Research Article |
Corresponding author: Zachary Lahey ( zachary.lahey@usda.gov ) Corresponding author: Sharon A. Andreason ( sharon.andreason@usda.gov ) Academic editor: Petr Janšta
© 2022 Zachary Lahey, Alvin M. Simmons, Sharon A. Andreason.
This is an open access article distributed under the terms of the CC0 Public Domain Dedication.
Citation:
Lahey Z, Simmons AM, Andreason SA (2022) Encarsia hera Lahey & Andreason (Hymenoptera, Aphelinidae): a charismatic new parasitoid of Aleurocybotus Quaintance & Baker (Hemiptera, Aleyrodidae) from Florida. Journal of Hymenoptera Research 94: 89-104. https://doi.org/10.3897/jhr.94.94677
|
A new, biparental species of the genus Encarsia Förster (Hymenoptera: Aphelinidae), E. hera Lahey & Andreason, sp. nov., is characterized based on morphological and molecular data. The parasitoid was reared from the puparia of its host, an undescribed species of the grass-feeding aleyrodine genus Aleurocybotus Quaintance & Baker (Hemiptera: Aleyrodidae) collected in Gainesville, Florida. The same whitefly is newly recorded from Charleston, South Carolina, where it is a pest of ornamental Muhly grass [Muhlenbergia capillaris (Lam.) Trin. (Poaceae)]. A phylogenetic analysis based on a fragment of 28S ribosomal DNA in 34 Encarsia species placed E. hera, sp. nov., within the E. luteola-group, a result concordant with its morphology. A key to the Encarsia species reared from Aleurocybotus is provided.
DNA, new species, phylogenetics, whitefly
Florida is home to the largest number of whitefly (Hemiptera: Aleyrodidae) species in the United States (
Species of Aleurocybotus are unusual among whiteflies in that they feed exclusively on grasses (Poaceae) and sedges (Cyperaceae) (
Natural enemies associated with Aleurocybotus include several species of chalcidoid parasitoid Hymenoptera in four genera: Encarsia Förster and Eretmocerus Haldeman (Aphelinidae) (
The genus Encarsia contains approximately 450 described species (
Immature and adult Aleurocybotus were collected in 2022 from infested ornamental Muhly grass [Muhlenbergia capillaris (Lam.) Trin. (Poales: Poaceae)] in Gainesville, Florida (Alachua County) and Charleston, South Carolina (Charleston County), USA. Representative series of unparasitized puparia and other whitefly life stages were collected into 95% ethanol and slide-mounted following the protocol of Martin (2004), except that clearing of specimens took place in an ATL lysis buffer-Proteinase K solution, the first step in a non-destructive DNA extraction protocol that retains the cuticle of the insect for subsequent morphological examination. Parasitoid specimens were reared directly from their host. Parasitized whitefly puparia were excised from portions of leaf tissue using a cork borer (5 mm diameter), placed in size 0 gelatin capsules (Pure Planet Products, Scottsdale, Arizona), and monitored daily for emergence. Reared parasitoid specimens were killed directly in 95% ethanol and stored at -20 °C until DNA extraction.
Genomic DNA was extracted from Aleurocybotus puparia, adults, and single wasps using a DNeasy Blood and Tissue Kit (Qiagen, Hilden, Germany). Individual specimens were first removed from ethanol and allowed to air dry on a Kimwipe for approximately 30 s. The specimen was then transferred to an Eppendorf tube containing 90 µl ATL lysis buffer to which 20 µl proteinase K was added. Tissue digestion was achieved by incubating the reaction mixture for 8 hrs at 56 °C. Tubes were agitated periodically, by hand, to ensure the specimen remained in the reaction mixture at the bottom of the tube. Most specimens were satisfactorily cleared after 8 hrs in the reaction mixture, but some were left for 24 hrs without damaging the specimen. Following tissue digestion, specimens were removed from the reaction mixture directly into distilled water where they remained until slide-mounting. Extracted parasitoids were placed on microscope slides following the protocol of
The standard 5' barcode region of the cytochrome c oxidase subunit I (COI) gene (
Primer | Orientation | Region | Sequence (5'–3') | Reference |
MChaF1 | Forward | COI A | CCTCGAATAAATAATATAAGATT |
|
HCO2198 | Reverse | TAAACTTCAGGGTGACCAAAAAATCA |
|
|
LCO1490M | Forward | COI B | CAACAAATCATAAAGATATTGG |
|
MChaR1 | Reverse | CCYGTTCCAAYAAATATTCT |
|
|
D23F | Forward | 28S-D2-3 | GAGAGTTCAAGAGTACGTG |
|
D3B | Reverse | TCGGAAGGAACCAGCTACTA |
|
CUIDs, host records, GenBank accession numbers, and sequence lengths associated with the Encarsia specimens newly sequenced for this study.
