A database of wing diversity in the Hawaiian Drosophila

Abstract

Background: Within genus Drosophila, the endemic Hawaiian species offer some of the most dramatic examples of morphological and behavioral evolution. The advent of the Drosophila grimshawi genome sequence permits genes of interest to be readily cloned from any of the hundreds of species of Hawaiian Drosophila, offering a powerful comparative approach to defining molecular mechanisms of species evolution. A key step in this process is to survey the Hawaiian flies for characters whose variation can be associated with specific candidate genes. The wings provide an attractive target for such studies: Wings are essentially two dimensional, and genes controlling wing shape, vein specification, pigment production, and pigment pattern evolution have all been identified in Drosophila.

Methodology/principal findings: We present a photographic database of over 180 mounted, adult wings from 73 species of Hawaiian Drosophila. The image collection, available at FlyBase.org, includes 53 of the 112 known species of "picture wing" Drosophila, and several species from each of the other major Hawaiian groups, including the modified mouthparts, modified tarsus, antopocerus, and haleakalae (fungus feeder) groups. Direct image comparisons show that major wing shape changes can occur even between closely related species, and that pigment pattern elements can vary independently of each other. Among the 30 species closest to grimshawi, diverse visual effects are achieved by altering a basic pattern of seven wing spots. Finally, we document major pattern variations within species, which appear to result from reduced diffusion of pigment precursors through the wing blade.

Conclusions/significance: The database highlights the striking variation in size, shape, venation, and pigmentation in Hawaiian Drosophila, despite their generally low levels of DNA sequence divergence. In several independent lineages, highly complex patterns are derived from simple ones. These lineages offer a promising model system to study the evolution of complexity.

Figure 1. Overview of relationships among major species groups and picture wing subgroups.

Schematic based on chromosomal inversions, DNA sequence data, and morphology , , , . Arrow indicates the proposed single introduction of Drosophila to an island west of Kauai. Blue backgrounds, picture wing subgroups; green backgrounds, modified mouthparts, modified tarsus, and antopocerus groups; pink background, haleakalae/fungus feeder group. Lines schematically indicate consensus phylogenetic relationships. Examples of increasing pattern complexity in the adiastola and grimshawi subgroups are shown. See Figs. 2– 7 for species names. Hawaii map courtesy of geology.com and mapresources.com.

Figure 2. The adiastola and primaeva/attigua subgroups of picture wing species.

D. adiastola, cilifera, clavisetae, hamifera, setosimentum, spectabilis, and truncipenna are shown as sexually dimorphic pairs, ornata and primaeva/attigua as single examples. In all figures, anterior is up and proximal is to the left. Inset, chromosome inversion-based lineage for the species shown (see text).

Figure 3. The planitibia subgroup of picture wing species.

The planitibia complex: differens, hemipeza, heteroneura, planitibia, and silvestris. The neopicta complex: neopicta (npi) and nigribasis. The cyrtoloma complex (right column): cyrtoloma, melanocephala, neoperkinsi (npk), oahuensis, and obscuripes. The picticornis complex: picticornis. Inset, chromosome inversion-based lineage for the species shown (see text). The six species in the large box arose from an ancestral population that was polymorphic for the inversions that now differ among these species; see Carson for details.

Figure 4. The glabriapex/4b subgroup of picture wing species:

D. aglaia, assita, basisetae, digressa, fasciculisetae, glabriapex, hexachaetae, macrothrix, montgomeryi, punalua, and virgulata. Lower, chromosome inversion-based lineage for the species shown (see text).

Figure 5. The grimshawi/4b+ subgroup of picture wing species:

D. affinidisjuncta, balioptera, bostrycha, craddockae, crucigera, disjuncta, engyochracea, grimshawi, hawaiiensis, heedi, hirtipalpus, limitata, murphyi, orphnopeza, orthofascia, recticilia, silvarentis, sproati, and villosipedis. Inset, chromosome inversion-based lineage for the species shown (see text).

Figure 6. The antopocerus and haleakalae/fungus feeder groups.

Upper six panels, antopocerus group species D. longiseta, stigma, adunca, and cognata. Sexual dimorphism is shown for longiseta and stigma. The extended male antennal structures, characteristic of the antopocerus group, can be seen co-mounted with the cognata wing. Lower six panels, haleakalae/fungus feeder group: dolichotarsus, nigra, cilifemorata, and fungiperda. Sexual dimorphism is shown for dolichotarsus and nigra.

Figure 7. Other non-picture wing species.

The anomalipes group: anomalipes and quasianomalipes. “Modified mouthparts group”: clydonia, aethostoma, mimica, kambysellisi, polliciforma, and diminuens. The ornate pattern of clydonia is rare among the small, non-picture wing species. The curved L3 vein in clydonia is a characteristic of the species . “Modified tarsus group”: basimacula, petalopeza, spiethi, and dasycnemia.

Figure 8. Analysis of pattern variation using color-coded overlays of wing photos.

A. Pattern elements can vary independently. Left, engyochracea (yellow), orphnopeza (cyan), and sproati (magenta) are overlaid. Black indicates where all three coincide. Wings were uniformly skewed in Photoshop to maximize overlap of the margins and veins. Names of longitudinal veins are indicated; L1 is the costal or marginal vein. Arrow, the spot over L2 varies much more than the other spots. Right, positions of the variable spot on L2 are compared in the three species: upper, orphnopeza; middle, sproati; lower, engyochracea; the same region of the wing is shown in each case. B. Two specimens from the antopocerus group are overlaid: tanythrix (orange) and longiseta (blue). The wings were resized to overlay the anterior crossvein, L2 and L3, but the photos were not skewed. Arrow indicates where the anterior margin has a bump in longiseta but is concave in tanythrix. C. Sexual dimorphism in cilifera: a female (upper) and male (middle) are overlayed (lower; female in orange, male in blue). Wings were slightly rescaled to align the veins.

Figure 9. Variants that uncouple the prepattern from the vein-dependent pattern.

A–B. Wings from grimshawi mutant lines. A. weak veins mutant with a gap in L4 (arrow); dark pigment is absent from the distal L4 vein fragment. B. Wing notching in a Nihoa mutant is associated with a shortened L4 and a reduced distal spot (arrow). In both A and B, the prepattern of dark hairs is not affected . C. Rare, natural variant of clavisetae with incomplete pigmentation; this defect is seen in both wings. Compare the central crossvein in the variant (arrow) to that of a typical clavisetae female (inset). D–E. Wings from two hamifera males. D. Normal pattern. (This wing and the one in Fig. 2 are a pair from one male). E, F. Pair of wings from a different male. As in C, the intervein regions have not fully pigmented; see for example the spot indicated by the arrow.