Diversity in the weapons of sexual selection: horn evolution in the beetle genus Onthophagus (Coleoptera: Scarabaeidae)

Both ornaments and weapons of sexual selection frequently exhibit prolific interspecific diversity of form. Yet, most studies of this diversity have focused on ornaments involved with female mate choice, rather than on the weapons of male competition. With few exceptions, the mechanisms of divergence in weapon morphology remain largely unexplored. Here, we characterize the evolutionary radiation of one type of weapon: beetle horns. We use partial sequences from four nuclear and three mitochondrial genes to develop a phylogenetic hypothesis for a worldwide sample of 48 species from the dung beetle genus Onthophagus (Coleoptera: Scarabaeidae). We then use these data to test for multiple evolutionary origins of horns and to characterize the evolutionary radiation of horns. Although our limited sampling of one of the world's most species-rich genera almost certainly underestimates the number of evolutionary events, our phylogeny reveals prolific evolutionary lability of these exaggerated sexually selected weapons (more than 25 separate gains and losses of five different horn types). We discuss these results in the context of the natural history of these beetles and explore ways that sexual selection and ecology may have interacted to generate this extraordinary diversity of weapon morphology.     

Is diversification in male reproductive traits driven by evolutionary trade-offs between weapons and nuptial gifts?

Many male animals have evolved exaggerated traits that they use in combat with rival males to gain access to females and secure their reproductive success. But some male animals invest in nuptial gifts that gains them access to females. Both these reproductive strategies are costly in that resources are needed to produce the weapon or nuptial gift. In closely related species where both weapons and nuptial gifts are present, little is known about the potential evolutionary trade-off faced by males that have these traits. In this study, we use dobsonflies (order Megaloptera, family Corydalidae, subfamily Corydalinae) to examine the presence and absence of enlarged male weapons versus nuptial gifts within and among species. Many dobsonfly species are sexually dimorphic, and males possess extremely enlarged mandibles that they use in battles, whereas in other species, males produce large nuptial gifts that increase female fecundity. In our study, we show that male accessory gland size strongly correlates with nuptial gift size and that when male weapons are large, nuptial gifts are small and vice versa. We mapped weapons and nuptial gifts onto a phylogeny we constructed of 57 species of dobsonflies. Our among-species comparison shows that large nuptial gift production evolved in many species of dobsonfly but is absent from those with exaggerated weapons. This pattern supports the potential explanation that the trade-off in resource allocation between weapons and nuptial gifts is important in driving the diversity of male mating strategies seen in the dobsonflies, whereas reduced male–male competition in the species producing large spermatophores could be an alternative explanation on their loss of male weapons. Our results shed new light on the evolutionary interplay of multiple sexually selected traits in animals.     

Functional significance of an unusual chela dimorphism in a marine decapod: specialization as a weapon?

The squat lobster Munida rugosa has an unusual chela dimorphism exhibited mainly by large males. Some individuals have 'arched' chelae in which there is a gap between the dactylus and the pollex when closed, and others have a 'straight' morphology in which the dactylus and pollex oppose along most of their length. Geometric morphometric analysis indicated that, compared with males, the arched morphology does not develop fully in females, so further investigation was confined to males. In males, the distal part of the chela was similar in both the forms and seemed to be adapted to hold and shred prey items. Both morphologies had a major cylindrical tooth on the inner proximal part of the dactylus, but the arched morphology had a higher and wider propodus, a greater major tooth-pollex distance and a greater force generation than the straight morphology. The findings suggest that the arched chela morphology in M. rugosa is a sexually selected trait adapted to inflict puncture wounds on opponents during agonistic interactions. The arched morphology, therefore, appears to have evolved in males by means of sexual selection because it enhanced the function of the chela as a weapon, while retaining functionality for feeding.     

