Drosophila bromeliae

Grimaldi, David A., 2016, Revision of the Drosophila bromeliae Species Group (Diptera: Drosophilidae): Central American, Caribbean, and Andean Species, American Museum Novitates 2016 (3859), pp. 1-56 : 4-15

THE DROSOPHILA BROMELIAE SPECIES GROUP

Drosophila Group B: Sturtevant, 1921: 72.

Drosophila bromeliae species group: Patterson and Stone, 1952: 20; Silva and Martins, 2004; Val and Marques, 1996.

DIAGNOSIS: A well-defined monophyletic group of small to medium-sized drosophilids (ca. 0.5–1.10 mm thorax length), body dull/bright yellowish to light brown; setae golden to dark brown-bronze in color, never black; arista with 3–4 dorsal and 1–2 ventral branches (usually 4-2); facial carina well developed, flat, but thinner than antennal pedicel and basal flagellomere, median sulcus faint or lacking; mesoscutum with one or two pairs of fine prescutellar setae; male genitalia simple (see below), ejaculatory apodeme either so vestigial as to be unobservable or completely lost; oviscapt slender, length 2.5–3.0× greatest width, with pegs; few very mature eggs, or even first-instar larvae are laid; eggs with two short subapical filaments.

GENERAL DESCRIPTION ( ADULTS): Coloration of body generally yellowish to light brown, dull to slightly pollinose; never shiny; setae golden to dark brownish bronze in color, never black (fig. 1). Head: With very little variation in proportions and setation; eyes large, light to dull, dark red, with sparse interfacetal setulae frontally; dense, short setulae laterad (3 setulae surrounding each facet: fig. 3B); eye oval to slightly egg shaped in lateral view. Facial carina well developed, with anterior surface flattened and either lacking median sulcus or with faint sulcus; width of carina always less than that of antennal pedicel (fig. 3A). Gena shallow, depth usually less than 0.1× that of eye. One pair vibrissae present, subtended by row of 7–10 finer, shorter setae near ventral margin of gena. Length of frons moderate, frontal index varies from 0.93–1.55. Frontal vittae golden, microscopically striate and microtrichose, shiny, converge in anterior third (figs. 2, 4A). Fronto-orbital plates and ocellar triangle smooth, darker. Ocellar setae always divergent; base of ocellar seta either lying on tangent between median and lateral ocelli, or slightly outside tangent; postocellar setae generally short, orientations parallel, convergent, or even slightly cruciate at tips (fig. 2). Three fronto-orbital setae always present: proclinate (or1), anterior reclinate (or2) (ca. half the length and thickness of other fronto-orbitals), and posterior reclinate (or3). Seta or3 is slightly thicker and shorter than or1; or2 is midway between other two fronto-orbital setae, or closer to or1. Ipsilateral seta or1, or3, and inner vertical always in line, with or2 usually slightly lateral to this tangent (fig. 2A–C, E, F), occasionally medial to tangent (fig. 2D). Inner verticals convergent, base of each very close to base of outer vertical; outer verticals strongly divergent. Inner and outer verticals approximately equal in length. Antenna with scape and pedicel yellowish to brown, pedicel with several setulae and microtrichia, including very fine longer ones on mesal surface; basal flagellomere slightly darker than pedicel, with uniformly short microtrichia (without long setulae). Arista with short, ringlike basal segment; terminal segment with 3–4 dorsal and 1–2 ventral branches (exclusive of short terminal fork) (usually 4-2 dorsal-ventral branches), lengths of longest branches about 0.5× length of entire arista (fig. 4A). Clypeus narrow, barely wider than widest portion of facial carina. Proboscis and palp generally yellowish, palp bilaterally asymmetrical (fig. 4-C), with longest setae on ventral margin; labellum small, lateral surfaces slightly sclerotized, without microtrichia, with short, stiff setae (fig. 3C); labellar lobe with 5–6 pseudotracheae; distal portion of proboscis (theca: labium + labellum) usually held forward in pointed specimens, at right angle to basal portion of proboscis. Cibarium (studied for only D. bromeliae ) with floor having broad, sclerotized hypopharyngeal bulb ( Grimaldi, 1990), with four sensilla/sieve pores over broad apex; medial sensilla short, trichodea type, in 2 rows of 7 each; posterior sensilla arranged in 2 even, long rows of approximately 15 long, blunt sensilla trichodea (fig. 4E). Labrum with acute, microtrichose apex (fig. 4E) .

Thorax: Mesonotum yellowish to light brown, slightly pollinose; not shiny (fig. 1); with 6 or 8 irregular rows of acrostichal setulae. Two pairs of dorsocentral setae; prescutellar setae present in 1–3 pairs (usually just one), central pair always longest, lateral pairs often scarcely larger than acrostichal setae (figs. 3D, E; 4F–G). Lengths of prescutellar setae variable, as described for individual species. Scutellum with two pairs of setae; anterior scutellars (sc) slightly shorter and thinner than posterior sc; anterior sc strongly convergent, but not crossing; posterior scutellars often cruciate for 0.3–0.5× their length. Pleura same color as or slightly darker than notum (fig. 1). Notopleural area with three setae; two supraalar setae; two postpronotal setae. Katepisternum with two large setae, anterior seta slightly shorter than posterior one.

