Costly sexual dimorphism in Cyclommatus metallifer stag beetles

Abstract

Summary1. In many animal species, male armature has evolved through sexual selection. This male weaponry can increase reproductive success, but only if the owner overcomes the associated costs. 2. Male stag beetles bear one of the most extreme examples of male weaponry: their mandibles can be almost as long as their own body. We question whether the armature of male Cyclommatus metallifer negatively affects terrestrial locomotion (stability and cost). If so, we investigate whether these effects are potentially compensated by morphological and/or behavioural features, as seen in other specialized insect species. Conspecific females are used to represent the non-dimorphed condition. 3. The presence of the huge male mandibular apparatus shifts the body centre of mass (bCOM) anteriorly. Concomitantly, the male fore limbs are 28% longer and are systematically positioned in a more anterior angular sector than in females. Thus, the rostral border of the support area of the leg tripod also moves forward. This suggests a stability enhancing mechanism. However, in contrast to load-carrying ants, the anteriorly placed bCOM still creates two pronounced statically instable periods each locomotor cycle. 4. Due to the static instability, males must adjust their locomotor behaviour: they walk at higher cycle frequencies when compared to females of the same size, to ensure they proceed to the next stance before bumping to the ground with their heavy heads. 5. Contrary to other specialized load-carrying insect species, the (muscle) mass specific mechanical cost of transport of males exceeds that of females by 40%. 6. Since neither stability nor cost of transport benefit from the male forelimb size and positioning, their role in guaranteeing adequate terrestrial locomotion while carrying an enlarged mandibular apparatus seems doubtful. Instead, the long limbs are themselves functional in fights, by pitching the body upwards in order to throw opponents backwards. 7. The oversized male stag beetle armature comes at high ecological costs: locomotion economics as well as stability clearly suffer from the large mandibles. The observed limb length dimorphism does not prevent this, but should probably be considered part of sexual selection, rather than a compensation for its consequences.

Latitudinal cline in weapon allometry and phenology of the European stag beetle

“…The advantages of bearing enlarged weapons becomes particularly evident during stag beetles male-male interaction, giving an enhanced capacity for dislodging the opponent, both in interspecific and intraspecific contests (Hongo andOkamoto 2013, Lagarde et al 2005), thus shortening the battle duration (Goyens et al 2015a) and finally resulting in increased mating opportunities. However, exaggerated mandibles can be costly in terms of impairing locomotion and stability (Goyens et al 2015b) and constraining flight ability (Goyens et al 2015c). Despite the great investment in SSC by major males, Romiti et al (2016) suggested that functional constraints, (for example, enhanced mechanical stress and reduced flight performance), may have shaped the mandibles of larger L. cervus males.…”

Finite-element modelling reveals force modulation of jaw adductors in stag beetles

“…However, females (as a proxy for the hypothetical non-dimorphic male; cf. [10,11]) bite 66% less forcefully than males do at the medial protrusions (even after size-normalization, [10]). Therefore, male tip biting may still be considered 'forceful' biting, yet limited due to trade-offs between structural weight and locomotion.…”

Cost of flight and the evolution of stag beetle weaponry

“…The equilibrating external forces and moments needed to maintain this steady state can derive only from the wings and must be considered as the net effect (in terms of forces and moment transfer) from the wings to the body as averaged over a wing beat cycle. These net forces and moments apply on the rigid body almost vertically above the experimentally determined position of the body centre of mass [10]. Horizontal and vertical forces (wing, aerodynamic and gravity) must cancel each other out to proceed in a steady horizontal manner (figure 2).…”

“…The non-dimorph state is represented by the scaled female morphology, because the male and female morphology is very alike in stag beetle species without sexual dimorphism [10,22] ( figures 1 and 4a,c,d). The non-dimorph model was scaled in such a way that the posterior body part (meso-and metathorax þ abdomen) was as large as in the complete model [10]. For both the without mandibles and non-dimorph model, the total mass was reduced to conform to our weight measurements (on fresh material with an analytical microbalance; MT5; Mettler Toledo, Columbus, OH; precision: 5 mg; table 1), and the position of the centre of mass was adapted according to the altered model volume.…”

“…Consequently, our CFD models highlight an evolutionary constraint: natural selection on flight cost hampers the sexual selection towards heavier armaments in male stag beetles. This is in addition to the negative effect of armature weight on the cost and stability of male terrestrial locomotion [10].…”