Diverse Cretaceous larvae reveal the evolutionary and behavioural history of antlions and lacewings

Nature Communications, Aug 2018

Myrmeleontiformia are an ancient group of lacewing insects characterized by predatory larvae with unusual morphologies and behaviours. Mostly soil dwellers with a soft cuticle, their larvae fossilize only as amber inclusions, and thus their fossil record is remarkably sparse. Here, we document a disparate assemblage of myrmeleontiform larvae from the mid-Cretaceous amber (99 Ma) of Myanmar, evidence of a considerable diversification. Our cladistic analysis integrating extant and extinct taxa resolves the fossils as both stem- and crown-groups. Similarities between extinct and extant species permit inferences of larval ethology of the fossil species through statistical correlation analyses with high support, implying that morphological disparity matched behavioural diversity. An improved understanding of the evolutionary history of antlions and relatives supports the conclusion that hunting strategies, such as camouflage and fossoriality, were acquired early within the lineage.

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Diverse Cretaceous larvae reveal the evolutionary and behavioural history of antlions and lacewings

Abstract Myrmeleontiformia are an ancient group of lacewing insects characterized by predatory larvae with unusual morphologies and behaviours. Mostly soil dwellers with a soft cuticle, their larvae fossilize only as amber inclusions, and thus their fossil record is remarkably sparse. Here, we document a disparate assemblage of myrmeleontiform larvae from the mid-Cretaceous amber (99 Ma) of Myanmar, evidence of a considerable diversification. Our cladistic analysis integrating extant and extinct taxa resolves the fossils as both stem- and crown-groups. Similarities between extinct and extant species permit inferences of larval ethology of the fossil species through statistical correlation analyses with high support, implying that morphological disparity matched behavioural diversity. An improved understanding of the evolutionary history of antlions and relatives supports the conclusion that hunting strategies, such as camouflage and fossoriality, were acquired early within the lineage. Introduction The immature stages of insects embody a wealth of biological information, particularly so for holometabolous insects whereby the larval stages can often lead dramatically different lives from those of their corresponding adults1,2,3,4. Data from larvae are vital in everything from effective biological control programs to the elucidation of major evolutionary patterns5. Despite the importance of larvae for understanding evolutionary relationships and biological phenomena among insects6,7, the fossil record of insect larvae remains a largely untapped resource. This is the result of several factors such as difficulty in properly identifying particular larval forms, distinguishing among stages, and often poor preservation owing to their frequently soft integument. Nonetheless, fossil larvae, when studied properly, have proven to be a rich source of information for evolutionary studies8,9. The preservation of larvae in amber, whereby their finer features are preserved with greater fidelity than via other modes of fossilization, allows for life-like comparison between extinct and extant larval forms. The lacewings, antlions, owlflies, and their relatives comprise the insect order Neuroptera, and for more than 150 years the study of lacewing larvae has proven critical to understanding broad evolutionary patterns across the clade10. In addition, not only have larvae been vital to resolving relationships among neuropteran lineages, but these larvae also exhibit unique and remarkable biologies. Neuropteran larvae are famed for their various modes of predatory behaviour, using in some cases exogenous materials as camouflage for approaching prey and avoiding their own predators, to excavating elaborate funnels in which to entrap surface-dwelling victims, as is famous among antlions11 (Fig. 1). Neuroptera are also an ancient lineage, with many clades extending back to the Triassic and Jurassic, and the group as a whole is known from as far back as the Permian5,12,13. Neuroptera, together with Megaloptera and Raphidioptera, form the superorder Neuropterida, in turn sister to Coleoptera+Strepsiptera12 (Fig. 2). Among this diversity, the clade Myrmeleontiformia, comprising the superfamilies Psychopsoidea and Myrmeleontoidea13, includes some of the largest and most diverse of all lacewings, particularly among antlions, Myrmeleontidae. Myrmeleontiform lacewings are among the most characteristic insects of arid environments worldwide. Fig. 1 Diversity and biology of extant Myrmeleontiformia. a Halter halteratus (Forskål), Nemopteridae. b Libelloides latinus (Lefèbvre), Ascalaphidae. c Myrmeleon fasciatus (Navás), Myrmeleontidae. d Larva of Pterocroce capillaris (Klug), Nemopteridae. e Larva of Libelloides latinus (Lefèbvre), Ascalaphidae. f Larva of Macroleon quinquemaculatus (Hagen), Myrmeleontidae. g Camouflaging larva of Bubopsis agrionoides (Rambur), Ascalaphidae. h Fossorial larva of Creoleon lugdunensis (Villiers), Myrmeleontidae. Photos credits: a by Cosmin O. Manci; b, h by Claudio Labriola; c–g by Davide Badano Full size image Fig. 2 Simplified cladogram of the internal relationships of Neuropteroidea. The larva of the nemopterid Pterocroce capillaris (Klug) highlights Neuropterida Full size image Although myrmeleontiform adults are usually predators, like their larvae, they are of delicate appearance, varying from dragonfly-like to butterfly-like species, with massive and often conspicuously marked wings (Fig. 1a–c). Their campodeiform larvae are voracious ambush predators, with massive trap jaws and sometimes with bizarre body types, including those with elongate, slender necks or bodies covered in “spiny” or branched tubercles (Fig. 1d–f). Moreover, these insects are characterized by a wide range of ecological adaptations, spanning from arboreal to deep-soil dwellers11 (Fig. 1g, h). Such morphological and ecological disparity is remarkable in a relatively small group (at least by insect standa (...truncated)


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Davide Badano, Michael S. Engel, Andrea Basso, Bo Wang, Pierfilippo Cerretti. Diverse Cretaceous larvae reveal the evolutionary and behavioural history of antlions and lacewings, Nature Communications, 2018, Issue: 9, DOI: 10.1038/s41467-018-05484-y