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Weber, Jesse N.; Kojima, Wataru; Boisseau, Romain P.; Niimi, Teruyuki; Morita, Shinichi; Shigenobu, Shuji; Gotoh, Hiroki; Araya, Kunio; Lin, Chung-Ping; Thomas-Bulle, Camille; Allen, Cerisse E.; Tong, Wenfei; Lavine, Laura Corley; Swanson, Brook O.; Emlen, Douglas J.
Current biology, 10/2023, Letnik: 33, Številka: 20Journal Article
What limits the size of nature’s most extreme structures? For weapons like beetle horns, one possibility is a tradeoff associated with mechanical levers: as the output arm of the lever system—the beetle horn—gets longer, it also gets weaker. This “paradox of the weakening combatant” could offset reproductive advantages of additional increases in weapon size. However, in contemporary populations of most heavily weaponed species, males with the longest weapons also tend to be the strongest, presumably because selection drove the evolution of compensatory changes to these lever systems that ameliorated the force reductions of increased weapon size. Therefore, we test for biomechanical limits by reconstructing the stages of weapon evolution, exploring whether initial increases in weapon length first led to reductions in weapon force generation that were later ameliorated through the evolution of mechanisms of mechanical compensation. We describe phylogeographic relationships among populations of a rhinoceros beetle and show that the “pitchfork” shaped head horn likely increased in length independently in the northern and southern radiations of beetles. Both increases in horn length were associated with dramatic reductions to horn lifting strength—compelling evidence for the paradox of the weakening combatant—and these initial reductions to horn strength were later ameliorated in some populations through reductions to horn length or through increases in head height (the input arm for the horn lever system). Our results reveal an exciting geographic mosaic of weapon size, weapon force, and mechanical compensation, shedding light on larger questions pertaining to the evolution of extreme structures. •Biomechanical costs of extreme structures are often hidden by compensatory traits•We trace the evolution of long horns in a beetle and measure the effect on strength•Horns increased in length twice, yielding weapons with weaker lifting forces•Some populations later grew taller heads or shorter horns, restoring lifting force Weber et al. document a biomechanical tradeoff associated with the evolution of an exaggerated animal weapon. When beetle horns got long, they also got weaker—a cost that was later ameliorated in some populations. Reconstructing the sequence of evolution of this weapon provides a rare glimpse of an ephemeral and elusive cost to extreme structures.
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