Butterflies from the subtropical genus Heliconius are an excellent model for investigating the role of behavioural innovation in evolution. They exhibit a remarkable, novel feeding strategy by actively collecting and feeding on pollen, which provides a reliable source of protein, allowing females to continue laying eggs for up to six months.

H.erato cybria by Luca Livraghi

Since the 19th century, the neotropical butterfly genus Heliconius and its striking diversity of wing patterns, has served as a textbook example of Müllerian mimicry. Yet these butterflies are far more than a canvas for pretty patterns. In the early 1970s field studies observed Heliconius collecting and feeding upon pollen – an extraordinary behaviour otherwise unknown in butterflies. Heliconius gather pollen by probing flowers and collecting it as a lumped mass on the proboscis, which is then mixed with saliva and externally digested before being drawn up the proboscis. Pollen feeding in Heliconius has since been shown to co-occur with a constellation of behavioural, neuroanatomical, life history, morphological and physiological traits absent in their non-pollen-feeding relatives. Our Review highlights how Heliconius can serve as a key example of behavioural innovation triggering an adaptive shift across a suite of multiple, interrelated traits. The relatively recent emergence of Heliconius (~ 18 mya) makes it an ideal system for investigating the evolutionary consequences of pollen feeding.

Pollen provides adult butterflies with a consistent supply of protein, allowing Heliconius to continually produce eggs throughout their greatly extended lifespans of up to six months. In contrast, most other butterflies depend on protein accumulated during the larval stage, which is eventually depleted. These substantial reproductive benefits raise the question of why pollen feeding is so rare within butterflies. Surprisingly, Heliconius show no novel morphological structures associated with pollen feeding and only minor modifications to the proboscis, and pollen processing behaviour may be derived from grooming behaviours. Heliconius saliva appears key to pollen digestion and may have played a central role in the evolution of pollen feeding – although our understanding of this physiological adaptation is currently limited.

H. melomene by Wyatt Toure

The foraging behaviours of Heliconius, however, reveal a degree of behavioural sophistication rarely reported in Lepidoptera. Pollen is primarily collected from relatively rare Cucurbitaceous vines, and in visiting these plants Heliconius establish traplines – routes along which specific plants are regularly visited. This suggests a well-developed capacity for spatial navigation, likely learnt using visual landmarks. These behavioural innovations are potentially associated with major changes in brain structure and function. Indeed, Heliconius have dramatically enlarged mushroom bodies, structures in the insect brains associated with learning and memory, which are 3 to 4 times larger than is typical of Lepidoptera. We suspect that the cognitive demands of trapline foraging drove this expansion of the mushroom bodies, but this hypothesis has not yet been directly tested.

Heliconius are already an important model for studying the genomic bases of speciation and colour pattern evolution. However, we argue that these butterflies and their remarkable dietary innovation can also help to answer fundamental questions in evolutionary biology relating to behavioural novelty, brain evolution, life histories and aging processes.

About the author

I am a PhD student at the University of Cambridge. Under the supervision of Dr Stephen Montgomery, I am investigating the selective pressures driving, and behavioural consequences of the dramatic expansion of the mushroom bodies, brain regions connected with learning and memory, in Heliconius butterflies, the only known pollen feeding lepidopterans. My work involves comparative experiments across Heliconius and closely related species, incorporating both behavioural and neuroanatomical data. Together with other members of the Evolution of Brains and Behaviour Lab (EBAB Lab), we aim to develop Heliconius as an important model for brain evolution.

Fletcher Young

What was your experience like publishing in Proceedings B?

Publishing with Proceedings B was a very positive process. Both reviewers provided extensive and detailed comments on the original manuscript which greatly improved the final paper. We are also impressed by the speed of publication following acceptance.

Proceedings B is looking to publish more high-quality research articles and reviews in behaviour, cognition and evolution. If you have an idea for a review, we strongly encourage you to submit a proposal by completing our proposal template and sending it to the journal. More information about the journal and the submission process can be found on our website.

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Image credits: 

1) H. erato cyrbia - Luca Livraghi

2) H. melomene - Wyatt Toure

3) Fletcher Young 

 

 

 

 

 

 

Authors

  • Fletcher Young

    Fletcher Young