Section: Ecology
Topic: Ecology, Population biology

Influence of mimicry on extinction risk in Aculeata: a theoretical approach

10.24072/pcjournal.342 - Peer Community Journal, Volume 3 (2023), article no. e113.

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Positive ecological interactions can play a role in community structure and species co-existence. A well-documented case of mutualistic interaction is Mullerian mimicry, the convergence of colour pattern in defended species living in sympatry. By reducing predation pressure, Mullerian mimicry may limit local extinction risks of defended species, but this positive effect can be weakened by undefended mimics (Batesian mimicry). While mimicry was well-studied in neotropical butterflies, it remains surprisingly poorly studied in wasps and bees (Hymenoptera: Aculeata). However, only females are defended in Aculeata and this female-limited defence may modulate the effect of Mullerian mimicry on extinction risks. Here, we focus on the effect of Mullerian mimicry on extinction risk in Aculeata, using a population dynamics model for two species. We show that Mullerian mimicry has a positive effect on species co-existence, but this effect depends on the sex-ratio. We found that the probability of extinction increases as the proportion of undefended males increases in the population, however co-existence still occurs if females are sufficiently abundant or noxious. Furthermore, we detected a destabilising effect of dual sex-limited mimicry (when each sex resembles a different model) on species co-existence. In a context of massive population decline caused by anthropic activities, our findings highlight the potential importance of Mullerian mimicry as an overlooked mechanism linked to extinction risk in wasp and bee species.

Published online:
DOI: 10.24072/pcjournal.342
Type: Research article
Keywords: Mullerian mimicry, mutualism, population dynamics, aculeata, sex-ratio, coexistence
Boutin, Maxime 1; Costa, Manon 2; Fontaine, Colin 3; Perrard, Adrien 1, 4; Llaurens, Violaine 5

1 Institut d’Écologie et des Sciences de l’Environnement de Paris (iEES Paris) – UMR 7618 [Sorbonne Université, CNRS, INRAE, IRD, UPEC], 4 place Jussieu, F – 75005 Paris, France
2 Institut de Mathématiques de Toulouse ; UMR5219. Université de Toulouse ; CNRS – UPS, F-31062 Toulouse Cedex 9, France
3 Centre d′Ecologie et des Sciences de la Conservation, UMR 7204 MNHN-CNRS-Sorbonne Université, Muséum national d′Histoire naturelle, F-75005 Paris, France
4 Université Paris Cité, 85 boulevard Saint-Germain, F – 75006 Paris, France
5 Institut de Systématique, Evolution, Biodiversité (ISYEB), Muséum National d'Histoire Naturelle, CNRS, Sorbonne Université, EPHE, Université des Antilles, CP50, 75005 Paris, France
License: CC-BY 4.0
Copyrights: The authors retain unrestricted copyrights and publishing rights
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Boutin, Maxime; Costa, Manon; Fontaine, Colin; Perrard, Adrien; Llaurens, Violaine. Influence of mimicry on extinction risk in Aculeata: a theoretical approach. Peer Community Journal, Volume 3 (2023), article  no. e113. doi : 10.24072/pcjournal.342. https://peercommunityjournal.org/articles/10.24072/pcjournal.342/

Peer reviewed and recommended by PCI : 10.24072/pci.ecology.100511

Conflict of interest of the recommender and peer reviewers:
The recommender in charge of the evaluation of the article and the reviewers declared that they have no conflict of interest (as defined in the code of conduct of PCI) with the authors or with the content of the article.

[1] Banks, H.; Banks, J.; Bommarco, R.; Laubmeier, A.; Myers, N.; Rundlöf, M.; Tillman, K. Modeling Bumble Bee Population Dynamics with Delay Differential Equations, Ecological Modelling, Volume 351 (2017), pp. 14-23 | DOI

[2] Bastolla, U.; Fortuna, M.; Pascual-García, A.; Ferrera, A.; Luque, B.; Bascompte, J. The Architecture of Mutualistic Networks Minimizes Competition and Increases Biodiversity, Nature, Volume 458 (2009) no. 7241, pp. 1018-1020 | DOI

[3] Bates, H. W. XXXII. Contributions to an Insect Fauna of the Amazon Valley. Lepidoptera: Heliconidae., Transactions of the Linnean Society of London, Volume 23 (1862) no. 3, pp. 495-566 | DOI

[4] Bergelson, J.; Crawley, M. Mycorrhizal Infection and Plant Species Diversity, Nature, Volume 334 (1988) no. 6179, p. 202-202 | DOI