The fitness advantage of a high-performance weapon

Weapons used in combat between males are usually attributed to sexual selection, which operates via a fitness advantage for males with weapons of better 'quality'. Because the performance capacity of morphological traits is typically considered the direct target of selection, Darwin's intrasexual selection hypothesis can be modified to predict that variation in reproductive success should be explained by variation in performance traits relevant to combat. Despite such a straightforward prediction, tests of this hypothesis are conspicuously lacking. We show that territorial male collared lizards with greater bite-force capacity sire more offspring than weaker biting rivals but exhibit no survival advantage. We did not detect stabilizing or disruptive selection on bite-force capacity. Taken together, these results support the hypothesis that superior weapon performance provides a fitness advantage through increased success in male contests. Sexual selection on weapon performance therefore appears to be a force driving the evolution and maintenance of sexual dimorphism in head shape.  © 2009 The Linnean Society of London, Biological Journal of the Linnean Society , 2009, 96 , 840–845.     

Males that drop a sexually selected weapon grow larger testes

Costly sexually selected weapons are predicted to trade off with postcopulatory traits, such as testes. Although weapons can be important for achieving access to females, individuals of some species can permanently drop (i.e. autotomize) their weapons, without regeneration, to escape danger. We capitalized on this natural behavior to experimentally address whether the loss of a sexually selected weapon leads to increased testes investment in the leaf‐footed cactus bug, Narnia femorata Stål (Hemiptera: Coreidae). In a second experiment, we measured offspring production for males that lost a weapon during development. As predicted, males that dropped a hind limb during development grew significantly larger testes than the control treatments. Hind‐limb autotomy did not result in the enlargement of other nearby traits. Our results are the first to experimentally demonstrate that males compensate for natural weapon loss by investing more in testes. In a second experiment we found that females paired with males that lost a hind limb had 40% lower egg hatching success than females paired with intact males, perhaps because of lower mating receptivity to males with a lost limb. Importantly, in those cases where viable offspring were produced, males missing a hind limb produced 42% more offspring than males with intact limbs. These results suggest that the loss of a hind‐limb weapon can, in some cases, lead to greater fertilization success.     

Songs versus colours versus horns: what explains the diversity of sexually selected traits?

Papers on sexual selection often highlight the incredible diversity of sexually selected traits across animals. Yet, few studies have tried to explain why this diversity evolved. Animals use many different types of traits to attract mates and outcompete rivals, including colours, songs, and horns, but it remains unclear why, for example, some taxa have songs, others have colours, and others horns. Here, we first conduct a systematic survey of the basic diversity and distribution of different types of sexually selected signals and weapons across the animal Tree of Life. Based on this survey, we describe seven major patterns in trait diversity and distributions. We then discuss 10 unanswered questions raised by these patterns, and how they might be addressed. One major pattern is that most types of sexually selected signals and weapons are apparently absent from most animal phyla (88%), in contrast to the conventional wisdom that a diversity of sexually selected traits is present across animals. Furthermore, most trait diversity is clustered in Arthropoda and Chordata, but only within certain clades. Within these clades, many different types of traits have evolved, and many types appear to have evolved repeatedly. By contrast, other major arthropod and chordate clades appear to lack all or most trait types, and similar patterns are repeated at smaller phylogenetic scales (e.g. within insects). Although most research on sexual selection focuses on female choice, we find similar numbers of traits (among sampled species) are involved in male contests (44%) and female choice (55%). Overall, these patterns are largely unexplained and unexplored, as are many other fundamental questions about the evolution of these traits. We suggest that understanding the diversity of sexually selected traits may require a shift towards macroevolutionary studies at relatively deep timescales (e.g. tens to hundreds of millions of years ago).     

