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Variation in horn morphology and fighting styles in rhinoceros beetles. ( A ) Trypoxylus dichotomus males have a long, forked head horn that is used like a pitchfork to lift and twist opponents off tree trunks during fights. ( B ) Dynastes hercules males have a long head horn and long thoracic horn that are used together similar to pliers to lift, squeeze, and then toss opponents to the ground. ( C ) Golofa porteri males have a long, slender head horn that is used similar to a fencing sword to both lift opponents off narrow shoots and push them sideways off balance. Vectors represent the typical forces experienced by horns during fights: vertical bending (red), lateral bending (blue), twisting (green). Illustrations by David J. Tuss.
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Animal weapons are among nature’s most diverse structures. Intuitively, species have different types of weapons because they fight in different ways, yet no studies have directly tested whether weapons perform better at the animals’ own style of fighting than they do at others. We constructed biomechanical models of the horns of differ...
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... in this study, Trypoxylus dichoto- mus, Golofa porteri, and Dynastes hercules, have very different horn morphologies and distinct fighting styles. In all three spe- cies, males insert their head horn underneath an opponent to pry him from the substrate, but the specific maneuvers used, and therefore the forces the horns experience, are different (Fig. 1). The head horns of Trypoxylus males are long and forked and function like a pitchfork, prying and twisting opponents off the trunks and branches of trees (24,27). The head horns of Dynastes males are long and work together with a long thoracic horn like the pincer arms of pliers to lift and squeeze opponents off of trees and toss them ...
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Sexual selection has equipped male rhinoceros beetles with large horns on their head and prothorax to aid in battle over access to females. Horns are used to pry and dislodge opponents from resource sites that attract females, so an optimal horn should be able both to withstand the high stresses imposed during fights, and to resist deflection in re...
Citations
... However, since weapons are also used in an offensive manner, there is selection on weapons to functionally withstand the forces used when attacking (e.g. McCullough, 2014;McCullough et al., 2014). Thus, it can become challenging to tease apart the role that differing selective pressures have on the material properties, and ultimately the damage resistance, of a weapon when it is used in both an offensive and defensive manner (e.g. ...
... Overall, incorporating a comparison between sexual and nonsexual traits can elucidate different mechanisms driving hypermetric scaling within species, and demonstrates why the existence of positive allometry on its own should not be evidence of sexual selection.A further drawcard to examining allometry among brentine weevils is that we were able to characterise trait exaggeration in head size across two modes (length and width), suggesting diverse ways in which males use their heads as weapons. Previous work using finite element modelling found that the male weapons of different rhinoceros beetle species are structurally adapted for use in different fighting styles specific to each species, whether it be for lifting, pushing, or squeezing an opponent(McCullough et al., 2014). For brentine weevils, the goal of a contest is to remove rivals from the tree logs that females use for oviposition. ...
Understanding variation in trait allometry and the drivers of variation in sexually selected traits is a major theme in evolutionary biology. The static allometries of sexually selected traits are often positive due to disproportional investment by large individuals into trait size. Comparative studies of weapon allometry are rare, and typically focus on variation along a single dimension (e.g. length), despite weapons often diverging dramatically in shape. Furthermore, studies predominantly focus on groups where weapons have evolved as novel structures (e.g. horns), despite most weapons arising from modifications of existing structures.
We test the hypothesis that sexual selection drives variation in static allometry using a phylogenetic comparative approach with 59 brentine weevil species showing remarkable variation in trait exaggeration and sexual size dimorphism (SSD).
Contrasting two dimensions of head size exaggeration (a sexually selected trait) and elytron length (a nonsexual trait), positive static allometry was common across both measures of male head size, but not females, and there was positive covariance between male head static allometry and SSD across species. Positive static allometry for male elytron length was less common, but did show positive covariance with SSD, possibly due to the function of wings as compensatory structures for bearing large weapons.
Our findings support the hypothesis that sexual selection drives the evolution of allometries both within and among species, and that the modification of existing structures to be used as weapons does not limit the potential for positive static allometry.
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... Furthermore, it is important to consider that diversity in animal weapons extends beyond what we can easily see and measure. For example, a functional weapon requires more than morphological expansions and other modifications (Lailvaux & Irschick, 2006;McCullough et al., 2014). Indeed, selection should also act on the internal structure and material properties of weapons to enhance functionality and reduce structural failure. ...
