Phylogeny of Mantodea based on molecular data: evolution of a charismatic predator

Abstract. The previously unknown phylogenetic relationships among Mantodea (praying mantids) were inferred from DNA sequence data. Five genes (16S rDNA, 18S rDNA, 28S rDNA, cytochrome oxidase II and histone 3) were sequenced for sixty‐three taxa representing major mantid lineages and outgroups. The monophyly of mantid families and subfamilies was tested under varying parameter settings using parsimony and Bayesian analyses. The analyses revealed the paraphyly of Hymenopodidae, Iridopterygidae, Mantidae, and Thespidae and the monophyly of the Amorphoscelidae subfamily Paraoxypilinae. All represented subfamilies of Iridopterygidae and Mantidae appear paraphyletic. Mantoididae is sister group to the rest of the sampled mantid taxa. Lineages congruent with current subfamilial taxonomy include Paraoxypilinae, Hoplocoryphinae, Hymenopodinae, Acromantinae and Oligonicinae. The mantid hunting strategy is defined as either generalist, cursorial or ambush predators. By mapping hunting strategy onto our phylogeny, we reconstructed the ancestral predatory condition as generalist hunting, with three independent shifts to cursorial hunting and one shift to ambush hunting, associated with the largest radiation of mantid species.     

Immunocytochemical distribution of pigment-dispersing hormone in the cephalic ganglia of polyneopteran insects

Material detectable with antisera to the pigment-dispersing hormone (PDH) is regarded as a component of the circadian clock residing in some insects in the optic lobe. This paper demonstrates that the position of the PDH-positive neurones and the course of their processes are similar in all representatives of the insect cohort Polyneoptera. A basic morphological pattern, which includes the proximal frontoventral (Pfv), distal posteriodorsal (Dpd) and posterioventral (Dpv) clusters of PDH-positive neurones, was found in the examined species of locusts, crickets, walking sticks, cockroaches, earwigs and termites. The Pfv cluster is located close to the accessory medulla and usually consists of a set of smaller and a set of larger perikarya. The Dpd and Dpv clusters occupy a dorsal and a ventral position, respectively, at the distal edge of the medulla. These clusters are lacking in stonefly and praying mantid species. The fan-like arrangement of PDH-positive fibres within the frontal medulla face (the locusts and the praying mantid have an additional, smaller fan on the posterior medulla face) is another characteristic feature of Polyneoptera. One (two in the locusts and the praying mantid) nerve bundle runs from the optic lobe to the lateral protocerebrum where it ramifies. One branch gives rise to a fibre network frontally encircling brain neuropile in the area of mushroom bodies. One thin fibre in the crickets and the earwig, and several thicker and anastomosing fibres in the other insects, connect the brain hemispheres. The arrangement of other PDH-positive structures specifies taxa within Polyneoptera. Specific features comprise the presence of PDH-positive perikarya in protocerebrum (walking stick and termite), deutocerebrum (cricket, walking stick, and one cockroach species), tritocerebrum (another cockroach species), and the suboesophageal ganglion (cricket, walking stick and termite). In the walking stick and the termite, PDH-positive fibres pass from the cephalic to the frontal ganglion and from there via the recurrent nerve to the corpora cardiaca where they make varicosities indicative of peptide release into the haemolymph.     

Spermatophore feeding and mating behaviour in praying mantids (Mantodea: Liturgusidae)

In a number of insects, males transfer sperm to females via an externally attached spermatophore, which females subsequently remove and consume. Here I report the first study of spermatophore feeding in a praying mantid. While studies of praying mantid mating behaviour have largely focused on sexual cannibalism, this behaviour is not known in the genus Ciulfina . The general patterns of mating behaviour and spermatophore feeding are described for four species: Ciulfina rentzi , Ciulfina klassi , Ciulfina biseriata and Ciulfina baldersoni . Copulation duration and postcopulatory spermatophore attachment duration were found to vary both inter- and intraspecifically. Ciulfina rentzi exhibited a considerably longer mean copulation duration and a considerably shorter mean postcopulatory spermatophore attachment duration than the other Ciulfina species. Smaller males copulated for longer durations in C. rentzi and C. klassi . For C. baldersoni , both copulation duration and postcopulatory spermatophore attachment duration increased with female mass. The genus Ciulfina is highlighted as an intriguing new system in which to test hypotheses surrounding the function of spermatophore feeding and the significance of copulation duration.     

