Concept: Batesian mimicry
- Proceedings of the National Academy of Sciences of the United States of America
- Published over 5 years ago
A near-perfect mimetic association between a mecopteran insect species and a ginkgoalean plant species from the late Middle Jurassic of northeastern China recently has been discovered. The association stems from a case of mixed identity between a particular plant and an insect in the laboratory and the field. This confusion is explained as a case of leaf mimesis, wherein the appearance of the multilobed leaf of Yimaia capituliformis (the ginkgoalean model) was accurately replicated by the wings and abdomen of the cimbrophlebiid Juracimbrophlebia ginkgofolia (the hangingfly mimic). Our results suggest that hangingflies developed leaf mimesis either as an antipredator avoidance device or possibly as a predatory strategy to provide an antiherbivore function for its plant hosts, thus gaining mutual benefit for both the hangingfly and the ginkgo species. This documentation of mimesis is a rare occasion whereby exquisitely preserved, co-occurring fossils occupy a narrow spatiotemporal window that reveal likely reciprocal mechanisms which plants and insects provide mutual defensive support during their preangiospermous evolutionary histories.
- Proceedings. Biological sciences / The Royal Society
- Published about 5 years ago
The great majority of plant species in the tropics require animals to achieve pollination, but the exact role of floral signals in attraction of animal pollinators is often debated. Many plants provide a floral reward to attract a guild of pollinators, and it has been proposed that floral signals of non-rewarding species may converge on those of rewarding species to exploit the relationship of the latter with their pollinators. In the orchid family (Orchidaceae), pollination is almost universally animal-mediated, but a third of species provide no floral reward, which suggests that deceptive pollination mechanisms are prevalent. Here, we examine floral colour and shape convergence in Neotropical plant communities, focusing on certain food-deceptive Oncidiinae orchids (e.g. Trichocentrum ascendens and Oncidium nebulosum) and rewarding species of Malpighiaceae. We show that the species from these two distantly related families are often more similar in floral colour and shape than expected by chance and propose that a system of multifarious floral mimicry-a form of Batesian mimicry that involves multiple models and is more complex than a simple one model-one mimic system-operates in these orchids. The same mimetic pollination system has evolved at least 14 times within the species-rich Oncidiinae throughout the Neotropics. These results help explain the extraordinary diversification of Neotropical orchids and highlight the complexity of plant-animal interactions.
Venom systems have evolved on multiple occasions across the animal kingdom, and they can act as key adaptations to protect animals from predators . Consequently, venomous animals serve as models for a rich source of mimicry types, as non-venomous species benefit from reductions in predation risk by mimicking the coloration, body shape, and/or movement of toxic counterparts [2-5]. The frequent evolution of such deceitful imitations provides notable examples of phenotypic convergence and are often invoked as classic exemplars of evolution by natural selection. Here, we investigate the evolution of fangs, venom, and mimetic relationships in reef fishes from the tribe Nemophini (fangblennies). Comparative morphological analyses reveal that enlarged canine teeth (fangs) originated at the base of the Nemophini radiation and have enabled a micropredatory feeding strategy in non-venomous Plagiotremus spp. Subsequently, the evolution of deep anterior grooves and their coupling to venom secretory tissue provide Meiacanthus spp. with toxic venom that they effectively employ for defense. We find that fangblenny venom contains a number of toxic components that have been independently recruited into other animal venoms, some of which cause toxicity via interactions with opioid receptors, and result in a multifunctional biochemical phenotype that exerts potent hypotensive effects. The evolution of fangblenny venom has seemingly led to phenotypic convergence via the formation of a diverse array of mimetic relationships that provide protective (Batesian mimicry) and predatory (aggressive mimicry) benefits to other fishes [2, 6]. Our results further our understanding of how novel morphological and biochemical adaptations stimulate ecological interactions in the natural world.
