CNRS UMR7205 Systematique et evolution
Batesian mimicry, morphospace occupancy, and the shaping of warning signal diversity in butterfly communities
Author(s): Le Poul, Y, Chazot, N, Elias, M, Joron, M
Mimicry as a defensive strategy is one of the most compelling example of adaptation. Mimicry communities often involve numerous species, and both mutualistic (Müllerian) and deceptive (Batesian) mimics coexist. In deceptive mimicry, palatable prey mimic unprofitable species (e.g. chemically defended prey which predators avoid) with a negative impact on avoidance learning by predators. In mutualistic mimicry, appearances of defended prey converge on a similar warning signal, thereby reinforcing it and decreasing the per-capita cost of training predators. Theoretical and experimental studies on mimicry phenotypes abound, but studies empirically testing their predictions in real mimicry communities remain scarce. Indeed, the quantitative distribution of phenotypes within and among mimicry complexes is largely unknown, and how phenotypic variations are influenced by the type of mimicry, selection intensity, and/or phylogeny remains unaddressed. We first developed a novel framework that enables for the automatic and precise quantification and comparison of colour pattern. We then used this tool on over 2000 specimens, consisting of 130 butterfly species, collected from distinct Neotropical butterfly communities in the Peruvian Amazon. We quantified the distribution of phenotypes and their structure into a number of separate mimicry optima, using a morphological space encompassing the variation and frequencies of all coexisting colours patterns. We analysed this structure to extract the ecological and phylogenetic patterns underlying the coexistence of multiple mimicry groups within a given locality. We then demonstrated the influence of deceptive vs. mutualistic mimics on phenotypic variability around a mimicry optimum in order to address the effective impact of deception on mimicry.
Centre for Ecology and Conservation
Brood parasites and mimicry: a sensory ecology approach
Author(s): Stevens, M
Cuckoos and other brood parasites are cheats – they lay their eggs in the nests of other birds, leaving all parental care to the hosts. A striking outcome of coevolution in many systems is egg and chick mimicry by parasites to deceive host parents into accepting young that they would otherwise reject. To understand interactions between host and parasite requires investigating the use of sensory information by both parties. I will discuss work my collaborators and I have done to understand several parasitic systems by considering the visual system of the receiver and the use of sensory information in decision-making (e.g. egg/chick rejection). I will show how mimicry of host eggs by parasites can be highly refined in terms of bird vision, and in turn how hosts use the most reliable information to discriminate between and identify their own and foreign eggs. I will then discuss how coevolution can drive different host species down alternative lines of defence, such as egg polymorphism, highly refined rejection behaviour, or chick rejection. Furthermore, I will discuss long-term data indicating how interactions between host and parasite can lead to rapid changes in egg phenotype over short timescales, and the nature of this change. Finally, I will discuss how parasites can exploit limitations in host sensory and cognitive systems to defeat host defences.
Department of Animal Ecology and Tropical Biology
Consequences of an arms race on the cuticular hydrocarbon profiles of an insect host and its three brood parasites
Author(s): Schmitt, T, Wurdack, M, Kroiss, J, Strohm, E, Niehuis, O
Parasites and their hosts have conflicting interests – to either successfully exploit the host or to defend against the parasite attack. This situation sets the board for an evolutionary arms race between both species. The species pair then follows a trajectory through repeated cycles of fine tuning of the parasite’s attack strategies and evasive actions of the host. As a special case, brood parasites need to avoid detection by the host in order to neither be attacked while in the nest nor risk the nest to be abandoned by the host afterwards. Insect brood parasites may avoid olfactory detection by mimicking the host’s cuticular hydrocarbon (CHC) profile. In this case, the arms race would lead to optimized chemical mimicry in the parasite. The host could e.g. change the CHC composition in order to escape a mimetic match. The most straightforward parasitic associations consist of one parasite and one host. More complex variations are possible but very rare: one parasite may use several hosts or several parasites may specialize in one single host. In this study, a solitary host and its three host-specific brood parasites serve as a model of such a multi enemy / single target system. We compare the CHC profiles and predict that a brood parasite whose intrusion is detectable by the host should develop chemical mimicry. The host in return should establish counterstrategies. Competition between parasites may fuel the perfection of mimicry or the development of completely new intrusion strategies. We find two chemotypes of the host that differ greatly in their CHC composition. Evolving a second CHC profile might be the outcome of escaping a parasite’s mimicry. However, a second parasite species has evolved a close match of their CHC composition compared to the alternative chemotype. The third parasite produces its very own CHC bouquet – it has developed a new strategy for invading host nests and can no longer be fended off by the host.