[5] Bertness, M.; Callaway, R. Positive interactions in communities, Trends in Ecology & Evolution, Volume 9 (1994) no. 5, pp. 191-193 | DOI

[6] Bertness, M.; Leonard, G. The Role of Positive Interactions in Communities : Lessons from Intertidal Habitats, Ecology, Volume 78 (1997) no. 7, pp. 1976-1989 | DOI

[7] Biesmeijer, J. C.; Roberts, S. P. M.; Reemer, M.; Ohlemüller, R.; Edwards, M.; Peeters, T.; Schaffers, A. P.; Potts, S. G.; Kleukers, R.; Thomas, C. D.; Settele, J.; Kunin, W. E. Parallel Declines in Pollinators and Insect-Pollinated Plants in Britain and the Netherlands, Science, Volume 313 (2006) no. 5785, pp. 351-354 | DOI

[8] Boppré, M.; Vane-Wright, R.; Wickler, W. A Hypothesis to Explain Accuracy of Wasp Resemblances, Ecology and Evolution, Volume 7 (2017) no. 1, pp. 73-81 | DOI

[9] Boussens‐Dumon, G.; Llaurens, V. Sex, competition and mimicry: an eco‐evolutionary model reveals unexpected impacts of ecological interactions on the evolution of phenotypes in sympatry, Oikos, Volume 130 (2021) no. 11, pp. 2028-2039 | DOI

[10] Boutin, M. Maxime-Btn/AculeataMimicrySexratio: V.2, Zenodo (2023) | DOI

[11] Bronstein, J. L. Our Current Understanding of Mutualism, The Quarterly Review of Biology, Volume 69 (1994) no. 1, pp. 31-51 | DOI

[12] Brower, J. V. Z. Experimental Studies of Mimicry. IV. The Reactions of Starlings to Different Proportions of Models and Mimics, The American Naturalist, Volume 94 (1960) no. 877, pp. 271-282 | DOI

[13] Brower, L. Ecological chemistry, Scientific American, Volume 220 (1969) no. 2, pp. 22-29 | DOI

[14] Brower, L. P.; van Brower, J.; Corvino, J. M. Plant poisons in a terrestrial food chain., Proceedings of the National Academy of Sciences, Volume 57 (1967) no. 4, pp. 893-898 | DOI

[15] Brower, L. P.; Pough, F. H.; Meck, H. R. Theoretical Investigations Of Automimicry, I. Single Trial Learning, Proceedings of the National Academy of Sciences, Volume 66 (1970) no. 4, pp. 1059-1066 | DOI

[16] Bruno, J.; Stachowicz, J.; Bertness, M. Inclusion of Facilitation into Ecological Theory, Trends in Ecology & Evolution, Volume 18 (2003) no. 3, pp. 119-125 | DOI

[17] Cane, J. H.; Dobson, H. E. M.; Boyer, B. Timing and size of daily pollen meals eaten by adult females of a solitary bee (Nomia melanderi) (Apiformes: Halictidae), Apidologie, Volume 48 (2016) no. 1, pp. 17-30 | DOI

[18] Chazot, N.; Willmott, K.; Santacruz Endara, P.; Toporov, A.; Hill, R.; Jiggins, C.; Elias, M. Mutualistic Mimicry and Filtering by Altitude Shape the Structure of Andean Butterfly Communities, The American Naturalist, Volume 183 (2014) no. 1, pp. 26-39 | DOI

[19] Chesson, P. Mechanisms of Maintenance of Species Diversity, Annual Review of Ecology and Systematics, Volume 31 (2000) no. 1, pp. 343-366 | DOI

[20] Davis Rabosky, A.; Cox, C.; Rabosky, D.; Title, P.; Holmes, I.; Feldman, A.; McGuire, J. Coral Snakes Predict the Evolution of Mimicry across New World Snakes, Nature Communications, Volume 7 (2016) no. 1, p. 11484 | DOI

[21] Doyle, T.; Hawkes, W. L. S.; Massy, R.; Powney, G. D.; Menz, M. H. M.; Wotton, K. R. Pollination by hoverflies in the Anthropocene, Proceedings of the Royal Society B: Biological Sciences, Volume 287 (2020) no. 1927 | DOI

[22] Drossel, B.; Higgs, P.; Mckane, A. The Influence of Predator–Prey Population Dynamics on the Long-Term Evolution of Food Web Structure, Journal of Theoretical Biology, Volume 208 (2001) no. 1, pp. 91-107 | DOI

