Neuroterus valhalla, Brandão-Dias & Zhang & Pirro & Vinson & Weinersmith & Ward & Forbes & Egan, 2022

Brandão-Dias, Pedro F. P., Zhang, Yuanmeng Miles, Pirro, Stacy, Vinson, Camila C., Weinersmith, Kelly L., Ward, Anna K. G., Forbes, Andrew A. & Egan, Scott P., 2022, Describing biodiversity in the genomics era: A new species of Nearctic Cynipidae gall wasp and its genome, Systematic Entomology 47 (1), pp. 94-112 : 100-103

publication ID	https://doi.org/ 10.1111/syen.12521
DOI	https://doi.org/10.5281/zenodo.5903592
persistent identifier	https://treatment.plazi.org/id/9B48474C-E814-8E14-FCD2-999E1905E9CD
treatment provided by	Diego
scientific name	Neuroterus valhalla
status	sp. nov.

Treatment

Neuroterus valhalla sp. nov. Brandão-Dias, Zhang, Weinersmith, Forbes & Egan

Diagnosis: Neuroterus valhalla keys to couplet 6 in Kinsey (1923) in the subgenus Diplobius, which can be recognized by the presence of malar sulcus, 13 antennal segments, absence of parapsidal grooves, simple tarsal claws or with a very short tooth, and induces polythalamous leaf/stem galls and monothalamous anther galls. Only N. valhalla and three other Neuroterus species ( N. floricola Kinsey, N. verrucum Pujade-Villar, and N. fusifex Pujade-Villar & Ferrer-Suay ) are known to induce catkin or stem galls, all of which have alutaceous to delicate coriaceous mesoscutum ( Kinsey, 1923; Pujade-Villar et al., 2014, 2016). Neuroterus valhalla is the only species recorded from oak section Virentes, while the other three are found on oak section Quercus . Neuroterus floricola Kinsey , which are only known from the sexual generation and induces simple catkin galls similar to N. valhalla but on Quercus douglasii Hook. & Arn. in California, can be differentiated based on the presence of very faint anterior parallel lines in N. floricola which are absent in N. valhalla ( Kinsey, 1923) . The two Mexican species are N. verrucum, which is only known from the asexual generation that induces cryptic stem galls on Quercus laeta Liebm. , and N. fusifex , which is only known from the sexual generation also found on Q. laeta in Mexico, induces multilocular, ovoid catkin galls. It is possible these two Mexican species are alternate generations of each other given the morphological and host use similarities, but a revision of the genus is beyond the scope of this paper. Nevertheless, N. valhalla differs from both Mexican species by the indistinct epistomal sulcus and clypeo-pleurostomal line and the transfacial distance slightly longer than the height of eye.

Material examined. Holotype: USA, TX, Houston, Rice University Campus , 29.718 N, 95.400 W, 11.III.2020 (Egan Lab Leg.), Em. 18.III.2020, Catkin gall on Quercus virginiana . USNMENT01448617 , GoogleMaps paratypes same locality as holotype 3♀, USNMENT01558416 , GoogleMaps 01558515 , GoogleMaps 01558518 . GoogleMaps Same locality and data as holotype, Em. 26.II.2020, gall in nodes of branches, 3ǒ, asexual generation, USNMENT01558623 , GoogleMaps 01558269 , GoogleMaps 01558597 . GoogleMaps

Sexual generation

Females

Body length = 1.1 mm (n = 4).

Colour: Body brown. Mandibles light yellow, antennae and apices of femur, basal area of tibia and whitish, tarsomeres dark brown ( Figure 3a View Fig ).

Head: Transverse in dorsal view, 3.0 × as wide as high in front view and slightly wider than mesosoma ( Figure 5a View Fig ). Lower face alutaceous to smooth, with sparse setae, without striae radiating from clypeus. Gena 1.5 × as wide as transverse diameter of eye, not visible in frontal view; malar space 0.3 × as long as eye height, malar sulcus present; mandibles tridentate. Ocellar area slightly elevated; POL:OOL:LOL ratio 2.5:1:1.5. Transfacial distance 1.1 × the height of eye; diameter of torulus (including rims) 1.1 × that of intertorular distance; inner margins of eyes very slightly converge ventrally. Clypeus small, rounded, alutaceous in the centre, smooth lateral. Anterior tentorial pits distinct, epistomal and clypeo-pleurostomal line absent ( Figure 5a View Fig ). Frons, vertex and interocellar area alutaceous, shiny and glabrous. Occipital carina absent. Antenna ( Figure 5d View Fig ) with 13 antenomeres; pedicel rounded; F1 1.6 × as long as F2, not enlarged or curved; ratio of antennal segments: 1.7:1.1:1.9:1.4:1.3:1.1:1.3:1.4:1.2:1.2:1.0:1.0:1.7; placodeal sensilla on F3-F13, and erect setae in all antennal segments.

Mesosoma: Around 1.1 times as long as high in lateral view, glabrous ( Figure 5b View Fig ). Pronotum alutaceous and shiny. Mesoscutum 1.1 × as long as wide in dorsal view, weakly alutaceous, smooth in the centre, with very few sparse setae laterally. Notauli anterior parallel, parapsidal lines and parascutal carina absent. Scutellum weak alutaceous, around 0.8 × as long as mesoscutum, broader than long, not overhanging metanotum, surface with some sparse short setae, slightly pointed distally; scutellar foveae absent; superficial, shiny anterior scutellar depression present. Mesopleuron and mesopleural triangle alutaceous ( Figure 5f View Fig ), almost without setae; axillula alutaceous ( Figure 5c View Fig ), with few sparse setae; dorsellum alutaceous, subrectangular, metapleural sulcus reaching mesopleuron at half of its height. Propodeum alutaceous, glabrous; medial carina present, with rugose carinae. Nucha short alutaceous to smooth.

