Abstract
Batesian mimics benefit from their phenotypic similarity to their models. An apparent paradox is the presence of many inaccurate mimics in nature. Many hypotheses have been proposed to explain their existence, including the relaxed selection hypothesis, which postulates that the level of mimetic resemblance avoided by predators is context-dependent. More specifically, predators avoid mimics of lower resemblance that imitate highly noxious models due to the high cost of mistakenly attacking such models. We tested this hypothesis using data on 93 pairs of ant-mimicking spider species and their models. We measured the mimetic resemblance in each spider to its putative model. Then, we estimated the noxiousness of ant models on the basis of their defensive arsenal (i.e. mandibles, spines, sting, and chemical defense). In support of the relaxed selection hypothesis, we found a negative correlation between model noxiousness and mimetic accuracy. The proportion of the variability in mimetic accuracy explained by model noxiousness was not high, indicating that other factors influence the evolution of mimetic accuracy. Finally, this comparative analysis provides evidence of the influence of model noxiousness on mimetic accuracy in a Batesian mimicry system.
References
Antwiki (2021) http://www.antwiki.org/Main_Page
Alcock J (1970) Punishment levels and the response of black-capped chickadees (Parus atricapillus) to three kinds of artificial seeds. Anim Behav 18:592–599
Anderson B, de Jager ML (2020) Natural selection in mimicry. Biol Rev 95:291–304
Bates HW (1862) XXXII. Contributions to an Insect Fauna of the Amazon Valley. Lepidoptera: Heliconidæ Trans Linn Soc Lond 23:495–566
Blanchard BD, Nakamura A, Cao M, Chen ST, Moreau CS (2020) Spine and dine: A key defensive trait promotes ecological success in spiny ants. Ecol Evol 10:5852–5863
Blum MS (1992) Ant venoms: chemical and pharmacological properties. J Toxicol - Toxin Rev 11:115–164
Bosselaers J, Jocqué R (2002) Studies in Corinnidae: cladistic analysis of 38 corinnid and liocranid genera, and transfer of Phrurolithinae. Zool Scripta 31:241–270
Brodie ED Jr, Howard RR (1973) Experimental study of Batesian mimicry in the salamanders Plethodon jordani and Desmognathus ochrophaeus. Am Midl Nat 90:38–46
Bulbert MW, Herberstein ME, Cassis G (2014) Assassin bug requires dangerous ant prey to bite first. Curr Biol 24:R220–R221
Carlin NF, Gladstein DS (1989) The “bouncer” defense of Odontomachus ruginodis and other odontomachine ants (Hymenoptera: Formicidae). Psyche 96:1–19
Caro T, Ruxton G (2019) Aposematism: unpacking the defences. Trends Ecol Evol 34:595–604
Caves EM, Brandley NC, Johnsen S (2018) Visual acuity and the evolution of signals. Trends Ecol Evol 33:358–372
Ceccarelli FS (2008) Behavioral mimicry in Myrmarachne species (Araneae, Salticidae) from North Queensland, Australia. J Arachnol 36:344–351
Cloudsley-Thompson JL (1995) A review of the anti-predator devices of spiders. Bull Br Arachnol Soc 10:81–89
Cushing PE (1997) Myrmecomorphy and myrmecophily in spiders: a review. Fla Entomol 80:165–193
Cushing PE (2012) Spider-ant associations: an updated review of myrmecomorphy, myrmecophily, and myrmecophagy in spiders. Psyche 2012:1–23
Cuthill IC (2014) Evolution: the mystery of imperfect mimicry. Curr Biol 24:R364–R366
Darst CR, Cummings ME (2006) Predator learning favours mimicry of a less-toxic model in poison frogs. Nature 440:208–211
Dean WRJ, Milton SJ (2018) Ants (Formicidae) as food for birds in southern Africa: opportunism or survival? Ostrich 89:1–4
