Introduction

The speciose family Ichneumonidae is currently divided into about 38 subfamilies (Quicke et al. 2009), although some groupings are treated differently by different authors (see, for example, the website of the American Entomological Institute: http://www.amentinst.org/). This large number of subfamilies has been divided into a number of subfamily groupings, largely by the pioneering work of Wahl (1986, 1990, 1991) and Gauld (1985), with the details refined by Quicke et al. (2009). Although we are working towards a relatively stable higher classification of the Ichneumonidae, there are many areas of uncertainty, such as the classification of the various Ctenopelmatinae tribes in relation to several other subfamilies (Gauld and Wahl 2006; Quicke et al. 2009). Another area of difficulty is the pimpliformes group of subfamilies. Relationships within this clade (see Wahl 1986, 1990; Wahl and Gauld 1998; Quicke et al. 2009) have proved difficult to reconstruct, partly because of missing biological and larval information for some enigmatic taxa and partly because the 28S D2 ribosomal RNA data do not provide much support for subfamily or tribal relationships in this area. It can be inferred that the pimpliformes underwent a rapid radiation which has resulted in few discrete morphological apomorphies and the recognition of various very small groups of species as discrete subfamilies. One such subfamily is Collyriinae, comprising only one genus, Collyria Schiødte, until recently. After this paper was accepted for publication, Kuslitzky and Kasparyan (2011) described a second genus of Collyriinae, Aubertiella Kuslitzky and Kasparyan, 2011, which we have not been able to include in the phylogenetic analyses here. Although excluded from the pimpliformes by Gauld (1997) and Wahl and Gauld (1998), Collyria shows some clear pimpliform apomorphies, such as the basally elongated propodeum, and clearly grouped with the pimpliformes in Quicke et al.’s (2009) combined morphological and molecular phylogenetic analyses. As the Collyriinae is a subfamily now containing only two genera, defined by some unusual character states within the Ichneumonidae, the current diagnosis of the subfamily was, until Kuslitzky and Kasparyan (2011), the diagnosis of the original genus, Collyria, and now requires reassessment with the addition of more plesiomorphic genera.

Two of the authors (M-LS and S-PS) received a single specimen of a distinctive ichneumonid collected in Jiangxi province, P.R. China. Unfortunately, further fieldwork by M-LS and S-PS in the type locality has failed to uncover any further specimens. This specimen proved very difficult to place in any subfamily, with a combination of character states that could almost equally feasibly place it in Poemeniinae or Collyriinae. For example, both subfamilies have an elongate propodeum with the spiracle only a little anterior to the middle; they both often lack transverse carinae on the propodeum; the hind coxa is elongate; the first metasomal segment is usually of a similar, elongate shape; the first abscissa of hind wing vein cu is much shorter than vein cu-a. This specimen, which obviously represents an undescribed species and genus, lacks the apomorphies of Collyria, namely the decurved ovipositor with small serrations along the lower margin and the distinctive claw characters (fore and mid tarsal claws each with a median tooth), although it does have lobate fore and mid claws, in common with several pimpliform taxa. The new specimen lacks the principle apomorphies of the Poemeniinae, namely the ventral continuation of the epomia parallel to the lower margin of the pronotum and the laterally expanded foramen magnum (although this is difficult to see in the single new specimen). As well as the character states that are common to Poemeniinae and Collyria, the new specimen shows three characters of the head that led us to believe that its affinities are closer to Collyria, namely the short antennae, the presence of a bifurcate carina from the dorsal half of the face to between the antennae, and a weak median tubercle on the clypeus. After much deliberation, we hypothesised that this specimen represents a new genus of Collyriinae. To test this hypothesis, we coded the specimen of Bicurta sinica sp. n. and Collyria coxator (Villers) for Wahl and Gauld’s (1998) morphological characters, to establish the position of these genera within the pimpliformes.

