Jeyaraney Kathirithamby

Review of the Order Strepsiptera

The morphology, biology and life history of the immature stages, the free‐living and the neotenic females (of the suborders Mengenillidia and Stylopidia respectively) and the free‐living males of the order Strepsiptera are discussed. Strepsiptera are entomophagous parasitoids and are known to parasitize seven orders and thirty‐five families of Insecta. The morphological and physiological changes they cause to the host insect are outlined. The classification of the order is revised; the geographical distribution, phylogenetic system and keys to the families, subfamilies and genera (when possible) are given. As the sexes are dimorphic, separate keys are provided for adult males and neotenic females.

Host-Parasitoid Associations in Strepsiptera

Strepsiptera are obligate endoparasitoids that exhibit extreme sexual dimorphism and parasitize seven orders and 33 families of Insecta. The adult males and the first instar larvae in the Mengenillidia and Stylopidia are free-living, whereas the adult females in Mengenillidia are free-living but in the suborder Stylopidia they remain endoparasitic in the host. Parasitism occurs at the host larval/nymphal stage and continues in a mobile host until that hosts adult stage. The life of the host is lengthened to allow the male strepsipteran to complete maturation and the viviparous female to release the first instar larvae when the next generation of the hosts larvae/nymphs has been produced. The ability of strepsipterans to parasitize a wide range of hosts, in spite of being endoparasitoids, is perhaps due to their unique immune avoidance system. Aspects of virulence, heterotrophic heteronomy in the family Myrmecolacidae, cryptic species, genomics, immune response, and behavior of stylopized hosts are discussed in this chapter.

Tiny genomes and endoreduplication in Strepsiptera.

Using flow cytometry, the genome sizes of two species of Strepsiptera were studied: that of male Caenocholax fenyesi texensis Kathirithamby & Johnston (Myrmecolacidae) at 108 Mb, which is the smallest insect genome documented to date; and those of male and female Xenos vesparum Rossi (Stylopidae), which are 1C = 130 and 133 Mb, respectively. The genome sizes of the following were analysed for comparative purposes: (a) the Hessian fly, Mayetiola destructor (Say), which was previously reported to be the smallest among insects: the male measured at 1C = 121 Mb and the female at 1C = 158 Mb; and (b) the female parasitic, haplodiploid, microhymenopteran wasp, Trichogramma brassicae Bezdenko, which measured at 1C = 246 Mb. The hosts of the strepsipterans were also measured: male Solenopsis invicta Buren, the red imported fire ant (host of male C. f. texensis), which is 1C = 753.3 Mb, and female Polistes dominulus Christ, the paper wasp (host of X. vesparum), is 1C = 301.4 Mb. Endoreduplication (4C) of the genome of the thorax of the male strepsipteran, and higher levels of endoduplication (4, 8, 16C) in the body of the larger female was observed. In contrast, little or no endoreduplication was observed, either in the Hessian fly, or in the parasitic wasp.

Prevalence of the parasite Strepsiptera in Polistes as detected by dissection of immatures

Summary. hough the paper wasp genus, Polistes, is well studied, we know little of the incidence of parasitism in this group. Here we present details of 45 nest dissections for 4 species: P. dominulus (Christ), P. gallicus (L.), P. stabilinus Richards and P. carnifex (F.) to detail levels of parasitism of colony members by the obligate parasitic group of insects, the Strepsiptera. All 4 species showed evidence of parasitism among immature members. For 3 species, more than 50% of inspected nests were parasitized and the levels of parasitism among brood (larvae and pupae) was very high and did not differ significantly between parasitized nests. One species, P. stabilinus, suffered very low levels of parasitism, which may be related to its habitat choice. The number of parasites per host was positively related to the proportion of infected brood (parasite prevalence) and in some cases reached phenomenally high levels, which casts doubt on previ ously assumed mechanisms of infection for nest-making Hymenoptera, i.e. phoresy. We also document cases of egg parasitism and encapsulation in Polistes nests. Our data show that parasitism levels greatly varied among areas. Finally, the recent debate on the competitive advantage of P. dominulus in its introduced range, USA, has credited an absence of strepsipteran parasites of this species in facilitating its spread. For the first time, we document levels of parasitism for this species in its nature P range and this would appear to corroborate previous claims. We place our work in the context of other studies of parasitism of social insects and posit that the genus Polistes may have much to offer to this field.