de Jager ML, Anderson B (2019) When is resemblance mimicry? Funct Ecol 33:1586–1596
De Solan T, Aubier TG (2019) The evolutionary importance of cues in protective mimicry. Front Ecol Evol 7:283
Dias BC, Willemart RH (2013) The effectiveness of post-contact defenses in a prey with no pre-contact detection. Zoology 116:168–174
Dittrich W, Gilbert F, Green P, McGregor P, Grewcock D (1993) Imperfect mimicry: a pigeon’s perspective. Proc Roy Soc Lond B Biol 251:195–200
Duncan CJ, Sheppard PM (1965) Sensory discrimination and its role in the evolution of Batesian mimicry. Behaviour 24:269–282
Durkee CA, Weiss MR, Uma DB (2011) Ant mimicry lessens predation on a North American jumping spider by larger salticid spiders. Environ Entomol 40:1223–1231
Edmunds M (2000) Why are there good and poor mimics? Biol J Linn Soc 70:459–466
El-Sayed AM (2021) The Pherobase: Database of Insect Pheromones and Semichemicals. http://www.pherobase.com
Eisner T, Eisner M, Siegler M (2005) Secret weapons: defenses of insects, spiders, scorpions, and other many-legged creatures. Harvard University Press, London
Evans MA (1965) Mimicry and the Darwinian heritage. J Hist Ideas 26:211–220
Gall BG, Spivey KL, Chapman TL, Delph RJ, Brodie ED Jr, Wilson JS (2018) The indestructible insect: Velvet ants from across the United States avoid predation by representatives from all major tetrapod clades. Ecol Evol 8:5852–5862
Gajski D, Petráková L, Pekár S (2020) Ant-eating spider maintains specialist diet throughout its ontogeny. J Zool 311:155–163
Goodale MA, Sneddon I (1977) The effect of distastefulness of the model on the predation of artificial Batesian mimics. Anim Behav 25:660–665
Grafen A (1989) The phylogenetic regression. Phil Trans Roy Soc Lond Ser B Biol Sci 326:119–157
Hashimoto Y, Endo T, Yamasaki T, Hyodo F, Itioka T (2020) Constraints on the jumping and prey-capture abilities of ant-mimicking spiders (Salticidae, Salticinae, Myrmarachne). Sci Rep 10:1–11
Hirai T, Matsui M (2000) Myrmecophagy in a ranid frog Rana rugosa: specialization or weak avoidance to ant eating. Zool Sci 17:459–466
Hollis KL (2017) Ants and antlions: The impact of ecology, coevolution and learning on an insect predator-prey relationship. Behav Proc 139:4–11
Hölldobler B, Wilson EO (1990) The ants. Harvard University Press, Massachusetts
Honma A, Oku S, Nishida T (2006) Adaptive significance of death feigning posture as a specialized inducible defence against gape-limited predators. Proc Roy Soc Lond B Biol 273:1631–1636
Ito F, Taniguchi K, Billen J (2016) Defensive function of petiole spines in queens and workers of the formicine ant Polyrhachis lamellidens (Hymenoptera: Formicidae) against an ant predator, the Japanese treefrog Hyla japonica. Asian Myrmecol 8:81–86
Kikuchi DW, Pfennig DW (2013) Imperfect mimicry and the limits of natural selection. Q Rev Biol 88:297–315
Kunte K (2009) The diversity and evolution of Batesian mimicry in Papilio swallowtail butterflies. Evolution 63:2707–2716
Leclercq S, Braekman JC, Daloze D, Pasteels JM (2000) Fort Chem Organ Nat 79:115–229
Lindström L, Alatalo RV, Mappes J (1997) Imperfect Batesian mimicry — the effects of the frequency and the distastefulness of the model. Proc Roy Soc Lond B Biol 264:149–153
Lindström L, Alatalo RV, Lyytinen A, Mappes J (2004) The effect of alternative prey on the dynamics of imperfect Batesian and Müllerian mimicries. Evolution 58:1294–1302
Maddison WP (2015) A phylogenetic classification of jumping spiders (Araneae: Salticidae). J Arachnol 43:231–292
McLean DJ, Cassis G, Kikuchi DW, Giribet G, Herberstein ME (2019) Insincere flattery? Understanding the evolution of imperfect deceptive mimicry. Q Rev Biol 94:395–415
