Captain America without the shield: elytra loss and the evolution of alternative defence strategies in beetles

The formation of protective covers called elytra is considered to be a crucial morphological adaptation that has greatly supported the extraordinary radiation of beetles. However, in some beetle lineages, a reduction of elytra has occurred. Evolutionary consequences of this mysterious biological phenomenon have never been systematically discussed. In this study, a suggestive analogy to pop culture was used to illustrate a wide range of incredible defence strategies that can be found in several groups of beetles characterised by reduced elytra. This might include for instance: the hardening of the abdominal tergites, Batesian mimicry, aposematic coloration, chemical protection or defensive bioluminescence. It is not clear whether these new inventions have evolved as a direct response to the elytra loss, but it is very likely that the alternative defence strategies, common in brachelytrous beetles, might compensate for the loss of the primary protective structures. The use of suggestive analogies to pop culture icons, constitutes a promising tool for scientists to construct new theoretical templates, as well as to communicate and promote their recent findings, bridging the gap between researchers and the public.


Introduction
Captain America (sensu Steve Rogers (Johnston 2011)) is considered to be one of the most popular and oldest concepts of superhero in pop culture (Wright 2003). His key attribute is the large, almost uncrushable shield that allows him to protect himself against most types of physical attack and other external loads, and it can also be used as an improvised offensive weapon (Johnston 2011). We can consider a hypothetical situation when Captain America loses his key feature. Would he still be a superhero without his shield? Or rather, along with the loss of the shield-would he also lose his key advantages over opponents and competitors? This seemingly ridiculous question might be quite useful as a thought experiment to help in understanding the consequences of the mysterious biological phenomenon-loss of large, protective shields (elytra) in several, distantly related groups of beetles (Coleoptera).
Beetles are truly superheroes within the Animal Kingdom. When considering the number of species as a measure of evolutionary success-beetles are the undisputed winners of this ancient race. With more than 380,000 described extant species, Coleoptera encompasses almost a quarter of all known animal species on Earth (Beutel et al. 2016). It is widely considered that one particular morphological adaptation-the transformation of soft, flight forewings into hardened, rigid shields called elytra, was a key step in the evolutionary history of this taxa, which has largely supported the extraordinary beetle radiation (Crowson 1981;Grimaldi and Engel 2005;Beutel et al. 2016;Goczał and Beutel 2023). Beetle elytra were likely already formed in the Carboniferous period (Boudinot et al. 2022;Luo et al. 2022;Goczał and Beutel 2023) through the long, gradual process of progressive forewings sclerotization achieved by the co-option of a group of genes moderating body sclerotization to the wing gene network (Tomoyasu et al. 2009;Fédrigo and Wray 2010). Formation of elytra has provided primitive beetle ancestors with lots of new opportunities. It has allowed them to explore new niches, especially cryptic subcortical microhabitat, which has resulted in a reduction of competition and predation pressure, protection against dehydration, and gaining access to new food resources (Grimaldi and Engel 2005;Beutel et al. 2016). Studies on modern beetles 1 3 have provided evidence that the presence of elytra provides a wide range of benefits. Elytra not only mechanically protect the delicate internal organs of the abdomen and hind wings but are also involved in many additional functions including body thermoregulation, water saving, flight, swimming, water harvesting, mimicry and camouflage or acoustic communication (Sun and Bhushan 2012;Linz et al. 2016;Goczał and Beutel 2023). In the face of these highly adaptive benefits arising from the presence of elytra-it is very interesting why elytra reduction has occurred in some beetle lineages?
The phenomenon of elytra loss is called brachelytry (Jolivet 2005), and its drivers and underscored mechanisms remain largely unexplored (Goczał et al. 2018;Yamamoto 2019). So far, it is only known that elytra loss has independently occurred with a different intensity several times in the evolutionary history of beetles, and most probably it had different drivers in different groups (Goczał et al. 2018;Kim et al. 2020). There are many potential explanations of elytra loss, including especially increased manoeuvrability or resource saving (Jolivet 2008;Goczał et al. 2018;Yamamoto 2019;Kim et al. 2020), but none of them have ever been empirically tested. Another question related to this mysterious phenomenon, is how brachelytrous beetles can successfully withstand selection pressure without their key attribute providing so many significant advantages?

Armour instead of a shield
When Captain America (sensu Steve Rogers (Johnston 2011)) loses his most prevalent disc-shaped shield made out of extremely resistant fictional metal-vibranium, he often uses an improvised buckler composed of other less durable metals, e.g. steel (Waid et al. 1998). A similar strategy has evolved in the large rove beetle family (Staphylinidae). In the vast majority of rove beetles, shields are markedly shortened and most of the abdomen remains uncovered, and, thus, potentially vulnerable to physical attacks. It has been shown, however, that many rove beetle lineages have overcome this issue through improved sclerotization of the exposed abdominal (upper) tergites (plates) (Grimaldi and Engel 2005;Parker 2017;Kim et al. 2020). Thick cuticle layers of abdominal tergites form a kind of 'plate armour' (Fig. 1A), which is harnessed as a protective feature in place of the reduced elytra.