The Evolution of Positive Allometry of Weaponry in Horned Lizards (Phrynosoma)

The allometry of weapons and other conspicuous structures has long fascinated biologists. Recently, a debate has arisen about the roles of sexual and natural selection in driving the allometry of structures, with some authors suggesting that positive allometry is exclusively the result of sexual selection. Although some studies, often focusing on weapons, support this hypothesis, others have shown that many naturally selected structures also exhibit positive allometry. We study the allometry of the cranial horns in 14 species of horned lizards (Phrynosoma). These horns are purely defensive weapons and so are under natural, as opposed to sexual, selection. In almost all cases, the length of these horns is positively allometric through ontogeny (intraspecifically) and through evolution (interspecifically). Our findings demonstrate that positive allometry can be the product of natural selection, suggesting that the function of structures may dictate allometry and not the type of selection. For example, it is possible that weapons tend to be positively allometric. Our findings also suggest that longer horns may arise through the prolongation of horn growth, and that the horns that are most effective at defense from predators attacking a lizard from above are integrated with one another. Finally, we find that species with unusual horn morphologies have diverged from other species in their horn allometries, indicating that the evolution of morphological diversity can be mediated through the evolution of allometry.     

Do reproductive characteristics of the species explain differences in the investment in weapon size present in males?

Sexually selected traits, such as male weapons, are highly variable in shape and size across species. However, little is known about the mechanisms that may govern this variation. Because males with greater investment in weapon size tend to win more fights, but also pay higher costs related to weapon development and maintenance, larger weapons should be expected only in species in which victory in male–male fights generate reproductive benefits that outweigh investment costs. Here, we hypothesized that the reproductive characteristics that increase the chances of winners to access females or to fertilize eggs will favor the evolution of larger weapons. To evaluate this hypothesis, we conducted a meta-analysis using arthropods as model organisms. To measure investment in weapon size, we gathered both Pearson correlation coefficient and the standardized (but non centralized) slope values for the relationship between weapon size and body size. We found that none of the reproductive characteristics we investigated was related to male weapon size. Thus, it seems that greater certainty of accessing a female or fertilizing female eggs with a victory does not modulate the investment in male weapon size. Perhaps the cost–benefit ratio between weapon size investment and reproductive success is not the main factor driving the variation in weapon size.     

Functional equivalence of morphologies enables morphological and ecological diversity

Diversity in organismal forms among taxa is thought to reflect distinct selection pressures across environments. The central assumption underlying this expectation is that taxa experiencing similar selection have similar response to that selection. However, because selection acts on trait function, taxa similarity in selection response depends crucially on the relationship between function and morphology. Further, when a trait consists of multiple parts, changes in function in response to selection can result from modification of different parts, and adaptation to the same environment might result in functional but not morphological similarity. Here, we address the extent to which functional and morphological diversity in masticatory apparatus of soricid shrews reflects a shared ecological characteristic of their diet type. We examine the factors limiting morphological variation across shrew species by assessing the relative contribution of trait function (biomechanics of the jaw), ecology, and phylogeny to species similarity in mandibular traits. We found that species that shared diet type were functionally but not morphologically similar. The presence of multiple semi-independently varying traits enabled functional equivalence of composite foraging morphologies and resulted in variable response to selection exerted by similar diet. We show that functional equivalence of multiple morphologies enabled persistence of differences in habitat use (e.g., habitat moisture and coverage) among species that specialize on the same diet. We discuss the importance of developmental and functional integration among traits for evolutionary diversification of morphological structures that generate equivalent functions.     

Asymmetric Forceps Increase Fighting Success among Males of Similar size in the Maritime Earwig

Extreme asymmetric morphologies are hypothesized to serve an adaptive function that counteracts sexual selection for symmetry. However, direct tests of function for asymmetries are lacking, particularly in the context of animal weapons. The weapon of the maritime earwig, Anisolabis maritima, exhibits sizeable variation in the extent of directional asymmetry within and across body sizes, making it an ideal candidate for investigating the function of asymmetry. In this study, we characterized the extent of weapon asymmetry, characterized the manner in which asymmetric weapons are used in contests, staged dyadic contests between males of different size classes, and analyzed the correlates of fighting success. In contests between large males, larger individuals won more fights and emerged as the dominant male. In contests between small males, however, weapon asymmetry was more influential in predicting overall fighting success than body size. This result reveals an advantage of asymmetric weaponry among males that are below the mean size in the population. A forceps manipulation experiment suggests that asymmetry may be an indirect correlate of a morphologically independent factor that affects fighting ability.     