Department of Zoology
Flexible deceptive tactics of the fork-tailed drongo
Author(s): Flower, TP
Animals commonly deceive each other, but just as in Aesop’s fable ‘The boy who cried wolf’, deceptive signals cease to work when they are made too often. However, deceptive species might evade this frequency constraint by tactically varying their deceptive signal, thus maintaining their deception racket. My research investigates the behaviour of a South African bird, the Fork-tailed Drongo (Dicrurus adsimilis), which uses deceptive false alarm calls, including the mimicked alarms of other species, to scare host species and steal their food. Using a combination of observations and experiments undertaken on a wild population of individually recognisable drongos habituated to close observation, I show the benefits drongos gain from employing vocal mimicry to vary their false alarm calls. Drongos most frequently mimicked the alarm calls of a host species when using false alarms to steal food from that specific host. Furthermore, an experiment demonstrated that these mimetic alarm calls were more likely to deceive a host than the drongos own alarm calls. A second experiment showed that hosts reduced their response when the same false alarm call type was repeated, but increased their response again when the call type was changed. In natural conditions, drongos were more likely to change the type of alarm call they made when a previous false alarm call was unsuccessful and evidence indicates that this increased the likelihood drongos stole food. By tactically varying a deceptive signal, drongos exploit signals in the environment more likely to deceive a host, and potentially evade the frequency dependent constraints which typically restrict the pay-offs from deception. Results highlight that in communication systems, feedback from a receiver’s previous response provides valuable information to signallers. Furthermore, they raise questions regarding the mechanisms that enable animals to produce apparently sophisticated communication behaviour.
Department of Biological and Environmental Science
Is variation in chemical defence parasitism on a public good?
Author(s): Mappes, J
An individual's chemical defences (toxins) contribute to a ‘common good’ by educating predators about the distastefulness of the population, hence deterring future attacks on the toxic individuals themselves and other individuals of similar appearance. Defensive chemicals are found in both simple and complex organisms including bacteria, fungi, animals and plants. Variation in defensive chemicals both within and among prey populations has been reported repeatedly in chemical ecology literature but it has received far too little attention from evolutionary ecologists. If some individuals lack defences (‘automimics’) they may exploit the common protection profiting from reduced attack rates but paying no individual cost of toxicity themselves. I will discuss whether variation in chemical defence and automimicry are examples of “environmental noise” or whether we need to seek evolutionary explanations for them. I will also discuss examples where understanding the dynamics of deception (e.g. Batesian mimicry) may have important consequences for successful conservation management.
Department of Biology
Reproductive competition between polygynous parasite queens in ant colonies
Author(s): Larsen, J, Stürup, M, Schiøtt, M, Nash, DR
One of the most remarkable and complex parasitic interactions is social parasitism, where a parasite exploits a complete societies, rather than an individual organism. By integrating into a society the parasite gains protection against predators and diseases, and can redirect resources from the host to increase its own fitness. Among the most specialized social parasites are the inquilines that exploit social insect colonies. Inquilines are usually close relatives of their host and so share ancestral characteristics (Emery’s rule). They are dependent on being fully integrated into their host’s colony throughout their lives in order to reproduce. Most inquiline ants have completely lost their sterile worker caste. An exception to this is Acromyrmex insinuator, a parasite of the fungus-growing ant Acromyrmex echinatior. Studies have shown that a threshold proportion of parasite workers in the colony are essential for parasite reproduction. Multiple invasions of parasite queens into host colonies suggest that each parasite queen may need to produce fewer parasite workers and that the reproductive phase can be achieved more quickly. Polygyny among parasite queens is expected to select for intraspecific hyperparasitism, where some queens might cheat by only producing sexual offspring, effectively parasitizing the worker force produced by other queens. We investigated hyperparasitism in A. insinuator by genotyping parasite offspring, workers and alates in polygynous nests to investigate any bias in the production of reproductive castes relative to workers. Hyperparasitism may provide a pathway towards speciation, and can shed light on the evolution of social parasites.
