Multi-modal locomotor costs favor smaller males in a sexually dimorphic leaf-mimicking insect

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.

A second view on the evolution of flight in stick and leaf insects (Phasmatodea)

“…In comparison to the other ocelli-bearing clades, the distribution of ocelli within Phylliidae appears more ambiguous. While females are sedentary and flightless, all males are volant and depend on flight for mate localisation [ 69 , 89 , 98 ], thus, it is questionable whether there have been multiple independent secondary losses of ocelli as estimated by our analysis. Particularly the phylogenetically incoherent degree of ocelli development in the species of Phyllium , where ocelli may be absent or weakly, moderately or well developed (not coded in our analysis), suggests that the ocellar system is a disparate character, which might have gradually and independently re-evolved in several phylliid lineages.…”

Convergent Evolution of Adhesive Properties in Leaf Insect Eggs and Plant Seeds: Cross-Kingdom Bioinspiration

“…This kind of camouflage evolved quite early in phasmids in general [ 52 , 53 , 54 , 55 , 56 , 57 ] and leaf insects in particular [ 58 , 59 ]. One result of this type of camouflage is a strong sexual dimorphism in Phylliidae [ 60 ] due to the fact that females are sedentary and imitate leaves in the canopy and males need to be mobile to find their mates to reproduce [ 61 ]. As a result, the eggs of all phylliids are dropped from the place where the females hide.…”

Beyond winglets: evolutionary scaling of flight-related morphology in stick insects (Phasmatodea)

“…In the direction of flight gain, a positive static margin may be necessary for flapping flight in fully-winged insects. So far, kinematics of wing flapping and flight performance have only been documented in males of a leaf insect (Boisseau et al, 2022). These predictions should be confirmed using actual body-leg postures and body kinematics, along with stability analysis, from flight of phasmids with various sized wings.…”

“…The processes of wing reduction and flight transition in phasmids remain largely understudied, despite the hypothesis that relaxed selection for flight (i.e., aerodynamic utility) underpins short-winged or wingless species within an arboreal context (Zeng et al, 2020). A recent study showed ascending flight in leaf insects, a group of leaf-mimicking phasmids (Boisseau et al, 2022).…”

“…Thus far, flight kinematics has only been studied in a single species of phasmid (Boisseau et al, 2022). For a preliminary assessment of the correlation between flight capacity and wing size, we made highspeed video films of flight in phasmid taxa with different sized wings (see Methods ).…”