Smart-designed flight apparatus
The future successor of Captain America in the Disney Plus series 'The Falcon and the Winter Soldier' (Skogland 2021), previously known as Falcon, possesses an improved uniform, which allows him to fly (Skogland 2021). The ability of active flight also serves as an effective defensive strategy in many groups of beetles, which are able to escape quickly using their membranous, hind wings. In the vast majority of Coleoptera, elytra serve as very effective protective covers for the vulnerable hind wings, which are folded and hidden beneath the elytra when not in use. However, the largely shortened elytra of rove beetles were too short to cover oneway folded flight wings. The evolutionary response to this obstacle was the development in this group of a unique, sophisticated 2-way asymmetric wing folding mechanism (Fig. 1A), which allows rove beetles to fold their hind wings in a specific 'origami style', and therefore the wings can still be fully covered even by very short elytra (Saito et al. 2014;Parker 2017).

Deterrent uniforms
Every superhero, including Captain America, has a unique uniform, covered with characteristic symbols and colours. It generates a kind of social information, regarding the potential risk of interaction with the individual possessing a particular type of uniform. This can effectively discourage some potential opponents from taking aggressive actions. Within the Animal Kingdom, it has been demonstrated many times that prey can use social information to avoid predators (Hämäläinen et al. 2022). This strategy can also be found within some groups of soldier beetles (Cantharidae), e.g. in genus Chauliognathus (Fabricius) or soft-winged flower beetles (Melyridae), e.g. in genus Balanophorus Macleay ( Fig. 1B) with shortened elytra. The warning, bright coloration of their body and elytra, constitutes social information suggesting that beetles are toxic or unpalatable, which might effectively deter potential predators.

Mimicry
There is also a group of beetles with reduced elytra and exposed hind wings. Such examples might be found in the subfamily Necydaline (whole members) or Cerambycinae (e.g. tribe Molorchini, Hesthesini) of the longhorn beetles (Cerambycidae). In this case, most of the hind wing remains unprotected, which leads to the question of how these insects might protect their vulnerable hind wings and exposed abdomen against predators? There is a long list of superheroes who can change their physical appearance (e.g. the villain Chameleon from Marvel Comics who first appeared in The Amazing Spider-Man #1 (Lee et al. 1963)), deceptively resembling dangerous characters. A closer look at the general appearance of the above-mentioned longhorn beetles reveals that they constitute brilliant examples of a mimicry strategy (Švácha and Lawrence 2014), confusingly resembling wasps (e.g. genus Necydalis Linneaus or genus Hesthesis Newman, Fig. 1C). The similarity to the potentially dangerous (venomous) insects may, therefore, serve as an effective antipredator defence strategy, and the exposure of hind wings might be an important part of this biological masquerade.

Chemical repellents
Another possible option to withstand opponents' pressure in the face of the loss of a key protective structure is a development of a completely new active defence strategy. It is not an  (Skogland 2021) and starts to wield the vibranium Captain America shield (Skogland 2021). In many cases, dangerous visual appearance might not be enough to discourage potential enemies. The ability to produce and release repelling or unattractive substances, therefore might be a more effective method in deterring opponents. The fictional character called Odiphus (Stinkor), known from He-Man and the Masters of the Universe, has a unique ability to release a toxic odour from his body (Hartle 2002). A similar defence can be identified in some groups of beetles that have lost their shields. In many groups of rove beetles, the specific defensive glands can be found at the end of the abdomen (Kim et al. 2020) (Fig. 1A). When the beetle is attacked, it releases a defensive secretion and directs it towards the offender through abdominal movements (Huth and Dettner 1990).

Deadly cannonade
One of the deadliest superpowers, known from the Marvel Universe, is an ability to explode, bringing fatal damage to enemies, while coming out unscathed oneself. For instance, Robert Hunter (Nitro) from Marvel Comics who first appeared in the in Captain Marvel #34 (Englehart and Starlin 1974), has an ability to self-explode and recover afterward (Englehart and Starlin 1974). Even this unique ability can be found in some specific groups of beetles with abbreviated elytra. In the flanged bombardier beetles (Carabidae: Paussinae) and the crepidogastrine bombardier beetles (Carabidae: Crepidogastrini) (Fig. 1D) two highly reactive chemical components are produced and stored separately in the special chambers within the abdomen. When the insect is disturbed, both components are directed to the hardened reaction chamber, where a strongly exo-energetic oxidation reaction takes place. It generates an explosive emission of hot gases which is sprayed toward an opponent, and could even be fatal to smaller enemies.