Ecological and evolutionary constraints on regional avifauna of passerines in China

Strong correlations between species diversity and climate have been widely observed, but the mechanism underlying this relationship is unclear. Here, we explored the causes of the richness–climate relationships among passerine birds in China by integrating tropical conservatism and diversification rate hypotheses using path models. We found that assemblages with higher species richness southwest of the Salween–Mekong–Pearl River Divide are phylogenetically overdispersed and have shorter mean root distances (MRDs), while species-rich regions northeast of this divide (e.g., north Hengduan Mountains–south Qinling Mountains) are phylogenetically clustered and have longer MRDs. The results of the path analyses showed that the direct effect of climatic factors on species richness was stronger than their indirect effects on species richness via phylogenetic relatedness, indicating that neither tropical conservatism nor diversification rate hypotheses can well explain the richness–climate relationship among passerines in China. However, when path analyses were conducted within subregions separately, we found that the tropical conservatism hypothesis was well supported in the southwestern Salween–Mekong–Pearl River Divide, while the diversification rate hypothesis could explain the richness–climate relationship well in the northeastern divide. We conclude that the diversity patterns of passerines in different subregions of the Eastern Himalayas-Mountains of Southwest China may be shaped by different evolutionary processes related to geological and climatic histories, which explains why the tropical conservatism or diversification rate hypothesis alone cannot fully explain the richness–climate relationships.     

The tale of the shrinking weapon: seasonal changes in nutrition affect weapon size and sexual dimorphism,but not contemporary evolution

Sexually selected traits are often highly variable in size within populations due to their close link with the physical condition of individuals. Nutrition has a large impact on physical condition, and thus, any seasonal changes in nutritional quality are predicted to alter the average size of sexually selected traits as well as the degree of sexual dimorphism in populations. However, although traits affected by mate choice are well studied, we have a surprising lack of knowledge of how natural variation in nutrition affects the expression of sexually selected weapons and sexual dimorphism. Further, few studies explicitly test for differences in the heritability and mean‐scaled evolvability of sexually selected traits across conditions. We studied Narnia femorata (Hemiptera: Coreidae), an insect where males use their hind legs as weapons and the femurs are enlarged, to understand the extent to which weapon expression, sexual dimorphism and evolvability change across the actual range of nutrition available in the wild. We found that insects raised on a poor diet (cactus without fruit) are nearly monomorphic, whereas those raised on a high‐quality diet (cactus with ripe fruit) are distinctly sexually dimorphic via the expression of large hind leg weapons in males. Contrary to our expectations, we found little evidence of a potential for evolutionary change for any trait measured. Thus, although we show weapons are highly condition dependent, and changes in weapon expression and dimorphism could alter evolutionary dynamics, our populations are unlikely to experience further evolutionary changes under current conditions.     

Juvenile hormone regulates extreme mandible growth in male stag beetles

The morphological diversity of insects is one of the most striking phenomena in biology. Evolutionary modifications to the relative sizes of body parts, including the evolution of traits with exaggerated proportions, are responsible for a vast range of body forms. Remarkable examples of an insect trait with exaggerated proportions are the mandibular weapons of stag beetles. Male stag beetles possess extremely enlarged mandibles which they use in combat with rival males over females. As with other sexually selected traits, stag beetle mandibles vary widely in size among males, and this variable growth results from differential larval nutrition. However, the mechanisms responsible for coupling nutrition with growth of stag beetle mandibles (or indeed any insect structure) remain largely unknown. Here, we demonstrate that during the development of male stag beetles (Cyclommatus metallifer), juvenile hormone (JH) titers are correlated with the extreme growth of an exaggerated weapon of sexual selection. We then investigate the putative role of JH in the development of the nutritionally-dependent, phenotypically plastic mandibles, by increasing hemolymph titers of JH with application of the JH analog fenoxycarb during larval and prepupal developmental periods. Increased JH signaling during the early prepupal period increased the proportional size of body parts, and this was especially pronounced in male mandibles, enhancing the exaggerated size of this trait. The direction of this response is consistent with the measured JH titers during this same period. Combined, our results support a role for JH in the nutrition-dependent regulation of extreme mandible growth in this species. In addition, they illuminate mechanisms underlying the evolution of trait proportion, the most salient feature of the evolutionary diversification of the insects.     

