When a key innovation becomes redundant: Patterns, drivers and consequences of elytral reduction in Coleoptera

Abstract

The transformation of the fore wings into strongly sclerotized protective covers (elytra) is considered a fundamental evolutionary innovation of the megadiverse order Coleoptera. Surprisingly, these multifunctional structures have been reduced in many distantly related groups of beetles. Patterns, drivers and the evolutionary implications of this modification have never been comprehensively discussed. In the present study, we surveyed the entire order Coleoptera to analyse the patterns of elytral shortening and loss, with a special focus on prevalence, forms, degree of reduction and the functional background of this significant deviation from the coleopteran ground plan. Our analysis revealed that about 20% of all extant species (roughly 88,000 out of 442,275 spp.), distributed across all four suborders, have shortened or even absent elytra. The elytral loss was more frequent within the polyphagan series Elateriformia and Staphyliniformia. Moreover, we found that elytral reduction has independently occurred multiple times in the evolutionary history of Coleoptera and that it has been driven by a wide array of selective drivers. One of the main drivers is the improved flexibility of the uncovered abdomen and the correlated increased manoeuvrability in narrow spaces, as well as the option of using the flexible abdomen as a steering organ or to facilitate mating. Another common driver is mimicry, where exposed metathoracic wings potentially improve the overall similarity to hymenopteran models. Exposure of the abdomen can facilitate the targeted release of defensive abdominal gland secretions and was most likely a crucial step towards establishing relations with social insects enhanced by chemical communication. In the Elateriformia, and rarely in other lineages, elytral loss is a consequence of paedomorphosis, related to a specific resource‐allocation strategy. In many groups of beetles with reduced elytra, alternative defensive strategies can be found. This includes, for instance, aposematic coloration, chemical defence, mimicry or bioluminescence. Direct drivers of elytral loss in many groups remain unclear, and more studies are needed to understand the evolutionary background and implications of this significant morphological modification in Coleoptera.

The evolutionary history of Coleoptera (Insecta) in the late Palaeozoic and the Mesozoic

“…Densely tuberculate and incompletely sclerotized elytra with thin window punctures, today only preserved in the archostematan families Cupedidae (36 described extant species; Goczał et al, 2024) and Ommatidae (six described extant species; Goczał et al, 2024), indeed belong to the groundplan of Coleoptera in the broadest sense (e.g., Friedrich et al, 2009). This is indicated by the presence of this condition in †Tshekardocoleidae, †Permocupedidae and other extinct groups (Figure 3a-c; Boudinot et al, 2023;Ponomarenko, 1969).…”

“…Species of †Ochthebiites Ponomarenko, possibly belonging to Hydraenidae, are known from Karatau (164.7-155.7 Ma) in Kazakhstan and from the Jurassic of the Russian Federation (189.6-155.7 Ma) (Chatzimanolis, 2018). Agyrtidae (70 described extant species; Goczał et al, 2024) are represented by nine extinct species (Chatzimanolis, 2018). The agyrtid genus †Mesecanus Newton is described from Jurassic formations of Russia and China.…”

“…However, the authors discuss the phylogeny and taxonomy of the 'nitidulid' group of families without phylogenetic analysis or a consistent phylogenetic evaluation of potential apomorphies. A fossil of the small cucujoid family Cyclaxyridae (two described extant species; Goczał et al, 2024) from burmite was described by Wu et al (2018). The new species was placed in the extant genus Cyclaxyra…”

“…One of their most intriguing aspects is their extreme extant diversity. With approximately 442,000 described species, they are by far the largest group of organisms on a comparable taxonomic level (e.g., Bouchard et al, 2017;Goczał et al, 2024;Smith & Marcot, 2015;Stork et al, 2015). Consequently, an 'inordinate fondness for beetles' was ascribed to the Creator ('if he exists') by the Scottish Indian geneticist and evolutionary biologist John B.S.…”

Evolution, types, and distribution of flight control devices on wings and elytra in bark beetles

“…Our knowledge on the flight-control devices is particularly poor in the order Coleoptera (beetles). Although beetles account for about one fifth of all animal species on our planet 12 and exhibit spectacular flight apparatus modification (transformation of fore wings into hardened elytra, together with the development of a sophisticated hind wing folding mechanism), all current knowledge on flight-related mechanosensors located on wings in this order is confined to a morphological analysis of a single species Dytiscus marginalis Linnaeus (Dytiscidae) from the first half of the twentieth century 13 , 14 . Although the distribution of flight-related mechanosensors on beetles' elytra has been recently investigated morphologically in several species (but not in bark beetles) 10 , 15 , 16 , existing studies have not taken into account the phylogenetic background and were thus not suited for evaluating mechanosensor diversity patterns across larger monophyletic group of beetles.…”