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Molecular and Morphometrical Revision of the Zaprionus Tuberculatus Species Subgroup (Diptera: Drosophilidae), with Descriptions of Two Cryptic Species

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Molecular and Morphometrical Revision of the Zaprionus Tuberculatus Species Subgroup (Diptera: Drosophilidae), with Descriptions of Two Cryptic Species SYSTEMATICS Molecular and Morphometrical Revision of the Zaprionus tuberculatus Species Subgroup (Diptera: Drosophilidae), with Descriptions of Two Cryptic Species AMIR YASSIN1 Laboratoire Evolution, Ge´nomes et Spe´ciation, Centre National de la Recherche ScientiÞque, av. de la Terrasse, 91198 Gif-sur-Yvette, France Downloaded from https://academic.oup.com/aesa/article/101/6/978/2758498 by guest on 27 September 2021 Ann. Entomol. Soc. Am. 101(6): 978Ð988 (2008) ABSTRACT Zaprionus is an important drosophilid genus in the Afrotropical region. Here, two new species, Z. burlai n. sp. and Z. tsacasi n. sp., are described from Tanzania and Sa˜o Tome´, respectively. The two species show incomplete reproductive isolation with Z. tuberculatus Malloch and Z. sepsoides Duda, respectively, with intercrosses producing fertile females but sterile males. The latter two have long been considered sibling species and together with three other species (Z. mascariensis Tsacas & David, Z. kolodkinae Chassagnard & Tsacas, and Z. verruca Chassagnard & McEvey) form the tuberculatus subgroup. The phylogenetic relationships of these seven species of the subgroup were revised in light of mitochondrial (COII) gene sequences and wing morphometrics. Mitochondrial DNA Þrmly distinguished most of the species, except for a triad of Z. tuberculatus, Z. verruca, and Z. burlai. Wing morphometrics was able to distinguish between closely related species and also indicated the altitudinal origin of each species. Most species can be identiÞed through internal anatomy of the reproductive system (testis and seminal recep- tacle lengths), and the discovery of the new species with incomplete reproductive isolation may help in understanding the genetic basis of this variation through interspeciÞc hybridization. The molecular phylogeny reconÞrmed the Malagasy origin of the subgroup during the Late Pliocene. Colonization of Africa probably involved two independent events during the Pleistocene. KEY WORDS COII barcoding, Africa paleobiogeography, wing shape, cryptic speciation, interspe- ciÞc hybridization Zaprionus (Coquillett 1901) is a pan-tropical dros- species (Tsacas et al. 1981, Chassagnard and Tsacas ophilid genus divided into two geographically disjunc- 1993). Even within the most widespread and most tive subgenera: the subgenus Zaprionus s.s. (46 spe- studied species, Z. indianus, two cryptic species en- cies) located in the Afrotropical region, and the demic in tropical Africa were discovered using mo- subgenus Anaprionus (10 species) found in the Ori- lecular and morphometrical analyses (Yassin et al. ental and Australasian region. Yassin et al. (2008a) 2008b). revised the phylogeny of the genus based on molec- The Z. tuberculatus species subgroup has been ular markers, and they suggested a recent origin of the erected as a member of the armatus group of the genus in the Oriental region of Ϸ10Ð13 million years subgenus Zaprionus s.s. (Chassagnard and Tsacas ago (MYA), followed by the colonization of Africa via 1993). It was originally created as a complex of three the maritime route of the islands of the Indian Ocean species characterized by the presence of a spur borne Ϸ7 MYA. The subgenus Zaprionus is very common in on a salient tubercle on the medioventral margin of the Africa (Tsacas et al. 1981). Recently, three African forefemur (Tsacas et al. 1977), namely, Z. tuberculatus, species (Z. indianus Gupta, Z. tuberculatus Malloch, Z. sepsoides Duda, and Z. mascariensis Tsacas & David. and Z. ghesquierei Collart) have been introduced into The two former species are widespread throughout the Palearctic region (Chassagnard and Kraaijeveld the Afrotropical region and the islands of the Indian 1991), with Z. indianus further expanding its range in Ocean, whereas Z. mascariensis is restricted to the India and the Americas (David et al. 2006, Yassin et al. insular Indian Ocean. A molecular phylogenetic revi- 2008b). Due to its lack of sexual dimorphism, high sion of the subgenus (Yassin et al. 2008a) revealed that ecological diversity, and its great morphological uni- 1) the subgroup is a member of the inermis group, and formity, Zaprionus is thought to harbor many cryptic its forefemoral ornamentation is not homologous to that of other species of the armatus group; 2) the subgroup is polyphyletic with two species from the 1 Current address: De´partement Syste´matique et Evolution, Mu- se´um National dÕHistoire Naturelle, UMR 5202 GPS3, 16 rue Buffon, inermis group, Z. kolodkinae Chassagnard & Tsacas 75005 Paris, France (e-mail: [email protected]). and Z. verruca Chassagnard & McEvey, and endemic 0013-8746/08/0978Ð0988$04.00/0 ᭧ 2008 Entomological Society of America November 2008 YASSIN:SYSTEMATICS OF Z. tuberculatus SUBGROUP 979 to Madagascar. In addition, two new species, Z. burlai Molecular Analysis. Mitochondrial DNA was ex- n. sp. from Tanzania and Z. tsacasi n. sp. from Sa˜o tracted from single ßies by using