Perilampus neodiprioni Yoo & Darling, 2024

Yoo, Jeong Jae & Darling, D. Christopher, 2024, Integrative taxonomic revision of the Nearctic Perilampus hyalinus species complex (Hymenoptera, Chalcidoidea, Perilampidae) resolves 100 years of confusion about the host associations of P. hyalinus Say, Journal of Hymenoptera Research 97, pp. 1301-1383 : 1301-1383

Perilampus neodiprioni Yoo & Darling sp. nov.

Figs 8 , 9

Type locality.

Canada, Ontario, Haliburton County.

Type material.

Holotype. “ CANADA: ONT. Haliburton Hwy 16, 3.8 m. E. Minden Ex: Neodiprion lecontei in red pine plantation. VIII. 28.93. DC Darling ”, “ Lab Reared 1994 S. Perlman M. Sc. thesis ”, “ BOLD COI- 5 P Sequence, 325 bp ”. The holotype is card-mounted (Female ROME 183975 , ROM). ROM Online Collection .

Paratypes. Canada: 3 males. Ontario: 3 males. Nipissing Dist., Algonquin P. P., Cameron Road : (3 males: ROME 152669 - CNC; BOLD: AEE 8879 ; ITS 2; ROME 152668 - ROME; BOLD: AEE 8879 ; ITS 2; ROME 183971 - ROME; BOLD: AEE 8879 ) . USA: 1 female, 2 males. Massachusetts: 1 female, 2 males. Franklin Co., Montague, Montague Plains WMA : (1 female: ROME 162273 - USNM; BOLD: AEE 8879 ; ITS 2. 2 males: ROME 162275 - ROME; BOLD: AEE 8879 ; ITS 2; ROME 162274 - USNM; BOLD: AEE 8879 ; ITS 2) .

Material examined.

Canada: 79 females, 97 males. USA: 36 females, 33 males. (Suppl. materials).

Additional material examined.

Belize: 9 females, 4 males. Stann Creek District: 9 females, 4 males. 4 1 / 2 mis., Stann Creek Valley : (4 females: ROME 185928 - USNM; ROME 185929 - USNM; ROME 199572 - USNM; ROME 199573 - USNM. 1 male: ROME 185926 - USNM) ; 5 1/2 mi Stann Creek Valley : (1 male: ROME 201411 - FSCA) ; Stann Creek Valley : (5 females: ROME 185927 - USNM; ROME 199574 - USNM; ROME 199575 - USNM; ROME 199576 - USNM; ROME 199578 - USNM. 2 males: ROME 199571 - USNM; ROME 199577 - USNM) .

Etymology.

The specific epithet is a noun in the genitive case meaning “ of Neodiprion ”, in reference to the species’ predilection for pine sawflies and their primary parasitoids.

Description.

Female (Fig. 8 ). Length: 3.5–5.0 mm. Color: head iridescent greenish blue or violet, usually without black coloration between lateral ocellus and frontal carina; mesosoma, and metasoma iridescent greenish blue or violet; clypeus ventral margin black (Fig. 8 I ); antenna with scape and pedicel weakly iridescent greenish blue or violet, flagellum brown or black, lighter ventrad and distad.

Head (Fig. 8 G – I ): in dorsal view transverse, width slightly greater than twice length, HW / HL 2.1–2.2. Frontal carina: in anterior view straight to weakly sinuate below midlevel of eye; in dorsal view gradually narrowed V shape around median ocellus, FC / MOD 1.5–1.9; distance from lateral ocellus short, FCLO / LOD 0.6–0.7. Scrobal cavity: in anterior view wide, SW / HW about 0.5. Ocelli (Fig. 8 G ): a line between anterior margin of lateral ocelli reaching anterior margin of median ocellus or nearly bisecting median ocellus. POL / OOL 1.8–2.0. Ocellar ratios LOD: POL: OOL: LOL 1, 3.0–3.3, 1.6–1.8, 1.1–1.4. Vertex: with strong to weak transverse striations, without large piliferous punctures. Parascrobal area: in lateral view gradually narrowed towards lower eye margin; width narrow, PSW / EL about 0.3; sculpture strongly to weakly striate, rarely smooth, without large piliferous punctures. Gena: entirely or mostly striate along outer eye margin with narrow and short smooth area, striate behind. Malar space: MSL / EH 0.2–0.3. Lower face (Fig. 8 H, I ): with setae sparse laterad torulus, and usually sparse below. Clypeus (Fig. 8 I ): CW / CH 1.3–1.4; ventral margin concave; setae evenly distributed, or with small bare area without setae medially.