[23] Dunn, R.; Harris, N.; Colwell, R.; Koh, L.; Sodhi, N. The Sixth Mass Coextinction : Are Most Endangered Species Parasites and Mutualists?, Proceedings of the Royal Society B: Biological Sciences, Volume 276 (2009) no. 1670, pp. 3037-3045 | DOI

[24] Edgar, J. A.; Cockrum, P. A.; Frahn, J. L. Pyrrolizidine alkaloids in Danaus plexippus L. and Danaus chrysippus L., Experientia, Volume 32 (1976) no. 12, pp. 1535-1537 | DOI

[25] Elias, M.; Gompert, Z.; Jiggins, C.; Willmott, K. Mutualistic Interactions Drive Ecological Niche Convergence in a Diverse Butterfly Community, PLoS Biology, Volume 6 (2008) no. 12, p. 300 | DOI

[26] Emlen, J. Batesian Mimicry : A Preliminary Theoretical Investigation of Quantitative Aspects, The American Naturalist, Volume 102 (1968) no. 925, pp. 235-241 | DOI

[27] Evans, H. E. Studies on Neotropical Pompilidae (Hymenoptera) IV. Examples of Dual Sex-Limited Mimicry in Chirodamus, Psyche: A Journal of Entomology, Volume 75 (1968) no. 1, pp. 1-22 | DOI

[28] Franklin, A. Mullerian and Batesian Mimicry Can Influence Population and Community Dynamics, Peer Community in Ecology, Volume 100511 (2023) | DOI

[29] Gross, K. Positive interactions among competitors can produce species-rich communities, Ecology Letters, Volume 11 (2008) no. 9, pp. 929-936 | DOI

[30] Hallmann, C. A.; Sorg, M.; Jongejans, E.; Siepel, H.; Hofland, N.; Schwan, H.; Stenmans, W.; Müller, A.; Sumser, H.; Hörren, T.; Goulson, D.; de Kroon, H. More than 75 percent decline over 27 years in total flying insect biomass in protected areas, PLOS ONE, Volume 12 (2017) no. 10 | DOI

[31] Hay, M. Associational Plant Defenses and the Maintenance of Species Diversity: Turning Competitors into Accomplices, The American Naturalist, Volume 128 (1986) no. 5, pp. 617-641 | DOI

[32] Heal, J. Colour Patterns of Syrphidae. III. Sexual Dimorphism in Eristalis Arbustorum, Ecological Entomology, Volume 6 (1981) no. 2, pp. 119-127 | DOI

[33] Hines, H.; Witkowski, P.; Wilson, J.; Wakamatsu, K. Melanic Variation Underlies Aposematic Color Variation in Two Hymenopteran Mimicry Systems, PLOS ONE, Volume 12 (2017) no. 7, p. 0182135 | DOI

[34] Holling, C. S. The Functional Response of Predators to Prey Density and its Role in Mimicry and Population Regulation, Memoirs of the Entomological Society of Canada, Volume 97 (1965) no. S45, pp. 5-60 | DOI

[35] Holt, R. D. Species Coexistence, Encyclopedia of Biodiversity, Elsevier, 2013, pp. 667-678 | DOI

[36] Howarth, B.; Edmunds, M.; Gilbert, F. Does The Abundance Of Hoverfly (Syrphidae) Mimics Depend On The Numbers Of Their Hymenopteran Models?, Evolution, Volume 58 (2004) no. 2, pp. 367-375 | DOI

[37] Huheey, J. E. Studies of Warning Coloration and Mimicry. IV. A. Mathematical Model of Model‐Mimic Frequencies, Ecology, Volume 45 (1964) no. 1, pp. 185-188 | DOI

[38] Hunter, J. Matplotlib : A 2D Graphics Environment, Computing in Science & Engineering, Volume 9 (2007) no. 3, pp. 90-95 | DOI

[39] Jensen, T. S.; Nielsen, O. F. Rodents as seed dispersers in a heath-oak wood succession, Oecologia, Volume 70 (1986) no. 2, pp. 214-221 | DOI

[40] Jones, R. S.; Davis, S. C.; Speed, M. P. Defence Cheats Can Degrade Protection of Chemically Defended Prey, Ethology, Volume 119 (2012) no. 1, pp. 52-57 | DOI

[41] Joron, M.; Iwasa, Y. The Evolution of a Mullerian Mimic in a Spatially Distributed Community, Journal of Theoretical Biology, Volume 237 (2005) no. 1, pp. 87-103 | DOI

[42] Koh, L. P.; Dunn, R. R.; Sodhi, N. S.; Colwell, R. K.; Proctor, H. C.; Smith, V. S. Species Coextinctions and the Biodiversity Crisis, Science, Volume 305 (2004) no. 5690, pp. 1632-1634 | DOI