Strepsiptera and triungula in Cretaceous amber

The first definitive strepsipteran is reported from the Cretaceous, named Cretostylops engeli, n.gen., n.sp., which is an adult male in amber from the mid-Cretaceous (approximately Cenomanian) of northern Myanmar (Burma). A triungulin from the Late Cretaceous (Campanian, c. 80 myo) of Manitoba, Canada is possibly a strepsipteran. The triungulin is described in detail but its morphology does not conform to any known clade of Recent strepsipterans. Other Cretaceous triungula reported here are in Burmese amber and are probably of the family Rhipiphoridae (Coleoptera), and bizarre (possibly coleopteran) triungula in mid-Cretaceous (Turonian, c. 90 myo) amber from New Jersey, USA. Phylogenetic analysis confirms the primitive position of Cretostylops among families of Strepsiptera, but it is not as primitive as Protoxenos in Eocene Baltic amber. Protoxenos and Cretostylops are still too highly modified to address the controversial relationships of Strepsiptera among insect orders, but the generalized structure of the mandible is inconsistent with the hypothesis that this order is the sister group to Diptera or closely related to Mecopterida. Phylogeny of living and Recent Strepsiptera suggests an origin of the order in the Early Cretaceous or Late Jurassic, which is also inconsistent with this order being a sister group to the much older Diptera.

Assessing the odd secondary structural properties of nuclear small subunit ribosomal RNA sequences (18S) of the twisted‐wing parasites (Insecta: Strepsiptera)

We report the entire sequence (2864 nts) and secondary structure of the nuclear small subunit ribosomal RNA (SSU rRNA) gene (18S) from the twisted‐wing parasite Caenocholax fenyesi texensis Kathirithamby & Johnston (Strepsiptera: Myrmecolacidae). The majority of the base pairings in this structural model map on to the SSU rRNA secondary and tertiary helices that were previously predicted with comparative analysis. These regions of the core rRNA were unambiguously aligned across all Arthropoda. In contrast, many of the variable regions, as previously characterized in other insect taxa, had very large insertions in C. f. texensis. The helical base pairs in these regions were predicted with a comparative analysis of a multiple sequence alignment (that contains C. f. texensis and 174 published arthropod 18S rRNA sequences, including eleven strepsipterans) and thermodynamic‐based algorithms. Analysis of our structural alignment revealed four unusual insertions in the core rRNA structure that are unique to animal 18S rRNA and in general agreement with previously proposed insertion sites for strepsipterans. One curious result is the presence of a large insertion within a hairpin loop of a highly conserved pseudoknot helix in variable region 4. Despite the extraordinary variability in sequence length and composition, this insertion contains the conserved sequences 5′‐AUUGGCUUAAA‐3′ and 5′‐GAC‐3′ that immediately flank a putative helix at the 5′‐ and 3′‐ends, respectively. The longer sequence has the potential to form a nine base pair helix with a sequence in the variable region 2, consistent with a recent study proposing this tertiary interaction. Our analysis of a larger set of arthropod 18S rRNA sequences has revealed possible errors in some of the previously published strepsipteran 18S rRNA sequences. Thus we find no support for the previously recovered heterogeneity in the 18S molecules of strepsipterans. Our findings lend insight to the evolution of RNA structure and function and the impact large insertions pose on genome size. We also provide a novel alignment template that will improve the phylogenetic placement of the Strepsiptera among other insect taxa.

