Skip to main content Accessibility help
×
Home

Life history of aggression in Anastatus disparis (Hymenoptera: Eupelmidae) with extreme male–male combat

Published online by Cambridge University Press:  17 July 2020

Peng-Cheng Liu
Affiliation:
The College of Ecology and Environment, Anhui Normal University, Anhui Province, China
De-Jun Hao
Affiliation:
The College of Forestry, Nanjing Forestry University, Jiangsu Province, China
Wei Hu
Affiliation:
The College of Ecology and Environment, Anhui Normal University, Anhui Province, China
Jian-Rong Wei
Affiliation:
The College of Life Science, Hebei University, Hebei Province, China
Jian-Jun Wang
Affiliation:
Liaoning Academy of Forestry Science, Shenyang Province, China
Corresponding
E-mail address:

Abstract

Aggressive behaviour is common in animals and typically has lifetime consequences. As younger males have higher residual reproductive value than older males and lose more from injuries than older males do, the propensity for fighting tends to increase with age in many empirical reports and species. However, fighting patterns in those empirical reports cannot confirm the hypothesis that individuals cannot readily inflict injuries on their opponents. To address this shortcoming, a parasitoid wasp species, Anastatus disparis (Hymenoptera: Eupelmidae), was used as an experimental model to explore the characteristics of aggression from a life-history perspective; this wasp exhibits extreme fighting, resulting in contestants experiencing injury and death. Results showed that the energetic costs of fighting to injury significantly shortened life and caused the loss of most mating ability. Inconsistent with general predictions, the frequency and intensity of fighting in A. disparis significantly decreased with male age. Further study results showed significantly more young males were received by and successfully mated with virgin females, and most genes related to energy metabolism were downregulated in aged males. Our study provided supporting evidence that young A. disparis males show more aggression likely because of their resource holding potential and sexual attractiveness decline with age.

Type
Research Paper
Copyright
Copyright © The Author(s), 2020. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below.