Mclver JD, Stonedahl G (1993) Myrmecomorphy: morphological and behavioral mimicry of ants. Annu Rev Entomol 38:351–377
Meyers JJ, Herrel A (2005) Prey capture kinematics of ant-eating lizards. J Exp Biol 208:113–127
Michálek O, Kuhn-Nentwig L, Pekár S (2019) High specific efficiency of venom of two prey-specialized spiders. Toxins 11:687
Nelson XJ, Jackson RR (2006) Vision-based innate aversion to ants and ant mimics. Behav Ecol 17:676–681
Nelson XJ, Jackson RR, Li D, Barrion AT, Edwards GB (2006a) Innate aversion to ants (Hymenoptera: Formicidae) and ant mimics: experimental findings from mantises (Mantodea). Biol J Linn Soc 88:23–32
Nelson XJ, Li D, Jackson RR (2006b) Out of the frying pan and into the fire: a novel trade-off for Batesian mimics. Ethology 112:270–277
Nelson XJ (2012) A predator’s perspective of the accuracy of ant mimicry in spiders. Psyche 2012:1–5
Oliveira PS, Sazima I (1984) The adaptive bases of ant-mimicry in a Neotropical aphantochilid spider (Araneae: Aphantochilidae). Biol J Linn Soc 22:145–155
Oliveira PS (1986) Ant-mimicry in some spiders from Brazil. Bull Soc Zool Fr 111:297–311
Oliveira PS (1988) Ant-mimicry in some Brazilian salticid and clubionid spiders (Araneae: Salticidae, Glubionidae). Biol J Linn Soc 33:1–15
Pagel M (1999) Inferring the historical patterns of biological evolution. Nature 401:877–884
Paradis E (2006) Analysis of Phylogenetics and Evolution with R. Springer, New York
Pekár S (2004) Predatory behavior of two European ant-eating spiders (Araneae. Zodariidae) J Arachnol 32:31–41
Pekár S (2014) Is inaccurate mimicry ancestral to accurate in myrmecomorphic spiders (Araneae)? Biol J Linn Soc 113:97–111
Pekár S (2021) Drivers of the evolution of mimetic accuracy in myrmecomorphic spiders: body size, habitat stratification and geographic zone. Glob Ecol Biogeogr (submitted)
Pekár S, Brabec M (2016) Marginal models via GLS: a convenient yet neglected tool for analysis of correlated data in behavioural sciences. Ethology 122:621–631
Pekár S, Jarab M (2011) Life-history constraints in inaccurate Batesian myrmecomorphic spiders (Araneae: Corinnidae, Gnaphosidae). Eur J Entomol 108:255–260
Pekár S, Toft S (2015) Trophic specialisation in a predatory group: the case of prey-specialised spiders (Araneae). Biol Rev 90:744–761
Pekár S, Mayntz D, Ribeiro T, Herberstein ME (2010) Specialist ant-eating spiders selectively feed on different body parts to balance nutrient intake. Anim Behav 79:1301–1306
Pekár S, Jarab M, Fromhage L, Herberstein ME (2011) Is the evolution of inaccurate mimicry a result of selection by a suite of predators? A case study using myrmecomorphic spiders. Am Nat 178:124–134
Pekár S, Petráková L, Bulbert MW, Whiting MJ, Herberstein ME (2017) The golden mimicry complex uses a wide spectrum of defence to deter a community of predators. eLife 6:e22089
Penney HD, Hassall C, Skevington JH, Abbott KR, Sherratt TN (2012) A comparative analysis of the evolution of imperfect mimicry. Nature 483:461–464
Polis GA (1979) Prey and feeding phenology of the desert sand scorpion Pamroctonus mesaensis (Scorpionidae: Vaejovidae). J Zool 188:333–346
Rasband WS (1997) ImageJ U. S. National Institutes of Health, Bethesda, Maryland, USA URL https://imagej.nih.gov/ij/ 1997-2018
R Core Team (2019) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL https://www.R-project.org/
Redford KH, Dorea JG (1984) The nutritional value of invertebrates with emphasis on ants and termites as food for mammals. J Zool 203:385–395
