Behavioural and ecological interactions between Heliconius butterflies, their predators and host plants

Heliconius butterflies exhibit Müllerian mimicry, in which two or more unpalatable species share a mutual advantage from having a common conspicuous colour pattern. These tropical butterflies have impressive visual signals, which are under conflicting selection pressures, as they are used in choosing potential mates and defending against visual predators through aposematic coloration. As both selection pressures are likely to be strong, different elements of the signal might be adapted for different receivers. Here, I combine sensory ecology with behavioural ecology to explain Heliconius colours signals of different co-mimic pairs. I explore how mimicry in Heliconius is perceived both from the perspective of predators and conspecifics, using visual abilities of both butterflies and birds. The different visual sensitivities of avian predators, H. erato females and males make them to perceive Heliconius coloration in different ways. My work suggests that having the ability to see in the ultra-violet light range enables higher discrimination between co-mimics both for birds and butterflies. Heliconius warning colours transmit a consistent signal across time of the day and habitat in a tropical forest for avian vision. In contrast through Heliconius vision there is evidence that patterns are more conspicuous in their own habitats. All these traits could facilitate communication between co-mimics and reduce the cost of confusion in courtship while still maintaining the advantages of Müllerian mimicry against predation. I conducted a field experiment to show that attack rates on a novel distasteful butterfly reduced over time, suggesting that Heliconius wing colouration can enhance aversion among predators. Finally, I have shown that Heliconius butterflies use leaf shape as a cue to approach their host plants, demonstrating the potential for Heliconius to drive negative frequency dependent selection on the leaf shape of their Passiflora host plants. Overall these results highlight ecological interactions between Heliconius butterflies, their predators and host plants.CAPES Brazil Cambridge Trus

The appearance of mimetic Heliconius butterflies to predators and conspecifics.

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.ERC, CAPES, STR

Estimating the age of Heliconius butterflies from calibrated photographs.

Mating behaviour and predation avoidance in Heliconius involve visual colour signals; however, there is considerable inter-individual phenotypic variation in the appearance of colours. In particular, the red pigment varies from bright crimson to faded red. It has been thought that this variation is primarily due to pigment fading with age, although this has not been explicitly tested. Previous studies have shown the importance of red patterns in mate choice and that birds and butterflies might perceive these small colour differences. Using digital photography and calibrated colour images, we investigated whether the hue variation in the forewing dorsal red band of Heliconius melpomene rosina corresponds with age. We found that the red hue and age were highly associated, suggesting that red colour can indeed be used as a proxy for age in the study of wild-caught butterflies

The sensory ecology of speciation

In this chapter, we explore the potential influence of sensory ecology on speciation, including but not limited to the concept of sensory drive, which concerns the co-evolution of signals and sensory systems with the local environment. The sensory environment can influence individual fitness in a variety of ways, thereby affecting the evolution of both pre- and post-mating reproductive isolation. Previous work focused on sensory drive has undoubtedly advanced the field, but we argue that it may have also narrowed our understanding of the broader influence of the sensory ecology on speciation. Moreover, the clearest examples of sensory drive are largely limited to aquatic organisms, which may skew the influence of contributing factors. We review the evidence for sensory drive across environmental conditions, and in this context discuss the importance of more generalized effects of sensory ecology on adaptive behavioral divergence. Finally, we consider the potential of rapid environmental change to influence reproductive barriers related to sensory ecologies. Our synthesis illustrates the importance of sensory conditions for local adaptation and divergence in a range of behavioral contexts and extends our understanding of the interplay between sensory ecology and speciation

Responsiveness of the broad bean weevil, Bruchus rufimanus , to Vicia faba genotypes

International audienceThe broad bean weevil, Bruchus rufimanus Boh. (Coleoptera: Chrysomelidae), also called bruchid beetle, is a major pest of Vicia faba L. (Fabaceae) given that larvae develop inside the seeds causing direct quality losses in agricultural products. Recurrent chemical applications are inappropriate because they represent a serious threat to pollinators in general. In addition, biological control approaches that have been attempted so far showed limited effectiveness, which makes studies of methods to control bruchid populations extremely important. Breeding resistant cultivars is the most adequate approach to achieve efficient levels of pest resistance and promote sustainable agriculture. To explore the mechanisms underlying bruchid resistance, we explored B. rufimanus behavior at different life stages and preference in plant feeding, oviposition, and larval survival into adulthood on a range of susceptible and resistant broad bean cultivars (genotypes), both in greenhouse experiments and in the field. Our greenhouse results showed that females, compared to males, prefer flowers from some genotypes over others, although the choices made did not correspond with egg-laying preference. Egg-laying preference was also affected by cultivars. This attraction for egg-laying was associated with the number of seeds per pod produced by the genotypes. In the field flowering date influenced bruchid infestation. Also the survival of larvae into adulthood was greater in certain genotypes over others. The results of our study lay the groundwork for further analyses to finely dissect V. faba resistance towards bruchids and pave the way for the development of methods to predict potential resistant genotypes in research and breeding programs

Butterfly Learning and the Diversification of Plant Leaf Shape

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 towards 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

Indução de nectários extraflorais em Passiflora suberosa L. (Passifloraceae)

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La Libertad: La Libertad - Año XV Número 4289 - 1933 diciembre 16 (16/12/1933)

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Anatomia foliar de sete espécies do gênero Passiflora L. (Passifloraceae) no estado do Rio Grande do Sul

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