Neuroterus valhalla Brandão-Dias &amp; Zhang &amp; Pirro &amp; Vinson &amp; Weinersmith &amp; Ward &amp; Forbes &amp; Egan 2022, sp. nov.
Creators: name: Brandão-Dias, Pedro F. P.
name: Zhang, Yuanmeng Miles
name: Pirro, Stacy
name: Vinson, Camila C.
name: Weinersmith, Kelly L.
name: Ward, Anna K. G.
name: Forbes, Andrew A.
name: Egan, Scott P.
Publisher: name: Zenodo
Year: 2022
Subjects: Biodiversity
Taxonomy
Animalia
Arthropoda
Insecta
Hymenoptera
Cynipidae
Neuroterus
Neuroterus valhalla

description: <i>Neuroterus valhalla</i> <b>sp. nov</b>. Brandão-Dias, Zhang, Weinersmith, Forbes &amp; Egan Diagnosis: <i>Neuroterus valhalla</i> keys to couplet 6 in Kinsey (1923) in the subgenus <i>Diplobius</i>, 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 <i>N. valhalla</i> and three other <i>Neuroterus</i> species (<i>N. floricola</i> Kinsey, <i>N.</i> <i>verrucum</i> Pujade-Villar, and <i>N. fusifex</i> Pujade-Villar &amp; 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). <i>Neuroterus valhalla</i> is the only species recorded from oak section <i>Virentes</i>, while the other three are found on oak section <i>Quercus</i>. <i>Neuroterus floricola</i> Kinsey, which are only known from the sexual generation and induces simple catkin galls similar to <i>N. valhalla</i> but on <i>Quercus douglasii</i> Hook. &amp; Arn. in California, can be differentiated based on the presence of very faint anterior parallel lines in <i>N. floricola</i> which are absent in <i>N. valhalla</i> (Kinsey, 1923). The two Mexican species are <i>N. verrucum</i>, which is only known from the asexual generation that induces cryptic stem galls on <i>Quercus laeta</i> Liebm., and <i>N. fusifex</i>, which is only known from the sexual generation also found on <i>Q. laeta</i> 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, <i>N. valhalla</i> 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 <i>Quercus virginiana</i>. USNMENT01448617, paratypes same locality as holotype 3&amp;female;, USNMENT01558416, 01558515, 01558518. Same locality and data as holotype, Em. 26.II.2020, gall in nodes of branches, 3ǒ, asexual generation, USNMENT01558623, 01558269, 01558597. Sexual generation Females Body length <i>=</i> 1.1 mm (n <i>=</i> 4). Colour: Body brown. Mandibles light yellow, antennae and apices of femur, basal area of tibia and whitish, tarsomeres dark brown (Figure 3a). Head: Transverse in dorsal view, 3.0 <i>×</i> as wide as high in front view and slightly wider than mesosoma (Figure 5a). Lower face alutaceous to smooth, with sparse setae, without striae radiating from clypeus. Gena 1.5 <i>×</i> as wide as transverse diameter of eye, not visible in frontal view; malar space 0.3 <i>×</i> 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 <i>×</i> the height of eye; diameter of torulus (including rims) 1.1 <i>×</i> 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). Frons, vertex and interocellar area alutaceous, shiny and glabrous. Occipital carina absent. Antenna (Figure 5d) with 13 antenomeres; pedicel rounded; F1 1.6 <i>×</i> 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). Pronotum alutaceous and shiny. Mesoscutum 1.1 <i>×</i> 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 <i>×</i> 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), almost without setae; axillula alutaceous (Figure 5c), 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). Forewing: Hyaline, slightly longer than body. Coastal margin with cilia; Radial cell around four times as long as wide; Rs straight; areolet large; Rs <i>+</i> M incomplete, Cu1 separated (Figure 3a). Metasoma: Shorter than head <i>+</i> mesosoma (Figure 3a), 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 <i>×</i> 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). Males Unknown. Asexual Generation Body length <i>=</i> 1.1 mm (n <i>=</i> 3). Colour: Mostly brown, tarsi, scape, pedicel and the first two antennal segments light yellow. Structure and sculptures as the sexual generation (Figure 3c) with the following differences: 12 antennal segments, ocelli not raised and tarsal claw almost simple. <b>Gall:</b> 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). <b>Etymology:</b> 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). <i>Life history</i> <b>Biology:</b> Like most other known members of Cynipini, <i>Neuroterus valhalla</i> has two alternating generations that induce galls where their larvae feed (Figure 1). The stem node (asexual) generation wasp (Figures 1C and 3a) develops over the course of approximately 11 months within minute crypt galls found on the stem nodes (Figures 1E and 3f 1), from which it will emerge in synchrony with the host’s flowering phenology, typically during February (Figure 4). 