Identifying a causal agent of sexual selection on weaponry in an insect

In many animal species, males do not seek females directly butinstead locate and defend sites that contain spatially or temporallylimited resources essential to female survival and reproduction.Resident males that successfully repel conspecific rivals canmate with females attracted to these resources. In theory, increasingresource value increases harem size and thus increases the opportunity(I_mates) for and strength of sexual selection on traits crucialto male resource-holding potential and mating success. I experimentallytested this hypothesis in the field using the Wellington treeweta, Hemideina crassidens (Orthoptera: Tettigonioidea: Anostostomatidae),a sexually dimorphic insect in which males use their enlargedmandibles as weapons in male–male contests over accessto females sheltering in tree cavities (galleries). By manipulatinggallery size, I showed that, compared with smaller galleries,larger galleries housed larger harems. Variation in gallerysize was an important determinant of I_mates, but contrary toexpectation, greater opportunity existed in small galleriescompared with large galleries. As predicted, male weapon sizewas under stronger directional selection in large galleriesbecause the fitness benefits were greater under these conditionscompared with small galleries. My results help explain the positiveassociation between average weapon size and average gallerysize observed within and among tree weta populations in NewZealand.     

Intrasexually selected weapons

We propose a practical concept that distinguishes the particular kind of weaponry that has evolved to be used in combat between individuals of the same species and sex, which we term intrasexually selected weapons (ISWs). We present a treatise of ISWs in nature, aiming to understand their distinction and evolution from other secondary sex traits, including from ‘sexually selected weapons’, and from sexually dimorphic and monomorphic weaponry. We focus on the subset of secondary sex traits that are the result of same‐sex combat, defined here as ISWs, provide not previously reported evolutionary patterns, and offer hypotheses to answer questions such as: why have only some species evolved weapons to fight for the opposite sex or breeding resources? We examined traits that seem to have evolved as ISWs in the entire animal phylogeny, restricting the classification of ISW to traits that are only present or enlarged in adults of one of the sexes, and are used as weapons during intrasexual fights. Because of the absence of behavioural data and, in many cases, lack of sexually discriminated series from juveniles to adults, we exclude the fossil record from this review. We merge morphological, ontogenetic, and behavioural information, and for the first time thoroughly review the tree of life to identify separate evolution of ISWs. We found that ISWs are only found in bilateral animals, appearing independently in nematodes, various groups of arthropods, and vertebrates. Our review sets a reference point to explore other taxa that we identify with potential ISWs for which behavioural or morphological studies are warranted. We establish that most ISWs come in pairs, are located in or near the head, are endo‐ or exoskeletal modifications, are overdeveloped structures compared with those found in females, are modified feeding structures and/or locomotor appendages, are most common in terrestrial taxa, are frequently used to guard females, territories, or both, and are also used in signalling displays to deter rivals and/or attract females. We also found that most taxa lack ISWs, that females of only a few species possess better‐developed weapons than males, that the cases of independent evolution of ISWs are not evenly distributed across the phylogeny, and that animals possessing the most developed ISWs have non‐hunting habits (e.g. herbivores) or are faunivores that prey on very small prey relative to their body size (e.g. insectivores). Bringing together perspectives from studies on a variety of taxa, we conceptualize that there are five ways in which a sexually dimorphic trait, apart from the primary sex traits, can be fixed: sexual selection, fecundity selection, parental role division, differential niche occupation between the sexes, and interference competition. We discuss these trends and the factors involved in the evolution of intrasexually selected weaponry in nature.     