Sexually selected weapons, such as the antlers of deer, claws of crabs, and tusks of beaked whales, are strikingly diverse across taxa and even within groups of closely related species. Phylogenetic comparative studies have typically taken a simplified approach to investigating the evolution of weapon diversity, examining the gains and losses of entire weapons, major shifts in size or type, or changes in location. Less understood is how individual weapon components evolve and assemble into a complete weapon. We addressed this question by examining weapon evolution in the diverse, multi-component hind-leg and body weapons of leaf-footed bugs, Superfamily Coreoidea (Hemiptera: Heteroptera). Male leaf-footed bugs use their morphological weapons to fight for access to mating territories. We used a large multilocus dataset comprised of ultraconserved element loci for 248 species and inferred evolutionary transitions among component states using ancestral state estimation. Our results suggest that weapons added components over time with some evidence of a cyclical evolutionary pattern — gains of components followed by losses and then gains again. Further, our best estimate indicated that certain trait combinations evolved repeatedly across the phylogeny, suggesting that they function together in battle or that they are genetically correlated. This work reveals the remarkable and dynamic evolution of weapon form in the leaf-footed bugs and provides insights into weapon assembly and disassembly over evolutionary time.
... Scarab beetles represent one of the most diverse beetle lineages, where variations in size, shape, colour and pattern of adult secondary structures and body designs are apparent (Ahrens et al., 2014;Emlen et al., 2006;Gunter et al., 2016;Huang, 2016;Rowland & Miller, 2012). The diversity of adult male horns in scarab beetles, weapons for male-male competition and perhaps antipredator devices (Beebe, 1947;Jarman & Hinton, 1974;McCullough et al., 2014) have been intensively studied in the past two decades, where the genetic factors involved in the development of the horns have been identified in multiple lineages (e.g. in dung beetles and rhinoceros beetles; Emlen et al., 2006;Moczek & Rose, 2009;Ohde et al., 2018). However, the evolutionary history of the loci involved in male horn diversification has yet to be systematically studied among distantly related taxa, for example, from a phylogenetic perspective, or among closely related taxa, for example, from a population genetic perspective. ...
Beetles, despite their remarkable biodiversity and a long history of research, remain lacking in reference genomes annotated with structural variations in loci of adaptive significance. We sequenced and assembled high-quality chromosome-level genomes of four Hercules beetles which exhibit divergence in male horn size and shape and body colouration. The four Hercules beetle genomes were assembled to 11 pseudo-chromosomes, where the three genomes assembled using Nanopore data (Dynastes grantii, D. hyllus and D. tityus) were mapped to the genome assembled using PacBio + Hi-C data (D. maya). We demonstrated a striking similarity in genome structure among the four species. This conservative genome structure may be attributed to our use of the D. maya assembly as the reference; however, it is worth noting that such a conservative genome structure is a recurring phenomenon among scarab beetles. We further identified homologues of nine and three candidate-gene families that may be associated with the evolution of horn structure and body colouration respectively. Structural variations in Scr and Ebony2 were detected and discussed for their putative impacts on generating morphological diversity in beetles. We also reconstructed the demographic histories of the four Hercules beetles using heterozygosity information from the diploid genomes. We found that the demographic histories of the beetles closely recapitulated historical changes in suitable forest habitats driven by climate shifts.
... The unusual, triangular cross-sectional shape of this horn is also consistent with a history of selection for strong prying forces because it specifically resists buckling when the horn is lifted-even when horns are twisted during lifting, as occurs often given the ''pitchfork'' widening at the tip of this horn. 65,131 Consequently, any evolutionary increases in horn length that weakened male horn lifting strength (the paradox of the weakening combatant) could have negatively impacted male fight success in ways that offset the signaling advantages of an ever longer horn, potentially leading to the evolution of compensatory traits that restored strength to these weapons. ...
... Battles take place on the trunks of host trees, with males inserting their head horn under the prothorax of an opponent and attempting to scoop the rival off of the tree. Biomechanical studies of horn morphology indicate that the shape of the horn, particularly the triangular cross-section of the base of the horn, resists buckling when twisted and is well suited to the nature of the battles in this species 10 . ...
... Six modules represent embryonic expression patterns (Figs. 3c, S4, module [8][9][10][11][12][13]. Genes contained in the module 13 exhibited a constant pattern of expression from middle to late stages. ...
