Mecoptera

Zrzavý, Jan, 2008, Four chapters about the monophyly of insect ‘ orders’: A review of recent phylogenetic contributions, Acta Entomologica Musei Nationalis Pragae 48 (2), pp. 217-232 : 225-227

Mecoptera and Siphonaptera : death of one more, parasitic ‘order’

Mecoptera (scorpion flies) are a small holometabolous insect ‘order’ (approximately 600 extant described species in nine ‘families’). The living species of the Mecoptera represent a vestige of a long and diverse evolutionary history begining from the Permian period. Mecopterans have been defined by a medially divided 1st abdominal sternite, the female genital chamber formed by an invagination behind sternum 9, the bulbous male genital capsule with complex genitalia and large gonocoxites, a distinctive proventriculus lined with spicule-like acanthae, the fusion of clypeus and labrum, and the loss of some mouthpart muscles. The monophyly of each mecopteran family is well established by morphological characters. Relationships among the extant families have been analysed by WILLMANN (1987) and WHITING (2002a). Major areas of agreement include basal positions of the Nannochoristidae and Boreidae , and close relationships between the Panorpidae and Panorpodidae . The major difference between the two hypotheses concerned the Bittacidae (either closely related to the Panorpodidae , or one of the most basal clades). The phylogenetics of Mecoptera has centered around two problematic families, the Nannochoristidae and Boreidae (= Neomecoptera).

The Boreidae (‘snow fleas’) is a small group of 26 species distributed throughout North America and Eurasia. Adults emerge in winter and are associated with mosses. Their wings are reduced to small flaps in females and to hooks in males, which function to clasp the female during mating.

The Nannochoristidae (eight species from Australia, New Zealand and temperate South America) have unusual, aquatic larvae, a pigmented larval ‘eye spot’, and unique wing venation characteristics. A possible sister group relationship with the Diptera was proposed (see KRISTENSEN (1999) and references therein; BEUTEL & BAUM (2008)), though most evidence (see below) indicates that nannochoristids are basal mecopterans and their resemblance to flies is based largely on plesiomorphies.

A clade comprising Mecoptera and Siphonaptera (fleas) seems to be well supported (e.g., BEUTEL & GORB 2001, WHITING 2002a,b). A presumably derived feature is the absence of the outer group of microtubuli in the sperm flagellum. Another potential synapomorphy is the specific configuration of the acanthae in the proventriculus. Other features supporting this hypothesis are unspecific reductions, such as, for example, the absence of the extrinsic labral muscles or the absence of labial endite lobes (for detailed analyses of head structures see BEUTEL & BAUM (2008) and BEUTEL et al. (2008)). However, the monophyly of the traditional order Mecoptera has been challenged recently. A sister group relationship between the Boreidae and the Siphonaptera is strongly supported by molecular data ( WHITING 2002a,b) and a comprehensive combined analysis (75 morphological characters, 18S rDNA, 28S rDNA, cytochrome oxidase II, and cytochrome b ( WHITING et al. 2003)). Once the molecular data suggested this relationship, a reevaluation of morphology demonstrated that this is a highly plausible hypothesis (see BEUTEL & POHL (2006) for reviews).

The process of resilin secretion in fleas (pleural arch) and Boreus Latreille, 1816 (wing base) is similar, and different from that of the locust and the dragonfly. Both groups share the ability to jump when disturbed (probably via a similar mechanism) and both often feign death after their leaps. The proventricular spines in fleas and boreids have similar morphology. Other features are the absence of extrinsic labral muscles, absence of arolium, elongation of the labrum and maxillolabium, reduced or lost ocelli, reduced or lost larval legs, and sexual dimorphism in the ventral nerve cord (males having more ganglia than females). Among mecopteroids, only fleas and boreids form silken pupal cocoons. Phylogenetic analysis of longwavelength opsins from the three lineages (flea, snow flea, panorpid) revealed a high degree of similarity between flea and boreid opsins ( TAYLOR et al. 2005). Both groups have multiple sex chromosomes and sperm axoneme coiling around the mitochondrion. On the contrary, some spermatological similarities of Panorpa Linnaeus, 1758 , and Boreus (two longitudinal extra-axonemal rods and a glycocalyx consisting of longitudinal parallel ridges or filaments; see DALLAI et al. 2003) suggest either monophyly of the conventional Mecoptera (quite improbable if confronted with the huge amount of conflicting evidence), or homoplasy.