Materials and methods

For the phylogenetic analyses, codings were based on the matrix of Wahl and Gauld (1998) and on specimens in the Natural History Museum, London and in the Insect Museum, General Station of Forest Pest Management (GSFPM), State Forestry Administration, People’s Republic of China (the holotype of Bicurta sinica sp. n.).

The character codings for Bicurta gen. n. and Collyria are shown in Table 1 with the character numbers as in Wahl and Gauld (1998). Given that these genera share some distinctive characters that were not included in Wahl and Gauld’s analysis, two additional characters were included in our matrix.

Character 92. Dorsal face (0) lacking a bifurcate carina between the antennal sockets (Fig. 6); (1) possessing a bifurcate carina between the antennal sockets.

Character 93. Antenna length (0) normal, at least 0.8× length of fore wing; (1) short, only about 0.65-0.7× length of fore wing.

Both of these characters were coded as ‘0’ for other taxa in Wahl and Gauld’s (1998) matrix. For Collyria, characters of internal anatomy, ovipositor and larval morphology were taken from Quicke et al. (2009). Morphological terminology mostly follows Gauld (1991). Morphological terms are linked to anatomical concepts in the Hymenoptera Anatomy Ontology (Yoder et al. 2010). URIs are provided in Table 2. Note that, at the time of writing, wing vein nomenclature and several other morphological terms used here have not yet been included in the HAO.

We have also made some changes to the character codings employed by Wahl and Gauld (1998). Wahl and Gauld’s character 45 (number of bullae in fore wing vein 2m-cu) was re-coded for Agriotypinae (changed to ‘1’) and for Labeninae (to polymorphic), following Bennett (2001); their character 46 (shape of the areolet) has been re-coded as ‘?’, rather than ‘0’, for taxa lacking fore wing vein 3rs-m. Following Matsumoto and Broad (2011), Rodrigama Gauldhas been re-coded for character 19 (occipital carina is dorsally incomplete), 26 (epicnemial carina is present) and 34 (hind coxa is elongate). Note that Rossemia Humala is the valid name for Wahl and Gauld’s Sweaterella (Humala, 2003).

Phylogenetic analyses were carried out in TNT 1.1 (Goloboff et al. 2003), with all characters unordered and using default settings except for the following (as employed by Burks et al. 2011): ratchet weighting probability (up and down) of 5%, 200 iterations, drift of 50 cycles, tree fusing of five rounds, and find minimum length 25 times. Phylogenetic trees were edited in Winclada (Nixon 1999).

SEM images of uncoated specimens were taken using a Leo 1455VP low vacuum scanning electron microscope. Photographs of Bicurta sinica sp. n. were taken using a Canon Power Shot A650 IS and Cool Snap 3CCD attached to a Zeiss Discovery V8 Stereomicroscope and captured with QCapture Pro version 5.1.

Results Phylogenetic analyses

With characters unordered and unweighted, 12 trees of length 240 were found; the strict consensus is shown in Fig. 1. The relationships betweeen subfamilies are largely unresolved but Bicurta and Collyria are recovered as a clade, as are all other subfamilies with multiple representatives, except Cylloceriinae. Searching with implied weights of values ranging from k=1 to k=10 resulted in a single topology, shown in Fig. 2. This phylogeny is similar to that obtained by Wahl and Gauld (1998), except that Xoridinae shift to the sister group of the labeniformes plus ichneumoniformes and the genera of Poemeniinae are fully resolved. Bicurta+Collyria are recovered as a clade and as the sister group to Rhyssinae. As a test of the robustness of the results, characters 72 to 93 (which include both those characters missing for a large number of taxa and the two additional characters included in this study) were excluded and the analysis run using the same parameters. The topology of Collyriinae, Rhyssinae and Poemeniinae remained the same, although relationships within the remaining pimpliformes collapsed in the strict consensus (Fig. 3).