Mesosoma (Fig. 8 B – F, J – M ): Lateral panel of pronotum: slightly narrower than or about as wide as prepectus, LPP / PPT 0.7–0.9; without flange or with small rounded flange below level of mesothoracic spiracle in posterior oblique view (Fig. 8 D ). Mesofemoral depression: imbricate-alveolate (Fig. 8 L, M ), or weakly imbricate, rugulose, or smooth. Mesoscutum: punctures angulate, with narrow or slightly wide and weakly coriarious interspaces (Fig. 8 B ); lateral lobe usually weakly punctate with coriarious interspaces along notaulus (Fig. 8 C ); parascutal carina broadly curved, acuminate (Fig. 8 J ). Mesoscutellum: apex with inner margins gradually diverging (Fig. 8 K ), rarely rounded; punctures angulate, with narrow or slightly wide and weakly coriarious interspaces. Axilla: in lateral view imbricate dorsad and rugose-areolate (Fig. 8 F ) or carinate ventrad. Axillula (Fig. 8 E ): usually with one or more piliferous punctures dorsad. Fore wing: stigma small, 2.0–2.5 × as wide as postmarginal vein.

Male (Fig. 9 ). Length: usually smaller, 2.7–3.8 mm. As in female, except: Color: mesonotum sometimes with weak cupreous iridescence. Frontal carina (Fig. 9 D ): distance from lateral ocellus shorter, FCLO / LOD 0.5–0.6. Scape (Fig. 9 G, H ): pits sparse, covering 0.3–0.4 × scape length.

Diagnosis.

Perilampus neodiprioni can usually be distinguished by an axillula with one or more piliferous punctures dorsad (Fig. 8 E cf. Fig. 4 E ). The specimens with a smooth axillula are most similar to P. hyalinus , but can often be differentiated by the strongly imbricate to imbricate-alveolate sculpture of the mesofemoral depression (Fig. 8 L, M cf. Fig. 4 L, M ); and the gradually diverging inner margins of the apex of the mesoscutellum (Fig. 8 K cf. Fig. 4 K ).

Distribution

(Fig. 25 B ). South-eastern Canada and central and eastern USA: Canada (Ontario, Quebec), USA (Arkansas, Florida, Illinois, Massachusetts, Michigan, New York, North Carolina, Texas, Virginia, West Virginia, Wisconsin). Possibly Belize (Stan Creek District).

Host association.

Perilampus neodiprioni can develop as a primary parasitoid attacking Neodiprion sawflies (Fig. 26 B ), or as a hyperparasitoid that parasitizes dipteran (Fig. 26 D ) and hymenopteran parasitoids of Neodiprion sawflies (Fig. 26 C, E ). Hosts: Diprionidae ( Hymenoptera ). Neodiprion pratti banksianae Rohwer. Neodiprion excitans Rohwer. Neodiprion lecontei (Fitch) . Neodiprion merkeli Ross. Neodiprion pinetum (Norton) . Neodiprion rugifrons Middleton. Neodiprion swainei Middleton Neodiprion virginianus Rohwer. Tachinidae ( Diptera ). Vibrissina spinigera (Townsend) from N. swainei ( Tripp 1962) . Tachinids from N. lecontei and N. virginianus Ichneumonidae ( Hymenoptera ). Olesicampe lophyri (Riley) and Endasys subclavatus (Say) from N. swainei ( Tripp 1962) . Ichneumonids from N. lecontei .

Remarks.

Both COI and ITS 2 support P. neodiprioni as a distinct species (Fig. 1 , Suppl. material 5). There are 10 BINed specimens on BOLD ( AEE 8879) collected from the eastern and central Nearctic region north of Mexico, most of which are reared from Diprionidae that feed on pine trees. There are no completely reliable morphological characters to distinguish P. neodiprioni from P. hyalinus Say , the hyperparasitoids associated with Orthopteroidea. Imbricate-alveolate sculpture on the mesofemoral groove are found only in P. neodiprioni , but weakly imbricate, rugose, or smooth sculpture of mesofemoral groove are found in both species. Likewise, mesoscutellar teeth at the apex with steeply diverging inner margins are found only in P. hyalinus , but gradually diverging inner margins are found in both species. The presence of one or more piliferous punctures on axillula dorsad is a unique state found only in P. neodiprioni in the P. hyalinus species group. But its diagnostic value is somewhat limited because the axillula is punctate in 72 % and smooth in 28 % of the total studied specimens (n = 188). And the proportion of specimens with punctate axillula seems to show geographical variation: 84 % of 136 specimens in the northeastern USA and southeastern Canada, fewer than half in the central USA (9 of 20) and Florida (7 of 25), and all the specimens from Belize (17) are punctate.