Prey capture in mantids: Prothoracic tibial flexion reflex

We describe a prothoracic leg tibial flexion reflex (PTFR) of the praying mantis Tenodera aridifolia sinensis which is initiated by tactile stimulation of the movable spines of the ventro-medial border of the femur. This flexion reflex may be responsible for the continuous grasping of a captured prey by the mantid.     

Identification of the molecular origin and development of a panzootic caused by Beauveria bassiana in praying mantis populations in eastern China

A panzootic in praying mantid species Tenodera sinensis and Statilia maculate, caused by Beauveria bassiana, occurred in north, southwest and southeast regions of Anhui Province, eastern China in Autumn, 2009. A 3-d principal component analysis (PCA) of 123 isolates from three sites revealed that the B. bassiana populations were heterogeneous with obvious dominance. Furthermore, the causal source of the panzootic in Anhui was shown to be polyphyletic. The populations were homogenized into homogenous subunits for investigation of genetic structure by inter-simple sequence repeat (ISSR) markers. Variance was greater than 70%, largely due to genetic differences within populations and subpopulations. Genetic distances and genetic differentiation were negatively associated with geographic distances and it was speculated that this was due to the effects of monsoons and topography. Mantid isolates were divided into five pathotypes based on a two-way cluster analysis of genetic distance. Pathotype I consisted of the predominant subpopulations of Huangcangyu and Chashui populations, with a genetic distance of 0.120 and gene flow up to 1.833. This pathotype caused a widespread epizootic in north and southwest Anhui, and Pathotype III caused enzootic at Site A in September and then epizootic in October, while the other three pathotypes caused enzootics at all three investigation sites. The widespread epizootics and isolated enzootics composed the polyphyletic panzootic in Anhui. A strong gene flow between isolates from the two mantid species was identified, resulting in negligible gene differentiation. This indicated a lack of host specificity in mantid isolates of B. bassiana.     

Male mate choice in a sexually cannibalistic species: male escapes from hungry females in the praying mantid <Emphasis Type="Italic">Tenodera angustipennis</Emphasis>

While competing males and choosy females may be common in animal mating systems, male choice can evolve under certain conditions. Sexual cannibalism is such a condition because of the high mortality risk for males. In mantids, female body condition is associated with male mate preference, with fat females preferred, due to at least two reasons: females in poor nutritional condition are likely to attack and predate males, and fat females can potentially increase the number of offspring. Thus, the risk of cannibalism and female fecundity can influence male mating behavior. In this study, we attempted to separate these factors by using the praying mantid Tenodera angustipennis to examine whether male preference for fat female mantids was based on avoiding sexual cannibalism (cannibalism avoidance hypothesis) or preference for female fecundity (fecundity preference hypothesis). The feeding regimes were experimentally manipulated to discriminate between the effects of female fecundity and female hunger status on male and female mating behaviors. We found that recently starved females more frequently locomoted toward the male, and that male abdominal bending was less intensive and escape was sooner from recently starved females. These female and male behavioral responses to female hunger condition may reveal male avoidance of dangerous females in this mantid.     

Complicity or conflict over sexual cannibalism? Male risk taking in the praying mantis Tenodera aridifolia sinensis

Male complicity versus conflict over sexual cannibalism in mantids remains extremely controversial, yet few studies have attempted to establish a causal relationship between risk of cannibalism and male reproductive behavior. We studied male risk-taking behavior in the praying mantid Tenodera aridifolia sinensis by altering the risk imposed by females and measuring changes in male behavior. We show that males were less likely to approach hungrier, more rapacious females, and when they did approach, they moved more slowly, courted with greater intensity, and mounted from a greater distance. Similarly, when forced to approach females head-on, within better view and better reach of females, males also approached more slowly and courted with greater intensity. Thus, males behaved in a manner clearly indicative of risk avoidance, and we support the hypothesis of sexual conflict over sexual cannibalism.     

