Abstract
Structures used in intrasexual competition span a continuum, with pure weapons that are used exclusively in physical fights at one extreme and pure aggressive signals that are used exclusively to assess and threaten rivals at the other. We propose this weapon-signal continuum offers a framework for understanding the variation in allometric slopes among intra-sexually selected structures. We predict allometric slopes will become steeper as the relative importance of signaling increases, because aggressive signaling will favor the evolution of hypervariable structures that facilitate the assessment of subtle differences in body size. We provide preliminary empirical support for the continuum hypothesis using species with different types of armaments and offer suggestions for how to test the weapon-signal continuum among closely related species.

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References
Abernethy KA, White LJT, Wickings EJ (2002) Hordes of mandrills (Mandrillus sphinx): extreme group size and seasonal male presence. J Zool 258:131–137. https://doi.org/10.1017/S0952836902001267
Akre KL, Johnsen S (2014) Psychophysics and the evolution of behavior. Trends Ecol Evol 29:291–300. https://doi.org/10.1016/j.tree.2014.03.007
Alatalo RV, Hoglund J, Lundberg A (1988) Patterns of variation in tail ornament size in birds. Biol J Linn Soc 34:363–374. https://doi.org/10.1111/j.1095-8312.1988.tb01969.x
Arnott G, Elwood RW (2009) Assessment of fighting ability in animal contests. Anim Behav 77:991–1004. https://doi.org/10.1016/j.anbehav.2009.02.010
Backwell PRY, Passmore NI (1996) Time constraints and multiple choice criteria in the sampling behaviour and mate choice of the fiddler crab, Uca annulipes. Behav Ecol Sociobiol 38:407–416. https://doi.org/10.1007/s002650050258
Backwell PR, Christy JH, Passmore NI (1999) Female choice in the synchronously waving fiddler crab Uca annulipes. Ethology 105:415–421
Baker RH, Wilkinson GS (2001) Phylogenetic analysis of sexual dimorphism and eye-span allometry in stalk-eyed flies (Diopsidae). Evolution 55:1373–1385. https://doi.org/10.1111/j.0014-3820.2001.tb00659.x
Bean D, Cook JM (2001) Male mating tactics and lethal combat in the nonpollinating fig wasp Sycoscapter australis. Anim Behav 62:535–542. https://doi.org/10.1006/anbe.2001.1779
Berglund A, Bisazza A, Pilastro A (1996) Armaments and ornaments: an evolutionary explanation of traits of dual utility. Biol J Linn Soc 58:385–399
Bergman TJ, Sheehan MJ (2013) Social knowledge and signals in primates. Am J Primatol 75:683–694. https://doi.org/10.1002/ajp.22103
Bonduriansky R (2007) Sexual selection and allometry: a critical reappraisal of the evidence and ideas. Evolution 61:838–849. https://doi.org/10.1111/j.1558-5646.2007.00081.x
Briceño RD, Eberhard WG (1995) The functional morphology of male cerci and associated characters in 13 species of tropical earwigs (Dermaptera: Forficulidae, Labiidae, Carcinophoridae, Pygidicranidae). Smithsonian contributions to zoology. Smithsonian Institution Press, Washington D.C., pp 1–63
Briffa M (2008) Decisions during fights in the house cricket, Acheta domesticus: mutual or self assessment of energy, weapons and size? Anim Behav 75:1053–1062. https://doi.org/10.1016/j.anbehav.2007.08.016
Burkhardt D, de la Motte I (1987) Physiological, behavioural, and morphometric data elucidate the evolutive significance of stalked eyes in Diopsidae (Diptera). Entomol Gener 12:221–233. https://doi.org/10.1127/entom.gen/12/1987/221
Byers J, Hebets E, Podos J (2010) Female mate choice based upon male motor performance. Anim Behav 79:771–778. https://doi.org/10.1016/j.anbehav.2010.01.009
