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Independent evolution of similar traits in lineages inhabiting similar environments (convergent or repeated evolution) is often taken as evidence for adaptation by natural selection, and used to illustrate the predictability of evolution. Yet convergence is rarely perfect for two reasons. First, environments may not be as similar as they appear. Second, responses to selection are contingent upon available genetic variation and independent lineages may differ in the alleles, genetic backgrounds, and even the developmental mechanisms responsible for the phenotypes in question. Both impediments to convergence are predicted to increase as the length of time separating two lineages increases, making it difficult to discern their relative importance. We quantified environmental similarity and the extent of convergence to show how habitat and divergence time each contribute to observed patterns of morphological evolution in 212 species of stick and leaf insects (order Phasmatodea). Dozens of phasmid lineages independently colonized similar habitats, repeatedly evolving in parallel directions on a 23-trait morphospace, though the magnitude and direction of these shifts varied. Lineages converging toward more similar environments ended up closer on the morphospace, as did closely related lineages, and closely related lineages followed more parallel evolutionary trajectories to arrive there than more distantly related ones. Remarkably, after accounting for habitat similarity, we show that divergence time reduced the extent of convergence at a constant rate across more than 100 My of separation, suggesting even the magnitude of contingency can be predictable, given sufficient spans of time.more » « less
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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 advan- tages of additional increases in weapon size. However, in contemporary populations of most heavily weap- oned 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 gener- ation 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 ‘‘pitch- fork’’ 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.more » « less
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Abstract Background In most arthropods, adult females are larger than males, and male competition is a race to quickly locate and mate with scattered females (scramble competition polygyny). Variation in body size among males may confer advantages that depend on context. Smaller males may be favored due to more efficient locomotion leading to higher mobility during mate searching. Alternatively, larger males may benefit from increased speed and higher survivorship. While the relationship between male body size and mobility has been investigated in several systems, how different aspects of male body morphology specifically affect their locomotor performance in different contexts is often unclear. Results Using a combination of empirical measures of flight performance and modelling of body aerodynamics, we show that large body size impairs flight performance in male leaf insects ( Phyllium philippinicum ), a species where relatively small and skinny males fly through the canopy in search of large sedentary females. Smaller males were more agile in the air and ascended more rapidly during flight. Our models further predicted that variation in body shape would affect body lift and drag but suggested that flight costs may not explain the evolution of strong sexual dimorphism in body shape in this species. Finally, empirical measurements of substrate adhesion and subsequent modelling of landing impact forces suggested that smaller males had a lower risk of detaching from the substrates on which they walk and land. Conclusions By showing that male body size impairs their flight and substrate adhesion performance, we provide support to the hypothesis that smaller scrambling males benefit from an increased locomotor performance and shed light on the evolution of sexual dimorphism in scramble competition mating systems.more » « less
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