Confusing flashes
The strategy of deterring opponents using visual signals might not only be limited to the passive forms (e.g. modification of coloration or general appearance). Several characters known from the fictional Marvel Comics multiverse (Earth-616), including Glow (Ewing et al. 2016), have an ability to bioluminescence (Ewing et al. 2016), which could effectively confuse, or even deter some potential antagonists. Similar, bizarre strategy can be found in brachelytrous males of some glowworm beetles (Phengodidae), which possess specific organs called lanterns located on the exposed part of the abdomen (Viviani and Bechara 1997). These organs generate bioluminescence bright yellow or green flashes (Fig. 1E), which might potentially constitute aposematic signals for predators (Viviani and Bechara 1997;Powell et al. 2022).

Conclusion
Although the answer to the question-how Captain America could cope with the hypothetical loss of his key attributethe shield, remains the matter of conjecture, the analysis of the consequences of a similar event-parallel loss of a key primary defensive structures-the elytra (Fig. 1F) in several groups of beetles, might provide some interesting insights into the evolutionary implications of this mysterious phenomenon. The analysis has shown that in many groups of beetles with reduced elytra, the development of new defence strategies has occurred. So far, it is not clear whether these new innovations have evolved as a direct response to the elytra loss. It might also be possible that the formation of the long elytra became redundant when more effective defence strategies had emerged. In some circumstances, the elytra shortening might even contribute to the effectiveness of novel defensive innovations. Shortened elytra in wasp-mimicking cerambycids might potentially increase the mimicry performance, and flexible, uncovered abdomen of bombardier beetles might contribute to a better targeting of chemical weapons.
This thought experiment highlights the diversity of alternative defence strategies that can be found within various groups of beetles characterised by reduced elytra (Table 1). They might encompass the building of a highly resistant exoskeleton ('an armour instead of a shield' strategy), investing in an effective dispersal device coupled with its smart-designed protective features, deterring opponents using various visual signals ('warning uniform', bioluminescent light, or through mimicking dangerous insects) or via production and secretion of repelling or even explosive substances.
Thought experiments might advance biological science in many ways (Schlaepfer and Weber 2017). This might include identifying gaps and limitations of novel theories, along with helping in the exploration of their potential implications, revealing constraints that have not yet been taken into account, or even helping in designing of empirical experiments required to verify the hypotheses (Schlaepfer and Weber 2017).
Using suggestive analogies to pop culture, as an integral part of thought experiments, might be a useful tool both from the scientific and educational perspectives. Although, the fictional universe of superheroes is a matter of the author's imagination, even this supernatural world has some predictable and consistent laws and limitations, which makes it the promising platform for constructing and initial testing of various hypotheses referring to the real world. Most supernatural powers and abilities are in fact, properties, skills and powers known from the real world, but scaled to extremes and used in a different context. Scientists might, therefore, use this fictional world as a generous source of inspiration to outline novel scientific hypotheses and theories, e.g. regarding the drivers and possible routes of evolution of extreme adaptations, such as bizarre morphological structures or unusual physiological properties of organisms. Beetles are by far the largest group of animals in the world, inhabiting most terrestrial as well as water ecosystems. This required remarkable morphological and physiological adaptations (Crowson 1981;Beutel et al. 2016), and many of them are still poorly studied. Gaining of supernatural powers and abilities by fictional characters, might be therefore, a suggestive analogy helping in the exploration of unprecedented evolutionary trajectories of Coleoptera.
Worldwide recognition of the superhero characters known from cartoons and movies, also provides great opportunity for scientists to communicate and promote their findings, and thus to increase public awareness regarding the recent discoveries in a number of fields (Brown et al. 2017;Fitzgerald 2018;Price et al. 2022). Although scientists are now obligated to communicate their results through publication in scientific journals and conference presentations, these communication channels are often impenetrable for non-scientific communities. Using suggestive analogies to the widely recognised pop culture icons, is therefore, a promising tool, which can be applied to explain to the wider audience the recent findings regarding even complex natural phenomena (Brown et al. 2017;Fitzgerald 2018;Price et al. 2022). Last but not least, using the fascinating superhero genre to explain biological processes, might be an effective tool for teachers and educators, improving the effectiveness of students' learning (Brown et al. 2017;Fitzgerald 2018;Price et al. 2022). This approach might also effectively encourage children and students to become more interested in scientific advances, by simply showing them that the real world is often much more surprising and bizarre than the best fictional universe.
Acknowledgements I like to thank Stephen B. Heard and two anonymous reviewers for their valuable comments and suggestions on the earlier version of the manuscript. This study was financially supported by the Ministry of Science and Higher Education of the Republic of Poland within the framework of statutory (SUB/040013-D019) funds for the Faculty of Forestry, University of Agriculture in Krakow.
Author contributions J.G. Conceptualized the study, wrote the manuscript and prepared figures Data availability Not applicable.

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