The Japanese rhinoceros beetle Trypoxylus dichotomus is a giant beetle with distinctive exaggerated horns present on the head and prothoracic regions of the male. T. dichotomus has been used as a research model in various fields such as evolutionary developmental biology, ecology, ethology, biomimetics, and drug discovery. In this study, de novo assembly of 615 Mb, representing 80% of the genome estimated by flow cytometry, was obtained using the 10 × Chromium platform. The scaffold N50 length of the genome assembly was 8.02 Mb, with repetitive elements predicted to comprise 49.5% of the assembly. In total, 23,987 protein-coding genes were predicted in the genome. In addition, de novo assembly of the mitochondrial genome yielded a contig of 20,217 bp. We also analyzed the transcriptome by generating 16 RNA-seq libraries from a variety of tissues of both sexes and developmental stages, which allowed us to identify 13 co-expressed gene modules. We focused on the genes related to horn formation and obtained new insights into the evolution of the gene repertoire and sexual dimorphism as exemplified by the sex-specific splicing pattern of the doublesex gene. This genomic information will be an excellent resource for further functional and evolutionary analyses, including the evolutionary origin and genetic regulation of beetle horns and the molecular mechanisms underlying sexual dimorphism.
... The Hercules beetles (Dynastes MacLeay 1819, Coleoptera; Scarabaeidae) show remarkable phenotypic variation across species, where the variation has been hypothesized to be adaptive (particularly the body coloration and the male horn shape; Hinton and Jarman 1973;Jarman and Hinton 1974;Morón 1987;McCullough et al. 2014;Huang and Knowles 2016;Huang 2016). The adaptive phenotypic variation observed among species can even be found within a species (Morón 1987;Moctezuma and Sánchez-Huerta 2018). ...
... We argue that the Hercules beetles can become a model system to understand repeated and parallel phenotypic evolutions. The phenotypic diversity in beetles and the diverse lifehistory characteristics have attracted the attention of generations of evolutionary biologists (Beebe 1947;Emlen 2001;McCullough et al. 2014). The Hercules beetle was among the first series of scarab beetles named by Linné (Krell et al. 2012). ...
Although hybridization may complicate taxonomic practices, it can be common between animal species. Animal hybridization not only can help with generating phenotypic and species diversity in nature, but also with understanding the genetic and genomic basis of phenotypic evolution in the laboratory. We assessed the genetic composition of captive bred F1 hybrids between two Hercules beetle species using mitochondrial CO1 and nuclear loci from a double-digest restriction-site associated DNA sequencing (ddRADseq) library. We showed that the F1 hybrids were genetically clustered with samples from the maternal species, D. grantii, based on CO1 data. Nuclear genome data, on the other hand, clearly showed that the F1 individuals were genetically intermediate between D. maya, the paternal species, and D. grantii, based on a principal component analysis. Our results also revealed that sampling design may have a major impact on the inferred genetic structure and hybrid individuals using ddRADseq data sets. We discuss the importance and potential from studying the genomics of this hybrid progeny in terms ofunderstanding the origin and maintenance of both intraspecific and interspecific phenotypic divergence and convergence.
... Comparative biomechanics contributes diverse, foundational tools for measuring functional performance and its underlying mechanisms (Lauder, 1991;Biewener, 1992Biewener, , 2002Drucker and Lauder, 1999;Ashley-Ross and Gillis, 2002;Westneat, 2003;Brainerd et al., 2010;Vogel, 2013;McCullough et al., 2014;McInroe et al., 2016;Ilton et al., 2018). By evaluating the capacity of organisms (or their structures) to produce or resist forces that contribute to movement, either by parts of the body or of the whole body through the environment, biomechanical studies provide opportunities for critical insights into why some individuals (or species) execute tasks better or worse than others under specified conditions. ...