Legs: Yellowish, same color as or slightly lighter than notum and pleura, with typical array of setae; male protarsus without combs or fine, erect setae; mesotibia with stout, dark, ventroapical spurlike seta and shorter, dorsopreapical seta.

Wings: Clear, hyaline, never with patterns or infuscation; veins light, yellowish to infuscate (fig. 5). Venation very uniform. Costal vein ends at apex of M 1+2, though segment between apex of R 4+5 and M 1+2 thinner than proximal portion of C; heavy spinules end midway between apices of R 4+5 and M 1+2 to 3/4 distance from apex of R 4+5; subcosta reduced, length half that of cell Sc. Tip of wing at apex of vein R 4+5; tip rounded to slightly pointed. Small cells at base of wing present, but cell bm incompletely closed; cell cup very small, closed. Vein A 1 present, but short; anal lobe of wing present. Ranges of wing indices: C 1.19–2.40; 4-C 0.90–1.3; M 0.50–0.70.

Abdomen and terminalia: Abdominal tergites varying in color from dark yellowish to brown, sometimes uniform in color but often with diffuse dark bands on posterior margins of tergites. Tergal setae generally quite short, those on posterior margins longer. Male genitalia simple: Epandrium well developed, with setulae and microtrichia (except on ventral lobes), broadly connected laterally to cerci; hypandrium well developed, U-shaped to trapezoidal; no accessory lobes, pair of paramedian postgonites each with small apical setula; aedeagus a simple tube with enlarged distiphallus, the latter sometimes with a pair of ventrolateral spines; aedeagus in lateral view slightly to extensively arched. Aedeagal apodeme short; ejaculatory apodeme either so minute or vestigial as to be unobservable or completely lost. Subepandrial sclerite (decasternum) well developed, connecting surstyli. Surstylus with or without microtrichia, always with a row of 5–14 sclerotized prensisetae along dorsal portion of mesal margin (some thick setae ventral to prensisetae may be sclerotized); thinner, longer setae unsclerotized. Oviscapt with sclerotized pegs; oviscapt relatively long, length 2.5 to 3.0× greatest width in ventral view; apex of oviscapt narrow in lateral view, not broadly rounded. Spermathecal capsule sclerotized, simple; campanulate, sometimes with annuli on external surface.

IMMATURES: Eggs (known for D. bromeliae [herein], D. bromelioides [ Pavan and Cunha, 1947]): subovoid, ca. 0.5 mm, slightly flattened on surface from micropyle to apex; micropyle raised into short tubercle; one pair of short preapical filaments present (ca. 200 µm length), tips of filaments blunt but not expanded or flattened, occasionally slightly bifid (fig. 6A); chorionic pattern of hexagonal cells externally not well developed, but with minute (ca. 0.5 µm) pores throughout and areas having small groups of raised, craterlike structures (fig. 6B).

Mature larva (based on D. bromeliae , herein): Amphineustic, with pair of anterior and pair of posterior spiracles; length ca. 4 mm, with 9 segments have creeping welts, only 7 abdominal welts appreciably raised (fig. 7); welts with transverse, irregular rows of minute, poorly sclerotized hooks (poorly visible under light microscopy, vs. dark to black, well-formed hooks in many saprophagous Drosophila ). Antenna and maxillary palp typical, small and buttonlike; cephalic region with 4 transverse rows anterior to mandibles, separated by a median fissure; lateral to buccal atrium are another 8 rows of fine lamellae on each side; labial lobe well developed, apically comprised of 4 smaller lobes (figs. 7B, C).

Cephalopharyngeal skeleton (figs. 6C, D): typically cyclorrhaphan, mandibles (“mouth hooks”) and sclerites between these and cornuas heavily sclerotized, cornuas less sclerotized; mandible hooklike, with two pairs of teeth on ventral margin (each pair on ventrolateral margin, separated by longitudinal ventral groove on mandible); mandibular teeth bifid (each comprised of two smaller teeth, fig. 6D); dentary and hypopharyngeal sclerites well developed, hypopharyngeal sclerite roughly H-shaped (figs. 6C, D); pharynx hardly sclerotized, with ca. 6 deep ventral grooves and several finer ones (fig. 6C); tentorial phragma heavily sclerotized, grading to very lightly sclerotized dorsal and ventral cornuas; labial sclerite lightly sclerotized, with paramedian pair of perforations; dorsal bridge of tentorium fully connected, less sclerotized than phragma, highly perforated on lateral surfaces. Anterior spiracles with 6 branches, tips of each branch with fine, rounded, liplike structure over opening. Posterior spiracles fused at base, short, ca. 175 µm, glabrous, with array of ecdysial scars typical of cyclorrhaphans.