The functional morphology of the praying mantis forelimb (Dictyoptera: Mantodea)

The structure and function of the forelimbs of praying mantids are discussed. A large spine on the femur and the spine on the end of the tibia were shown experimentally to be important in the capture of unrestrained flies. These spines may function to narrow the gap through which a fly may escape while the tibia is closing on the femur. Some of the spines on the femur are hinged at their base; the structure, properties and possible functions of these spines are discussed.
Similar hinged spines are reported on the lorelimbs of Stomatopoda (CrustaceaI but were not found in the Mantispidac (Neuroptera:Insecta). The variation of forelimb structure within the Mantodea is briefly discussed. The theory that the optimum prev size can be predicted from the geometry of the mantid forelimb is critically discussed.     

Community effects of praying mantids: a meta-analysis of the influences of species identity and experimental design

Abstract 1. Generalist arthropod predators are ubiquitous in terrestrial ecosystems but experimental studies have yielded little agreement as to their effects on prey assemblages. Drawing on results from a suite of experimental field studies, a meta‐analysis was conducted of the impact of praying mantids (Mantodea: Mantidae) on arthropod assemblages in order to identify predictable and unpredictable effects of these extremely generalised predators. 2. Results across different experiments were synthesised using the log response ratio framework, with a focus on quantifying net mantid impacts on arthropod density across taxonomic orders and trophic levels of arthropods, paying special attention to the contribution of mantid species identity and experimental design variables, such as the use of cages, length of experiment, and manipulated mantid density. 3. Calculated on a per mantid‐day basis, the net impacts of Tenodera sinensis on arthropod density were generally weaker but more predictable than the effects of Mantis religiosa. Mantids in general had weak negative effects on density for most taxa but exhibited strong negative and positive effects on some taxa. Tenodera sinensis tended to have negative effects on Homoptera, Diptera, and Hemiptera and herbivores as a group, however M. religiosa exhibited greater variation in response of different taxa that appeared to be affected more strongly by experimental design. The effects of Stagmomantis carolina tended to be negative or non‐significant. 4. Experimental cages had little influence on either the sign or magnitude of net community impacts for T. sinensis, however cage experiments reversed the sign of the mean effect for two of six taxonomic orders when the experimental predator was M. religiosa. Cages also increased the variability of effect size greatly for M. religiosa but not for T. sinensis. 5. It was concluded that it is possible to use log response ratios to determine general, predictable trends in a well‐studied system. Similar meta‐analyses of generalist predator effects in other systems should produce predictions of how these predators influence food webs, an important step towards defining more clearly the influences of generalist predators on community structure and dynamics.     

Religious supplicant,seductive cannibal,or reflex machine? In search of the praying mantis

The original, prescientific Western belief that the mantis is a pious, helpful creature became a widely held explanation for the mantid's unique resting (apparently prayerful) posture, and for one of its cryptic displays (extending the forelegs straight out). This belief was a characteristic part of a broader discourse about nature in which ancient authority, religious beliefs, and superstition, but few original observations, mixed freely. Gradually, the belief in mantid gentleness and piousness became a commonplace through the continual retelling of the myths and superstitions surrounding this fascinating insect.By the seventeenth century, a growing interest in observation had begun to replace blind reliance on established wisdom and ancient authority. However, the various young sciences to which the period gave rise did not progress equally, and neither did the subdisciplines within each scientific field; biology, especially entomology, was particularly slow to free itself from past beliefs and contemporary superstitions. In the specific case of the praying mantis, the situation may have been at its worst.     

