The Female Reproductive System Structure, Copulatory Mechanism And Phylogenetic Analysis Of Panorpidae (Mecoptera)

Most insects are oviparous and amphigonous. The organs of reproductive system areimportant for insect reproduction. Previous studies mainly focus on male reproductive system,especially the species-specific diverse male genitalia, which have been widely used intaxonomy and phylogenetic analysis of insects. However, research of female reproductivesystem is considerably limited. Correspondingly, the significance of female genitalia intaxonomy and phylogenetic analysis has been greatly overlooked or neglected bytaxonomists.Mecoptera is one of the most primitive orders in holometabolous insects and representsan important link between the Hemimetabola and Holometabola. The systermatics of thescorpionflies Panorpidae, the most speciose family in Mecoptera, is in chaos in that theirphylogenetic study is far from sufficient. We used light and electron microscopy to study thefemale reproductive system of Panorpidae, including the internal reproductive system andexternal genitalia, copulatory mechanism, and mating tractics in aspects of anatomy, histology,and ultrastructure. We analyzed the phylogenetic relationship of Panorpidae based on thefemale genitalia, especially the genital plate, in combination with additional characters for thefirst time. The main results are as follows:The female reproductive system of Panorpidae is situated in the abdominal segmentsII–IX and comprises the internal reproductive system and the external genitalia. The former iscomposed of paired ovaries, lateral oviducts, common oviduct, spermatheca and accessoryglands; and the latter consists of a subgenital plate and a genital plate.The ovary of panorpids is of polytrophic type and consists of several ovarioles. Thewhole ovary is surrounded by a net-like membrane. The ovariole is enclosed by an innertunica propria and an outer tunica externa, which is also net-like. The ovariole is differentiatedinto a terminal filament, germarium, vitellarium and pedicel. In the germarium, germ cellundergoes two cycles of mitotic divisions and forms one oocyte and three nurse cells. Duringoogenesis, nurse cells provide nutrition for the oocyte until they have been consumed up and degenerated; the follicle cells multiply and differentiate into four subgroups to enclose thewhole egg chamber and the oocyte closely; the oocyte gradually grows and fills withnumerous yolk granules and lipid droplets. During the choriongenesis, follicle cells secrete aninner vitelline membrane, an outer chorion, and an extrachorion successively. The finestructure and formation of the eggshell in panorpids have been proposed for the first time.The ultrastructure and function of the oviduct, spermatheca and accessory glands ofPanorpidae have been studied for the first time. The paired lateral oviducts unite at theabdominal segment VI and connect to the common oviduct. They are responsible forexpelling the mature oocyte from the ovariole to the genital chamber. The lateral oviducts arethe products of the mesodermal cells, including the inner intima, epidermal cell layer, basallamina, and circular muscle layer; the common oviduct is of ectodermal origin and bears athicker muscle layer, including the inner intima, epidermal cell layer, basal lamina, circularand longitudinal muscle layers. The spermatheca of Panorpidae is composed of the apical sacand the elongate spermathecal duct. The spermatheca is enclosed by a chitinized layer, withthe epidermal cells lacking secretory functions. The epidermal cells of the spermathecal ductbear abundant cytoplasmic organelles and glandular units, indicating its strong secretoryactivity. Based on the ultrastructure of seprmatheca, we put forward the entering and releasingprocesses of the sperm. The epidermal cells in the female accessory glands of Panorpidaebelong to Class3cells and characterized by a developed secretory cell, a thin duct-formingcell and a cuticle duct. Based on the cytoplasmic features, the main component and synthesispathway of the secretion products are briefly discussed.In combination with female and male genitalia, we inferred the copulatory mechanism ofPanorpidae for the first time and found that the lock-and-key hypothesis is unlikely to beentirely validated in Panorpidae.Based on the observation of nuptial gift behaviour during the courtship and copulation,we found that the salivary glands of male scorpionfies are closely associated with matingtactics choice. The evolutional pathway of both salivary glands and mating tactics were firstproposed.Based on the study of the diversity of male salivary glands and eggshell, we reconfirmedthe paraphyly of Panorpa and proposed their significance in Panorpidae systmatics, providingmore evidence for studying the phylogenetic relationships of Panorpidae.A new genus Furcatopanorpa was erected with Panorpa longihypovalva Hua&Cai,2009as the type species. Correspondingly, Furcatopanorpa longihypovalva (Hua&Cai,2009), comb. nov. is transferred from the genus Panorpa.The phylogenetic relationship was analyzed with maximum parsimony based on female genital plates in combination with other characters, with Brachypanorpa Carpenter andPanorpodes MacLachlan in Panorpodidae as outgroups. The results show that the monophylyof the genus Sinopanorpa Cai&Hua is well supported. The genus Panorpa Linneus isreconfirmed to be paraphyletic and might deserve further split. The P. amurensis, P. centralis(=P. cornigera group), and P. diceras groups are evidently monophyletic and may merit ageneric status, respectively. However, the P. davidi group is definitely paraphyletic and needsfurther systematic study. The origin and evolutionary pathway of the female genital plate ofthe Panorpidae are briefly discussed.