Abstract
Myrmecophilous butterflies can establish complex symbiotic relationships with ants. A caterpillar wandering among the brood of the aggressive ponerine ant Neoponera villosa was found inside the core of a nest built in the myrmecophytic bromeliad Aechmea bracteata. This is the first caterpillar found living inside a ponerine ant nest. Its DNA barcode was sequenced, and an integrative approach was used to identify it as Pseudonymphidia agave, a poorly known member of the subtribe Pachythonina in the riodinid tribe Nymphidiini. The cuticle of the tank-like caterpillar lacks projections or tubercles and is covered dorsally by specialized flat setae that form an armor of small plates. Ant-organs potentially related to caterpillar-ant signaling, such as perforated cupola organs and tentacle nectary organs, are present. These morphological traits, together with evidence of social integration (direct contact with host brood, protective morphology, slow movement, no host aggressiveness), suggest that P. agave is a symbiotic, social parasite of N. villosa, preying on its host brood. However, several knowledge gaps remain, including oviposition site, dependence on bromeliad association, steps to colony integration, and larval diet through development. Carnivory has been reported in all known members of the subtribe Pachythonina (caterpillars prey on honeydew-producing hemipterans) suggesting a shift to myrmecophagy inside the ant nests as a possible evolutionary transition.
Highlights
Myrmecophilous butterflies can establish complex symbiotic relationships with ants
The presence of a P. agave larva among the members of a N. villosa colony is consistent with the idea that these taxa may exhibit specialized associations with ants, including long periods inside the ant nests[11,39,96]
Pseudonymphidia agave belongs to the recently erected subtribe Pachythonina (Nymphidiini), a clade diagnosed on the basis of genetic characters[37]
Summary
Myrmecophilous butterflies can establish complex symbiotic relationships with ants. A caterpillar wandering among the brood of the aggressive ponerine ant Neoponera villosa was found inside the core of a nest built in the myrmecophytic bromeliad Aechmea bracteata. Symbiotic associations between lepidopteran caterpillars and ants are diverse and widespread, spanning at least six lepidopteran superfamilies: Noctuoidea, Papilionoidea, Pyraloidea, Tineoidea, Gelechioidea, and Z ygaenoidea[18,19,20] These interactions range from commensalism or mutualism to social parasitism, and relationships may be facultative or obligate, occurring during only a portion or the whole life cycle of the myrmecophile[21,22]. Predation on ant brood has been documented in Lycaenidae, but not in the Riodinidae; members of both families exhibit complex myrmecophily with the evolution of specific ant-organs and behavioral strategies to integrate and exploit ant host c olonies[11] such as chemical signaling, vibrational and tactile mimicry, ant-dependent oviposition, release of brood-carrying behavior, trophallaxis and others[32,33,34] These obligate social parasite species are completely dependent on the ants to complete their life cycle[35]
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