Internal reproductive anatomy of the praying mantid Ciulfina klassi (Mantodea: Liturgusidae)

Using light and scanning electron microscopy, the internal male and female reproductive anatomy of the praying mantid Ciulfina klassi is identified and described. This is the first detailed study to investigate the internal reproductive morphology of any Mantodea. The female structures identified were (1) paired ovaries with primitive panoistic type ovarioles, (2) a single blind-ended spermatheca with secretory gland cells and surrounding layer of striated muscle, and (3) female accessory glands associated with the production of the ootheca (the egg casing). The male structures identified were (1) paired multi-tubular testes, in which different stages of spermatogenesis were observed, (2) tubular vasa deferentia, (3) seminal vesicles, (4) male accessory glands and (5) a single muscular ejaculatory duct. Knowledge of basic reproductive morphology can be used to infer function and so provide key information for future research into reproductive behavior and physiology in the Mantodea.     

Defensive behaviour in Ghanaian praying mantids

The defensive behaviour of 25 species of praying mantids from Ghana is described. All have camouflage as the primary defence mechanism, either a general resemblance to vegetation, or a specific resemblance to bark, sticks, leaves or grass. Secondary defence mechanisms include running, flying, thanatosis, secretion of fluid from the mouth, startle display and flash colouration. The early instars of several species are ant-mimics. The female Taracbodes afzelii often guards her ootheca and also the young nymphs, and she can distinguish her nymphs from intruding ants which are attacked. Some mantids have a green/brown polymorphism and there is evidence that the frequencies of the two forms vary seasonally. Other mantids are stick, grass or bark mimics, and the possible ways in which the adaptations of these forms have evolved are outlined. The startle display is probably a bluff which protects the mantid to some extent from avian predators. It does not appear to be directed against predaceous mammals. A curious "boxing display" is described from Oxypilus, Anasigerpes and Catasigerpes. It probably functions to space out individuals, not to discourage attacks from predators. The occurrence of this display is used as taxonomic evidence for the close relationship of these three genera.     

A paternity advantage for speedy males? Sperm precedence patterns and female re-mating frequencies in a sexually cannibalistic praying mantid

Scramble competition polygyny is expected when females and/or resources are widely dispersed and not easily monopolized by males, or when there is an abundance of mates during an extremely restricted reproductive period. Additional factors such as first male sperm precedence or low female re-mating rate might further explain the propensity of males to engage in scramble competition. The sexually cannibalistic praying mantid Pseudomantis albofimbriata exhibits a polygynous mating system, where females exist in low-density populations and male competition manifests as the race to find females rather than as direct physical fighting. Here, we aim to determine whether there is a paternity advantage for the first-male to mate and/or a low frequency of female re-mating. First, we determined sperm precedence patterns in P. albofimbriata using the sterile male technique. Second, we tested the likelihood of female re-mating in P. albofimbriata by comparing the close-range approach behaviour and frequency of successful mating attempts for males when paired with virgin as opposed to recently mated females, and by comparing the frequency of long-distance male attraction between virgin and mated females. We found no paternity advantage for the first male to mate, rather a second male advantage. Although mated females were not rejected by males when approached from close-range, they were chemically unattractive to males searching from a distance. Since initial mate attraction in many praying mantids, including P. albofimbriata, is mediated via long-distance chemical communication, we believe the latter result is more ecologically relevant and therefore more important. These results suggest that the relatively low frequency of female re-mating observed in P. albofimbriata may be an additional factor driving scramble competition in this system.     

Sexual deception in a cannibalistic mating system? Testing the Femme Fatale hypothesis

Animal communication theory holds that in order to be evolutionarily stable, signals must be honest on average, but significant dishonesty (i.e. deception) by a subset of the population may also evolve. A typical praying mantid mating system involves active mate searching by males, which is guided by airborne sex pheromones in most species for which mate-searching cues have been studied. The Femme Fatale hypothesis suggests that female mantids may be selected to exploit conspecific males as prey if they benefit nutritionally from cannibalism. Such a benefit exists in the false garden mantid Pseudomantis albofimbriata—females use the resources gained from male consumption to significantly increase their body condition and reproductive output. This study aimed to examine the potential for chemical deception among the subset of females most likely to benefit from cannibalism (poorly fed females). Females were placed into one of four feeding treatments (‘Very Poor’, ‘Poor’, ‘Medium’ and ‘Good’), and males were given the opportunity to choose between visually obscured females in each of the treatments. Female body condition and fecundity varied linearly with food quantity; however, female attractiveness did not. That is, Very Poor females attracted significantly more males than any of the other female treatments, even though these females were in significantly poorer condition, less fecund (in this study) and more likely to cannibalise (in a previous study). In addition, there was a positive correlation between fecundity and attractiveness if Very Poor females were removed from the analysis, suggesting an inherently honest signalling system with a subset of dishonest individuals. This is the first empirical study to provide evidence of sexual deception via chemical cues, and the first to provide support for the Femme Fatale hypothesis.     

