Insect Colouration: A Defensive Adaptation (BIOL2306 Lecture)

Case study: Is insect colouration a defensive adaptation? Ecology & Evolution BIOL2306 Dr. Benoit Guénard  Preys and Predators Preys and predators have divergent interests...

Case study: Is insect colouration a defensive adaptation? Ecology & Evolution BIOL2306 Dr. Benoit Guénard  Preys and Predators Preys and predators have divergent interests - Prey: not being eaten by predator - Predator: eat the prey Unbalanced outcome - pressure on prey much intense than on predator Praying mantis feeding on a beetle Why? Life-dinner principle: A prey may loose its life, while the predator may loose a meal  Predator-prey coexistence Data from MacLulich 1937 Predators in nature usually remain in 'balance' with their prey and rarely drive them to extinction, but can exert a top-down control Note also the importance of bottom-up control Both population-level mechanisms From Ricklefs 2008. The Economy of Nature Predator-prey coexistence result from defensive adaptations arising from strong selective pressure on preys to improve their defences  Terms and definitions Tetraponera sp. Protective adaptations: against hostile physical & chemical factors in the environment e.g. dark colouration of this arboreal ant being an adaptation against high UVB radiations Polyrhachis sp. Defensive adaptations: against attacks by other organisms (usually predators) Defensive e.g. adaptations spines present are very on thorax diversebeing and petiole (e.g.an morphological, adaptation againstchemical, predatorsbehavioural…) (birds, reptiles) because each prey must defend itself against @ Francois Brassard a range of predators  Evolutionary implications In defensive adaptations, the agents shaping adaptations are of biological nature (living organisms) Biological factors stimulate mutual evolutionary responses in the traits of interacting populations. In contrast, protective adaptations do not trigger reciprocal effect on the environment In defensive adaptations, biological agents foster diversity of adaptations, rather than promoting similarity In contrast, protective adaptations tend to lead to Long legs in desert convergence in response to similar physical ants stresses in the environment  Evolutionary implications Coevolution: Sequence of evolutionary responses resulting directly from the interaction between the two populations (e.g. prey and its predator). Adaptations in one population (e.g. prey species) promote the evolution of adaptations in the other (e.g. predator species) – note coevolution is not specific to predator/prey interactions Coloration is an example of a trait that can evolve in prey under Chameleon selection from predators, and Katydid sometimes lead to coevolutionary interactions  The “defensive arsenal” of preys Most species are both consumers (primary/secondary) and preys Primary defences act regardless of whether predator is present or the prey is aware of it Either the predator does not distinguish the prey from its background (crypsis in cryptic insects) or the prey is detected but not recognized as edible food (mimicry in mimetic insects) Crypsis & mimicry = primary defences Biston robustum presents both visual and chemical mimicry Crypsis and mimicry can be visual, audio, thermic or chemical in function of cues used by the predator for detection  Cryptic insects Cryptic predators  The “defensive arsenal” of preys Secondary defences are used when prey is detected and identified as potential food by predator - when primary defences failed – and can take different forms: - Escape behaviour (e.g. run, flight) - Chemical release or injection (e.g. sting) - Mechanical defences (e.g. bites, kick) Bombardier beetle Wasp Stick insect  Aposematic insects Species with good secondary defences (e.g. chemical defences) and which advertise them with bright colours or patterns – colour is the primary defence: warning colouration = aposematism Aposematic: appearance that warns off enemies because it denotes something unpleasant or dangerous Predators learn to avoid them or in some cases have evolved innate aversion But, production of chemicals or their absorption from plants is energetically costly Aposematic insects: Monarch butterfly Toxic as larva (caterpillar) and adult due to secondary compounds (cardenolides) ingested and stored from milkweed (Asclepias genus) during larval stage Higher concentrations of cardenolides decrease performance in adults (e.g. decrease migration success) Danaus plexippus Aposematic insects Dasymutilla asteria Contrast of a prey's colours against a background Limacodidae Opposite of crypsis Aposematic display Dasymutilla gloriosa often associated with other sensory modality: sound, smell, tastes or texture - Harmonia axyridis Reinforce the signal  What is the evidence for survival value of crypsis? Initially, some observational data were compiled: direct observations and analysis of gut contents (for vertebrates) Controversial due to lack of standardization and lack of data on relative abundance of cryptic vs. non-cryptic insects Need for testing hypotheses about the adaptive value of insect defences. E.g. Are cryptic insects eaten less often than non-cryptic insects? Need for experiments  Industrial melanism Peppered moth: Biston betularia typica morph: only form reported by 1850 carbonaria morph reported after 1850 in areas near industries (heavy pollution) typica morph Non-polluted areas Polluted areas carbonaria morph See Brakefield 2009 book chapter  Industrial melanism Polluted Unpolluted Released of marked typica and carbonaria morphs in woods near Birmingham (polluted) carbonaria typica typica carbonaria typica Local population frequencies carbonaria Bird predation experiment in polluted & unpolluted areas (same number of individuals) Recapture frequencies Kettlewell 1955, 1956, 1973  Other experiments on crypsis Stick insect: Timema cristinae. Polyrmorphic herbivorous insect On plants, predation of grey morph is higher On the ground, predation of green morph is higher Green morph more cryptic on foliage Predation by lizard in function Grey morph more cryptic on ground of background substrate Sandoval 1994  Limitations of crypsis Need to select the proper background / habitat - Conspicuous on wrong background Constrains the insect to a sedentary life style at least during daylight / limit habitats exploitable Need for secondary defences when primary defences fail or when not efficient against particular predators (e.g. using non-visual cues)  Evolution and maintenance of aposematism https://www.nickybay.com/page/2/  Defensive benefits of aposematism Predators must learn characteristics of aposemete (i.e. association of colours with 'unpleasantness' & learn to avoid aposemete) Important for aposemetes to not be killed or injured during learning process: e.g. hard cuticule, stinger, reflex bleeding, early predator detection Complete avoidance is not necessary for aposematism to work; aposematism merely has to provide lower mortality than crypsis for the warning signal to be beneficial  Survival value of aposematism Warning signals need to be easy to detect, discriminate and memorize by the predators Survival value of aposematism may depend on predators’ ability to learn (vertebrates only?) Innate avoidance of bright colours by some vertebrates Aposematic colours increase the speed and durability of avoidance learning, elicit avoidance in naive predators, and the probability of recognition in already experienced predators  Survival value of aposematism Heliconius erato Manipulative experiment: Altering the colour pattern of the forewing Control: add black paint on the forewing without altering the red pattern. Why? Treatment Average survival of altered (black wings) Control individuals was decreased by 40% (31.7 vs. 52.4 days) Frequency of major damages observed on altered individuals much higher  Limitations of aposematism Risk of death (or injury) during the predators’ learning period defence can never be 100% effective Aposematism is more likely to evolve in species that are abundant: this reduces the per capita risk of an individual of being sacrificed to inexperienced predators It is more advantageous to be cryptic if rare (i.e. population density is low), or if predators have poor memory (or can't learn) But there are other possibilities…  Forms of Mimicry Mimicry: resemblance of one species of insect/animal (the mimic) to another (the model) so that a third species (the predator) is deceived by the similarity & confuses the two (mimic & model) Chrysomelidae Prosoplecta sp. Beetle – the model Cockroach- the mimic @ Gernot Kunz Müllerian mimicry Batesian mimicry Peckhamian mimicry for some myrmecomorph spiders Müllerian mimicry Among aposemetes with similar warning colouration (i.e. have same ‘signal’) – all species are unpalatable Can engage hundreds of species across vast regions, e.g. Velvet ants (which are wasps of the Mutillidae family) Thus each species individually does not have to be abundant to wear aposematic coloration  Batesian mimicry A palatable species -the mimic- gains a degree of protection from predators by resembling an unpalatable species - the model Non palatable species Palatable species Timmermans et al. 2014, Proc B Condylodera tricondyloides Grasshopper (mimic) Tigger Beetle Cicindelinae (model) Amazing case of a Batesian mimicry between tiger beetles (model) and a grasshopper (mimic)  Batesian mimicry in Hong Kong Butterflies Ants (model) and jumping spiders (mimics – Salticidae) Mimic (shape and behaviour) Model  Survival value of Batesian mimicry 1) Give live bumblebees to naïve toad Then give robber flies (Asilidae) to trained toad (experimental treatment) Predator Model Mimic Brower et al. 1960. The American Naturalist  Survival value of Batesian mimicry 1) Give live bumblebees to naïve toad. Then give robber flies (Asilidae) to trained toad (experimental treatment) 2) Give dead bumblebees with stinger Predator removed to naïve toad. Then give robber flies (Asilidae) to toad (control treatment) Model Mimic Brower et al. 1960. The American Naturalist  Limitations of Batesian mimicry Batesian mimics generally require the presence of the model to gain significant protection The relative abundances of models and mimics influence the mean rates of predation on these types. Experiments shown that as the ratio models/mimics increases then the attack rates on both models and mimics on encounter with predators tends to decrease The mimic species must not become too common relative to the model, then the predators will learn of their presence and tend to increase their attacks But there is a solution for the mimic to increase in abundance… Batesian mimicry promotes polymorphism Mimic species will use multiple models for mimicry – thus generating polymorphism within the same species Batesian mimics often have several morphs (= colour forms) in one sex (sometimes both sexes) within the same species mimicking different species of aposematic models Timmermans et al. 2014, Proc B So is colouration all about predator defence? Not only. Colouration is also selected by other factors - Intraspecific sexual communication (e.g. spiders) - Social interactions facilitation (e.g. wasps) - Thermoregulation - UV protection (e.g. melanism) - Parasite defence These different selection pressures can show convergent or divergent directions For some species (nocturnal/ subterranean/ troglodytic) the role of colouration can be minimal (no light to reflect colours)  References Benson W. 1972. Natural selection for Müllerian mimicry in Heliconius erato in Costa Rica. Science 176: 936 939 Brower & Glazier 1975. Localization of Heart Poisons in the Monarch Butterfly. Science 188: 19–25. Ruxton G. 2009. Non-visual crypsis: a review of the empirical evidence for camouflage to senses other than vision. Phil. Trans. R. Soc. B 364, 549–557. Ruxton G. D., W. L. Allen, T. N. Sherratt, and M. P. Speed. 2018. Avoiding attack: the evolutionary ecology of crypsis, aposematism, and mimicry, 2nd edition. Oxford University Press, 277 pages. First edition available online through the library Sandoval C. 1994. Differential visual predation on morphs of Timema cristinae (Phasmatodeae: Timemidae) and its consequences for host range. Biological Journal of the Linnean Society 52: 341–356. Wilson J. et al. 2015. North American velvet ants form one of the world’s largest known Müllerian mimicry complexes. Current Biology 25: 704–706.