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.
Figure 1. Association of caterpillars of Blues and Hairstreaks (Lycaenidae) with ants range from absent to facultative (opportunistic) to obligate (compulsory), and from mutualistic to parasitic. At one end of the spectrum, caterpillars of species such as the Red Pierrot (Talicada nyseus; left) do not associate with ants directly, but are also not attacked by them as are most caterpillars. They have thick larval skins or cuticles characteristic of many lycaenid caterpillars, and appear to retain pore cupolae organs, but all other ant associated structures develop only to a rudimentary state. Caterpillars of facultative associates such as the Common Cerulean (Jamides celeno; centre) live with ants whenever they find the right ant species, but they are also fine without ants. In these species, the ant-associated organs are developed reasonably. At the other extreme, caterpillars of species such as the Lilac Silverline (Apharitis lilacinus, right) are obligate associates of ants, in which the ant-associated organs are remarkably developed. Females of such obligate associates lay eggs very close to ant nests. Caterpillars and pupae are constantly attended by ants, and they may live inside ant nests, often among the brood of ants. In some of these species, caterpillars do not feed on plants at all. Instead, they eat food regurgitated by the tending ants. In a rare turn of events, the caterpillars of some species may also slyly eat the ant brood, turning this association a bit sinister. Images by Krushnamegh Kunte.
In some species, the secretions of dew patches and nectar glands have been shown to alter the levels of neurotransmitters, particularly dopamine, in the brains of their attendant ants, causing them to slow their locomotory activity. This also makes the ants more faithful to the caterpillars and increase the level of aggression toward their parasites and predators. In cases like these, it is better to consider these apparently mutualistic interactions to be reciprocal parasitisms, where natural selection may turn the strategies used by each partner to outwit the other into a sophisticated coevolutionary arms race.Next, two other organs, called dew patches in some species and nectar glands in others, produce carbohydrate-rich secretions to attract and reward the tending ants. For the most part, these sugary secretions, which ants drink readily, keeps the ants interested in tending and protecting the caterpillars. Ants can sometimes be seen stroking the caterpillars with their antennae to encourage them to produce these secretions, and the caterpillars often comply. So this association can be beneficial for both parties. However, caterpillars can sometimes deceive the ants by luring them with these secretions but then reabsorbing the secretions before ants can take them. One supposes that the caterpillars have to juggle between keeping the tending ants happy so that they continue to receive protection, while minimizing the energetic cost of producing these nutritious secretions. Who isn’t tempted to skim off some profits from business partners once in a while?
Finally, caterpillars deter the ants by rhythmically everting a pair of tentacle organs or tactile organs when the density of tending ants increases too much, or when the caterpillar wants to move. Ciliary tufts at the tips of these organs also contain receptors of ant pheromones, and act as a compass to direct caterpillars toward ant aggregations.