On the mimetic association between nymphs of Hyalymenus spp. (Hemiptera: Alydidae) and ants

Nymphs of Hyalymenus , unlike adults, have a highly differentiated ant-like morphology. Both H. tarsatus and H. limbativentris feed mainly on reproductive parts of composites and solanaceous plants, respectively. Mimetic nymphs were observed on plants, together with ants, both day and night; adult Hyalymenus , however, are predominantly nocturnal. Ant-resemblance in nymphs is achieved by several structural adaptations which, when coupled with the mimic's zig-zag locomotion and constantly agitated antennae, produces a striking visual deception. Experiments in captivity showed that mimetic nymphs, but not adult Hyalymenus , are somewhat protected against attacks from the praying mantid Oxyopsis media found on their host plant. Colour and size changes through different nymphal instars of Hyalymenus allow the immature bugs to resemble, during their development, differently sized and coloured ant models. Similar-looking ant species seem to act as Mullerian mimics toward insectivorous vertebrates and invertebrates that avoid ants. It is suggested that nymphs of Hyalymenus gain Batesian protection by resembling available ant models of different Mullerian complexes. Density-dependent selection is thought to be responsible for the observed differences in mimetic morph proportions between populations of mimics, as well as for the mimetic strategy itself employed by nymphs of Hyalymenus.     

Geographic variation in genital morphology of Ciulfina praying mantids

Geographic variation in morphological traits is widespread and important to our current understanding of evolutionary processes. Although male genitalia are perhaps the most divergent morphological traits in animals, geographic variation in genital traits has received little attention and the mechanism driving such variation is unclear. The species isolation hypothesis of genital evolution makes explicit predictions about geographic variation in genitalia predicting patterns of genital divergence that reflect the risk of mating with related but incompatible species. The sexual selection and pleiotropy hypotheses, however, predict general levels of geographic variation that reflect divergent sexual selection pressures or genetic drift. To test these predictions, we investigated geographic variation in genital morphology in the praying mantid genus Ciulfina (Mantodea: Liturgusidae) using elliptic Fourier analysis. We found significant levels of geographic variation in the genital morphology of four Ciulfina species irrespective of the relative proximity of different populations to contact zones with other species. These results reject the species isolation hypothesis, and instead support either the sexual selection or pleiotropy hypotheses to explain patterns of genital evolution in this genus.     

Mate location, antennal morphology, and ecology in two praying mantids (Insecta: Mantodea)

The sensory systems employed by animals to locate potential mates are diverse. Among insects, chemical and acoustic signals are commonly used over long distances, with visual signals playing a role in close-range orientation and courtship. Within groups that exhibit a scramble competition mating system, selection on mate searching ability will be particularly strong. Clearly, aspects of the species ecology, such as habitat complexity and population density, will be crucial in the evolution of mate searching systems and sexual signals. Praying mantids exhibit both chemical and visual sexual signalling behaviour, and also vary in their ecology. This study employs scanning electron microscopy of antennal sensory morphology and behavioural assays to investigate the relative importance of chemical and visual signalling in two Australian praying mantid species: Pseudomantis albofimbriata and Ciulfina biseriata . As predicted, the high level of habitat complexity, low population density and strong male dispersal capability of P. albofimbriata corresponded to the use of airborne sex pheromones. Conversely, the open habitat, high population density, and poor dispersal of C. biseriata corresponded to a greater reliance on short-range visual cues for mate location.  © 2007 The Linnean Society of London, Biological Journal of the Linnean Society , 2007, 91 , 307–313.     