Cheverud JM (1982) Relationships among ontogenetic, static, and evolutionary allometry. Am J Phys Anthropol 59:139–149. https://doi.org/10.1002/ajpa.1330590204
Clutton-Brock TH, Albon SD, Gibson RM, Guinness FE (1979) The logical stag: adaptive aspects of fighting in red deer (Cervus elaphus L.). Anim Behav 27:211–225. https://doi.org/10.1016/0003-3472(79)90141-6
Crane J (1975) Fiddler crabs of the world: ocypodidae: genus Uca. Princeton University Press, Princeton, NJ
Danforth BN (1991) The morphology and behavior of dimorphic males in Perdita portalis (Hymenoptera: Andrenidae). Behav Ecol Sociobiol 29:235–247
Dennenmoser S, Christy JH (2013) The design of a beautiful weapon: compensation for opposing sexual selection on a trait with two functions. Evolution 67:1181–1188. https://doi.org/10.1111/evo.12018
Eberhard WG, Rodríguez RL, Huber BA et al (2018) Sexual selection and static allometry: the importance of function. Q Rev Biol 93:207–250
Emlen DJ (1997) Alternative reproductive tactics and male-dimorphism in the horned beetle Onthophagus acuminatus (Coleoptera: Scarabaeidae). Behav Ecol Sociobiol 41:335–341. https://doi.org/10.1007/s002650050393
Emlen DJ (2008) The evolution of animal weapons. Annu Rev Ecol Evol Syst 39:387–413. https://doi.org/10.1146/annurev.ecolsys.39.110707.173502
Emlen DJ (2014) Animal weapons: the evolution of battle. Henry Holt and Company, New York
Gould SJ (1966) Allometry and size in ontogeny and phylogeny. Biol Rev 41:587–638. https://doi.org/10.1111/j.1469-185X.1966.tb01624.x
Gould SJ (1973) Positive allometry of antlers in the “Irish Elk”, Megaloceros giganteus. Nature 244:375–376. https://doi.org/10.1038/244375a0
Gould SJ (1974) The origin and function of “bizarre” structures: antler size and skull size in the “Irish elk” Megaloceros giganteus. Evolution 28:191–220
Goyens J, Dirckx J, Dierick M et al (2014) Biomechanical determinants of bite force dimorphism in Cyclommatus metallifer stag beetles. J Exp Biol 217:1065–1071. https://doi.org/10.1242/jeb.091744
Goyens J, Dirckx J, Aerts P (2015) Mechanoreceptor distribution in stag beetle jaws corresponds to the material stress in fights. Arthropod Struct Dev 44:201–208. https://doi.org/10.1016/j.asd.2015.03.003
Graham ZA, Garde E, Heide-Jørgensen MP, Palaoro AV (2020) The longer the better: evidence that narwhal tusks are sexually selected. Biol Lett 16:20190950. https://doi.org/10.1098/rsbl.2019.0950
Green AJ (2000) The scaling and selection of sexually dimorphic characters: an example using the Marbled Teal. J Avian Biol 31:345–350. https://doi.org/10.1034/j.1600-048X.2000.310310.x
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. Academic Press, New York, pp 167–220
Hardy ICW, Briffa M (2013) Animal contests. Cambridge University Press, Cambridge, UK
Huxley JS (1932) Problems of relative growth. Methuen, London
Hyatt GW (1977) Field studies of size-dependent changes in waving display and other behavior in the fiddler crab, Uca pugilator (Brachyura, Ocypodidae). Mar Behav Physiol 4:283–292. https://doi.org/10.1080/10236247709386960
Hyatt GW, Salmon M (1978) Combat in the fiddler crabs Uca pugilator and U. pugnax: a quantitative analysis. Behaviour 65:182–211. https://doi.org/10.1163/156853978X00602
Jennions MD, Backwell PRY (1996) Residency and size affect fight duration and outcome in the fiddler crab Uca annulipes. Biol J Linn Soc 57:293–306. https://doi.org/10.1111/j.1095-8312.1996.tb01851.x
Kawano K (1997) Cost of evolving exaggerated mandibles in stag beetles (Coleoptera: Lucanidae). Ann Entomol Soc Am 90:453–461
