Life history and evolution of the enigmatic Cretaceous–Eocene Alienopteridae: A critical review

Alienopteridae are among the most perplexing fossil insects and once conspicuous members of Cretaceous Dictyoptera (now including cockroaches, termites and mantises). However, the precise nature of their life history, evolution, and phylogenetic affinities remained controversial and open to debate. Here we report new alienopterid nymphs from mid-Cretaceous Kachin amber (approximately 99 Ma) and define three nymphal morphotypes, along with proposed interpretations of their life style. We also re-evaluate the systematic position of Alienopteridae, and of the recently erected order Aethiocarenodea. Geometric morphometric analyses suggest that morphotype I nymphs exhibit distinct morphological specializations that were most likely associated with ant mimicry, like immature stages of some modern crown mantises. Remarkably, mimetic association between these nymphs and stem-group ants provides the earliest record of ant mimicry (myrmecomorphy), which is contemporary with the earliest ants and their eusociality. We discuss different interpretations of the life history of alienopterid adults, especially wasp mimicry, and conclude that Teyia was likely a wasp mimic. The nymphs (morphotype I) and adults of Teyia resemble different models, which provides the first fossil record of transformational mimicry, implying that this behaviour had already evolved by the mid-Cretaceous. In addition, one alienopterid nymph laden with pollen clumps provides evidence for gymnosperm pollination and a previously unknown gymnosperm-insect association. This suggests that extinct dictyopterans might have been among the earliest pollinators, with a hitherto undervalued role in pollination ecology. Our phylogenetic analysis provides evidence that Alienopteridae and Umenocoleidae together constitute a monophyletic group (Alienoptera), which is placed as sister taxon of Mantodea. Alienoptera including Umenocoleidae were supported as a separate lineage, and mainly characterized by sclerotized shell-like tegmina and unique leg structures, their main diversification probably occurred before the J/K boundary, and we suggest a common evolutionary origin during the Late Jurassic.