Does a single meal affect female reproductive output in the sexually cannibalistic praying mantid Iris oratoria?

1. One explanation of the evolution of sexual cannibalism, the female’s consumption of a male during or following courtship or copulation, is that this behaviour increases the female’s fitness. This study tests the assumption that a single meal increases female reproductive output significantly in the sexually cannibalistic praying mantid Iris oratoria L. 2. In 38 mating trials, seven of the females cannibalised the males. In order to augment the number of females that fed, an additional nine females were each fed one cricket nymph at the end of the mating trial. 3. Three measures of female reproductive output – the occurrence of oviposition, the mass of the first ootheca, and the number of eggs in the first ootheca – increased significantly with female feeding condition, which was a reflection of food consumed before the mating trial. Females that copulated later in the season tended to lay lighter oothecae. 4. The females’ consumption of a meal during the mating trial, either a conspecific male or a cricket, did not influence any measure of reproductive output significantly, although possible effects upon subsequent oothecae cannot be ruled out. 5. If, as the present study suggests, a single meal provides a negligible or delayed benefit to female reproductive output, the evolution of sexual cannibalism might lie in alternative explanations, which include possible fitness benefits to cannibalistic females in the nymphal stage or possible paternity benefits to the cannibalised males.     

Behavioral response of mantid Tenodera aridifolia (Mantodea: Mantidae) to windy conditions as a cryptic approach strategy for approaching prey

Crypsis can be either defensive or aggressive in function, and the first evidence that crypsis reduces the probability of being detected by a predator was collected almost a century ago. Crypsis in mantids may reduce the probability that a mantid will be detected by its prey, but no experiments have been carried out to test this idea. We tested the hypothesis that the approach strategy of the mantid Tenodera aridifolia (Stoll) toward prey when the wind is blowing is adaptive. Significantly less time elapsed between the discovery of the prey by the predator and capture action under windy conditions than under windless conditions. Approach behaviors (walking and body swaying) were observed more frequently under windy than under windless conditions. When the wind stopped, mantids became still, and they changed their behavior in response to alternately changing wind conditions. Moreover, the discovery rate of the predator mantids by conspecific prey mantids was significantly lower on swaying leaves than on fixed leaves. The capturing rate of the prey by the mantid was significantly higher under windy conditions than under windless conditions. We suggest that the strategy of approaching prey quickly when the wind blowing is adaptive for reducing the risk of discovery and escape by the prey.     

You Are What You Eat: Food Limitation Affects Reproductive Fitness in a Sexually Cannibalistic Praying Mantid

Resource limitation during the juvenile stages frequently results in developmental delays and reduced size at maturity, and dietary restriction during adulthood can affect longevity and reproductive output. Variation in food intake can also result in alteration to the normal pattern of resource allocation among body parts or life-history stages. My primary aim in this study was to determine how varying juvenile and/or adult feeding regimes affect particular female and male traits in the sexually cannibalistic praying mantid Pseudomantis albofimbriata. Praying mantids are sit-and-wait predators whose resource intake can vary dramatically depending on environmental conditions within and across seasons, making them useful for studying the effects of feeding regime on various facets of reproductive fitness. In this study, there was a significant trend/difference in development and morphology for males and females as a result of juvenile feeding treatment, however, its effect on the fitness components measured for males was much greater than on those measured for females. Food-limited males were less likely to find a female during field enclosure experiments and smaller males were slower at finding a female in field-based experiments, providing some of the first empirical evidence of a large male size advantage for scrambling males. Only adult food limitation affected female fecundity, and the ability of a female to chemically attract males was also most notably affected by adult feeding regime (although juvenile food limitation did play a role). Furthermore, the significant difference/trend in all male traits and the lack of difference in male trait ratios between treatments suggests a proportional distribution of resources and, therefore, no trait conservation by food-limited males. This study provides evidence that males and females are under different selective pressures with respect to resource acquisition and is also one of very few to show an effect of juvenile food quantity on adult reproductive fitness in a hemimetabolous insect.