Taxon | CUID | Host | GenBank Accession | Sequence Length (bp) |
---|---|---|---|---|
Encarsia citrella | OSUC 835434 | Aleuroplatus sp. | > OP133209 (28S) | 901 |
Encarsia protransvena | OSUC 835443 | Parabemisia myricae | > OP133210 (28S) | 742 |
Encarsia sp. | OSUC 835445 | Tetraleurodes sp. | > OP133211 (28S) | 746 |
OSUC 835446 | > OP133212 (28S) | 745 | ||
Encarsia lahorensis | OSUC 835456 | Dialeurodes citri | > OP133213 (28S) | 1,085 |
Encarsia sp.a | OSUC 863826 | Unknown | > OP133214 (28S) | 713 |
Encarsia hera | OSUC 863846 | Aleurocybotus sp. | > OP146609 (28S) | 494 |
> OP270223 (COI) | 673 | |||
OSUC 863847 | > OP133215 (28S) | 750 | ||
> OP270224 (COI) | 674 |
Phylogenetic analyses were conducted following
The specimens listed in the Material Examined section of the species description have been accessioned in The Ohio State University’s Museum of Biological Diversity database (https://mbd-db.osu.edu/). The numbers prefixed with “OSUC” are unique identifiers for the individual specimens. Details of the data associated with these specimens may be accessed at the above URL by entering the unique specimen identifier (e.g., OSUC 863846) in the form (note the blank space after the acronym).
Morphological terminology follows
Slide-mounted specimens were imaged with a Keyence BZ-X810. Photographs of card-mounted insects were captured using a Macroscopic Solutions Macropod Micro Kit, with optical slices rendered in Helicon Focus. Composite images from each imaging system were imported into Adobe Photoshop 2022 to correct for brightness and contrast.
The slide-mounted holotype (OSUC 863846) and paratype (OSUC 863847) of E. hera, sp. nov., are deposited in the Smithsonian National Museum of Natural History (
Encarsia luteola-group.
Encarsia hera, sp. nov., can be differentiated from other members of the E. luteola-group by outstanding coloration of the mesoscutellum and metasoma. Most E. luteola-group species have a concolorous mesoscutellum and a predominately yellow metasoma. Encarsia hera, sp. nov., differs from these species by the paired brown patches in the posterior half of the mesoscutellum and the predominantly brown metasoma of the female. Encarsia guadeloupae Viggiani also has a dark metasoma; however, in that species T1 is completely dark and the clava is 2-merous, whereas the lateral portions of T1 are yellow and the clava is 3-merous in E. hera, sp. nov.
Encarsia hera Lahey & Andreason, female holotype (OSUC 863846) 1 Antenna, lateral view 2 Mesotarsus, dorsal view 3 Fore wing, lateral view. Scale bars in millimeters.
Encarsia hera Lahey & Andreason, female paratype (OSUC 863886), habitus, dorsal view. Scale bar in millimeters.
(female). Coloration. Body: predominately dark brown. Head: dark brown, except for pale areas on frons adjacent to compound eyes and a transverse strip on vertex anterior to ocellar bars. Antenna: yellow, except for fuscous apical clavomere (F6). Mesosoma: dark brown, except for yellow lateral and posteromedial margin of mesoscutum, mesoscutal side lobe, anterodorsal portion of acropleuron, and most of mesoscutellum. Mesoscutellum: predominately yellow with two conspicuous brown spots in posterolateral half. Fore and hind wings: hyaline, venation fuscous. Legs: pale yellow, except for fuscous apical tarsomere (tarsomeres 4 + 5 fused) on midleg and apical three tarsomeres on hindleg. Metasoma: dark brown, except for lateral portions of T1 which appear transparent/opalescent. Ovipositor: third valvulae yellow.
Head. Antennal formula: 1-1-3-3. Length of pedicel relative to F1: 0.8. Length of F1 relative to F2: 0.9. Length of F2 relative to F3: approximately equal. Number of multiporous plate sensilla on F1–F6: 1-2-2-3-3-3. Sculpture of stemmaticum: aciculate. Sculpture of frons ventral to transfacial line: indiscernible. Sculpture of frons dorsal to transfacial line: transversely imbricate.
Mesosoma. Number of setae on midlobe of mesoscutum: 16. Number of setae on side lobe of mesoscutum: 2. Number of setae on axilla: 1. Proximity of campaniform sensilla on mesoscutellum: ≥ 5 sensillar widths apart. Distance between anterior pair of mesoscutellar setae: equal to distance between posterior pair of mesoscutellar setae. Length of mesoscutellar setae: anterior pair distinctly shorter than posterior pair. Tarsal formula: 5-4-5. Length of midtibial spur: 0.8× length of midbasitarsus.
Metasoma. Number of paired setae on T1–T6: 0-1-2-1-3-3. Length of ovipositor: 0.8× length of midtibia. Apical portion of 3rd valvulae: chisel-tipped, inner margin longer than outer margin. Length of 3rd valvulae relative to 2nd valvifer: 0.7×.