References

Abe, J, Kamimura, Y, Kondo, N and Shimada, M (2003) Extremely female biased sex ratio and lethal male-male combat in a parasitoid wasp, Melittobia australica (Eulophidae). Behavioral Ecology 14, 3439.CrossRefGoogle Scholar
Alekseyenko, OV, Chan, YB, Li, R and Kravitz, EA (2013) Single dopaminergic neurons that modulate aggression in Drosophila. Proceedings of the National Academy of Sciences of the United States of America 110, 61516156.CrossRefGoogle ScholarPubMed
Arnott, G and Elwood, RW (2009) Assessment of fighting ability in animal contests. Animal Behaviour 77, 9911004.CrossRefGoogle Scholar
Austad, SN (1983) A game theoretical interpretation of male combat in the bowl and doily spider (Frontinella Pyramitela). Animal Behaviour 31, 5973.CrossRefGoogle Scholar
Batchelor, TP, Santini, G and Briffa, M (2012) Size distribution and battles in wood ants: group resource-holding potential is the sum of the individual parts. Animal Behaviour 83, 111117.CrossRefGoogle Scholar
Baxter, CM and Dukas, R (2017) Life history of aggression: effect of age and sexual experience on male aggression towards males and females. Animal Behaviour 123, 1120.CrossRefGoogle Scholar
Briffa, M and Elwood, RW (2004) Use of energy reserves in fighting hermit crabs. Proceedings of the Royal Society of London Series B-Biology Sciences 271, 373379.CrossRefGoogle ScholarPubMed
Briffa, M and Sneddon, LU (2007) Physiological constraints on contest behaviour. Functional Ecology 21, 627637.CrossRefGoogle Scholar
Budnik, V and White, K (1987) Genetic dissection of dopamine and serotonin synthesis in the nervous system of Drosophila melanogaster. Journal of Neurogenetics 4, 309331.CrossRefGoogle ScholarPubMed
Chapin, KJ, Peixoto, PEC and Briffa, M (2019) Further mismeasures of animal contests: a new framework for assessment strategies. Behavioral Ecology 30, 11771185.CrossRefGoogle Scholar
Chapman, M and Kramer, D (1996) Guarded resources: the effect of intruder number on the tactics and success of defenders and intruders. Animal Behaviour 52, 8394.CrossRefGoogle Scholar
Charnov, EL and Stephens, DW (1988) On the evolution of host selection in solitary parasitoids. American Naturalist 132, 707722.CrossRefGoogle Scholar
Dahms, EC (1984) A review of the biology of species in the genus Melittobia (Hymenoptera: Eulophidae) with interpretations and additions using observations on Melittobia australica. Memoirs of the Queensland Museum 21, 337360.Google Scholar
Darilay, AT and Naranjo, JD (2011) A pretest for using logrank or Wilcoxon in the two-sample problem. Computational Statistics & Data Analysis 55, 24002409.CrossRefGoogle Scholar
de Almeida, RM, Ferrari, PF, Parmigiani, S and Miczek, KA (2005) Escalated aggressive behavior: Dopamine, serotonin and GABA. European Journal of Pharmacology 526, 5164.CrossRefGoogle ScholarPubMed
DeCarvalho, TN, Watson, PJ and Field, SA (2004) Costs increase as ritualized fighting progresses within and between phases in the sierra dome spider, Neriene litigiosa. Animal Behaviour 68, 473482.CrossRefGoogle Scholar
Enquist, M and Leimar, O (1983) Evolution of fighting behavior-decision rules and assessment of relative strength. Journal of Theoretical Biology 102, 387410.CrossRefGoogle Scholar
Enquist, M and Leimar, O (1987) Evolution of fighting behavior-the effect of variation in resource value. Journal of Theoretical Biology 127, 187205.CrossRefGoogle Scholar
Enquist, M and Leimar, O (1990) The evolution of fatal fighting. Animal Behaviour 39, 19.CrossRefGoogle Scholar
Ewald, PW and Carpenter, FL (1978) Territorial responses to energy manipulations in the Anna hummingbird. Oecologia 31, 277292.CrossRefGoogle ScholarPubMed
Gibbons, JD and Chakraborti, S (2003) Nonparametric Statistical Inference, 4th Edn. New York: Marcel Dekker, pp. 298307.Google Scholar
Grabherr, M, Haas, BJ, Yassour, M, Levin, JZ, Thompson, DA, Amit, I, Adiconis, X, Fan, L, Raychowdhury, R, Zeng, Q, Chen, Z, Mauceli, E, Hacohen, N, Gnirke, A, Rhind, N, Palma, FD, Birren, BW, Nusbaum, C, Lindbladtoh, K, Friedman, N and Regev, A (2011) Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nature Biotechnology 29, 644652.CrossRefGoogle ScholarPubMed
Guo, X and Dukas, R (2020) The cost of aggression in an animal without weapons. Ethology 126, 2431.CrossRefGoogle Scholar
Haley, MP (1994) Resource-holding power asymmetries, the prior residence effect, and reproductive payoffs in male northern elephant seal fights. Animal Behaviour 34, 427434.Google Scholar
Hamilton, WD (1979) Wingless and fighting males in fig wasps and other insects. In Blum, MS, Blum, NA (eds), Sexual Selection and Reproductive Competition in Insects. New York: Academic Press, pp. 167220.Google Scholar
Hardy, ICW and Briffa, M (2013) Animal Contests. Cambridge: Cambridge University Press.CrossRefGoogle Scholar
Hof, PR and Mobbs, CV (2010) Handbook of the Neuroscience of Aging. New York: Academic Press.Google Scholar
Huntingford, F and Turner, A (1987) Animal Conflict. London, UK: Chapman & Hall.CrossRefGoogle Scholar
Innocent, TM, Savage, J, West, SA and Reece, SE (2007) Lethal combat and sex ratio evolution in a parasitoid wasp. Behavioral Ecology 18, 709715.CrossRefGoogle Scholar
Jenssen, TA, Decourcy, KR and Congdon, JD (2005) Assessment in contests of male lizards (Anolis carolinensis ): how smaller males should respond when size matters? Animal Behaviour 69, 13251336.CrossRefGoogle Scholar
Kapranas, A, Maher, AMD and Griffin, CT (2016) Higher relatedness mitigates mortality in a nematode with lethal male fighting. Journal of Evolutionary Biology 29, 344351.CrossRefGoogle Scholar
