Exaggerated sexually selected weapons maintained with disproportionately low metabolic costs in a single species with extreme size variation

Larger individuals typically have lower mass-specific metabolic rates compared to small ones (hypometric scaling). This trend is most evident across species where body size differences can be extreme. Yet, within-species studies are critical to decipher the morphological and physiological mechanisms responsible. However, in most species, the relatively small range in body and appendage size of the same life stage often precludes such intraspecific comparisons. Sexually selected weapons are among the most exaggerated traits in nature; these traits can account for a large portion of body mass and contribute to whole-body energetic maintenance costs. Often larger individuals possess disproportionally larger weapons relative to their body size, yet little is known about how large individuals meet the predicted increased energetic demands of maintaining disproportionately large weapons. New Zealand giraffe weevils, Lasiorhynchus barbicornis (Coleoptera: Brentidae) exhibit an extreme 30-fold range in male body mass as well as hypermetric scaling of sexually selected rostra used as weapons in male–male competition. We compare intra- and interspecific resting metabolic rates by compiling measurements across 26 arthropod species whose size ranges overlap with L. barbicornis. The scaling of metabolic rate across this pooled interspecific sample was not significantly different from the intraspecific scaling of metabolic rate we found in L. barbicornis (slope of log–log relationship with body mass = 0.67). Male and female L. barbicornis had a similar scaling of metabolic rate with body size, despite differing substantially in the scaling of rostra, legs and antennae. However, large structures that scaled with positive allometry in males (rostra and legs) were increasingly composed of cuticle in larger individuals. The largest males invest ~60% less metabolically active tissue into rostra (weapons) compared to the smallest males. Our findings reveal hypometric scaling relationships of inter- and intraspecific metabolic rates across a shared size range in a diverse group of arthropods. Our intraspecific study uncovers a tremendous difference in weapon architecture as individuals scale up in size; we find that large males bear disproportionally larger weapons at a lower relative metabolic cost. This cost-saving mechanism may play a key role in shaping the hypermetric scaling of sexually selected traits. A free Plain Language Summary can be found within the Supporting Information of this article.