The functional capacities of animals are a primary factor determining survival in nature. In this context, understanding the biomechanical performance of animals can provide insight into diverse aspects of their biology, ranging from ecological distributions across habitat gradients to the evolutionary diversification of lineages. To survive and reproduce in the face of environmental pressures, animals must perform a wide range of tasks, some of which entail tradeoffs between competing demands. Moreover, the demands encountered by animals can change through ontogeny as they grow, sexually mature or migrate across environmental gradients. To understand how mechanisms that underlie functional performance contribute to survival and diversification across challenging and variable habitats, we have pursued diverse studies of the comparative biomechanics of amphidromous goby fishes across functional requirements ranging from prey capture and fast-start swimming to adhesion and waterfall climbing. The pan-tropical distribution of these fishes has provided opportunities for repeated testing of evolutionary hypotheses. By synthesizing data from the lab and field, across approaches spanning high-speed kinematics, selection trials, suction pressure recordings, mechanical property testing, muscle fiber-type measurements and physical modeling of bioinspired designs, we have clarified how multiple axes of variation in biomechanical performance associate with the ecological and evolutionary diversity of these fishes. Our studies of how these fishes meet both common and extreme functional demands add new, complementary perspectives to frameworks developed from other systems, and illustrate how integrating knowledge of the mechanical underpinnings of diverse aspects of performance can give critical insights into ecological and evolutionary questions.
... This increased fluctuating asymmetry stems from directional selective pressure on the weapon, which induces genetic stress and developmental instability (Møller, 1992;Manning and Chamberlain, 1993). Sexual selection mediated through fighting also appears to drive exceptional diversification of weapon shapes, even among closely-related weapon-bearing taxa (Lundrigan, 1996;Caro et al., 2003;McCullough et al., 2014;Emberts et al., 2021). Lastly, sexually selected weapons tend to show positive evolutionary allometry with body size, thus large-bodied species tend to possess disproportionally larger weapons (Gould, 1973;Kodric-Brown et al., 2006). ...
From dissuading predators to gaining an edge on intraspecific rivals, animals have evolved weapons to meet various needs. Those with the most extreme weapons often use them to battle conspecifics, but some weapons defend against predation and others signal prowess to prospective mates and rivals. Many fishes have evolved armaments, but humans rarely observe these structures in action due to the inaccessibility of many weapon-bearing fish species. For example, how sculpins use the diverse horn-like spines that project from their head remains a mystery. We deduced the function of the weaponized preopercle in the 16 species of sculpins in the subfamily Oligocottinae by determining whether they exhibit three well-documented hallmarks of offensive weapons in terrestrial animals: ontogenetic change, sexual dimorphism, and fluctuating asymmetry. Geometric morphometrics of micro-computed tomography (lCT) scans show no sexual dimorphism in preopercular spine shape but reveal phylogenetically widespread ontogenetic shape change. Fluctuating asymmetry is low to moderate across species. Taken together, these results suggest that despite their varied reproductive habits, frequent territoriality, and possession of weapons that resemble bovid horns, oligocottine sculpins evolved their spines primarily to defend against predators.
... McCullough et al. (28) identified three modes of combat for structures of dynastines: shoveling/prying, grasping, and fencing. While the end goal of all fights is to dislodge or overturn the opponent, the slight differences in how this is achieved place specific constraints on both the shape of, and variation in, the cephalic and pronotal horns of the beetles employing them (29). ...
... While the end goal of all fights is to dislodge or overturn the opponent, the slight differences in how this is achieved place specific constraints on both the shape of, and variation in, the cephalic and pronotal horns of the beetles employing them (29). In order to test our hypothesis that the fork structure in Walliserops was used in combat, we used landmark-based geometric morphometrics to quantify and measure the shape and variation in the weapons of the beetles representing the diagnostic morphologies of the three combat behaviors proposed by McCullough et al. (28). These and the exemplar morphologies were then compared to the putative weapon of the trilobite W. trifurcatus. ...
... We suggest that the variation in shape for each taxon and groupings seen in the PCA and ANOVA analyses reflect the three combat strategies of shoveling/prying, grasping, and fencing/lifting as outlined by McCullough et al. (28). The most significant correlation to function seems to be in the curvature of the cephalic weapon. ...
The Devonian trilobite Walliserops carries a remarkable anterior cephalic trident posing a challenge to functional interpretation. A unique teratological specimen of Walliserops trifurcatus showing four, rather than three tines, is inconsistent with possible hypotheses connecting the trident to feeding techniques and suggests a sexually selected function. Malformations in a variety of living organisms support this conclusion. Morphometric comparisons to similar structures used for intraspecific combat in dynastine beetles show that the trident occupies a comparable shape space consistent with the hypothesis that it was a sexual combat weapon, the oldest reported example of its kind. This lends further credibility to the idea that some trilobites may have been strongly sexually dimorphic.