Pupa (known for D. speciosa [ Silva and Martins, 2004], D. bromeliae [herein], and D. bromelioides [ Pavan and Cunha, 1947]): Light reddish brown; total length of anterior “horn” (everted anterior spiracle) 0.40–0.60 mm, base slightly longer than half total length (longer than everted spiracular tracheae, longest tracheae in center); anterior spiracle with 6 tracheae ( bromeliae ), 9–12 ( speciosa ), 11 ( bromelioides ).

COMMENTS: Patterson and Stone (1952) erroneously mentioned that no prescutellar setae were present in the bromeliae group. Species are externally very homogeneous. Male and/or female terminalia are distinctive for some species, but ones in the bromeliae subgroup (see below) are very similar. Female genitalic features showing significant variation are the following: length in proportion to the width of the oviscapt in ventral view; number of ovisensilla pegs; size and proportions of spermathecal capsule. Male genitalic features include: shape of the hypandrium in full ventral view; shape of the aedeagus in lateral view (i.e., length; amount of curvature, as measured by the aedeagal angle); shape of the distiphallus in full ventral view; number of prensisetae on the surstylus, presence/absence of darkened setae on ventral portion of the surstylus, and sometimes the shape of prensisetae and vestiture of surstylus. Nongenitalic structures that are important for separating species include the following: body size, coloration, size and number of prescutellar setae (sizes can be rather variable intraspecifically), shape and width of facial carina, extent to which the posterior scutellar setae cross (i.e., are cruciate), number of dorsal branches of arista, and slight differences in the orientation and length of crossvein dm-cu.

Relationships: Monophyly of the bromeliae group is virtually certain based on morphological evidence, summarized above in the diagnosis. Relationships of the group, however, to other Drosophilinae have not been explored, although the bromeliae group is probably closely related to several other Neotropical flower-breeding groups. Pavan and da Cunha (1947) mentioned that D. bromelioides belongs in Sophophora (probably because the egg has two subapical filaments), but all other morphological evidence indicates that this similarity is only convergent. The large study on Neotropical drosophilids by Vilela and Bächli (1990) did not discuss the bromeliae group.

Flies in the bromeliae group are quite similar to those in the large genus Scaptodrosophila , of which there are hundreds of described and undescribed species in the Old World tropics. Similarities include the prescutellar setae, narrow carina, and flower-breeding habits. Scaptodrosophila markedly differs, however, from the bromeliae group by its distinctive male genitalia, in which there is a pair of projecting postgonite lobes, each with a longitudinal row of sensilla trichodea; one or more pairs of thick, long, stiff, projecting setae on the posterior margin of the hypandrium flanking the aedeagus; and the hypandrium being a short, broad, usually hemispherical plate. Moreover, an ejaculatory apodeme is present in Scaptodrosophila (distinctly absent in the D. bromeliae group), there are typically three large katepisternal setae (instead of two), and the eggs have 3–4 pairs of filaments (not the one pair seen in the D. bromeliae group). Morphological (e.g., Grimaldi, 1990) and molecular evidence (e.g., Robe et al., 2005; Morales-Hojas and Vieira, 2012) consistently places Scaptodrosophila at or near the base of the Drosophilinae , and so similarity to the D. bromeliae group appears to be just highly convergent.

With little question, the Drosophila bromeliae group lies within the “ virilis - repleta radiation” of Drosophila, sensu Throckmorton (1975) , morphologically distinguished in part by a lateral fusion of the male cercus to the epandrium, and the lack of a hypandrial “hood” (a posterodorsal lobe lying above the aedeagus and articulating laterally to the posterior ends of the hypandrial arms). Males in the “ immigrans-tripunctata radiation,” in contrast, have a completely separated cercus and possess the hypandrial “hood.” There is consistent molecular evidence for these two major clades of Drosophila (e.g., Robe et al., 2005; Morales-Hojas and Vieira, 2012).

It is quite likely that the bromeliae group, in fact, is closely related to several other species groups of Neotropical flower breeders such as the dreyfusi and flavopilosa groups. These flies tend to be light to very light in body color (even a whitish yellow), pollinose, never with black setae, and generally possess a narrow facial carina. The male genitalia in these groups are quite similar, often with a pair of subapical spines on the distiphallus. While the eggs of species in the dreyfusi group have four filaments (e.g., Pavan and Breuer, 1954), for those species in the flavopilosa group that have filaments (most do not) they possess a single pair of short, stublike filaments ( Wheeler et al., 1962; Brncic, 1983). Each of these groups appears to be monophyletic, having distinctive, syapomorphic features: a retractorlike oviscapt with large teeth and a spermatheca lacking an introvert in the flavopilosa group; and for the dreyfusi group, minute spermathecae. Unfortunately, molecular studies (e.g., Robe et al., 2005; Morales-Hojas and Vieira, 2012) have not yet included any bromeliae group exemplars.