Mimicry is one of the oldest concepts in biology, but it still presents many puzzles and continues to be widely debated. Simulation of wasps with a yellow-black abdominal pattern by other insects (commonly called “wasp mimicry”) is traditionally considered a case of resemblance of unprofitable by profitable prey causing educated predators to avoid models and mimics to the advantage of both (Figure 1a). However, as wasps themselves are predators of insects, wasp mimicry can also be seen as a case of resemblance to one’s own potential antagonist. We here propose an additional hypothesis to Batesian and Müllerian mimicry (both typically involving selection by learning vertebrate predators; cf. Table 1) that reflects another possible scenario for the evolution of multifold and in particular very accurate resemblances to wasps: an innate, visual inhibition of aggression among look-alike wasps, based on their social organization and high abundance. We argue that wasp species resembling each other need not only be Müllerian mutualists and that other insects resembling wasps need not only be Batesian mimics, but an innate ability of wasps to recognize each other during hunting is the driver in the evolution of a distinct kind of masquerade, in which model, mimic, and selecting agent belong to one or several species (Figure 1b). Wasp mimics resemble wasps not (only) to be mistaken by educated predators but rather, or in addition, to escape attack from their wasp models. Within a given ecosystem, there will be selection pressures leading to masquerade driven by wasps and/or to mimicry driven by other predators that have to learn to avoid them. Different pressures by guilds of these two types of selective agents could explain the widely differing fidelity with respect to the models in assemblages of yellow jackets and yellow jacket look-alikes.
Abstract Because predation is the main cause of avian nest failure, selection should favor strategies that reduce the probability of nest predation. We describe apparent Batesian mimicry in the morphology and behavior of a Laniocera hypopyrra nestling. On hatching, the nestling had a distinctive bright orange color and modified feathers all over its body, and 6 days after hatching, it started to move its head very slowly from side to side (in a “caterpillar” movement) when disturbed. These traits gave it a resemblance to a hairy, aposematic caterpillar. This species has a long nestling period for its size (20 days), perhaps due to slow provisioning rates (about one feeding per hour). We argue that the slow growth rate, combined with high nest predation, favors the evolution of antipredation mechanisms such as the unique morphological and behavioral characteristics of L. hypopyrra nestlings.
Batesian mimicry, a phenomenon in which harmless organisms resemble harmful or unpalatable species, has been extensively studied in evolutionary biology. Model species may differ from population to population of a single mimetic species, so different predation pressures might have driven micro-evolution towards better mimicry among regions. However, there is scant direct evidence of micro-evolutionary change over time in mimicry traits. Papilio polytes shows female-limited Batesian mimicry. On Okinawa, one mimicry model is Pachliopta aristolochiae, which was not present on the island until 1993. In P. polytes, the size of the hind-wing white spot, a mimetic trait, is maternally heritable. Among specimens collected between 1961 and 2016, the average white spot size was unchanged before the model’s arrival but has rapidly increased since then. However, white spot size showed greater variance after the model’s establishment than before. This suggests that before 1993, white spot size in this population was not selectively neutral but was an adaptive trait for mimicking an unpalatable native, Byasa alcinous, which looks like P. aristolochiae apart from the latter’s hind-wing white spot. Thus, some females switched their model to the new one after its arrival.
Although the forces behind the evolution of imperfect mimicry remain poorly studied, recent hypotheses suggest that relaxed selection on small-bodied individuals leads to imperfect mimicry. While evolutionary history undoubtedly affects the development of imperfect mimicry, ecological community context has largely been ignored and may be an important driver of imperfect mimicry. Here we investigate how evolutionary and ecological contexts might influence mimetic fidelity in Müllerian and Batesian mimicry systems. In Batesian hoverfly systems we find that body size is not a strong predictor of mimetic fidelity. However, in Müllerian velvet ants we find a weak positive relationship between body size and mimetic fidelity when evolutionary context is controlled for and a much stronger relationship between community diversity and mimetic fidelity. These results suggest that reduced selection on small-bodied individuals may not be a major driver of the evolution of imperfect mimicry and that other factors, such as ecological community context, should be considered when studying the evolution of imperfect mimicry.
