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Do males that experience weapon damage have greater reproductive potential than intact males in polygynous scenarios?

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Abstract

Males with damaged weapons often lose intraspecific contests; however, recent research suggests these males may use post-copulatory means to mitigate reduced reproduction. When intraspecific competition is absent, can weapon-damaged males produce more offspring in multi-mating scenarios relative to intact males? We examined the reproductive potential of weapon-damaged males in Narnia femorata (Hemiptera: Coreidae), a species that exhibits resource defense polygyny and is known to increase testes size when developmental weapon damage occurs. We induced weapon damage during development. Upon sexual maturation, we provided intact and weapon-damaged males with access to four unmated females successively and without any competitors. The mating partners of weapon-damaged males were more likely to have their eggs hatch. Furthermore, weapon-damaged males produced more offspring, though only with larger females. These results suggest that weapon-damaged males have enhanced fertilization outcomes, potentially minimizing reproductive costs of weapon damage.

Significance statement

Weapon damage is common in nature and can reduce pre-copulatory success. However, few studies have examined the reproductive consequences of weapon damage. We tested the hypothesis that weapon-damaged males can compensate for a pre-copulatory disadvantage through increased investment in traits that improve post-copulatory fertilization success. To examine the reproductive potential of weapon-damaged males, we provided males with four females in succession, then measured reproductive outcomes. We found that mating partners of weapon-damaged males were more likely to have their eggs hatch relative to the mating partners of intact males. Furthermore, we found that weapon-damaged males produced a larger number of offspring than intact males. This evidence reveals that weapon damage allows males to boost reproductive outcomes in non-competitive contexts.

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Our data file used for analyses is included as an electronic file in the Supplementary Material.

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References

  • Abràmoff MD, Magalhães PJ, Ram SJ (2004) Image processing with ImageJ. Biophoton Int 11:36–42

    Google Scholar 

  • Adamo SA, Robert D, Hoy RR (1995) Effects of a tachinid parasitoid, Ormia ochracea, on the behavior and reproduction of its male and female field cricket hosts (Gryllus spp). J Insect Physiol 41:269–277

    Article  CAS  Google Scholar 

  • Allen P, Miller CW (2020) The hidden cost of group living for aggregating juveniles in a sexually dimorphic species. Biol J Linn Soc 131:39–49

    Article  Google Scholar 

  • Andersson MB (1994) Sexual selection. Princeton University Press, Princeton, NJ

    Book  Google Scholar 

  • Avila FW, Sirot LK, LaFlamme BA, Rubinstein CD, Wolfner MF (2011) Insect seminal fluid proteins: identification and function. Annu Rev Entomol 56:21–40

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Benoit JB, Bose J, Bailey ST, Polak M (2020) Interactions with ectoparasitic mites induce host metabolic and immune responses in flies at the expense of reproduction-associated factors. Parasitol 147:1196–1205

    Article  CAS  Google Scholar 

  • Berzins IK, Caldwell RL (1983) The effect of injury on the agnostic behavior of the stomatopod, Gonodactylus bredini (Manning). Mar Behav Physiol 10:83–96

    Article  Google Scholar 

  • Birkhead TR, Møller AP (1998) Sperm competition and sexual selection. Academic Press, London, UK

    Google Scholar 

  • Bonduriansky R (2001) The evolution of male mate choice in insects: a synthesis of ideas and evidence. Biol Rev 76:305–339

    Article  CAS  PubMed  Google Scholar 

  • Cavender K, Ricker T, Lyon M, Shelby E, Miller CW, Moore PJ (2021) The trade-off between investment in weapons and fertility is mediated through spermatogenesis in the leaf-footed cactus bug Narnia femorata. Authorea. https://doi.org/10.22541/au.161046099.92330872/v1

  • Cirino LA (2020) Consequences of environmental heterogeneity on reproductive output in the leaf-footed cactus bug Narnia femorata (Hemiptera: Coreidae). University of Florida, Doctoral dissertation

    Google Scholar 

  • Cirino LA, Miller CW (2017) Seasonal effects on the population, morphology and reproductive behavior of Narnia femorata (Hemiptera: Coreidae). Insects 8

  • Clutton-Brock TH (1982) The functions of antlers. Behaviour 79(2-4):108–124

    Article  Google Scholar 

  • Dumser JB, Davey KG (1974) Endocrinological and other factors influencing testis development in Rhodnius prolixus. Can J Zool 52:1011–1022

