Mating Behaviors Of The Swordtail Cricket Laupala Cerasina Otte And The Hangingfly Bittacus Planus Cheng

Mating behavior is a widespread phenomenon of the sexually reproducing animals. In most insects, males provide nuptial gifts to the female before, during, and after copulation. The size/number of the nuptial gift, the female and male genitalia, and the associated structures play important roles in the courtship and mating process. However, the relationship between the nuptial gift size and the paternity share of the gift-providing male, the coevolution of the mating-related structures and mating strategy, the sperm ejaculatory mechanism, and the role of the nuptial gift still remain largely unknown.Gryllidae(commonly called crickets) is a large family of Grylloidea in the hemimetabolous order Orthoptera. Because of the special singing behavior during courtship and mating, it has attracted numerous researchers. Moreover, the Hawaiian swordtail cricket Laupala is one of the insect groups that undergo the highest rate of speciation among arthropods.Bittacidae(commonly called hangingflies) is the second largest family in the holometabolous order Mecoptera. The adults are unable to stand on a surface but hang on the edges of leaves or twigs of plants by their prehensile forelegs. Because of the strict requirement for the environmental condition, they are considered as an important ecological indicator and have significant implications on the monitor of ecological environment and the protection of biological diversity.Though there are many studies on the mating behaviors of hemimetabolous and holometabolous insects, the comparative studies are considerably rare. In this study, we use the widely distributed Hawaiian swordtail cricket Laupala cerasina Otte, 1994 as the example of the hemimetabolous insect, observed its detailed courtship and mating behavior. Besides, we conducted a competitive mating behavior study using the statistical methods directly tested the relationship beteween the nuptial gift size and the gift-giving male’s paternity share and the sperm usage pattern of the polyandrous female crickets for the first time. In the holometabolous insects, we use Bittacus planus Cheng, 1949, a dominant species of Bittacidae in the Qinlin Mountains, as the study species to investigate the detailed courtship and mating behavior via the filed observation. We studied the co-evolution between the faceto-face mating position and the peculiar male genitalia and the fine structure of the sperm pump and its ejaculatory mechanism of Bittacus planus using light and scanning electron microscopy in aspects of anatomy and histology. The main results are as follows:1. The mating behavior of Laupala cerasina. Laupala cerasina has elaborate courtship and mating behavior, which lasts one day. Firstly, the male attracts the nearby female via the courtship song. After the female approached, the male and female communicate with each other via the physical contact of the antenna. The male then produced serials of spermless microspermatophore(hereafter “micro”) to the female. The micro is attached to the female after the short copulation. Since the micro is spermless and will be removed and eaten by the female, it was considered as a kind of nuptial gift. One hour before the sunset, the male produced a sperm-filled macrospermatophore(hereafter “macro”), which is approximately three times the diameter of micro. The sperm intake happens after the macro copulation during. The female removes and eats the macro after the sperm intake.2. The sperm usage pattern and the relationship between nuptial gift size and giftgiving male’s paternity share of Laupala cerasina. From the competitive mating in Laupala cerasina, we found considerable first male sperm precedence regardless of gift contribution. Furthermore, offspring from second-mated males tended to be laid later and be part of larger families. However, there was no relationship between nuptial gift size and the gift-giving male’s paternity share, which leaves the function of nuptial gifts in this species a mystery.3. Co-evolution of the mating behavior and external genitalia of Bittacus planus. During courtship, male hangingflies usually provide nuptial gifts to the female. During the copulation, male and female hanging on the plants and taking a face-to-face mating position. To accommodate this specific mating position, the male twists his abdomen temporarily about 180°. Meanwhile, the extremely elongated penisfilum in the aedeagal complex corresponds to the elongated spermathecal duct of the female. In Bittacidae, the gonostyli are greatly reduced while the epandrial lobes, which are modified from the 9th tergum, are well-developed. According to our observation, we proposed that the epandrial lobes serve as claspers to grasp the female subgenital plate during copulation, replacing the function of gonostyli. The modified proctiger(modified to the upper and lower branch) assists the penisfilum to stretch and to enter into the female spermathecal duct.4. Structures of male sperm pump and its ejaculatory mechanism of Bittacus planus. During the copulation of Bittacus planus, the liquid sperm was transferred to the female via a special sperm transfer device “sperm pump” to the female reproductive duct. The sperm pump is mainly consisted of a piston, which is fused with a piston-carrying sclerite, a pumping chamber enclosed by the genital folds, which comprises the posterior region of the ejaculatory sac, a phallobase, an ostial sclerite, and other associated structures and muscles. The piston crown plays an important role in the piston movement. The ostial sclerite serves as a discharge valve in the sperm pump and is controlled by a pair of antagonistic muscles. No depressor muscles were found attached to the piston. So we proposed that the sperm pumping activity is mainly controlled by the combination of the levator of the piston and the retractor and protractor of the ostial sclerite.Finally, we compared mating behaviors of the swordtail crickets and the hangingflies, and the evolution of nuptial gift and male and female genitalia are briefly discussed.