Sexual Selection,Ontogenetic Acceleration,and Hypermorphosis Generates Male Trimorphism in Wellington Tree Weta

Strong sex-specific selection on traits common to both sexes typically results in sexual dimorphism. Here we find that Wellington tree weta (Hemideina crassidens) are sexually dimorphic in both head shape and size due to differential selection pressures on the sexes: males use their heads in male-male combat and feeding whereas females use theirs for feeding only. Remarkably, the sexes share a common ontogenetic trajectory with respect to head growth. Male head shape allometry is an extension of the female’s trajectory despite maturing two instars earlier, a feat achieved through ontogenetic acceleration and hypermorphosis. Strong sexual selection also favours the evolution of alternative reproductive strategies in which some males produce morphologically different weapons. Wild-caught male H. crassidens are trimorphic with regard to weapon size, a rare phenomenon in nature, and weapon shape is related to each morph’s putative mating strategy.     

Harder,better, faster,stronger: Weapon size is more sexually dimorphic than weapon biomechanical components in two freshwater anomuran species

Sexual selection influences the evolution of morphological traits that increase the likelihood of monopolizing scarce resources. When such traits are used during contests, they are termed weapons. Given that resources are typically linked to monopolizing mating partners, theory expects only males to bear weapons. In some species, however, females also bear weapons, although typically smaller than male weapons. Understanding why females bear smaller weapons can thus help us understand the selective pressures behind weapon evolution. However, most of our knowledge comes from studies on weapon size, while the biomechanics of weapons, such as the size of the muscles, efficiency, and shape are seldom studied. Our goal was to test if the theoretical expectations for weapon size sexual dimorphism also occur for weapon biomechanics using two aeglid crab species. Males of both species had larger claws which were also stronger than female claws. Male claws were also more efficient than females' claws (although we used only one species in this analysis). For weapon shape, though, only one species differed in the mean claw shape. Regarding scaling differences, in both species, male claws had higher size scaling than females, while only one species had a higher shape scaling. However, male weapons did not have higher scaling regarding strength and efficiency than females. Thus, males apparently allocate more resources in weapons than females, but once allocated, muscle and efficiency follow a similar developmental pathway in both sexes. Taken together, our results show that sexual dimorphism in weapons involves more than differences in size. Shape differences are especially intriguing because we cannot fully understand its causes. Yet, we highlight that such subtle differences can only be detected by measuring and analysing weapon shape and biomechanical components. Only then we might better understand how weapons are forged.     

Dual role of plasma membrane electron transport systems in defense

Because oxidative stress is one of the main sources of severe cellular damage, cells have different defense weapons against reactive oxygen species. Ubiquitous plasma membrane redox systems play a role in defense against oxidative stress damage. On the other hand, a tightly controlled and localized production of reactive oxygen species by a plasma membrane NADPH oxidase can be used as a potent microbicidal weapon. This dual, prooxidant and antioxidant role of plasma membrane electron transport systems in defense is studied and discussed.     

Dual Role of Plasma Membrane Electron Transport Systems in Defense

Bcause oxidative stress is one of the main sources of severe cellular damage, cells have different defense weapons against reactive oxygen species. Ubiquitous plasma membrane redox systems play a role in defense against oxidative stress damage. On the other hand, a tightly controlled and localized production of reactive oxygen species by a plasma membrane NADPH oxidase can be used as a potent microbicidal weapon. This dual, prooxidant and antioxidant role of plasma membrane electron transport systems in defense is studied and discussed.     

On the evolution of reproductive restraint in malaria

Malaria is one of the leading causes of death among infectious diseases in the world, claiming over one million lives every year. By these standards, this highly complex parasite is extremely successful at generating new infections. Somewhat surprisingly, however, many malaria species seem to invest relatively little in gametocytes, converting only a small percentage of circulating asexual parasite forms into this transmissible form. In this article, we use mathematical models to explore three of the hypotheses that have been proposed to explain this apparent 'reproductive restraint' and develop a novel, fourth hypothesis. We find that only one of the previous three hypotheses we explore can explain such low gametocyte conversion rates, and this hypothesis involves a very specific form of density-dependent transmission-blocking immunity. Our fourth hypothesis also provides a potential explanation and is based on the occurrence of multiple infections and the resultant within-host competition between malaria strains that this entails. Further experimental work is needed to determine which of these two hypotheses provides the most likely explanation.