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), where minute golden oval galls will develop (Figures 1B and 3c 1). The catkin (sexual) generation wasps (Figures 1A and 3d) will then swiftly develop over the course of about 3 weeks within these gall structures and emerge in March (Figure 4). 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 and 3e), completing the cycle. <b>Host:</b> The population studied here uses <i>Q. virginiana</i> as its host. Additionally, we have incidentally collected two adult <i>N. valhalla</i> individuals emerging from <i>Quercus geminata</i> (Weinersmith et al., 2020), which were confirmed to be the same lineage (Figure 2). <b>Distribution:</b> 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, <i>Q. geminata</i> and <i>Q. virginiana</i>, across the coastal southeastern United States, and potentially throughout the range of American live oaks in the subsection Virentes. <i>Genome description</i> 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), and the smallest genome reported to date within the tribe Cynipini (Table 2). The assembly has a scaffold N50 of 344 Kbp, L50 of 14, and an average coverage of 110 <i>×</i>. Auniversal single-copy ortholog search (BUSCO) resulted in 94.5% of Eukaryotic genes present, 81.6% of which are complete. <i>Neuroterus valhalla</i> is highlighted in bold. A repetitive element annotation revealed that interspaced repeats represent 64.5% of the genome (Table 3), most of which are unclassified repetitive sequences (42.7%), and retrotransposons (10.94%). Apreliminary <i>in-silico</i> 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). 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). As expected, the biggest assignment overlap was with <i>B. kinseyi</i>, which is the only other Cynipidae wasp with an annotated genome (13,561 genes in 7623 orthogroups, Tables S3 and S4), followed by <i>Nasonia vitripennis</i> (10,359 genes in 6428 orthogroups, Tables S3 and S4), which has the best annotated genome of the Chalcidoidea. The same analysis revealed that the genome of both <i>N. valhalla</i> and <i>B. kinseyi</i> 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. <i>Neuroterus valhalla within the Cynipini phylogeny</i> Both the COI phylogeny (Figure 2) and UCE phylogeny (Figure 6) have recovered the genus <i>Neuroterus</i> as polyphyletic, despite the different taxa represented in each data type. Yet, <i>N. valhalla</i> grouped with other Nearctic <i>Neuroterus</i> species in both datasets, while Palearctic <i>Neuroterus</i> species consistently grouped with representatives of other Cynipini genera such as <i>Cynips</i> and <i>Andricus</i>. Additionally, every Cynipini genus represented by more than one species was recovered as polyphyletic. Those included <i>Andricus</i> Hartig, <i>Cynips</i> L., <i>Callirhytis</i> Foerster, <i>Disholcaspis</i> Dalla Torre &amp; Keiffer and <i>Dryocosmus</i> Giraud. This taxonomic disagreement suggests that a larger, global revision of the genera within the Cynipini is needed.
description: Published as part of <i>Brandão-Dias, Pedro F. P., Zhang, Yuanmeng Miles, Pirro, Stacy, Vinson, Camila C., Weinersmith, Kelly L., Ward, Anna K. G., Forbes, Andrew A. &amp; Egan, Scott P., 2022, Describing biodiversity in the genomics era: A new species of Nearctic Cynipidae gall wasp and its genome, pp. 94-112 in Systematic Entomology 47 (1)</i> on pages 100-103, DOI: 10.1111/syen.12521, http://zenodo.org/record/5903588
description: {"references": ["Kinsey, A. C. (1923) The gall wasp genus Neuroterus (Hymenoptera). Indiana University Studies, 58, 1 - 150.", "Pujade-Villar, J., Tovar, D. C., Ruiz, U. M. B. &amp; Melika, G. (2014) First record of Neuroterus galls on twigs in Mexico with description of two new species (Hym.: Cynipidae). Butlleti de la Institucio Catalana d'Historia Natural, 78, 3 - 9.", "Pujade-Villar, J., Garcia-Martinon, R. D., Equihua-Martinez, A. &amp; Estrada-Venegas, E. (2016) Neuroterus fusifex Pujade-Villar and Ferrey-Suay n. sp. (Hymenoptera: Cynipidae): first record of galls on catkins in Mexico. Folia Entomologica Mexicana, 2, 75 - 83.", "O'Donoghue, H. (2007) From asgard to valhalla: the remarkable history of the norse myths. Bloomsbury Publishing, London.", "Weinersmith, K. L., Forbes, A. A., Ward, A. K., Brandao-Dias, P. F. P., Zhang, Y. M. &amp; Egan, S. P. (2020) Arthropod community associated with the asexual generation of Bassettia pallida (Hymenoptera: Cynipidae). Annals of the Entomological Society of America, 113, 373 - 388."]}