Kelly CD (2005) Allometry and sexual selection of male weaponry in Wellington tree weta, Hemideina crassidens. Behav Ecol 16:145–152. https://doi.org/10.1093/beheco/arh141
Klingenberg CP, Zimmermann M (1992) Static, ontogenetic, and evolutionary allometry: a multivariate comparison in nine species of water striders. Am Nat 140:601–620. https://doi.org/10.1086/285430
Klopp EB (2012) Craniodental features in male Mandrillus may signal size and fitness: an allometric approach. Am J Phys Anthropol 147:593–603. https://doi.org/10.1002/ajpa.22017
Knell RJ (2009) On the analysis of non-linear allometries. Ecol Entomol 34:1–11. https://doi.org/10.1111/j.1365-2311.2008.01022.x
Knell RJ, Fortey RA (2005) Trilobite spines and beetle horns: sexual selection in the Palaeozoic? Biol Lett 1:196–199. https://doi.org/10.1098/rsbl.2005.0304
Knell RJ, Pomfret JC, Tomkins JL (2004) The limits of elaboration: curved allometries reveal the constraints on mandible size in stag beetles. Proc Roy Soc B 271:523–528. https://doi.org/10.1098/rspb.2003.2641
Kodric-Brown A, Sibly RM, Brown JH (2006) The allometry of ornaments and weapons. Proc Natl Acad Sci USA 103:8733–8738. https://doi.org/10.1073/pnas.0602994103
Lappin AK, Husak JF (2005) Weapon performance, not size, determines mating success and potential reproductive output in the collared lizard (Crotaphytus collaris). Am Nat 166:426–436. https://doi.org/10.1086/432564
Lemaître JF, Vanpé C, Plard F, Gaillard JM (2014) The allometry between secondary sexual traits and body size is nonlinear among cervids. Biol Lett 10:20130869. https://doi.org/10.1098/rsbl.2013.0869
Levinton JS, Allen BJ (2005) The paradox of the weakening combatant: trade-off between closing force and gripping speed in a sexually selected combat structure. Funct Ecol 19:159–165. https://doi.org/10.1111/j.0269-8463.2005.00968.x
Levinton JS, Judge ML (1993) The relationship of closing force to body size for the major claw of Uca pugnax (Decapoda: Ocypodidae). Funct Ecol 7:339–345. https://doi.org/10.2307/2390214
Loxton RG, Nicholls I (1979) The functional morphology of the praying mantis forelimb (Dictyoptera: Mantodea). Zool J Linn Soc 66:185–203. https://doi.org/10.1111/j.1096-3642.1979.tb01908.x
Maldonado H, Levin L, Pita JCB (1967) Hit distance and the predatory strike of the praying mantis. Z Vgl Physiol 56:237–257. https://doi.org/10.1007/BF00333669
McCullough EL, Simmons LW (2016) Selection on male physical performance during male–male competition and female choice. Behav Ecol 27:1288–1295. https://doi.org/10.1093/beheco/arw033
McCullough EL, Zinna RA (2013) Sensilla density corresponds to the regions of the horn most frequently used during combat in the giant rhinoceros beetle Trypoxylus dichotomus (Coleoptera: Scarabaeidae: Dynastinae). Ann Entomol Soc Am 106:518–523. https://doi.org/10.1603/AN12155
McCullough EL, Ledger KJ, O’Brien DM, Emlen DJ (2015) Variation in the allometry of exaggerated rhinoceros beetle horns. Anim Behav 109:133–140. https://doi.org/10.1016/j.anbehav.2015.08.013
McCullough EL, Miller CW, Emlen DJ (2016) Why sexually selected ornaments are not weapons. Trends Ecol Evol 31:742–751. https://doi.org/10.1016/j.tree.2016.07.004
McCullough EL, Chou C-C, Backwell PRY (2020) Cost of an elaborate trait: a trade-off between attracting females and maintaining a clean ornament. Behav Ecol 31:1218–1223. https://doi.org/10.1093/beheco/araa072
Melnycky NA, Weladji RB, Holand Ø, Nieminen M (2013) Scaling of antler size in reindeer (Rangifer tarandus): sexual dimorphism and variability in resource allocation. J Mammal 94:1371–1379. https://doi.org/10.1644/12-MAMM-A-282.1
Miller DC (1973) Growth in Uca, 1. Ontogeny of asymmetry in Uca pugilator (Bosc) (Decapoda, Ocypodidae). Crustaceana 24:119–131