In these analyses, the monophyly of Collyriinae is attested by numerous homoplasies and two synapomorphies: the presence of a bifurcate carina on the upper face extending to between the antennal sockets and the short antennae. The sister group relationship of Collyriinae to Rhyssinae was unexpected and is supported by a single apomorphy, the absence of the posterior transverse carina of the propodeum. The monophyly of Poemeniinae+Rhyssinae+Collyriinae is again weakly supported by one unambiguous apomorphy (the small and subrectangular clypeus) and two homoplasies (hind wing vein 2/Cu originating close to vein M and the elongate last visible tergite of the female). In contrast, Quicke et al. (2009), in their combined morphological and molecular analyses, found Collyria to nest within the Diptera-parasitizing clade of pimpliformes, in a topology that seemed to be overwhelmingly influenced by the morphology dataset.

Definition of Collyriinae

The Collyriinae, now comprising the genera Aubertiella, Bicurta gen. n. and Collyria, can be defined by the following characters, based on the phylogenetic analyses presented here and on the description of Aubertiella (Kuslitzky and Kasparyan 2011), although only the first two are autapomorphic for the subfamily: dorsal part of face with bifurcate carina extending between antennal sockets (character not mentioned by Kuslitzky and Kasparyan 2011); antennae short; clypeus with median tubercle; posterior transverse carina of propodeum absent; hind coxa elongate; fore and mid claws with teeth; fore wing vein 3rs-m absent; hind wing vein Cu1much closer to vein M than to A; first tergite lacking longitudinal carinae; glymmae absent; last visible tergite of female elongate (apparently only an apomorphy of Bicurta and Collyria, not Aubertiella - Kuslitzky and Kasparyan 2011); and the ovipositor lacking ventral, apical teeth. The monophyly of Collyria is attested to by an autapomorphy not included in the analysis: the ventral ovipositor valve is weakly serrate along the median ~0.5 (which we contend are not ‘teeth’ as usually defined in the Ichneumonoidea as they are not ridges across the depth of the apical part of the lower valve). The monophyly of Bicurta is supported by some rather weak characters, including the pale markings on the face and malar space; the more posteriorly displaced propodeal spiracle (compared to Collyria); the large, lobe-like teeth on the fore and mid tarsal claws (which may be plesiomorphic with respect to the narrower teeth of Collyria); fore wing vein 2m-cu with one bulla; the first tergite and sternite fused; and the first sternite more than half the length of the tergite.

An expanded phylogenetic matrix, encompassing the genera of Acaenitinae, could reveal some rather different patterns of relationships within the pimpliformes. Several acaenitine genera share character states with collyriines and some poemeniines, such as short antennae, a median tubercle on the clypeus, hind wing vein Cu1 originating close to M and the propodeum lacking transverse carinae. However, acaenitines have a distinctive apomorphic female hypopygium, very different to that of the Collyriinae, Poemeniinae or Rhyssinae.

Taxonomy Discussion

Unfortunately, nothing is known of the biology of Bicurta sinica sp. n. Where known, species of Collyria are koinobiont egg-larval endoparasitoids of stem-sawflies (Hymenoptera: Cephidae) (Salt 1931; Wahl et al. 2007). This is an unusual strategy within Ichneumonidae and presumably accounts for the distinctive ovipositor of Collyria; slender, lacking apical teeth or a notch but with serrations on the lower valves for cutting through grass stems. The slender, featureless ovipositor of Bicurta could well be indicative of oviposition into insect eggs, but this must remain as speculation for now.

An expanded phylogenetic matrix, encompassing the genera of Acaenitinae, could reveal some rather different patterns of relationships within the pimpliformes. Several acaenitine genera share character states with collyriines and some poemeniines, such as short antennae, a median tubercle on the clypeus, hind wing vein Cu1 originating close to M and the propodeum lacking transverse carinae, and it is interesting that various older authors included Collyria within the Acaenitinae (or equivalent grouping). Obviously, acaenitines have a distinctively apomorphic female hypopygium, very different to that of the Collyriinae, Poemeniinae or Rhyssinae.