Podagrion mantis

Podagrion mantis was first described in 1886 by W.H. Ashmead, and was the first species of its genus to have been described from the United States. All species in the genus are parasitoid wasps known only to parasitize mantids. They have been observed most often utilizing the egg case (ootheca) of Stagmomantis carolina, but have also been reported to choose S. limbata or Tenodera angustipennis as hosts, showing a high degree of specialization.

The ootheca is made up of tanning agents and structural proteins that, while being deposited, is watery and tacky, but soon hardens into a stiff foam. The female Podagrion can parasitize the ootheca in either the fresh or hardened state. The female uses her long ovipositor to deposit an egg into the ootheca; as the eggs are developing they consume the mantid larvae before emerging as an adult.

The cumulative effect of several generations of parasitoid wasps on ootheca are estimated to cause over 30% loss of developing mantids and there is a clear negative correlation between parasitoid burden and mantid eclosure.

Morphology
Podagrion species are only 2-3mm, with the female's ovipositor effectively doubling her length. The most distinct characteristic of this tiny wasp is the enlarged, clawed femur. Together with the tibia, the resemblance of this structure to the raptorial forelegs of the mantis, it parasitizes is striking. Other diagnostic characteristics include a thorax flattened to be nearly as high as it is long, clubbed antennae, and in females, a long ovipositor that is surrounded by stabilizing valves.

Podagrion are most likely found worldwide, with members of the Torymidae family mainly being distributed in the Afrotropical, Neotropics, and Australia. P. mantis has been found all throughout the Americas. The wasps are a beautiful metallic green with a muted yellow on antennae and lower portions of legs. Interestingly, of the samples studied by Grissell and Goodpasture, the only major difference between those observed in North America was a difference in coloration, with no other morphological distinctions. Most displayed a dark green coloration, but those found in the southeastern U.S. were more bronzed with yellow hind femora.

Evolution and taxonomy
The superfamily to which Podagrion wasps belong to, Chalcidoidea, is extremely diverse. About 23,000 species have been described, but in actuality the group is estimated to be closer to 500,000 species. Classification below the family level Torymidae, has been revised several times. A recent comprehensive phylogenetic assessment by Janšta, using nuclear coding proteins EF-1α and Wg, ribosomal nuclear genes 18S and 28S, and mitochondrial COI was performed to gain better understanding of origins, dispersal, and relationships among the group. The conclusion placed the genus Podagrion as a monophyletic group, having arisen out of the Palearctic region with the ancestral usage of Mantodea eggs. This assessment agrees with the shared morphology of the animals, all retaining a long ovipositor and a micropilose area on the clava, which is a sensilla-rich area on the antennae aiding the females in finding a suitable site for egg deposition through tapping on the surface of the site. Podagrion is most closely related to the genera Podagrionini and Mantiphagia.

Sexual behavior and reproduction
Parasitoid males emerge one to five days before the females and attempt to wait on the ootheca for the females' arrival. Emerged males have the goal to take possession of the ootheca and will be aggressive with any other emerging or arriving males. They use their powerful hind legs to remove competitors from the ootheca. If no activity (either the emergence of females or appearance of competitive males) happens for long enough, he may fly off. The possessing male will palpate the surface of the ootheca with his antennae, drumming the tips frequently onto the surface at a perpendicular angle. Females may excavate their eclosure tunnels, but then remain immobile inside, possibly waiting for the male's stimulus in order to emerge. When a male finds a female to give his attention to, he stands over her and beats his antennae up and down on her head and the edge of her eclosure tunnel. He will then fan his wings and lift his abdomen repeatedly, creating an audible buzzing sound. He will alternate between these two behaviors until the female emerges. As she emerges, he orients himself behind her, continually palpating her head with his antennae. In response to his palpation, she tucks her antennae as she is emerging. He mounts her, continually swinging his antennae over her eyes in a scissor-like motion, at this point the female's antennae are projected away from her body. He dismounts the female in order to copulate and she assumes a copulation posture. The male's alternation of palpation and buzzing may be abandoned as he attempts to mate with successive females.

As these insects are very small, their dispersal area is limited and sibling pairings frequently occur. The regular inbreeding is thought to not be deleterious because their level of genetic recombination is low due to a small number of chromosomes. The karyotype of P. mantis has not been described, but the highest number found so far in the genus is ten.

Like many Hymenoptera, fertilization is not required for oviposition, in which case all offspring will be haploid males.

Females may deposit eggs into hardened egg cases, sawing and rocking her ovipositor through the foam, and may even lay her own eggs inside the ootheca she has recently emerged from. It is also reported that female wasps may be phoretic on female mantids, hanging onto the host and waiting until she lays her ootheca, parasitizing it immediately before it has a chance to dry and harden

Unlike their hosts, which have one generation per year (univoltine) with egg deposition occurring in summer or fall and hatching in spring or summer, Podagrion wasps are multivoline, with as little as 35 days between generations. Therefore, parasitoid larva in one egg case can be found in varying developmental stages, displaying that a female wasp can deposit her eggs inside it at various times and it may be used by more than one female as an oviposition site. There may also be an overwintering generation, that remains dormant with the mantis eggs for a longer period of time, emerging before they do. And as there are no viable mantis ootheca during the middle of the summer, Fagan and Folarin report that the last generation of parasitoids may delay development, oversummering inside the empty ootheca, awaiting the deposition of new egg cases by their host in the fall.

Development
The cleavage pattern of these insects has not been explicitly described in scientific literature. However, the general pattern to that of other Hymenoptera is likely to apply, though there have been some novel adaptations for endoparasitic wasps. The plesiomorphic state of hymenopteran development consists of a centrolecithal, anhydropic (non-swelling) egg which exhibits superficial cleavage and the animals are protostomic. These parasitoids are classified as ectoparasites, as eggs are deposited on top of an individual mantis egg inside the cell of an ootheca. The development of the parasitoid takes place external to the egg, and at the end of its development the contents of the egg have been entirely consumed, however its membrane remains. The wasps develop in the reverse orientation of the mantids they share the egg case with. When depositing on a horizontal surface, a praying mantis will most often lay her ootheca on the underside, so that when the mantises hatch, they are facing the earth and can utilize gravity to exit the egg and undergo their first molt. The wasp eggs are oriented oppositely, with their posterior end facing the earth and their anterior end facing the substrate on which the ootheca has been deposited. The number of adult wasps emerging from egg cases varies widely, producing only a few to over a hundred. As each developing wasp consumes one mantid larva, there will not be more parasitoids than there were mantids deposited. To emerge from the ootheca the wasps cut a small round hole in the substrate side, often utilizing the pathways already cut for them by previous wasps. It is therefore difficult to determine the number of parasitoids that have emerged from the ootheca.