a DNA extraction kit Tome´, with incomplete reproductive isolation with Z. (QAIGEN, Hilden, Germany). Polymerase chain re- tuberculatus and Z. sepsoides, respectively, are de- action ampliÞcation, COII primers, and sequencing scribed here. This increases the number of members protocols were as described in Yassin et al. (2008b). of the tuberculatus subgroup from three to seven spe- Nucleotide sequences were viewed and manually ed- cies. ited using Molecular Evolutionary Genetics Analysis Z. tuberculatus and Z. sepsoides are similar at the (MEGA) version four (Tamura et al. 2007). Table 1 morphological level, and they can only be distin- shows GenBank accession numbers for the different guished on the basis of internal anatomical structures species and populations used in this study. MEGA also (testis length and shape of egg velae). This requires was used to reconstruct phylogenies using neighbor- freshly killed specimens or laboratory cultures, which joining (NJ) (Saitou and Nei 1987) and maximum Downloaded from https://academic.oup.com/aesa/article/101/6/978/2758498 by guest on 27 September 2021 may eliminate the use of museum-pinned or alcohol- parsimony (MP). Maximum likelihood (ML) and Bayes- preserved material. Recent advances in molecular and ian inference (BI) were performed using PHYML morphometrical tools should help to delimit cryptic (Guindon and Pascual 2003) and MrBayes version 3.1 species easier (see Bickford et al. 2007). Here, the (Ronquist and Huelsenbeck 2003), respectively, by us- seven species of the tuberculatus subgroup were re- ing the GTR ϩ⌫substitution model (Tavare´ 1986) as vised in light of molecular analysis of the mitochon- proposed by the FindModel program (Tao 2005). drial cytochrome oxidase subunit two (COII) gene Monophyly-conÞdence limits were determined at 50% and morphometrical analysis of wing venation. It has cut-off after 500 bootstrap iterations (NJ, MP, and recently argued that the species identiÞcation utility ML) or 50% posterior probability after a run of of COII is equivalent to that of COI in the DNA 2,000,000 generations (BI). Divergence times were barcoding project in Diptera (Roe and Sperling 2007). estimated using the Drosophila mutational rate of Because neither DNA sequences nor morphometrical 1.1 ϫ 10Ϫ8 substitution per site per year (Tamura et al. analyses are substitutes for morphological alpha-tax- 2004) under a relaxed UCLN clock model (Drum- onomy (Schlick-Steiner et al. 2007), detailed descrip- mond et al. 2006) as implemented in the BEAST ver- tions of the two new cryptic species are included here. sion 1.4 package (Drummond and Rambaut 2007). The morphological evolution and historical biogeog- Morphometrical Analysis. Right wings of 10 males raphy of the subgroup also are discussed. per species were mounted in 20% glycerol and pho- tographed using a digital camera attached to a stereo- Materials and Methods scope (Lecia, Wetzlar, Germany). Only Þve males were available for Z. verruca. For Z. tuberculatus and Specimen Preparation and Morphological Descrip- Z. sepsoides, individuals from the same geographical tion. Flies were collected using fermenting banana traps or by net sweeping over rotten fruit. Laboratory location (Eshowe, South Africa) were used. Ten vein cultures were maintained at 21ЊC on standard Dro- intersections and terminations were landmarked by sophila medium, following the precautions described using the TpsDig 2 software package (Rohlf 2006) as for Zaprionus in David et al. (2006). Z. kolodkinae and shown in Fig. 2. Interlandmark distances were esti- Z. verruca ßies were only available as frozen material mated using PAST version 1.68 (Hammer et al. 2001) of the type strains. package. Formulae for Drosophila wings (McEvey Formal morphological description of the new spe- 1990) were estimated from interlandmark distances as ϭ ϭ ϭ cies followed standard Drosophila terminology and follows: C-index a/b, 4v-index c/d, 4c-index ϭ ϭ ϭ index formulae (McEvey 1990). Specimens were de- b/d, 5x-index e/f, M-index e/d, and ac-index posited in Laboratoire Evolution, Ge´nomes et Spe´cia- b/i (Fig. 2). The C3-fringe index, the ratio of the tion, Gif-sur-Yvette, France (LEGS), as living cul- length of the heavy to the light setation in third costal tures, frozen and alcohol-preserved material, and in section, was included in the morphological descrip- the Muse´um National dÕHistoire Naturelle, Paris, tion but not in the morphometrical analysis. Overall France (MNHN) as pinned material. For comparative shape variation among species was analyzed using purposes, male genitalia of the seven species were multivariate analysis of variance (MANOVA) with dissected, mounted on microscopic slides (Fig. 1), and species as the main effect as implemented in PAST. A preparations are stored in LEGS. Anatomical struc- multivariate version of the discriminant function anal- tures were abbreviated as follows: fw, front width; ß, ysis is the canonical variate analysis (CVA) which front length; hw, head width; o, maximum diameter of produces a scatter plot of individuals along the two the eye; j, width of gena in line with o; ch, maximum Þrst canonical axes, producing maximal and second to width of gena; or1, proclinate orbital seta; or2, anterior maximal separation between all species.
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