    Article  CAS  PubMed  Google Scholar 

  • Economopoulos AP, Gordon HT (1971) Growth and differentiation of testes in large milkweed bug, Oncopeltus fasciatus (Dallas). J Exp Zool 177:391–405

    Article  CAS  PubMed  Google Scholar 

  • Elzinga JA, Chevasco V, Grapputo A, Mappes J (2011) Influence of male mating history on female reproductive success among monandrous Naryciinae (Lepidoptera: Psychidae). Ecol Entomol 36:170–180

    Article  Google Scholar 

  • Emberts Z, Miller CW, Kiehl D, St Mary CM (2017) Cut your losses: self-amputation of injured limbs increases survival. Behav Ecol 28:1047–1054

    Article  PubMed  PubMed Central  Google Scholar 

  • Emberts Z, St Mary C, Miller C (2016) Coreidae (Insecta: Hemiptera) limb loss and autotomy. Ann Entomol Soc Am 109:678–683

    Article  Google Scholar 

  • Emberts Z, St Mary CM, Herrington TJ, Miller CW (2018) Males missing their sexually selected weapon have decreased fighting ability and mating success in a competitive environment. Behav Ecol Sociobiol 72:81

    Article  Google Scholar 

  • Emlen D (2008) The evolution of animal weapons. Annu Rev Ecol Evol Syst 39:387–413

    Article  Google Scholar 

  • Evans JP, Garcia-Gonzalez F (2016) The total opportunity for sexual selection and the integration of pre- and post-mating episodes of sexual selection in a complex world. J Evol Biol 29:2338–2361

    Article  CAS  PubMed  Google Scholar 

  • Fry CL (2006) Juvenile hormone mediates a trade-off between primary and secondary sexual traits in stalk-eyed flies. Evol Dev 8:191–201

    Article  CAS  PubMed  Google Scholar 

  • Gillespie SR, Tudor MS, Moore AJ, Miller CW (2014) Sexual selection is influenced by both developmental and adult environments. Evolution 68:3421–3432

    Article  PubMed  Google Scholar 

  • Greenway EG, Cirino LA, Wilner D, Somjee U, Anagnostou ME, Hepple RT, Miller CW (2020) Extreme variation in testes size in an insect is linked to recent mating activity. J Evol Biol 33:142–150

    Article  PubMed  Google Scholar 

  • Hettyey A, Vagi B, Hevizi G, Torok J (2009) Changes in sperm stores, ejaculate size, fertilization success, and sexual motivation over repeated matings in the common toad, Bufo bufo (Anura: Bufonidae). Biol J Linn Soc 96:361–371

    Article  Google Scholar 

  • Hoadley L (1937) Autotomy in the brachyuran, Uca pugnax. Biol Bull 73:155–163

    Article  Google Scholar 

  • Honěk A (1993) Intraspecific variation in body size and fecundity in insects - a general relationship. Oikos 66:483–492

    Article  Google Scholar 

  • Jennings DJ, Boys RJ, Gammell MP (2017) Weapon damage is associated with contest dynamics but not mating success in fallow deer (Dama dama). Biol Lett 13(11):20170565

    Article  PubMed  PubMed Central  Google Scholar 

  • Johnson HE, Bleich VC, Krausman PR (2005) Antler breakage in tule elk, Owens Valley, California. J Wildl Manag 69:1747–1752

    Article  Google Scholar 

  • Johnson HE, Bleich VC, Krausman PR, Koprowski JL (2007) Effects of antler breakage on mating behavior in male tule elk (Cervus elaphus nannodes). Eur J Wildl Res 53:9–15

    Article  Google Scholar 

  • Jones TM (2001) A potential cost of monandry in the lekking sandfly Lutzomyia longipalpis. J Insect Behav 14:385–399

    Article  Google Scholar 

  • Joseph PN, Emberts Z, Sasson DA, Miller CW (2018) Males that drop a sexually selected weapon grow larger testes. Evolution 72:113–122

    Article  CAS  PubMed  Google Scholar 

  • Kant R, Minor MA, Trewick SA, Sandanayaka WRM (2012a) Body size and fitness relation in male and female Diaeretiella rapae. Biocontrol 57:759–766

    Article  Google Scholar 

  • Kant R, Trewick SA, Sandanayaka WRM, Godfrey AJR, Minor MA (2012b) Effects of multiple matings on reproductive fitness of male and female Diaeretiella rapae. Entomol Exp Appl 145:215–221

    Article  Google Scholar 

  • Karino K, Niiyama H, Chiba M (2005) Horn length is the determining factor in the outcomes of escalated fights among male Japanese horned beetles, Allomyrina dichotoma L. (Coleoptera: Scarabaeidae). J Insect Behav 18:805–815