Genetic analysis suggests there are at least two distinct COI clades of P. neodiprioni in the Nearctic region: Ontario and Massachusetts; and Virginia, West Virginia, and Texas (Suppl. material 2). However, these COI clades are delimited as a single species by the distance-based methods (Suppl. material 5). The geographical distribution of each clade coincides with the post-glacial re-colonization pathways of N. lecontei populations from the Atlantic coast and Texas refugia (Bagley et al. 2016). This pattern is likely an indication of the fragmentation and genetic differentiation of P. neodiprioni populations during glaciation, and eventual post-glacial range expansion of parasitoids following their recolonizing sawfly hosts prior to secondary contact. ITS 2 showed no genetic differentiation between the populations and both distance- and tree-based methods merged both populations as a single species (Suppl. materials 2, 5). This probably represents active interbreeding between the P. neodiprioni populations, which would result in full recombination of nuclear DNA, whereas the variation of non-recombinant COI accumulated during isolation was retained after secondary contact (Després 2019). Sequencing of Floridan specimens could reveal if there is a third distinct population of P. neodiprioni originated from the proposed southern glacial refugia near North and South Carolina that expanded their distribution with the sawfly hosts toward Florida (Bagley et al. 2016). The Belize specimens failed to sequence, and their potential genetic differentiation is yet to be explored. Specimens from Ontario and Massachusetts, which form one of the two COI clades, were selected as the type series.

Perilampus neodiprioni is the only species in the P. hyalinus species complex that exhibits an exclusive association with pine sawflies, more commonly as a primary parasitoid but also as a hyperparasitoid. An exception is a single P. neodiprioni specimen reared from Diprion similis (Hartig) in Ontario ( ROME 207314), but it lacks associated host remains and the collector had noted the uncertainty in their identification in the collection form. While it isn’t surprising that P. neodiprioni can develop on D. similis , this sawfly species is non-native in the Nearctic region and not relevant to the evolutionary history of P. neodiprioni .

A large number of P. neodiprioni specimens were reared from Neodiprion lecontei cocoons in the 1940 s at the Dominion Parasite Laboratory ( DPL) in Belleville, Ontario and subsequently transferred to the CNC. The 230 reared P. neodiprioni specimens are predominantly primary parasitoids (215) and only 15 are hyperparasitoids, 14 parasitoids of Ichneumonidae and one parasitoid of Tachinidae . The reared specimens from the other localities are also comprised of mostly primary parasitoids. Of the total 62 reared P. neodiprioni specimens associated with pine sawfly cocoons, 49 are primary parasitoids of Neodiprion spp. , 13 are hyperparasitoids, of which 11 are parasitoids of Ichneumonidae and two are parasitoids of Tachinidae . There are however, two reared series that are only or mostly hyperparasitoids: Masschusetts ( ROME 162273–162275, 3 of 3) and Arkansas ( ROME 152640–152643, 185915, 185916, and 185956, 6 of 7). Tripp (1962) and Wilkinson (1966) also documented Perilampus developing as both primary and hyperparasitoids associated with pine sawflies. It is unclear if P. neodiprioni can develop as hyperparastioids of the other primary parasitoids of pine sawflies with equal success. For example, Tripp (1962) and Hinks (1971) reported rare to no cases of Perilampus developing as hyperparasitoid on Diptera , but Wilkinson (1966) reported predominance of hyperparasitoids on Diptera . Reared specimens examined in this study show that it is rarer for P. neodiprioni to develop on dipteran parasitoids than on hymenopteran parasitoids in both the DPL collection (0.4 % vs 6 %) and from other localities (3.2 % vs 17.7 %).

Neodiprion species are often serious pests in boreal forests ( Alfaro and Fuentealba 2016; Johns et al. 2016) which suggests that P. neodiprioni could be an effective biological control agent, but this is complicated because this species can develop both as a primary parasitoid and as a hyperparasitoid. Evaluation of the biocontrol potential of P. neodiprioni will depend on the relative prevalence of other hymenopteran and dipteran primary parasitoids and their effectiveness as biological control agents — P. neodiprioni as a hyperparasitoid could interfere with the population dynamics of these strictly primary parasitoids ( Schooler et al. 2011).