Legs: Tarsal claws with short tooth. ( Figure 5e View Fig ).

Forewing: Hyaline, slightly longer than body. Coastal margin with cilia; Radial cell around four times as long as wide; Rs straight; areolet large; Rs + M incomplete, Cu1 separated ( Figure 3a View Fig ).

Metasoma: Shorter than head + mesosoma ( Figure 3a View Fig ), slightly longer than high in lateral view. Metasomal tergites without setae, smooth and shiny. Prominent part of ventral spine of hypopygium short, tapering to apex, around 1.4 × as long as wide, with very few long sparse setae laterally that extend beyond apex of spine.

Gall: In staminate flowers of catkin inflorescences. Single-chambered (monothalamous), often in clusters, smooth centre with trichomes on the border, golden yellow colour and oblong/oval shape. No larger than 1.2 mm. ( Figure 3b View Fig ).

Males

Unknown.

Asexual Generation

Body length = 1.1 mm (n = 3).

Colour: Mostly brown, tarsi, scape, pedicel and the first two antennal segments light yellow. Structure and sculptures as the sexual generation ( Figure 3c View Fig ) with the following differences: 12 antennal segments, ocelli not raised and tarsal claw almost simple.

Gall: Cryptic gall in nodes of branches, often found adjacent to leaf scars and side branches, monothalamous, no longer than 2.8 mm ( Figure 3d,e View Fig ).

Etymology: The species’ name refers to the location of the host tree on which it was first found: Outside of ‘Valhalla’, a graduate-student run bar on Rice University campus. The bar is named Valhalla, which is a great hall in Norse mythology where ‘Odin receives the souls of heroes fallen bravely in battle’ ( O’donoghue, 2007).

Life history

Biology: Like most other known members of Cynipini , Neuroterus valhalla has two alternating generations that induce galls where their larvae feed ( Figure 1 View Fig ). The stem node (asexual) generation wasp ( Figures 1C View Fig and 3a View Fig ) develops over the course of approximately 11 months within minute crypt galls found on the stem nodes ( Figures 1E View Fig and 3f View Fig 1 View Fig ), from which it will emerge in synchrony with the host’s flowering phenology, typically during February ( Figure 4 View Fig ). They will live as adults for approximately 2 days, as determined by lab rearing, only to find and oviposit in developing catkin buds ( Figure 3b View Fig ), where minute golden oval galls will develop ( Figures 1B View Fig and 3c View Fig 1 View Fig ). The catkin (sexual) generation wasps ( Figures 1A View Fig and 3d View Fig ) will then swiftly develop over the course of about 3 weeks within these gall structures and emerge in March ( Figure 4 View Fig ). Upon emergence, adults live for approximately 2 days, possibly mate (if males are confirmed in the future), and oviposit into stem nodes near a leaf insertion ( Figures 1D View Fig and 3e View Fig ), completing the cycle.

Host: The population studied here uses Q. virginiana as its host. Additionally, we have incidentally collected two adult N. valhalla individuals emerging from Quercus geminata ( Weinersmith et al., 2020) , which were confirmed to be the same lineage ( Figure 2 View Fig ).

Distribution: Confirmed in southeast Texas (Harris county) and the panhandle of Florida (Walton county). Most likely, extending to match much of the distribution of its host plants, Q. geminata and Q. virginiana , across the coastal southeastern United States, and potentially throughout the range of American live oaks in the subsection Virentes.

Genome description

The genome (GenBank accession WSXT00000000.1) has a GC content of 34.86%, and predicted size of 1.1 Mbp. This is a below-average genome size for the Cynipidae family (average 1.45 Mbp; Table 2 View Table 2 ), and the smallest genome reported to date within the tribe Cynipini ( Table 2 View Table 2 ). The assembly has a scaffold N50 of 344 Kbp, L50 of 14, and an average coverage of 110 ×. Auniversal single-copy ortholog search (BUSCO) resulted in 94.5% of Eukaryotic genes present, 81.6% of which are complete.

A repetitive element annotation revealed that interspaced repeats represent 64.5% of the genome ( Table 3 View Table 3 ), most of which are unclassified repetitive sequences (42.7%), and retrotransposons (10.94%). Apreliminary in-silico gene annotation approach using only ab initio and protein-based annotation tools resulted in 32,005 predicted genes, including 18,802 multiexon protein-coding genes ( Table S1 View Table 1 ).

In an ortholog gene group (orthogroup) analysis, 18044 (56.4%) of the genes were assigned to 8186 orthogroups, 61 of which were species-specific ( Table S2 View Table 2 ). As expected, the biggest assignment overlap was with B. kinseyi , which is the only other Cynipidae wasp with an annotated genome (13,561 genes in 7623 orthogroups, Tables S3 View Table 3 and S4), followed by Nasonia vitripennis (10,359 genes in 6428 orthogroups, Tables S3 View Table 3 and S4), which has the best annotated genome of the Chalcidoidea. The same analysis revealed that the genome of both N. valhalla and B. kinseyi has the two highest number of gene duplication events within genomes analysed (5411 and 11,461 respectively; Table S5). Given the low taxonomic resolution of the analysis, it is likely that most of these are associated with duplication events within Cynipidae .