Research into Heliconius butterflies has made a significant contribution to evolutionary biology. Here, we review our understanding of the diversification of these butterflies, covering recent advances and a vast foundation of earlier work. Whereas no single group of organisms can be sufficient for understanding life's diversity, after years of intensive study, research into Heliconius has addressed a wide variety of evolutionary questions. We first discuss evidence for widespread gene flow between Heliconius species and what this reveals about the nature of species. We then address the evolution and diversity of warning patterns, both as the target of selection and with respect to their underlying genetic basis. The identification of major genes involved in mimetic shifts, and homology at these loci between distantly related taxa, has revealed a surprising predictability in the genetic basis of evolution. In the final sections, we consider the evolution of warning patterns, and Heliconius diversity more generally, within a broader context of ecological and sexual selection. We consider how different traits and modes of selection can interact and influence the evolution of reproductive isolation.
Visual cues are important for insects to find flowers and host plants. It has been proposed that the diversity of leaf shape in Passiflora vines could be a result of negative frequency dependent selection driven by visual searching behavior among their butterfly herbivores. Here we tested the hypothesis that Heliconius butterflies use leaf shape as a cue to initiate approach toward a host plant. We first tested for the ability to recognize shapes using a food reward conditioning experiment. Butterflies showed an innate preference for flowers with three and five petals. However, they could be trained to increase the frequency of visits to a non-preferred flower with two petals, indicating an ability to learn to associate shape with a reward. Next we investigated shape learning specifically in the context of oviposition by conditioning females to lay eggs on two shoots associated with different artificial leaf shapes: their own host plant, Passiflora biflora, and a lanceolate non-biflora leaf shape. The conditioning treatment had a significant effect on the approach of butterflies to the two leaf shapes, consistent with a role for shape learning in oviposition behavior. This study is the first to show that Heliconius butterflies use shape as a cue for feeding and oviposition, and can learn shape preference for both flowers and leaves. This demonstrates the potential for Heliconius to drive negative frequency dependent selection on the leaf shape of their Passiflora host plants.
Adaptive coloration is under conflicting selection pressures: choosing potential mates and warning signaling against visually guided predators. Different elements of the color signal may therefore be tuned by evolution for different functions. We investigated how mimicry in four pairs of Heliconius comimics is potentially seen both from the perspective of butterflies and birds. Visual sensitivities of eight candidate avian predators were predicted through genetic analysis of their opsin genes. Using digital image color analysis, combined with bird and butterfly visual system models, we explored how predators and conspecifics may visualize mimetic patterns. Ultraviolet vision (UVS) birds are able to discriminate between the yellow and white colors of comimics better than violet vision (VS) birds. For Heliconius vision, males and females differ in their ability to discriminate comimics. Female vision and red filtering pigments have a significant effect on the perception of the yellow forewing band and the red ventral forewing pattern. A behavioral experiment showed that UV cues are used in mating behavior; removal of such cues was associated with an increased tendency to approach comimics as compared to conspecifics. We have therefore shown that visual signals can act to both reduce the cost of confusion in courtship and maintain the advantages of mimicry.
1. Birds are considered to be the primary selective agents for warning colouration in butterflies, and select for aposematic mimicry by learning to avoid brightly coloured prey after unpleasant experiences. It has long been thought that bright colouration plays an important role in promoting the avoidance of distasteful prey by birds.2. The hypothesis that warning colouration facilitates memorability and promotes predator avoidance was tested by means of a field experiment using distasteful model butterflies. Artificial butterflies with a Heliconius colour pattern unknown to local birds were generated using bird vision models, either coloured or achromatic, and hung in tree branches in a tropical forest. Two sequential trials were conducted at each site to test avoidance by naïve and experienced predators.3. There was a significant reduction in predation in the second trial. Also, coloured models were attacked less than achromatic models. Specifically, coloured butterflies were attacked significantly less in the second trial, but there was no significant decrease in predation on achromatic models.4. The present results imply an important role for colour in enhancing aversion of aposematic butterflies. It has also been demonstrated that previous experience of distasteful prey can lead to enhanced avoidance in subsequent trials, supporting mimicry theory.