The most convincing morphological evidence comes from research on ovarioles, which demonstrates that boreid ovaries are fundamentally different from those in other Mecoptera ( ŠTYS & BILIŃSKI 1990, BILIŃSKI & BÜNING 1998, BILIŃSKI et al. 1998). Fleas and boreids share the secondary loss of nurse cells (‘neopanoism’), completion of initial stages of oogenesis during postembryonic development, occurrence of rDNA amplification and resulting appearance of multiple nucleoli, differentiation of the late previtellogenic ooplasm into two clearly recognizable regions, and presence of accumulations of membrane-free, clathrin-like cages.

These data suggest that the Mecoptera , as currently constituted, are a paraphyletic assemblage. While it seems certain that the Boreidae and the Siphonaptera are sister groups, their placement relative to the other Mecoptera is not that well supported by the data. Moreover, while it seems clear that the Nannochoristidae should occupy a basal position, it is not clear whether it is a sister group to the flea-boreid clade or the whole Mecoptera (including the Siphonaptera ). The most comprehensive, morphology and four-gene molecular analysis ( WHITING et al. 2003) supports a major division of the Mecoptera into two clades: the Nannochoristidae-(Boreidae-Siphonaptera) and the Eumecoptera (= remaining Mecoptera ). This pattern is strongly supported also by the histology of nannochoristid ovaries ( SIMICZYJEW 2002). They are (neo)panoistic, with multiple nucleoli in the oocyte nucleus, which suggests an extrachromosomal amplification of the ribosomal DNA. The structure of the ovarioles and the course of oogenesis in nannochoristids thus share derived features with boreids and fleas, but differ significantly from all eumecopterans.

BEUTEL & BAUM (2008) have recently proposed a possible clade comprising the Nannomecoptera, Siphonaptera , and Diptera, supported by the presence of a labral food channel, the absence of the galea, a sheath for the paired mouthparts formed by the labium, very strongly developed labial palp muscles and cibarial dilators, and the presence of a well-defined postcerebral pharyngeal pumping chamber. Moreover, close affinities of the Nannomecoptera with the Diptera are suggested by the presence of a unique sensorial groove on the third maxillary palpomere, the elongate and blade-like lacinia, and possibly by the presence of a frontal apodeme and a primarily lamelliform mandible without teeth. The presence of a salivary channel on the laciniae and a subdivided labrum are shared derived features of Nannochorista and Siphonaptera . On the contrary, the secretion with a strongly developed intrinsic muscle of the salivary duct might be a possible synapomorphy of the Mecoptera including the Boreidae but excluding the Nannomecoptera. By all means, it seems that the Nannomecoptera, Neomecoptera, and Siphonaptera are closely related, and that the precise position of the Diptera within the mecopteroid complex requires more investigation.

The new phylogeny of the mecopteroid complex (= Eumecoptera, Nannomecoptera, Neomecoptera, Siphonaptera ) provides a plausible ecological scenario of the origin of fleas, a situation highly reminiscent of the proposed relationships between liposcelidid psocopterans and the lice. The transition from mosses into mammal nests and dens (during the Mesozoic period, as evidenced by the Late Jurassic-Early Cretaceous boreid Palaeoboreus Sukatcheva & Rasnitsyn, 1992 , and by the early Cretaceous stem-lineage flea Tarwinia Jell & Duncan, 1986 (see GRIMALDI & ENGEL (2005) and references therein) was followed by the Mesozoic/ Cenozoic radiation of the mammals (and their parasites) and by multiple, relatively recent colonizations of birds by the fleas. The fleas (2,380 described species) are by far the most speciose group of the otherwise relictual Mecoptera , a good example of the relatively recent radiation correlated with their parasitism ( WHITING et al. 2008).