Secondary Rhinaria Contribute to Major Sexual Dimorphism of Antennae in the Aphid Semiaphis heraclei (Takahashi)

Abstract

Sexual generation is an important generation in the life cycle of host-alternating aphids, and its population size determines the intensity of the peak in the next spring. Although male trapping techniques based on olfactory stimuli have been successfully established in the field, the biological basis of olfactory perception in males is unclear. In this study, we compared the morphology of antennae and the types, sizes, numbers, and distribution of sensilla between males and sexual females in the host-alternating aphid Semiaphis heraclei (Hemiptera: Aphididae). We found that flagellum length differentiation contributed to the majority of the sexual dimorphism of antennae. Most sensillum types or subtypes, including trichoid sensilla subtype I, campaniform sensilla, and primary rhinaria subtypes I and II, were enlarged in males. In addition, males bore more trichoid sensilla subtype I than sexual females. In particular, secondary rhinaria were present in males only and could not be detected in sexual females. These results revealed the structural basis of male olfactory perception. Our findings provide insight into the mechanism underlying chemical communication between sexual aphids and could thus be useful for pest control.

Keywords: antennal sensilla; male; scanning electron microscopy; sexual female; ultramorphology.

Figure 1

The antennae exhibit dramatic differences between sexes in Semiaphis heraclei (Takahashi). (A,B) Adult male (A) and sexual female (B). (C,D) Light microscope image of the antennae of male (C) and sexual female (D). (E,F) Scanning electron image of the antennae of male (E) and sexual female (F). (G,H) Diagram of the antennae of male (G) and sexual female (H). (I) Length of the antennae of males and sexual females. (J) Length of each segment of the antennae of males and sexual females. (K) Length of each flagellomere of the flagellum of males and sexual females. SC: scape; PE: pedicel; FL: flagellum; BA: base part; PT: processus terminalis. The bar chart shows the mean ± SEM of the data; the data of males and sexual females were analyzed by t test; Each dot in the bar chart represents the index value of each repeated measurement. **: p < 0.01. Scale bar = 200 μm.

Figure 2

The type of antennal sensilla or rhinaria identified on the antennae of both sexes in Semiaphis heraclei (Takahashi). (A,B) Trichoid sensillum subtype I (TS I) of male (A) and sexual female (B). (C,D) Trichoid sensillum subtype II (TS II) of male (C) and sexual female (D). (E,F) Campaniform sensillum (CaS) of male (E) and sexual female (F). (G,H) Primary rhinarium subtype I (PR I) of male (G) and sexual female (H). (I,J) Primary rhinarium subtype II (PR II) of male (I) and sexual female (J). (K) Secondary rhinarium (SR) of male. (L) Secondary rhinarium (SR) was absent from the antennae of sexual female. Scale bar = 5 μm.

Figure 3

The morphology of antennal sensilla or rhinaria in male Semiaphis heraclei (Takahashi). (A,B) Trichoid sensillum subtype I (TS I). (C,D) Trichoid sensillum subtype II (TS II). (E,F) Campaniform sensillum (CaS). (G,H) Primary rhinarium subtype I (PR I). (I) Primary rhinarium subtype II (PR II): large placoid sensillum (purple), two small placoid sensilla (yellow), and four coeloconic sensilla (with two sensory cones radiating outward (green) and the other two closed (blue)). (J) Large placoid sensillum (LPS). (K,L) Small placoid sensilla (SPS). (M) Coeloconic sensillum (CoS) with sensory cones radiating outward. (N) Coeloconic sensillum (CoS) with closed sensory cones. (O,P) Secondary rhinarium (SR). Scale bar = 1 μm.

Figure 4

Distribution of sensilla on the antennae in Semiaphis heraclei (Takahashi). (A) Overview of the position of sensilla on the antenna of male. (B) Four trichoid sensilla subtype II on the tip of the antenna. (C) A campaniform sensillum on the distal end of the pedicel. (D) A primary rhinarium subtype I and a primary rhinarium subtype II on the third and fourth flagellomeres. (E) Many trichoid sensilla subtype I on the second flagellomere of the flagellum. (F,G) Ventral side of the first flagellomere of males (F) and sexual females (G). (H,I) Ventral side of the second flagellomere of males (H) and sexual females (I). (J,K) Ventral side of the third flagellomere of males (J) and sexual females (K). TS I: trichoid sensillum subtype I; TS II: trichoid sensillum subtype II; CaS: campaniform sensillum; PR I: primary rhinarium subtype I; PR II: primary rhinarium subtype II; SR: secondary rhinarium. Scale bar = 10 μm.

Figure 5

Number of sensilla on each section of antennae in Semiaphis heraclei (Takahashi). (A) Trichoid sensillum subtype II (TS II). (B) Campaniform sensillum (CaS). (C) Primary rhinarium subtype I (PR I). (D) Primary rhinarium subtype II (PR II). (E) Trichoid sensillum subtype I (TS I). (F) Secondary rhinarium (SR). The bar chart shows the mean ± SEM of the data; the data of males and sexual females were analyzed by t test; Each dot in the bar chart represents the index value of each repeated measurement. **: p < 0.01.