Warning signals are an effective defence strategy for aposematic prey, but only if they are recognized by potential predators. If predators must eat prey to associate novel warning signals with unpalatability, how can aposematic prey ever evolve? Using experiments with great tits (Parus major) as predators, we show that social transmission enhances the acquisition of avoidance by a predator population. Observing another predator’s disgust towards tasting one novel conspicuous prey item led to fewer aposematic than cryptic prey being eaten for the predator population to learn. Despite reduced personal encounters with unpalatable prey, avoidance persisted and increased over subsequent trials. Next we use a mathematical model to show that social transmission can shift the evolutionary trajectory of prey populations from fixation of crypsis to fixation of aposematism more easily than was previously thought. Therefore, social information use by predators has the potential to have evolutionary consequences across ecological communities.
Animal communication is often deceptive; however, such dishonesty can become ineffective if it is used too often, is used out of context, or is too easy to detect [1-3]. Mimicry is a common form of deception, and most mimics gain the greatest fitness benefits when they are rare compared to their models [3, 4]. If mimics are encountered too frequently or if their model is absent, avoidance learning of noxious models is disrupted (Batesian mimicry ), or receivers become more vigilant and learn to avoid perilous mimics (aggressive mimicry ). Mimics can moderate this selective constraint by imperfectly resembling multiple models , through polymorphisms , or by opportunistically deploying mimetic signals [1, 7]. Here we uncover a novel mechanism to escape the constraints of deceptive signaling: phenotypic plasticity allows mimics to deceive targets using multiple guises. Using a combination of behavioral, cell histological, and molecular methods, we show that a coral reef fish, the dusky dottyback (Pseudochromis fuscus), flexibly adapts its body coloration to mimic differently colored reef fishes and in doing so gains multiple fitness benefits. We find that by matching the color of other reef fish, dottybacks increase their success of predation upon juvenile fish prey and are therefore able to deceive their victims by resembling multiple models. Furthermore, we demonstrate that changing color also increases habitat-associated crypsis that decreases the risk of being detected by predators. Hence, when mimics and models share common selective pressures, flexible imitation of models might inherently confer secondary benefits to mimics. Our results show that phenotypic plasticity can act as a mechanism to ease constraints that are typically associated with deception. VIDEO ABSTRACT.
- Proceedings of the National Academy of Sciences of the United States of America
- Published over 3 years ago
Understanding the evolutionary transition from interspecific exploitation to cooperation is a major challenge in evolutionary biology. Ant-aphid relationships represent an ideal system to this end because they encompass a coevolutionary continuum of interactions ranging from mutualism to antagonism. In this study, we report an unprecedented interaction along this continuum: aggressive mimicry in aphids. We show that two morphs clonally produced by the aphid Paracletus cimiciformis during its root-dwelling phase establish relationships with ants at opposite sides of the mutualism-antagonism continuum. Although one of these morphs exhibits the conventional trophobiotic (mutualistic) relationship with ants of the genus Tetramorium, aphids of the alternative morph are transported by the ants to their brood chamber and cared for as if they were true ant larvae. Gas chromatography-mass spectrometry analyses reveal that the innate cuticular hydrocarbon profile of the mimic morph resembles the profile of ant larvae more than that of the alternative, genetically identical nonmimic morph. Furthermore, we show that, once in the brood chamber, mimic aphids suck on ant larva hemolymph. These results not only add aphids to the limited list of arthropods known to biosynthesize the cuticular chemicals of their deceived hosts to exploit their resources but describe a remarkable case of plastic aggressive mimicry. The present work adds a previously unidentified dimension to the classical textbook paradigm of aphid-ant relationships by showcasing a complex system at the evolutionary interface between cooperation and exploitation.