Strepsiptera, Phylogenomics and the Long Branch Attraction Problem

Insect phylogeny has recently been the focus of renewed interest as advances in sequencing techniques make it possible to rapidly generate large amounts of genomic or transcriptomic data for a species of interest. However, large numbers of markers are not sufficient to guarantee accurate phylogenetic reconstruction, and the choice of the model of sequence evolution as well as adequate taxonomic sampling are as important for phylogenomic studies as they are for single-gene phylogenies. Recently, the sequence of the genome of a strepsipteran has been published and used to place Strepsiptera as sister group to Coleoptera. However, this conclusion relied on a data set that did not include representatives of Neuropterida or of coleopteran lineages formerly proposed to be related to Strepsiptera. Furthermore, it did not use models that are robust against the long branch attraction artifact. Here we have sequenced the transcriptomes of seven key species to complete a data set comprising 36 species to study the higher level phylogeny of insects, with a particular focus on Neuropteroidea (Coleoptera, Strepsiptera, Neuropterida), especially on coleopteran taxa considered as potential close relatives of Strepsiptera. Using models robust against the long branch attraction artifact we find a highly resolved phylogeny that confirms the position of Strepsiptera as a sister group to Coleoptera, rather than as an internal clade of Coleoptera, and sheds new light onto the phylogeny of Neuropteroidea.

More covert sex: The elusive females of myrmecolacidae

Among evolutionary biologists, considerable interest currently surrounds organisms that seem to be represented entirely by females. Here we discuss a less familiar problem - that of organisms in which females appear to be lacking. Our main example is the Myrmecolacidae (Strepsiptera), an unusual group of entomophagous parasites with dual hosts. Males parasitize ants and females parasitize orthopterans. Although the free-living adult males are frequently collected, the permanently endoparasitic neotenic females are elusive and are seldom encountered.

Remarkable stasis in some Lower Tertiary parasitoids: descriptions, new records, and review of Strepsiptera in the Oligo-Miocene amber of the Dominican Republic

Kathirithamby, J. & Grimaldi, D.: Remarkable stasis in some Lower Tertiary parasitoids: descriptions, new records, and review of Strepsiptera in the Oligo-Miocene amber of the Dominican Republic. Ent. scand. 24: 31-41. Copenhagen, Denmark. April 1993. ISSN 0013-8711. 25-30 million years of parasite stasis is recorded in amber from the Dominican Republic, by the finding of a species of strepsipteran morphologically indistinguishable from Bohartilla melagognatha Kinzelbach, 1969 (Bohartillidae), and two species very close to Caenocholax fenyesi (Pierce 1909) (Myrmecolacidae). A new record is made of a species previously described from Dominican amber, Myrmecolax glaesi Kinzelbach, 1983. The history of the Tertiary strepsipteran fauna is discussed. Minimal ages of taxa are extrapolated based on these amber and other fossils, higher-level cladistic relationships, and fossil dating of major host groups. These new findings are consistent with Kinzelbachs hypotheses of an ancient, Lower Cretaceous/Jurassic origin of the Strepsiptera.

The first molecular phylogeny of Strepsiptera (Insecta) reveals an early burst of molecular evolution correlated with the transition to endoparasitism.

A comprehensive model of evolution requires an understanding of the relationship between selection at the molecular and phenotypic level. We investigate this in Strepsiptera, an order of endoparasitic insects whose evolutionary biology is poorly studied. We present the first molecular phylogeny of Strepsiptera, and use this as a framework to investigate the association between parasitism and molecular evolution. We find evidence of a significant burst in the rate of molecular evolution in the early history of Strepsiptera. The evolution of morphological traits linked to parasitism is significantly correlated with the pattern in molecular rate. The correlated burst in genotypic-phenotypic evolution precedes the main phase of strepsipteran diversification, which is characterised by the return to a low and even molecular rate, and a period of relative morphological stability. These findings suggest that the transition to endoparasitism led to relaxation of selective constraint in the strepsipteran genome. Our results indicate that a parasitic lifestyle can affect the rate of molecular evolution, although other causal life-history traits correlated with parasitism may also play an important role.