Kapranas, A, Zenner, ANRL, Mangan, R and Griffin, CT (2020). Objective and subjective components of resource value in lethal fights between male entomopathogenic nematodes. Animal Behaviour 164, 149154.CrossRefGoogle Scholar
Kemp, DJ (2002) Sexual selection constrained by life history in a butterfly. Proceedings of the Royal Society of London Series B, Biological Sciences 269, 13411345.CrossRefGoogle Scholar
Kemp, DJ (2006) Ageing, reproductive value, and the evolution of lifetime fighting behaviour. Biological Journal of the Linnean Society 88, 565578.CrossRefGoogle Scholar
Komers, PE, Pelabon, C and Stenstrom, D (1997) Age at first reproduction in male fallow deer: age-specific versus dominance-specific behaviors. Behavioral Ecology 8, 456462.CrossRefGoogle Scholar
Li, B and Dewey, CN (2011) RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinformatics 12, 323.CrossRefGoogle ScholarPubMed
Li, BJ and Lou, JX (1992) Preliminary studies on Anastatus Disparis (Hymenoptera: Eupelmidae), an egg parasitoid of gypsy moth. Chinese Journal of Biological Control 8, 144.Google Scholar
Liu, PC and Hao, DJ (2019) Effect of variation in objective resource value on extreme male combat in a quasi-gregarious species, Anastatus disparis. BMC Ecology 19, 21.CrossRefGoogle Scholar
Liu, PC, Wei, JR, Wang, JJ, Liu, JX and Dong, LJ (2015) Relationship between the environmental temperatures and development of Anastatus Disparis (Ruschka)(Hymenoptera: Eupelmidae) and the sex ratio control of the offspring. Forest Pest and Disease 34, 914.Google Scholar
Liu, PC, Wei, JR, Tian, S and Hao, DJ (2017a) Male-male lethal combat in the quasi-gregarious parasitoid Anastatus Disparis (Hymenoptera: Eupelmidae). Scientific Reports 7, 11875.CrossRefGoogle Scholar
Liu, PC, Men, J, Zhao, B and Wei, JR (2017b) Fitness-related offspring sex allocation of Anastatus Disparis, a gypsy moth egg parasitoid, on different-sized host species. Entomologia Experimentalis et Applicata 163, 281286.CrossRefGoogle Scholar
Maynard Smith, J (1982) Evolution and the Theory of Games. Cambridge, UK: Cambridge University Press.CrossRefGoogle Scholar
Maynard Smith, J and Parker, G (1976) The logic of asymmetric contests. Animal Behaviour 24, 159175.CrossRefGoogle Scholar
Maynard Smith, J and Price, GR (1973) Logic of animal conflict. Nature 246, 1518.CrossRefGoogle Scholar
Mesterton-Gibbons, M, Dai, Y, Goubault, M and Hardy, IC (2017). Volatile chemical emission as a weapon of rearguard action: a game-theoretic model of contest behavior. Bulletin of Mathematical Biology 79, 24132449.CrossRefGoogle ScholarPubMed
Murray, MG (1987) The closed environment of the fig receptacle and its influence on male conflict in the old world fig wasp, Philotrypesis Pilosa. Animal Behaviour 35, 488506.CrossRefGoogle Scholar
Murray, MG and Gerrard, R (1985) Putting the challenge into resource exploitation: a model of contest competition. Journal of Theoretical Biology 115, 367389.CrossRefGoogle Scholar
Parker, GA (1974) Assessment strategy and the evolution of fighting behaviour. Journal of Theoretical Biology 47, 223243.CrossRefGoogle ScholarPubMed
Payne, RJH and Pagel, M (1997) Why do animals repeat displays? Animal Behaviour 54, 109119.CrossRefGoogle ScholarPubMed
Popova, NK (2006) From genes to aggressive behavior: the role of serotonergic system. Bioessays 28, 495503.CrossRefGoogle ScholarPubMed
Reece, SE, Innocent, TM and West, SA (2007) Lethal male-male combat in the parasitoid Melittobia acasta: are size and competitive environment important? Animal Behaviour 74, 11631169.CrossRefGoogle Scholar
Romualdi, C, Bortoluzzi, S, d'Alessi, F and Danieli, GA (2003) IDEG6: a web tool for detection of differentially expressed genes in multiple tag sampling experiments. Physiological Genomics 12, 159162.CrossRefGoogle ScholarPubMed
Sato, Y, Rühr, PT, Schmitz, H, Egas, M and Blanke, A (2016) Age-dependent male mating tactics in a spider mite-A life-history perspective. Ecology and Evolution 6, 73677374.CrossRefGoogle Scholar
Schuett, GW (1997) Body size and agnostic experience affect dominance and mating success in male copperheads. Animal Behaviour 54, 213214.CrossRefGoogle Scholar
Soma, KK, Scotti, MAL, Newman, AE, Charlier, TD and Demas, GE (2008) Novel mechanisms for neuroendocrine regulation of aggression. Frontiers in Neuroendocrinology 29, 476489.CrossRefGoogle ScholarPubMed
Thornhill, R and Alcock, J (1983) The Evolution of Insect Mating Systems. Cambridge, Massachusetts, USA: Harvard University Press.Google Scholar
West, SA, Flanagan, KE and Godfray, HCJ (1996) The relationship between parasitoid size and fitness in the field, a study of Achrysocharoides Zwoelferi (Hymenoptera: Eulophidae). Journal of Animal Ecology 65, 631639.CrossRefGoogle Scholar
Wong, DF, Wagner, HN, Dannals, RF, Links, JM, Frost, JJ, Ravert, HT, Wilson, AA, Rosenbaum, AE, Gjedde, A and Douglass, KH (1984). Effects of age on dopamine and serotonin receptors measured by positron tomography in the living human brain. Science (New York, N.Y.) 226, 13931396.CrossRefGoogle ScholarPubMed
Yamaguchi, T and Lin, D (2018) Functions of medial hypothalamic and mesolimbic dopamine circuitries in aggression. Current Opinion in Behavioral Sciences 24, 104112.CrossRefGoogle ScholarPubMed
Young, MD, Wakefield, MJ, Smyth, GK and Oshlack, A (2010) Gene ontology analysis for rna-seq: accounting for selection bias. Genome Biology 11, R14.CrossRefGoogle ScholarPubMed
Zenner, AN, O'Callaghan, KM and Griffin, CT (2014) Lethal fighting in nematodes is dependent on developmental pathway: male-male fighting in the entomopathogenic nematode Steinernema longicaudum. PLoS ONE 9, e89385.CrossRefGoogle ScholarPubMed