    Article  Google Scholar 

  • Karns GR, Ditchkoff SS (2012) Antler breakage patterns in white-tailed deer. Proc Ann Conf Southeast Assoc Fish Wildl Agencies 66:114–119

    Google Scholar 

  • King BH (2000) Sperm depletion and mating behavior in the parasitoid wasp Spalangia cameroni (Hymenoptera: Pteromalidae). Great Lakes Entomol 33:117–127

    Google Scholar 

  • Lane S, Briffa M (2017) The price of attack: rethinking damage costs in animal contests. Anim Behav 126:23–29

    Article  Google Scholar 

  • Makatiani JK, Bruce AY, Schulthess F, Takasu K (2013) Reproductive strategies of the larval parasitoid Microplitis croceipes. Entomol Exp Appl 148:223–233

    Article  Google Scholar 

  • Mattlin RH (1978) Population biology, thermoregulation and site preference of the New Zealand fur seal, Arctocephalus forsteri (Lesson, 1828), on the Open Bay Islands, New Zealand. University of Canterbury, Doctoral dissertation

    Google Scholar 

  • Michaud JP, Bista M, Mishra G, Singh O (2013) Sexual activity diminishes male virility in two Coccinella species: consequences for female fertility and progeny development. Bull Entomol Res 103:570–577

    Article  CAS  PubMed  Google Scholar 

  • Miller CW, Fletcher RJ, Gillespie SR (2013) Conspecific and heterospecific cues override resource quality to influence offspring production. PlosOne 8:1–7

    Article  Google Scholar 

  • Miller CW, Joseph PN, Kilner RM, Emberts Z (2019) A weapons-testes trade-off in males is amplified in female traits. Proc R Soc B 286:20190906

    Article  PubMed  PubMed Central  Google Scholar 

  • Nakatsuru K, Kramer DL (1982) Is sperm cheap? Limited male fertility and female choice in the lemon tetra (Pisces, Characidae). Science 216:753–755

    Article  CAS  PubMed  Google Scholar 

  • Nolen ZJ, Allen PE, Miller CW (2017) Seasonal resource value and male size influence male aggressive interactions in the leaf footed cactus bug, Narnia femorata. Behav Process 138:1–6

    Article  Google Scholar 

  • O'Neill DJ, Cobb JS (1979) Some factors influencing the outcome of shelter competition in lobsters (Homarius americanus). Mar Behav Physiol 6:33–45

    Article  Google Scholar 

  • Parker GA, Pizzari T (2010) Sperm competition and ejaculate economics. Biol Rev 85:897–934

    PubMed  Google Scholar 

  • Proctor DS, Moore AJ, Miller CW (2012) The form of sexual selection arising from male-male competition depends on the presence of females in the social environment. J Evol Biol 25:803–812

    Article  Google Scholar 

  • R Core Team (2021) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria Retrieved from https://www.R-project.org/

    Google Scholar 

  • Rubolini D, Galeotti P, Pupin F, Sacchi R, Nardi PA, Fasola M (2007) Repeated matings and sperm depletion in the freshwater crayfish Austropotamobius italicus. Freshw Biol 52:1898–1906

    Article  Google Scholar 

  • Sasson DA, Munoz PR, Gezan SA, Miller CW (2016) Resource quality affects weapon and testis size and the ability of these traits to respond to selection in the leaf-footed cactus bug, Narnia femorata. Ecol Evol 6:2098–2108

    Article  PubMed  PubMed Central  Google Scholar 

  • Simmons LW, Emlen DJ (2006) Evolutionary trade-off between weapons and testes. Proc Natl Acad Sci U S A 103:16346–16351

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Simmons LW, Lüpold S, Fitzpatrick JL (2017) Evolutionary trade-off between secondary sexual traits and ejaculates. Trends Ecol Evol 32:964–976

    Article  PubMed  Google Scholar 

  • Siva-Jothy MT (1987) Mate securing tactics and the cost of fighting in the Japanese horned beetle, Allomyrina dichotoma L. (Scarabaeidae). J Ethol 5:165–172

    Article  Google Scholar 

  • Small J, Cotton S, Fowler K, Pomiankowski A (2009) Male eyespan and resource ownership affect contest outcome in the stalk-eyed fly, Teleopsis dalmanni. Anim Behav 78:1213–1220

    Article  Google Scholar 

  • Sneddon LU, Huntingford FA, Taylor AC (1997) Weapon size versus body size as a predictor of winning in fights between shore crabs, Carcinus maenas (L.). Behav Ecol Sociobiol 41:237–242