[43] Kumazawa, F.; Asami, T.; Hayashi, T.; Yoshimura, J. Population Dynamics of Batesian Mimicry under Interspecific Competition, Evolutionary Ecology Research, Volume 8 (2006) no. 4, pp. 591-604

[44] Kunte, K. The Diversity And Evolution Of Batesian Mimicry In Papilio Swallowtail Butterflies, Evolution, Volume 63 (2009) no. 10, pp. 2707-2716 | DOI

[45] Kéfi, S.; Baalen, M.; Rietkerk, M.; Loreau, M. Evolution of Local Facilitation in Arid Ecosystems, The American Naturalist, Volume 172 (2008) no. 1, pp. 1-17 | DOI

[46] Leavey, A.; Taylor, C. H.; Symonds, M. R. E.; Gilbert, F.; Reader, T. Mapping the evolution of accurate Batesian mimicry of social wasps in hoverflies, Evolution, Volume 75 (2021) no. 11, pp. 2802-2815 | DOI

[47] Lindström, L.; Alatalo, R. V.; Mappes, J. Imperfect Batesian mimicry—the effects of the frequency and the distastefulness of the model, Proceedings of the Royal Society of London. Series B: Biological Sciences, Volume 264 (1997) no. 1379, pp. 149-153 | DOI

[48] Longair, R. W. Sex Ratio Variations In Xylophilous Aculeate Hymenoptera, Evolution, Volume 35 (1981) no. 3, pp. 597-600 | DOI

[49] Mallet, J.; Joron, M. Evolution of Diversity in Warning Color and Mimicry: Polymorphisms, Shifting Balance, and Speciation, Annual Review of Ecology and Systematics, Volume 30 (1999) no. 1, pp. 201-233 | DOI

[50] McKinney, W. Data Structures for Statistical Computing in Python, Proceedings of the 9th Python in Science Conference, 2010, pp. 56-61 | DOI

[51] Moeller, D. Facilitative interactions among plants via shared pollinators, Ecology, Volume 85 (2004) no. 12, pp. 3289-3301 | DOI

[52] Mora, R.; Hanson, P. Widespread Occurrence of Black-Orange-Black Color Pattern in Hymenoptera, Journal of Insect Science, Volume 19 (2019) no. 2, p. 13 | DOI

[53] Müller, F. Ituna and Thyridia: A Remarkable Case of Mimicry in Butterflies, Transactions of the Entomological Society of London, Volume 1879 (1879), pp. 20-29

[54] Nonacs, P. Foraging in a Dynamic Mimicry Complex, The American Naturalist, Volume 126 (1985) no. 2, pp. 165-180 | DOI

[55] Pedregosa, F.; Varoquaux, G.; Gramfort, A.; Michel, V.; Thirion, B.; Grisel, O.; Blondel, M.; Prettenhofer, P.; Weiss, R.; Dubourg, V.; Vanderplas, J.; Passos, A.; Cournapeau, D.; Brucher, M.; Perrot, M.; Duchesnay, É. Scikit-Learn : Machine Learning in Python, Journal of Machine Learning Research, Volume 12 (2011) no. 85, pp. 2825-2830

[56] Pilgrim, E. M.; Pitts, J. P. A Molecular Method for Associating the Dimorphic Sexes of Velvet Ants (Hymenoptera: Mutillidae), Journal of the Kansas Entomological Society, Volume 79 (2006) no. 3, pp. 222-230 | DOI

[57] Pitts, J. P.; Sadler, E. Association and description of the male of Aplochares imitator (Smith) (Hymenoptera: Pompilidae), Zootaxa, Volume 4300 (2017) no. 1 | DOI

[58] Plowright, R. C.; Owen, R. E. The Evolutionary Significance of Bumble Bee Color Patterns: A Mimetic Interpretation, Evolution, Volume 34 (1980) no. 4 | DOI

[59] Raup, D. The Role of Extinction in Evolution, Proceedings of the National Academy of Sciences, Volume 91 (1994) no. 15, pp. 6758-6763 | DOI

[60] Rowland, H.; Ihalainen, E.; Lindström, L.; Mappes, J.; Speed, M. Co-Mimics Have a Mutualistic Relationship despite Unequal Defences, Nature, Volume 448 (2007) no. 7149, pp. 64-67 | DOI