Muramatsu D (2011) The function of the four types of waving display in Uca lactea: effects of audience, sand structure, and body size. Ethology 117:408–415. https://doi.org/10.1111/j.1439-0310.2011.01884.x
Muramatsu D, Koga T (2016) Fighting with an unreliable weapon: opponent choice and risk avoidance in fiddler crab contests. Behav Ecol Sociobiol 70:713–724. https://doi.org/10.1007/s00265-016-2094-2
Murray MG (1987) The closed environment of the fig receptacle and its influence on male conflict in the Old World fig wasp, Philotrypesis pilosa. Anim Behav 35:488–506. https://doi.org/10.1016/S0003-3472(87)80274-9
O’Brien DM (2019) Static scaling and the evolution of extreme canine size in a saber-toothed cat (Smilodon fatalis). Integr Comp Biol 59:1303–1311. https://doi.org/10.1093/icb/icz054
O’Brien DM, Boisseau RP (2018) Overcoming mechanical adversity in extreme hindleg weapons. PLoS ONE 13:e0206997. https://doi.org/10.1371/journal.pone.0206997
O’Brien DM, Allen CE, Van Kleeck MJ et al (2018) On the evolution of extreme structures: static scaling and the function of sexually selected signals. Anim Behav 144:95–108. https://doi.org/10.1016/j.anbehav.2018.08.005
Panhuis TM, Wilkinson GS (1999) Exaggerated male eye span influences contest outcome in stalk-eyed flies (Diopsidae). Behav Ecol Sociobiol 46:221–227. https://doi.org/10.1007/s002650050613
Parker GA (1974) Assessment strategy and the evolution of fighting behaviour. J Theor Biol 47:223–243. https://doi.org/10.1016/0022-5193(74)90111-8
Pike KN, Tomkins JL, Buzatto BA (2017) Mixed evidence for the erosion of intertactical genetic correlations through intralocus tactical conflict. J Evol Biol 30:1195–1204. https://doi.org/10.1111/jeb.13093
Plavcan JM, van Schaik CP (1992) Intrasexual competition and canine dimorphism in anthropoid primates. Am J Phys Anthropol 87:461–477. https://doi.org/10.1002/ajpa.1330870407
Pomfret JC, Knell RJ (2006) Sexual selection and horn allometry in the dung beetle Euoniticellus intermedius. Anim Behav 71:567–576. https://doi.org/10.1016/j.anbehav.2005.05.023
Pope SD (2000) Testing function of fiddler crab claw waving by manipulating social context. Behav Ecol Sociobiol 47:432–437. https://doi.org/10.1007/s002650050687
Pratt AE, McLain DK, Lathrop GR (2003) The assessment game in sand fiddler crab contests for breeding burrows. Anim Behav 65:945–955. https://doi.org/10.1006/anbe.2003.2152
Preston BT, Stevenson IR, Pemberton JM et al (2003) Overt and covert competition in a promiscuous mammal: the importance of weaponry and testes size to male reproductive success. Proc R Soc B 270:633–640. https://doi.org/10.1098/rspb.2002.2268
Radwan J (1993) The adaptive significance of male polymorphism in the acarid mite Caloglyphus berlesei. Behav Ecol Sociobiol 33:201–208. https://doi.org/10.1007/BF00216601
Radwan J (2001) Male morph determination in Rhizoglyphus echinopus (Acaridae). Exp Appl Acarol 25:143–149. https://doi.org/10.1023/A:1010688516704
Radwan J, Czyż M, Konior M, Kolodziejczyk M (2000) Aggressiveness in two male morphs of the bulb mite Rhizoglyphus robini. Ethology 106:53–62. https://doi.org/10.1046/j.1439-0310.2000.00498.x
Reaney LT, Drayton JM, Jennions MD (2011) The role of body size and fighting experience in predicting contest behaviour in the black field cricket, Teleogryllus commodus. Behav Ecol Sociobiol 65:217–225. https://doi.org/10.1007/s00265-010-1030-0
Rico-Guevara A, Hurme KJ (2019) Intrasexually selected weapons. Biol Rev 94:60–101. https://doi.org/10.1111/brv.12436