Retaliatory parasites make an offer a host should not refuse
Author(s): Abou Chakra, M, Hilbe, C, Traulsen, A
Mafia like behavior occurs not only in humans, but is also observed in animals. For example, experimental evidence suggests that avian hosts tend to accept a certain degree of parasitism in order to avoid retaliating punishment from the brood parasite. Herein, we model the interaction between hosts and parasites to understand under which conditions it will be beneficial for the host to accept parasitism. In our model, the host's behavior is plastic, and thus, its response depends on the previous interactions with the parasite. We find that such learned behavior in turn is crucial for the evolution of retaliating parasites. The abundance of this kind of mafia behavior oscillates in time and does not settle to an equilibrium. Our results suggest that retaliation is a mechanism for the parasite to evade specialization and to induce acceptance by the host.
Institute for Biodiversity and Ecosystem Dynamics
Sneaking behaviour in young males: alternative male mating phenotypes in the two-spotted spider mite
Author(s): Sato, Y, Sabelis, MW, Egas, M
Sneaking behaviour as a strategy to compete for females has been observed in many taxa from insects to mammals. Often, the less competitive males who would lose contests over females against stronger males, display sneaking behavior in that they deceive their rivals by pretending to be female. To understand the evolution of observed sneaking behaviour, it is important to elucidate the mechanisms maintaining alternative mating strategies. Recently, we found three male mating phenotypes in a population of the two-spotted spider mite: territorial, sneaking and opportunistic. Opportunistic males wander around in search of females that are about to moult into the adult phase (teleiochrysalis). Territorial males spend much time in a mounted position on the dorsum of the teleiochrysalis females, and guard them by fighting intruding rival males. Sneaker males also spend much time in a mounted position, but they never show aggressive behaviour against intruders. Intruding males easily find and attack territorial males but fail to notice or even ignore sneaker males. Here, we focus on territorial and sneaker males in the two-spotted spider mite, and investigate which males display sneaking behaviour and how effective the sneaking behaviour is against territorial males. We show that young males display sneaking behaviour more often, and that young territorial males are three times more likely to lose their mounted position to old territorial males than young sneaker males. Old males are always territorial and rarely lose their position on the female dorsum to young males. Finally, young territorial males are observed to change their mating strategy to that of sneaker in the presence of old males. Our results suggest that old males are superior to young males in contests over females, and that in response to old males young males can phenotypically switch to sneaker behavior, thereby possibly improving their mating success.
Department of Biology
The evolution of imperfect mimicry in hover flies (Diptera: Syrphidae)
Author(s): Sherratt, TN, Penny, H, Abbott, K, Hassall, C, Skevington, J
Although exquisite examples of the outcomes of natural selection are widely celebrated, it has long been recognized that nature’s imperfections tell us more about the process of adaptation than its perfections. Here we consider the phenomenon of imperfect mimicry and the variety of evolutionary theories that have been postulated to understand it, concentrating on hover flies (Diptera: Syrphidae). First, we review what we know about the morphological, acoustic and behavioural similarity of hover fly mimics to their putative models (bees and wasps), asking whether mimicry is extended into the UV range of the reflectance spectrum, and whether the behavioural mimics tend to be good morphological mimics. Second, we take a phylogenetic approach to quantify how frequently evolutionary transitions between model types have evolved, and what features need to evolve to facilitate mimicry of a given model type. Taken together these empirical and comparative insights allow us to rule out some theories for imperfect mimicry and provide support for others, although there is much more to do to understand the maintenance of imperfect mimicry in this species rich group.