Wings. Length of fore wing: 2.7× width. Asetose area below stigma vein: absent. Length of marginal fringe: 0.3× maximum width of disc. Number of setae in basal cell region: 5. Arrangement of setae in basal cell: linear, originating and forming a 45° angle with submarginal vein. Number of setae on submarginal vein: 2. Number of setae along anterior of marginal vein: 8; 9.
(male). Coloration. Same as female, except for the darker mesoscutellum and T1 is dark throughout.
Morphology. Sculptural patterns very similar to female. Mesoscutellar sculpture: weak medially, large reticulations laterally. Number of antennomeres: 8. Condition of F6: articulate with F5, not fused or partially fused.
Florida (USA).
Aleurocybotus nr. cereus (Hemiptera: Aleyrodidae).
Named for the Hera of Greek mythology, one of the Twelve Olympians, Queen of the Gods, and protector of women from harm during childbirth.
Holotype
, female: USA: Florida, Gainesville, 29°36'3"N, 82°25'13"W, 19.vi.2022, ex. Aleurocybotus n. sp. on ornamental Muhly grass (Muhlenbergia capillaris), Z. Lahey, OSUC 863846 (deposited in
The alignment of the 28S-D2-3 region in the 36 taxa was 1,037 characters long (base pairs plus gaps) and the model of nucleotide evolution was SYM+I+G4. In all analyses, the E. luteola-group was recovered as monophyletic with maximum ultrafast bootstrap support (UFBS = 100; Fig.
Encarsia hera Lahey & Andreason, male paratype (OSUC 863887), habitus, dorsolateral view. Scale bar in millimeters.
Members of the E. luteola-group are recognized by having 4 mesotarsal segments and a fully setose wing disc (
The sister group relationship between E. formosa and E. hera, sp. nov., recovered in our study breaks the longstanding paradigm that E. formosa and E. luteola are likely each other’s most closely related living relative (
Encarsia longitarsis Myartseva, female paratype 6 Mesoscutellum, dorsal view 7 Antennal clava, lateral view, with arrow at the constriction between the last funicular and first claval segment 8 Metasoma, dorsal view, coloration of lateral metasoma boxed in white. Scale bars in millimeters.
1 | Tarsus of midleg 5-merous; head, mesosoma, and metasoma yellow | Encarsia protransvena Silvestri |
– | Tarsus of midleg 4-merous (Fig. |
2 |
2 | Mesoscutellum with two brown markings in posterior half (Fig. |
Encarsia hera Lahey & Andreason, sp. nov. |
– | Mesoscutellum concolorous throughout (Fig. |
3 |
3 | Dorsolateral surface of metasoma light yellow, concolorous with remainder of metasoma | Encarsia luteola Howard |
– | Dorsolateral surface of metasoma brown, contrasting with remainder of metasoma (Fig. |
Encarsia longitarsis Myartseva |
Maximum likelihood phylogeny of the 28S-D2-3 region in 34 Encarsia and two outgroup species. The number under the scale bar indicates the number of expected nucleotide substitutions per site. Ultrafast bootstrap supports values are indicated by colored circles at nodes. GenBank accession numbers beginning with OP correspond to specimens newly sequenced for this study.
The arthropod fauna of Florida is in a constant state of flux, notably because of its position as a botanical import hub of the countries that comprise the Caribbean, South America, Europe, and Asia (
The evidence for the undescribed whitefly as adventive is based on a comparison of its morphology with other described species of the genus. Puparia of the new Aleurocybotus secrete copious amounts of flocculent wax, a characteristic exhibited by both A. cereus and A. mojavensis von Ellenrieder & Bailey, species from Belize and California, respectively (
Surveys of parasitoid Hymenoptera primarily associated with Bemisia Quaintance & Baker in Florida, the Caribbean, and Latin America failed to recover E. hera, sp. nov., from that host (
The discovery of a new Encarsia species is not surprising. Encarsia is the most speciose genus in the family Aphelinidae and has been labeled ‘megadiverse’ based on a suite of morphological, genetic, and biological characteristics that account for the estimated 4,000 plus species thought to exist in nature (
We thank Greg Evans (USDA-APHIS) and Natalia von Ellenrieder (California Department of Food and Agriculture) for confirming the species status of the Aleurocybotus specimens from Florida and South Carolina. Lily Deeter (FDACS-DPI-
Maximum likelihood cladogram of the 28S-D2-3 region in 71 Encarsia and two outgroup species (1,070 sites, SYM+R3)
Data type: image (svg file)
Explanation note: Maximum likelihood cladogram of the 28S-D2-3 region in 71 Encarsia and two outgroup species (1,070 sites, SYM+R3). Ultrafast bootstrap supports values are indicated on branches. GenBank accession numbers beginning with OP correspond to specimens newly sequenced for this study. Branches in red correspond to members of the E. luteola-group.
Maximum likelihood cladogram of a trimmed version of the 28S-D2-3 dataset analyzed in Fig.
Data type: image (svg file)
Explanation note: Maximum likelihood cladogram of a trimmed version of the 28S-D2-3 dataset analyzed in Fig.