sociobiol. 2014;68:947–55.
Ugelvig LV, Kronauer DJC, Schrempf A, Heinze J, Cremer S. Rapid anti-pathogen response in ant societies relies on high genetic diversity. Proc R Soc B. 2010;277(1695):2821–8.
Pull CD, Brown MJ, Grasse AV, Schmitt T, Wiesenhofer F, Tragust S, et al. Destructive disinfection of infected brood prevents systemic disease spread in ant colonies. eLlife. 2018;7:e32073.
Cremer S. Social immunity in insects. Curr Biol. 2019;29(11):R458–63.
Cremer S, Heinze J. Stress grows wings: environmental induction of winged dispersal males in Cardiocondyla ants. Curr Biol. 2003;13(3):219–23.
Fang W, Pei Y, Bidochka MJ. Transformation of Metarhizium anisopliae mediated by Agrobacterium tumefaciens. Can J Microbiol. 2006;52(7):623–6.
Hajek AE, St Leger RJ. Interactions between fungal pathogens and insect hosts. Annu Rev Entomol. 1994;39(1):293–322.
Liu L, Li G, Sun P, Lei C, Huang Q. Experimental verification and molecular basis of active immunization against fungal pathogens in termites. Sci Rep. 2015;5:15106.
Walker TN, Hughes WOH. Adaptive social immunity in leaf-cutting ants. Biol Lett. 2009;5(4):446–8.
Reber A, Purcell J, Buechel SD, Buri P, Chapuisat M. The expression and impact of antifungal grooming in ants. J Evol Biol. 2011;24:954–64.
Rosengaus RB, Traniello JFA, Lefebvre ML, Carlock DM. The social transmission of disease between adult male and female reproductives of the dampwood termite Zootermopsis angusticollis. Ethol Ecol Evol. 2000;12(4):419–33.
Untergasser A, Nijveen H, Rao X, Bisseling T. Primer3Plus, an enhanced web interface to Primer3. Nucleic Acids Res. 2007;35:71–4.
Sheehan G, Farrell G, Kavanagh K. Immune priming: the secret weapon of the insect world. Virulence. 2020;11(1):238–46.
Klein A, Schrader L, Gil R, Manzano-Marín A, Flórez L, Wheeler D, et al. A novel intracellular mutualistic bacterium in the invasive ant Cardiocondyla obscurior. ISME J. 2016;10:376–88.
Errbii M, Keilwagen J, Hoff KJ, Steffen R, Altmüller J, Oettler J, et al. Transposable elements and introgression introduce genetic variation in the invasive ant Cardiocondyla obscurior. Mol Ecol. 2021;30(23):6211–28.
R Core Team. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. 2020. https://www.R-project.org.
Bates D, Mächler M, Bolker BM, Walker SC. Fitting linear mixed-effects models using lme4. J Stat Softw. 2015;67(1).
Hartig F, DHARMa. Residual Diagnostics for Hierarchical Regression Models. Compr R Arch Netw. 2020;1–26.
Benjamini Y, Hochberg Y. Controlling the false Discovery rate: a practical and powerful Approach to multiple testing. J R Stat Soc Ser B. 1995;57(1):289–300.
Wickham H, Chang W, Henry L, Pedersen TL, Takahashi K, Wilke C et al. ggplot2: Create Elegant Data Visualisations Using the Grammar of Graphics. 2018.