Mating Behavior And Copulatory Mechanism Of Panorpidae(Mecoptera)

Mating behavior is an important step in the reproductive activities of bisexual reproduction insects.The complex genitalia and abdominal grasping structures play an important role in mating behaviors.However,due to the concealment and the complexity of mating process,research on the copulatory mechanism of insects remains lacking so far.Special mating phenomena,including traumatic mating and evolutionary trade-off are only reported in a few groups.Panorpidae is the most speciose family in Mecoptera with approximately 500 described species,have complex grasping structures and interesting nuptial feeding behaviors.There are lots of studies on the nuptial feeding behavior of scorpionflies,however,the research on the copulatory mechanism and the functional morphology of male specific grasping structures have been neglected.In this study,based on the behavioral comparison,morphological observation,and experimental manipulation,we investigated the coupling genitalia,diverse mating patterns,function of special grasping structures,traumatic mating,and evolutionary trade-off between mating tactics of Panorpidae.The main results are as follows:(1)Copulatory mechanism and diverse mating patterns of Panorpidae :Cerapanorpa males provide a solid salivary mass to the female prior to copulation.The single anal horn clamps the female A8 in cooperation with the basally-constricted A7.The male hypovalves grasp the female cerci,and move up and down rhythmically.The paired parameres clasp both sides of the female tergite IX.The basal processes on male gonostyli grip the pleural membranes of the female genital chamber.Male aedeagus directly couples with the female medigynium to transmit sperm by connecting his phallotreme to the female's copulatory pore.Sinopanorpa males either adopt a coercive mating without any nuptial gift or secrete a salivary mass and do not provide the nuptial gift to the female until the genitalia establish a connection.Sinopanorpa males lack an anal horn on the tergum VI,but the corresponding position possesses a bunch of bristles,which can cooperate with the dorsal groove on A7 to seize the female abdomen.During copulation,the male sharp basal processes grasp both sides of the female genital segment to stabilize the medigynium but damage the pleural membranes of genital chamber.Traumatic mating is found in Mecoptera for the first time.Panorpa males usually adopt a salivary mass-providing mating tactic.The mating times,however,are significant different among species.The males of P.changbaishana and P.kunmingensis provide a salivary mass before meeting a female.P.fulvastra males,however,secrete the salivary mass after the female being attracted.P.liui males either adopt a coercive or the prey-providing mating tactic.Panorpa males lack an anal horn on tergum VI,and usually seize the female by the constricted A7 and A8.The diverse morphological traits of A7 and A8 may provide the structural basis for their different mating times.Neopanorpa males maintain an intermittent mouth-to-mouth mode prior to copulation,but do not exchange any edible food.Males of N.lui with a weakly-developed notal organ and N.carpenteri with a medium-sized notal organ secrete a salivary mass to the female.These males possess the elongated and expanded salivary glands.Males of N.longiprocessa with an extremely elongated notal organ and N.brisi with a medium-sized notal organ adopt a coercive mating tactic.Their salivary glands are either very short or elongated without inflation.The prominent basal processes grasp the female genital segment.The male aedeagus physically couples with the female medigynium to ensure the phallotreme to connect to the copulatory pore.(2)Mating pattern and sperm transferred mechanism of Panorpodidae :Panorpodes males provide a salivary mass as a nuptial gift prior to copulation,start to copulate with the female by the V-shaped position,then change to an end-to-end position by temporarily twisting the female abdominal segments VII-IX(A7-A9)by 180°.During mating the basal processes and the basal teeth of the gonostyli and the hypandrium are used to obtain copulation and sustain the coupling of genitalia.Through the advance and the return movement of sperm pump,male directly transfers seminal fluid to the female spermatheca with the connection of the male phellotreme to the female copulatory pore.Male sperm pump mainly consists of a piston,a pumping chamber,the anterior region of the aedeagal complex,the posterior region of the ejaculatory sac,and associated muscles.(3)The functions of special grasping organs of male Panorpidae:The single anal horn does not grasp the female A8 in cooperation with the basally-constricted A7 until C.dubia males establish the connection of genitalia.After the nuptial gift is consumed,the single anal horn only can prolong the coercive mating for 4.00 ± 2.90 min,(n = 10).Once the notal organ of N.longiprocessa males with an extremely-elongated notal organ is made wholly or partially invalid by low-temperature wax,the males are unable to establish a successful mating.When the notal organ is ineffective in N.lui males with a weakly-developed notal organ,the mating success and copulation duration are reduced significantly.When the sharp teeth are cut off,the mating success and copulation duration are reduced significantly for S.tincta males that adopt a nuptial feeding mating tactic.The results of sperm-transfer experiment show that the males adopted a coercive mating tactic cannot successfully transfer sperm due to the shorter copulation duration.(4)The benefits and costs of traumatic mating in Panorpidae:The sharp teeth of male D.magna injure the female genital segment to inflict copulatory wounds.By the encasement of low-temperature wax and the remating experiment,we find the injurious teeth can enhance male mating control through increasing the male mating success and copulation duration.Traumatic mating has little effect on the female mating refractory period,but significantly reduce the female remating duration with subsequent males.This benefits the first-mating male to obtain an advantage in sperm competition.The copulatory wounds do not affect the female pre-oviposition period,egg stage,and hatching rate,however,reduce the fecundity.This is one of the most important adverse effects of traumatic mating.(5)The evolutionary trade-off between mating tactics of Panorpidae:We observed the mating tactics of 32 species and measured the morphological traits of 17 species to find that the furcation degree of salivary glands and the length of the notal organ are closely related to male coercive and salivary mass-providing mating tactics.The more developed the salivary glands,the stronger the male secretion-providing ability.The longer the notal organ,the stronger the mating control.As the structural basis of the coercive and nuptial feeding mating tactics,the furcation degree of salivary glands and the length of the notal organ show a significantly negative correlation.The results demonstrate that an evolutionary trade-off has been evolved between the coercive and nuptial feeding mating tactics in Panorpidae.