Full text views

Full text views reflects PDF downloads, PDFs sent to Google Drive, Dropbox and Kindle and HTML full text views.

Total number of HTML views: 6
Total number of PDF views: 37 *
View data table for this chart

* Views captured on Cambridge Core between 17th July 2020 - 21st January 2021. This data will be updated every 24 hours.

Hostname: page-component-76cb886bbf-7fh6l Total loading time: 0.382 Render date: 2021-01-21T02:33:07.618Z Query parameters: { "hasAccess": "0", "openAccess": "0", "isLogged": "0", "lang": "en" } Feature Flags: { "shouldUseShareProductTool": true, "shouldUseHypothesis": true, "isUnsiloEnabled": true, "metricsAbstractViews": false, "figures": false, "newCiteModal": false }

Send article to Kindle

To send this article to your Kindle, first ensure no-reply@cambridge.org is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about sending to your Kindle. Find out more about sending to your Kindle.

Note you can select to send to either the @free.kindle.com or @kindle.com variations. ‘@free.kindle.com’ emails are free but can only be sent to your device when it is connected to wi-fi. ‘@kindle.com’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

Find out more about the Kindle Personal Document Service.

Life history of aggression in Anastatus disparis (Hymenoptera: Eupelmidae) with extreme male–male combat
Available formats
×

Send article to Dropbox

To send this article to your Dropbox account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your <service> account. Find out more about sending content to Dropbox.

Life history of aggression in Anastatus disparis (Hymenoptera: Eupelmidae) with extreme male–male combat
Available formats
×

Send article to Google Drive

To send this article to your Google Drive account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your <service> account. Find out more about sending content to Google Drive.

Life history of aggression in Anastatus disparis (Hymenoptera: Eupelmidae) with extreme male–male combat
Available formats
×
×

Reply to: Submit a response


Your details


Conflicting interests

Do you have any conflicting interests? *