Contributions to Zoology, 86 (3) – 2017Xin Tong; Lu Jiang; Bao-Zhen Hua: A unique mating pattern of Panorpodes kuandianensis (Mecoptera: Panorpodidae)

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This research is likely the first attempt to describe the mating behavior and the copulatory mechanism of the genus Panorpodes in Panorpodidae. P. kuandianensis is unique in mating behavior for the male and female to change the mating position from a V-shape to an end-to-end by temporarily twisting the female abdomen by 180°. Some specialized structures (such as the basal processes and basal teeth) play important roles in obtaining and maintaining a successful mating. This unique mating pattern is remarkably different from that of other Mecoptera studied (Cooper, 1974; Thornhill, 1981; Byers and Thornhill, 1983; Thornhill and Sauer, 1991; Byers, 1997; Ma et al., 2010; Zhong and Hua, 2013; Zhong et al., 2015a, b).

The genital and non-genital grasping devices are usually modified in internally inseminating species of insects to maintain the firm coupling of genitalia between the two sexes (Arnqvist, 1997; Matthews and Matthews, 2010; Chapman, 2013; Zhong et al., 2015a; Richmond et al., 2016), such as the specialized abdominal apparatus in water striders (Arnqvist and Rowe, 2002; Perry and Rowe, 2012) and the notal organ in scorpionflies (Mickoleit, 1971; Thornhill and Sauer, 1991; Zhong and Hua, 2013). The basal processes of gonostyli can restrict the movement of the female genital segments in P. kuandianensis, but are used to impede the genital plate from retreating in Neopanorpa longiprocessa (Zhong and Hua, 2013). The hypandrium with incrassate processes of Panorpodes likely plays a part in stimulating the cerci of the female during mating. A similar phenomenon is also reported in Panorpidae species (Zhong and Hua, 2013; Zhong et al., 2015a).

Flexion and rotation of the abdomen are considered to be adaptations for mating and storing the abdominal segments when not in use (McAlpine et al., 1981), and take place in the male terminal abdomen in the majority of insects. Well-known examples are the males of Diptera, the abdomens of which twist from 90° to 360° around the long axis of the abdomen to adapt the diverse mating positions (McAlpine et al., 1981; Bickel, 1990; Huber et al., 2007). For the reason of abdominal rotation, Bickel (1990) suggests that female sexual selection pressure promotes the rotation of male abdomen and encourages the circumversion of the terminal abdomen to couple in a male-above position, because a male on top of the female may not only grasp his mate more securely and control the timing of disengagement, but is also able to fend off any intruding males or to stimulate the female using his legs and mouthparts. By contrast, however, in P. kuandianensis the torsion occurs in the female. This phenomenon may be correlated with the abdominal morphologies of both sexes. The segments A7–A9 are thick and short in the male, but slender and concealed within A6 in the female (Zhong et al., 2011). In this case, it seems more convenient to rotate the female than the male abdomen. We suggest that during the copulation of insects either the active rotation in the male abdomen or the passive rotation in the female abdomen seems to have evolved to adapt to the sexual conflict, and is mainly beneficial to the male to dominate the mating process.

The position-changed mating is unusual in Mecoptera (Mickoleit, 1971; Cooper, 1974; Thornhill, 1981; Thornhill and Sauer, 1991; Byers, 1997; Gao and Hua, 2013; Zhong and Hua, 2013; Zhong et al., 2015a, b), but is common in Orthoptera (Alexander and Otte, 1967), Diptera (McAlpine et al., 1981), and Lepidoptera (Scott, 1986; Fänger and Naumann, 1998). The initial side-by-side mating position is sustained by the majority of Lepidoptera species, and changes to end-to-end immediately or shortly after establishing genital contact (Scott, 1986; Fänger and Naumann, 1998). For the possible reasons of the position-changed mating, McAlpine and Munroe (1968) believe that the initial position in Diptera is used to establish the interlock of their genitalia and usually takes place during flight. The secondary position is needed to continue copulation and transfer sperm and frequently occurs while the pair rests on a substrate. The position-changed mating in Panorpodes is likely an effective strategy of the male to dominate the mating and to compensate for the lacking of a notal organ, because the end-to-end mating position is frequently accompanied by the pulling behavior. At the pulling phase, the female is almost helpless, and the locomotion of the coupled pair usually depends on the male. This mating pattern may be best explained as a male strategy against female disengagement by turning away. However, details of the contact of the phallotreme of the male and the copulatory pore of the female have not been observed in this study. It may require subsequent preparations of histological serial sections and 3D reconstructions as applied in the fruit fly (Mattei and Wolfner, 2016) and the bushcricket (Wullf et al., 2015).