[61] Rowland, H.; Mappes, J.; Ruxton, G.; Speed, M. Mimicry between Unequally Defended Prey Can Be Parasitic : Evidence for Quasi-Batesian Mimicry, Ecology Letters, Volume 13 (2010) no. 12, pp. 1494-1502 | DOI

[62] Schmidt, J. Venom and the Good Life in Tarantula Hawks (Hymenoptera : Pompilidae): How to Eat, Not Be Eaten, and Live Long, Journal of the Kansas Entomological Society, Volume 77 (2004) no. 4, pp. 402-413 | DOI

[63] Schneider, S. S.; Deeby, T.; Gilley, D. C.; DeGrandi-Hoffman, G. Seasonal nest usurpation of European colonies by African swarms in Arizona, USA, Insectes Sociaux, Volume 51 (2004) no. 4, pp. 359-364 | DOI

[64] Seger, J. Partial Bivoltinism May Cause Alternating Sex-Ratio Biases That Favour Eusociality, Nature, Volume 301 (1983) no. 5895, pp. 59-62 | DOI

[65] Sekimura, T.; Fujihashi, Y.; Takeuchi, Y. A Model for Population Dynamics of the Mimetic Butterfly Papilio Polytes in the Sakishima Islands, Japan, Journal of Theoretical Biology, Volume 361 (2014), pp. 133-140 | DOI

[66] Stubblefield, J.; Seger, J. Sexual Dimorphism in the Hymenoptera, The Differences between the Sexes, 1994, pp. 71-103

[67] Trivers, R. L.; Hare, H. Haploidploidy and the Evolution of the Social Insect, Science, Volume 191 (1976) no. 4224, pp. 249-263 | DOI

[68] Vane-Wright, R. The Systematics of Drusillopsis Oberthür (Satyrinae) and the Supposed Amathusiid Bigaena van Eecke (Lepidoptera : Nymphalidae), with Some Observations on Batesian Mimicry, Transactions of the Royal Entomological Society of London, Volume 123 (1971) no. 1, pp. 97-123 | DOI

[69] Virtanen, P.; Gommers, R.; Oliphant, T.; Haberland, M.; Reddy, T.; Cournapeau, D.; Burovski, E.; Peterson, P.; Weckesser, W.; Bright, J.; Walt, S.; Brett, M.; Wilson, J.; Millman, K.; Mayorov, N.; Nelson, A.; Jones, E.; Kern, R.; Larson, E.; Mulbregt, P. SciPy 1.0 : Fundamental algorithms for scientific computing in Python, Nature Methods, Volume 17 (2020) no. 3, pp. 261-272 | DOI

[70] Waldbauer, G. Mimicry of Hymenopteran Antennaeby Syrphidae, Psyche: A Journal of Entomology, Volume 77 (1970) no. 1, pp. 45-49 | DOI

[71] Waldbauer, G. P.; Sheldon, J. K. Phenological Relationships Of Some Aculeate Hymenoptera, Their Dipteran Mimics, And Insectivorous Birds, Evolution, Volume 25 (1971) no. 2, pp. 371-382 | DOI

[72] Wallace, A. Tropical Nature, and Other Essays, Macmillan and Company, 1878

[73] Waskom, M. seaborn: statistical data visualization, Journal of Open Source Software, Volume 6 (2021) no. 60 | DOI

[74] Werren, J. Labile Sex Ratios in Wasps and Bees, BioScience, Volume 37 (1987) no. 7, pp. 498-506 | DOI

[75] Willadsen, P. Aculeate Hymenopterans as Aposematic and Mimetic Models, Frontiers in Ecology and Evolution, Volume 10 (2022), p. 827319 | DOI

[76] Williams, P. The distribution of bumblebee colour patterns worldwide: possible significance for thermoregulation, crypsis, and warning mimicry, Biological Journal of the Linnean Society, Volume 92 (2007) no. 1, pp. 97-118 | DOI

[77] Wilson, J.; Jahner, J.; Forister, M.; Sheehan, E.; Williams, K.; Pitts, J. North American Velvet Ants Form One of the World's Largest Known Mullerian Mimicry Complexes, Current Biology, Volume 25 (2015) no. 16, pp. 704-706 | DOI

[78] Wilson, J.; Williams, K.; Forister, M.; Dohlen, C.; Pitts, J. Repeated Evolution in Overlapping Mimicry Rings among North American Velvet Ants, Nature Communications, Volume 3 (2012) no. 1, p. 1272 | DOI

[79] Yamauchi, A. A Population Dynamic Model of Batesian Mimicry, Researches on Population Ecology, Volume 35 (1993) no. 2, pp. 295-315 | DOI

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