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triangulation as anti-predatory mechanism in snakes. Biota Neotrop. 12(3): http://www.biotaneotropica.org.br/v12n3/en/ abstract?short-communication+bn01912032012Abstract: Anti-predator mechanisms in snakes are diverse and complex, including mimetic behavior. Some snakes triangulate their head, probably mimicking other more dangerous snakes. However, there is a lack of studies that demonstrate the effectiveness of this behavior with natural predators. The aim of this study was to verify, using artificial snakes, if snakes with triangular heads are less susceptible to attack by predators, and if predatory attack is targeted to the head of serpents. Artificial snakes were systematically arranged on a road border. The rate of attacked models was 48.71%. Number of attacks on models with rounded head was significantly higher than in models with triangular head. There was a significant difference between the places of attack on the snakes in relation to different head shapes. Therefore, snakes that have head triangulation may be a less frequent target of attacks by predators than those without such behavior. Keywords: artificial models, defensive behavior, mimicry, predation rate, reptiles. Resumo: Mecanismos anti-predação em serpentes são diversos e complexos, incluindo comportamentos miméticos. Algumas serpentes triangulam a cabeça, possivelmente mimetizando outras serpentes mais perigosas. No entanto, são escassos os estudos demonstrando a eficiência deste comportamento frente a predadores naturais. O objetivo deste estudo foi verificar, utilizando serpentes artificiais, se os indivíduos com cabeça triangular são menos suscetíveis ao ataque de predadores e, se o ataque predatório é direcionado à cabeça das serpentes. Serpentes artificiais foram dispostas sistematicamente na margem de uma estrada. A taxa de modelos atacados foi 48,71%. O número de ataques em modelos de cabeça arredondada foi significativamente maior do que nos modelos com cabeça triangular. Houve diferença significativa entre as partes atacadas nas serpentes quando comparados aos diferentes formatos de cabeça. Portanto, as serpentes que possuem triangulação da cabeça podem ser um alvo menos frequente de ataques por predadores do que as que não possuem esse tipo de comportamento. Palavras-chave: modelos artificiais, comportamento defensivo, mimetismo, taxa de predação, répteis. Biota Neotrop., vol. 12, no. 3 spatial homogeneity of the surrounding vegetation. The models were exposed for 17 hours, overnight, and collected the next morning. In field, each model was analyzed for attack presence, number of attacks, part of the model that suffered the attack (head or other parts of the body) and type of attack. Data analysis was performed in the program Past (Hammer et al. 2001) using Chi-square test (α = 0.05) to compare proportion of attacks on triangular and round head snakes models and proportion of attacks in the head and body between the two kinds of snake models. ResultsFrom the 80 snake models, one of each treatment was excluded from analysis bec...
Microhabitat choice plays a major role in shaping local patterns of biodiversity. In butterflies, stratification in flight height has an important role in maintaining community diversity. Despite its presumed importance, the role of behavioural shifts in early stages of speciation in response to differences in habitat structure is yet to be established. Here, we investigated variation in flight height behaviour in two closely related Heliconius species, H. erato cyrbia and H. himera, which produce viable hybrids but are isolated across an environmental gradient, spanning lowland wet forest to high‐altitude scrub forest. Speciation in this pair is associated with strong assortative mating, but ecological isolation and local adaptation are also considered essential for complete reproductive isolation. We quantified differences in flight height and forest structure across the environmental gradient and tested the importance of resource distribution in explaining flight behaviour. We then used common garden experiments to test whether differences in flight height reflect individual responses to resource distribution or genetically determined shifts in foraging behaviour. We found that the two species fly at different heights in the wild, and demonstrated that this can be explained by differences in the vertical distribution of plant resources. In both the wild and captivity, H. himera choose to fly lower and feed at lower positions, closely mirroring differences in resource availability in the wild. Given expectations that foraging efficiency contributes to survival and reproductive success, we suggest that foraging behaviour may reflect local adaptation to divergent forest structures. Our results highlight the potential role of habitat‐dependent divergence in behaviour during the early stages of speciation.
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