The shift in ecology from hyperparasitoid associated with Lepidoptera to primary or hyperparasitoid associated with pine sawflies is suggested by the sister species relationship between P. neodiprioni and P. sirsiris (Suppl. material 1), and their associations with pine trees. Perilampus sirsiris is the only known hyperparasitoid in the P. hyalinus species complex that is associated with gymnosperms as well as angiosperms. It is possible that the common ancestor of P. neodiprioni and P. sirsiris was a hyperparasitoid species which expanded the oviposition sites to include pines, where planidia would have encountered both Lepidoptera caterpillars and Neodiprion larvae. Pine sawfly larvae were likely suitable hosts for planidia that inadvertently burrowed into this novel host, driving the evolution of parasitoid capable of developing as a primary parasitoid of Neodiprion sawflies.

Figures

Figure 1. Maximum likelihood tree of Perilampus hyalinus species group retrieved from the combined analysis of COI and ITS 2 (modified from Yoo 2023). Bootstrap support values are shown on the left side of the nodes. The roman numerals and black dots adjacent to the nodes indicate the major morphological clades recovered as monophyletic (I = P. hyalinus species group; II = P. carolinensis species complex; IIa = “ pseudocarolinensis ” clade; IIb = P. carolinensis clade; III = P. hyalinus species complex; IIIa = P. hyalinus clade 1; IIIb = P. hyalinus clade 2; IIIc = P. hyalinus clade 3; IIId = “ regalishyalinus ” clade. The morphospecies designation for the sequences is marked by vertical bars, colored according to their placements within their respective morphological subgroups. The names of the species described herein are indicated in white boxes.

Figure 4. Perilampus hyalinus Female A habitus, lateral view B habitus dorsal view C lateral lobe of mesoscutum along notaulus D lateral panel of pronotum, posterior oblique view E axillula F axilla G head, dorsal view H head, anterior view I lower face J parascutal carina K mesoscutellum apex L, M mesofemoral depression. [A ROME 185913; B, K ROME 189058; C, M ROME 185947; D, F ROME 189056; E, G ROME 162229; H ROME 167636; I ROME 189060; L ROME 162246]. Scale bar: 1 mm (A).

Figure 8. Perilampus neodiprioni Female A habitus, lateral view B habitus, dorsal view C lateral lobe of mesoscutum along notaulus D lateral panel of pronotum, posterior oblique view E axillula F axilla G head, dorsal view H head, anterior view I clypeus J parascutal carina K mesoscutellum apex L, M mesofemoral depression. [A – E, G, H, J, L Paratype, ROME 162273; F, M Paratype, ROME 198146; I ROME 181757; K ROME 189061]. Scale bar: 1 mm (A).

Figure 9. Perilampus neodiprioni Male A habitus, lateral view B lateral panel of pronotum, parascutal carina, and axilla C head, anterior view D head, dorsal view E lower face F lateral lobe of mesoscutum along notaulus G, H scape. [A – D, F Paratype, ROME 162274; E ROME 185922; G ROME 152634; H Paratype, ROME 97556]. Scale bars: 1 mm (A); 100 μm (G, H).

Figure 25. Distribution of the Nearctic species of the Perilampus hyalinus species complex A P. hyalinus (green circles) and P. crassus (red squares) B P. neodiprioni (cyan circles) P. monocteni (red stars) C P. sirsiris D P. seneca E P. arcus F P. pilosus (yellow stars) P. ute (blue triangles) P. sonora (red circles).

Figure 26. Cocoons, pupa, and host remains associated with reared specimens of Perilampus. A – C, E Neodiprion lecontei cocoons A, B P. neodiprioni as primary parasitoid C, E P. neodiprioni as hyperparasitoid, parasitoid of Ichneumonidae D Neodiprion virginianus cocoon, P. neodiprioni as hyperparasitoid, parasitoid of Tachinidae [insert: tachinid puparium spiracles] F Lepidoptera pupa, P. seneca as hyperparasitoid, parasitoid of Tachinidae G, H Monoctenus suffusus cocoons G P. monocteni as primary parasitoid H P. monocteni as hyperparasitoid, parasitoid of Tachinidae [insert: tachinid puparium spiracles]. Abbreviations: eh, emergence hole; ex, Perilampus pupa exuvia; Ic, ichneumonid cocoon; Lp, lepidopteran pupa; M, Monoctenus remains; Mc, Monoctenus cocoon; N, Neodiprion remains; Nc, Neodiprion cocoon; Tp, tachinid puparium. [associated Perilampus: A, B ROME 207376 C ROME 207377 D ROME 198223 E ROME 162273 F ROME 202000 G ROME 207330 H ROME 207328]. Scale bars: 1 mm.