Redford KH (1986) Dietary specialization and variation in two mammalian myrmecophages (variation in mammalian myrmecophagy). Rev Chil de Hist Nat 59:201–208
Redford KH (1987) Ants and termites as food. In: Genoways HH (ed) Current mammalogy. Springer, Boston, pp 349–399
Reiskind J (1977) Ant-mimicry in Panamanian clubionid and salticid spiders (Araneae: Clubionidae, Salticidae). Biotropica 9:1–8
Ruxton GD, Allen WL, Sherratt TN, Speed MP (2018) Avoiding attack: the evolutionary ecology of crypsis, aposematism, and mimicry. Oxford University Press, Oxford
Savage JM, Slowinski JB (1992) The colouration of the venomous coral snakes (family Elapidae) and their mimics (families Aniliidae and Colubridae). Biol J Linn Soc 45:235–254
Segovia JM, Del-Claro K, Willemart RH (2015) Delicate fangs, smart killing: the predation strategy of the recluse spider. Anim Behav 101:169–177
Schultz TR (2000) In search of ant ancestors. PNAS 97:14028–14029
Sculfort O, de Castro EC, Kozak KM, Bak S, Elias M, Nay B, Llaurens V (2020) Variation of chemical compounds in wild Heliconiini reveals ecological factors involved in the evolution of chemical defenses in mimetic butterflies. Eco Evol 10:2677–2694
Sherratt TN (2002) The evolution of imperfect mimicry. Behav Ecol 13:821–826
Sherratt TN, Peet-Paré CA (2017) The perfection of mimicry: an information approach. Philos T Roy Soc B 372:20160340
Smith SM (1975) Innate recognition of coral snake pattern by a possible avian predator. Science 187:759–760
Smith SM (1977) Coral-snake pattern recognition and stimulus generalisation by naive great kiskadees (Aves: Tyrannidae). Nature 265:535–536
Stevens M (2007) Predator perception and the interrelation between different forms of protective coloration. Proc Roy Soc B 274:1457–1464
Twomey E, Kain M, Claeys M, Summers K, Castroviejo-Fisher S, Van Bocxlaer I (2020) Mechanisms for color convergence in a mimetic radiation of poison frogs. Am Nat 195:E132–E149
Uésugi K (1996) The adaptive significance of Batesian mimicry in the swallowtail butterfly, Papilio polytes (Insecta, Papilionidae): associative learning in a predator. Ethology 102:762–775
Wheeler WC, Coddington JA, Crowley LM, Dimitrov D, Goloboff PA, Griswold CE, Hormiga G, Prendini L, Ramírez MJ, Sierwald P, Almeida-Silva LM, Álvarez-Padilla F, Arnedo MA, Benavides LR, Benjamin SP, Bond JE, Grismado CJ, Hasan E, Hedin M, Izquierdo MA, Labarque FM, Ledford J, Lopardo L, Maddison WP, Miller JA, Piacentini LN, Platnick NI, Polotow D, Silva-Dávila D, Scharff N, Szűts T, Ubick D, Vink C, Wood HM, Zhang JX (2017) The spider tree of life: phylogeny of Araneae based on target-gene analyses from an extensive taxon sampling. Cladistics 33:574–616
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We thank two anonymous reviewers for providing valuable suggestions that improved this manuscript.
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The study was supported by grant no. 19-09323S provided by the Czech Science Foundation.
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JMGS developed the Methods, collected data, participated in data curation, wrote the original draft, and edited the manuscript. SP conceived the idea, developed the methods, conducted the statistical analysis, and edited the manuscript. Both authors approved the submission of the manuscript.
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Segovia, J.M.G., Pekár, S. Relationship between model noxiousness and mimetic accuracy in myrmecomorphic spiders. Evol Ecol 35, 657–668 (2021). https://doi.org/10.1007/s10682-021-10126-9
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DOI: https://doi.org/10.1007/s10682-021-10126-9