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.

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). In this context, smaller males may be favored due to more efficient locomotion leading to higher mobility during mate searching while larger males may benefit from increased speed and higher survivorship. Understanding how body size affects different aspects of the locomotor performance of males is therefore essential to shed light on the evolution of this widespread mating system. Using a combination of empirical measures of flight performance and substrate adhesion, and modelling of body aerodynamics, we show that large body size impairs both flight and landing (attachment) 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, ascended more rapidly during flight, and had a lower risk of detaching from the substrates on which they walk and land. Our models revealed variation in body shape affected body lift and drag, but tradeoffs with weight meant that effects were negligible, suggesting that flight costs do not explain the evolution of strong sexual dimorphism in body shape in this species.