Olfactory performance explains duality of antennal architectural designs in Lepidoptera

Male attraction by females through sex pheromones is widespread among
Lepidoptera, and antennae are key olfactory organs during male
orientation. Broadly speaking, two designs of antennae coexist in
Lepidoptera: complex (pectinate) or stick-like (filiform) ones. Pectinate
antennae have attracted attention because of their multiscale geometry,
assumed to outperform filiform. Yet, the filiform design is by far more
common. We compare the olfactory performance of the two designs using
modeling, particle image velocimetry on 3D-printed scaled-up models, and
computational simulations. In terms of absolute odor capture, pectinate
antennae perform better at nearly all flying speeds. However, when
considering drag, filiform designs are more energy-efficient than
pectinate ones at low flight speeds, while the reverse holds at high
speeds. This is due to the differential scaling of drag and molecule
capture with flight speed. According to our results, small and slow moths
would bear filiform antennae whereas big and fast moths would have
pectinate ones, which is the general trend observed in Nature. We discuss
exceptions to this general pattern and how species could evolve from one
design to the other by investigating the influence of the antennal
structural elements.