    Article  Google Scholar 

  • Somjee U, Miller CW, Tatarnic NJ, Simmons LW (2017) Experimental manipulation reveals a trade-off between weapons and testes. J Evol Biol 31(1):57–65

    Article  PubMed  Google Scholar 

  • Somjee U, Woods HA, Duell M, Miller CW (2018) The hidden cost of sexually selected traits: the metabolic expense of maintaining a sexually selected weapon. Proc R Soc B 285:20181685

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Suzaki Y, Katsuki M, Miyatake T, Okada Y (2015) Relationships among male sexually selected traits in the bean bug, Riptortus pedestris (Heteroptera: Alydidae). Entomol Sci 18:278–282

    Article  Google Scholar 

  • Swierk L, Tennessen JB, Langkilde T (2015) Sperm depletion may not limit male reproduction in a capital breeder. Biol J Linn Soc 116:684–690

    Article  Google Scholar 

  • Umbers KDL, Tatarnic NJ, Holwell GI, Herberstein ME (2012) Ferocious fighting between male grasshoppers. PlosOne 7:e49600

    Article  CAS  Google Scholar 

  • Vessels HK, Bundy CS, McPherson JE (2013) Life history and laboratory rearing of Narnia femorata (Hemiptera: Heteroptera: Coreidae) with descriptions of immature stages. Ann Entomol Soc Am 106:575–585

    Article  Google Scholar 

  • Weir LK, Grant JWA (2010) Courtship rate signals fertility in an externally fertilizing fish. Biol Lett 6:727–731

    Article  PubMed  PubMed Central  Google Scholar 

  • Wilner D, Greenway EV, Cirino LA, Miller CW (2020) Long-term reproductive success is predicted by sexual behavior and impaired by temporary nutritional stress during sexual maturation. Behav Process 175:104122

    Article  Google Scholar 

  • Wong BBM, Candolin U (2005) How is female mate choice affected by male competition? Biol Rev 80:559–571

    Article  PubMed  Google Scholar 

  • Wong DM, Chou LS, Shiao SF, Bain A (2018) Body size and injury severity associated with mating strategies in male Philotrypesis taida fig wasps. Taiwania 63:227–231

    Google Scholar 

  • Xue L, Noll M (2000) Drosophila female sexual behavior induced by sterile males showing copulation complementation. Proc Natl Acad Sci U S A 97(7):3272–3275

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yasuda C, Suzuki Y, Wada S (2011) Function of the major cheliped in male-male competition in the hermit crab Pagurus nigrofascia. Mar Biol 158:2327–2334

    Article  Google Scholar 

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Acknowledgements

We would like to thank undergraduate research assistants including Bryanna Sharot, Meredith Lilley, Amberlika Guruvadoo, Daniela Gomez, and Stella Fedele for their dedication and work on this project. We would also like to thank the Camp Blanding Joint Training Center for allowing us to collect on their 72,000-acre training site (Florida Army and National Guard). Thank you to the Undergraduate Scholars Program at the University of Florida for providing support to SH Lenga. Finally, we thank the entire Miller Lab of Evolutionary Ecology, Z Emberts, TM Palmer, C St. Mary, PJ Moore, C Sergi, and RL Rodríguez for providing comments on an earlier version of this manuscript.

Funding

This study was supported by the National Science Foundation (IOS-1553100) and the UF Agricultural Experiment Station, the National Institute of Food and Agriculture, and the US Department of Agriculture (HATCH under FLA-ENY-005691).

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Authors and Affiliations

  1. Entomology & Nematology Department, University of Florida, Gainesville, FL, 32611, USA

    Lauren A. Cirino, S. Haley Lenga & Christine W. Miller

  2. Department of Biological Sciences, University of Wisconsin-Milwaukee, Lapham Hall, 3209 N Maryland Ave, Milwaukee, WI, 53201, USA

    Lauren A. Cirino

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  1. Lauren A. Cirino
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  2. S. Haley Lenga
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LAC and CWM conceived, designed, and analyzed the data for the study. LAC and SHL performed the experiment and collected the data. All three authors wrote the manuscript.

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Correspondence to Lauren A. Cirino.

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Cirino, L.A., Lenga, S.H. & Miller, C.W. Do males that experience weapon damage have greater reproductive potential than intact males in polygynous scenarios?. Behav Ecol Sociobiol 75, 83 (2021). https://doi.org/10.1007/s00265-021-03019-y

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