Rodríguez RL, Eberhard WG (2019) Why the static allometry of sexually-selected traits is so variable: the importance of function. Integr Comp Biol 59:1290–1302. https://doi.org/10.1093/icb/icz039
Searcy WA, Nowicki S (2005) The evolution of animal communication: reliability and deceptability in signaling systems. Princeton University Press, Princeton, New Jersey
Setchell JM, Wickings EJ (2005) Dominance, status signals and coloration in male mandrills (Mandrillus sphinx). Ethology 111:25–50. https://doi.org/10.1111/j.1439-0310.2004.01054.x
Shuker DM (2014) Sexual selection theory. In: Shuker DM, Simmons LW (eds) The evolution of insect mating systems. Oxford University Press, Oxford, pp 20–41
Simmons LW, Tomkins JL (1996) Sexual selection and the allometry of earwig forceps. Evol Ecol 10:97–104. https://doi.org/10.1007/BF01239350
Sneddon LU, Huntingford FA, Taylor AC, Orr JF (2000) Weapon strength and competitive success in the fights of shore crabs (Carcinus maenas). J Zool 250:397–403
Stewart KA, Van den Beuken TPG, Rhebergen FT et al (2018) Evidence for a third male type in a male-dimorphic model species. Ecology 99:1685–1687
Swallow JG, Wallace LE, Christianson SJ et al (2005) Genetic divergence does not predict change in ornament expression among populations of stalk-eyed flies. Mol Ecol 14:3787–3800. https://doi.org/10.1111/j.1365-294X.2005.02691.x
Tazzyman SJ, Iwasa Y, Pomiankowski A (2014) Signaling efficacy drives the evolution of larger sexual ornaments by sexual selection. Evolution 68:216–229. https://doi.org/10.1111/evo.12255
Thompson DW (1942) On growth and form. Cambridge University Press, Cambridge, UK
Tidière M, Lemaître JF, Pélabon C et al (2017) Evolutionary allometry reveals a shift in selection pressure on male horn size. J Evol Biol 30:1826–1835. https://doi.org/10.1111/jeb.13142
Tina FW, Jaroensutasinee M, Jaroensutasinee K (2016) Sex and size affecting time allocations for activities in Uca annulipes (H. Milne Edwards, 1837). Crustaceana 89:759–773
van Lieshout E, Elgar MA (2009) Armament under direct sexual selection does not exhibit positive allometry in an earwig. Behav Ecol 20:258–264. https://doi.org/10.1093/beheco/arp013
Vanpé C, Gaillard J, Kjellander P et al (2007) Antler size provides an honest signal of male phenotypic quality in roe deer. Am Nat 169:481–493. https://doi.org/10.1086/512046
Voje KL (2016) Scaling of morphological characters across trait type, sex, and environment: a meta-analysis of static allometries. Am Nat 187:89–98
Voje KL, Hansen TF (2013) Evolution of static allometries: adaptive change in allometric slopes of eye span in stalk-eyed flies. Evolution 67:453–467. https://doi.org/10.1111/j.1558-5646.2012.01777.x
Wilkinson GS, Reillo PR (1994) Female choice response to artificial selection on an exaggerated male trait in a stalk-eyed fly. Proc Roy Soc B 255:1–6. https://doi.org/10.1098/rspb.1994.0001
Yoshino K, Koga T, Oki S (2011) Chelipeds are the real weapon: cheliped size is a more effective determinant than body size in male–male competition for mates in a hermit crab. Behav Ecol Sociobiol 65:1825–1832
Zeil J, Hemmi JM (2006) The visual ecology of fiddler crabs. J Comp Physiol A 192:1–25. https://doi.org/10.1007/s00359-005-0048-7
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We thank Chrissie Painting and Emma Sherratt for the invitation to submit to this issue, and Daisuke Muramatsu, John Swallow, and Jerry Wilkinson for sharing their raw data.
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McCullough, E.L., O’Brien, D.M. Variation in allometry along the weapon-signal continuum. Evol Ecol 36, 591–604 (2022). https://doi.org/10.1007/s10682-022-10158-9
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