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Advanced X-ray MicroCT technology offers unparalleled insights into the functional morphology of specialized organs that mediate interactions between butterfly caterpillars and their ant hosts

The spectacular leaps of gazelles, group living in deer and monkeys, and fast flight in many insects are all linked by a common phenomenon―predation. In its various forms, predation has driven the evolution of a plethora of specialized structures (morphology) and behaviours among organisms. Insects, being especially vulnerable because of their small size, have evolved various strategies to avoid predators. For example, butterflies may either accumulate toxins (aposematism), mimic other toxic species (mimicry), avoid detection by predators by remaining inconspicuous (crypsis or camouflage), or look like inedible plant parts (masquerade) to escape predators.

Butterflies of the family Lycaenidae, popularly known as Blues and Hairstreaks, have gone in a completely unexpected direction to deal with their predators. Caterpillars and pupae of the majority of the approximately 5,200 lycaenid species do not avoid predatory ants at all. In fact, they seek and closely associate with ants, becoming strange bedfellows! Ants not only do not eat these caterpillars and pupae, but they actually care for them and aggressively protect them from other predators and parasitoids, thus creating an enemy-free space. Many of these associations have been perfected over millions of years via an evolutionary arms-race between the caterpillars and ants. How are these strange associations between predator and potential prey species sustained?

The lycaenid caterpillars are far from vulnerable in this association. Over tens of millions of years of evolution, this butterfly group has evolved a range of adaptations that have tamed their ferocious ant predators into protectors and providers. Lycaenid caterpillars typically have at least four types of specialized organs that produce chemical concoctions that modulate the nature of their ant associations, ranging from facultative to obligate, and mutually beneficial to behaviourally manipulative and parasitic. First, the body surface of lycaenid caterpillars has clusters of pheromone-secreting glands called pore cupolae. Pore cupolae are thought to secrete chemicals that secure favorable recognition by the ants, thereby subduing their aggression.