Adaptations for gas exchange enabled the elongation of lepidopteran proboscises

Jiang，Miao1,2; Zhang，Xinfang2; Fezzaa，Kamel3; Reiter，Kristen E.4; Kramer-Lehnert，Valerie R.4; Davis，Brandon T.4; Wei，Qi Huo1,2; Lehnert，Matthew S.4

2023-07-24

10.1016/j.cub.2023.06.014

Current Biology   Impact Factor & Quartile

0960-9822

1879-0445

The extensive biodiversification of butterflies and moths (Lepidoptera) is partly attributed to their unique mouthparts (proboscis [Pr]) that can span in length from less than 1 mm to over 280 mm in Darwin's sphinx moths. Lepidoptera, similar to other insects, are believed to inhale and exhale respiratory gases only through valve-like spiracles on their thorax and abdomen, making gas exchange through the narrow tracheae (Tr) challenging for the elongated Pr. How Lepidoptera overcome distance effects for gas transport to the Pr is an open question that is important to understanding how the Pr elongated over evolutionary time. Here, we show with scanning electron microscopy and X-ray imaging that distance effects on gas exchange are overcome by previously unreported micropores on the Pr surface and by superhydrophobic Tr that prevent water loss and entry. We find that the density of micropores decreases monotonically along the Pr length with the maxima proportional to the Pr length and that micropore diameters produce a Knudsen number at the boundary between the slip and transition flow regimes. By numerical estimation, we further show that the respiratory gas exchange for the Pr predominantly occurs via diffusion through the micropores. These adaptations are key innovations vital to Pr elongation, which likely facilitated lepidopteran biodiversification and the radiation of angiosperms by coevolutionary processes.

coevolution diffusion insect respiration micropore superhydrophobicity

SCI

English

NI Journal Papers ; NI论文

First

Argonne National Laboratory[DE-AC02-06CH11357];National Science Foundation[IOS-1354956];

Biochemistry & Molecular Biology ; Life Sciences & Biomedicine - Other Topics ; Cell Biology

Biochemistry & Molecular Biology ; Biology ; Cell Biology

WOS:001048995700001

CELL PRESS

BIOLOGY & BIOCHEMISTRY

2-s2.0-85165291652

Scopus

1.Department of Mechanical and Energy Engineering,Southern University of Science and Technology,Shenzhen,Guandong Province,China
2.Advanced Materials and Liquid Crystal Institute,Kent State University,Kent,44242,United States
3.Experimental Facilities Division,Advanced Photon Source,Argonne National Laboratory,Argonne,60439,United States
4.Department of Biological Sciences,Kent State University at Stark,North Canton,44720,United States

Jiang，Miao,Zhang，Xinfang,Fezzaa，Kamel,et al. Adaptations for gas exchange enabled the elongation of lepidopteran proboscises[J]. Current Biology,2023,33(14):2888-2896.e2.

Jiang，Miao.,Zhang，Xinfang.,Fezzaa，Kamel.,Reiter，Kristen E..,Kramer-Lehnert，Valerie R..,...&Lehnert，Matthew S..(2023).Adaptations for gas exchange enabled the elongation of lepidopteran proboscises.Current Biology,33(14),2888-2896.e2.

Jiang，Miao,et al."Adaptations for gas exchange enabled the elongation of lepidopteran proboscises".Current Biology 33.14(2023):2888-2896.e2.