Co-Evolution of the Mating Position and Male Genitalia in Insects: A Case Study of a Hangingfly

Qionghua Gao,Baozhen Hua,Therésa M Jones

doi:10.1371/journal.pone.0080651

Qionghua Gao, Baozhen Hua + Show 1 more

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https://doi.org/10.1371/journal.pone.0080651

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Journal: PloS one	Publication Date: Dec 3, 2013
Citations: 57	License type: CC BY 3.0

Affiliation: North West Agriculture and Forestry University

Abstract

Hangingflies are unique for the male providing a nuptial gift to the female during mating and taking a face-to-face hanging copulation with the female. Their male genitalia are peculiar for an extremely elongated penisfilum, a pair of well-developed epandrial lobes (9th tergum), and a pair of degenerated gonostyli. However, the co-evolution of their face-to-face copulation behavior and the male genitalia has rarely been studied hitherto. In this paper the mating behavior of the hangingfly Bittacus planus Cheng, 1949 was observed under laboratory conditions, and the morphology of the male and female external genitalia was investigated using light and scanning electron microscopy. The male provides an insect prey as a nuptial gift to the female in courtship and mating process, and commits a face-to-face copulation. During copulation, the male abdomen twists temporarily about 180° to accommodate their face-to-face mating position. The aedeagal complex has an extremely elongated penisfilum, corresponding to the elongated spermathecal duct of the female. The well-developed epandrial lobes serve as claspers to grasp the female subgenital plate during copulation, replacing the function of gonostyli, which are greatly reduced in Bittacidae. The modified proctiger assists the penisfilum to stretch and to enter into the female spermathecal duct. The possible reasons why this species might mate face-to-face are briefly discussed.

Highlights

In most animal species with internal fertilization, male genitalia are among the most diverse, complex, and rapidly evolving morphological structures [1,2,3]
The cryptic female choice states that male genitalia may differ in their ability to stimulate multiply-mated females to selectively use sperm from males with superior stimulatory capabilities of genital morphology over that of others to fertilize their eggs [1,17]
We show that as an intromittent organ through which the ejaculate is transferred to the female spermatheca, the elongated spring-like penisfilum of the male hangingfly is curled dorsally, in a direction opposite to that of the female genitalia when in the face-to-face hanging position, it is impossible for the penisfilum to touch the female genitalia unless the male twists his abdomen

Summary

Introduction

In most animal species with internal fertilization, male genitalia are among the most diverse, complex, and rapidly evolving morphological structures [1,2,3]. The pleiotropy hypothesis states that genital evolution is an indirect result of evolution of genetically correlated characters through accumulated pleiotropic effects of genes that code for both genital and general morphology [14] This hypothesis is not currently well supported [9,15]. The more convincing alternative hypothesis is that the evolution of species-specific genitalia arises through sexual selection and/or sexual conflict This hypothesis proposes that males and females are engaged in co-evolutionary arms races over control of copulation and insemination and includes three main mechanisms [9]: sperm competition, cryptic female choice, and sexual conflict. The provision of a nuptial gift prior to and during mating is an interesting strategy employed by male hangingflies (Mecoptera: Bittacidae) in their pursuit of a mate [24,25]

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