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Molecular Phylogeny of Allograpta (Diptera, Syrphidae) Reveals Diversity of Lineages and Non-Monophyly of Phytophagous Taxa

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Molecular Phylogeny of Allograpta (Diptera, Syrphidae) Reveals Diversity of Lineages and Non-Monophyly of Phytophagous Taxa Molecular Phylogenetics and Evolution 49 (2008) 715–727 Contents lists available at ScienceDirect Molecular Phylogenetics and Evolution journal homepage: www.elsevier.com/locate/ympev Molecular phylogeny of Allograpta (Diptera, Syrphidae) reveals diversity of lineages and non-monophyly of phytophagous taxa Ximo Mengual a,*, Gunilla Ståhls b, Santos Rojo a a Dpto. de Ciencias Ambientales/Instituto Universitario CIBIO, Universidad de Alicante, Apdo 99, E-03080 Alicante, Spain b Finnish Museum of Natural History, P.O. Box 17, FI-00014 University of Helsinki, Finland article info abstract Article history: Phylogenetic relationships of genera Allograpta, Sphaerophoria and Exallandra (Diptera, Syrphidae) were Received 20 November 2007 analyzed based on sequence data from the mitochondrial protein-coding gene cytochrome c oxidase sub- Revised 7 September 2008 unit I (COI) and the nuclear 28S and 18S ribosomal RNA genes. The three genera are members of the sub- Accepted 16 September 2008 family Syrphinae, where nearly all members feed as larvae on soft-bodied Hemiptera and other Available online 26 September 2008 arthropods. Phytophagous species have recently been discovered in two subgenera of Allograpta,sgFazia and a new subgenus from Costa Rica. Phylogenetic analyses of the combined datasets were performed Keywords: using parsimony, under static alignment and direct optimization, maximum likelihood and Bayesian Syrphidae inference. Congruent topologies obtained from all the analyses indicate paraphyly of the genus Allograpta Allograpta Sphaerophoria with respect to Sphaerophoria and Exallandra. Exallandra appears embedded in the genus Sphaerophoria, Exallandra and both genera are placed within Allograpta. The distribution of phytophagous taxa in Allograpta indi- Molecular phylogenetics cates that plant feeding evolved at least twice in this group. COI Ó 2008 Elsevier Inc. All rights reserved. 28S 18S Phytophagy 1. Introduction Members of the subfamily Syrphinae have larvae that are pre- dacious mostly on soft-bodied Hemiptera, but includes also taxa The family Syrphidae (hover or flower flies) comprises almost that prey on larvae of Neuroptera, other Diptera, Acari, Lepidop- 6000 described species and is nearly worldwide in distribution tera, Coleoptera or Thysanoptera (for a review see Rojo et al., (Thompson, 2006). Current classification of Syrphidae recognizes 2003). Hamrum (1966) concluded that the feeding habits of com- three subfamilies, Microdontinae, Eristalinae and Syrphinae, and mon Syrphinae species probably range from obligate aphid feeders 14 tribes in total (Thompson and Rotheray, 1998). Syrphids are (e.g. some Eupeodes) to facultative phytophagous–aphidophagous typically black with yellow and orange markings, particularly vis- forms as Melanostoma spp. to primarily phytophagous species like ible on abdomen. This coloration of many species causes them to Toxomerus politus, ‘‘the corn-feeding syrphid fly”. Literature records be confused with bees or wasps; they are excellent mimics of acu- on presumed or more well-documented phytophagy of Toxomerus leate Hymenoptera. The adults of the family have the ability to ho- politus larvae includes Riley and Howard (1888), Richardson ver motionless in the air and are associated with flowers, which are (1915), Rosewall (1916), and Smith (1974), reporting observations used as energy sources (pollen and nectar) and as mating sites. Syr- of pollen feeding and feeding on the sap from the saccharine cells phid larvae are very variable in structure, habits and feeding of Zea mays. Some taxa of genera Melanostoma and Platycheirus modes. All known microdontines are ant brood predators, while (tribe Bacchini) have been shown to facultatively feed on decaying the subfamily Eristalinae includes feeding modes as diverse as sap- vegetal matter (Goeldlin de Tiefenau, 1974; Rotheray and Gilbert, rophagy, phytophagy, mycophagy, and, immatures of the genus 1989). Volucella which are wasp and bee brood predators (Rotheray, 1993; Rotheray and Gilbert, 1999). The members of the eristaline 1.1. Allograpta Osten Sacken, 1875 tribe Pipizini are aphid predators, sharing this feeding mode with the subfamily Syrphinae. Genus Allograpta, member of the subfamily Syrphinae, was established for Scaeva obliqua Say, 1823 described from North * Corresponding author. Fax: +34 96 590 3815. America (USA). Allograpta comprises species of great morphologi- E-mail address: [email protected] (X. Mengual). cal variation, very slender to moderately robust (length 5.9– 1055-7903/$ - see front matter Ó 2008 Elsevier Inc. All rights reserved. doi:10.1016/j.ympev.2008.09.011 716 X. Mengual et al. / Molecular Phylogenetics and Evolution 49 (2008) 715–727 13.7 mm), with different patterns of yellow markings on abdomen concluded that the genus Allograpta is paraphyletic with respect (oblique markings, roundish spots or stripes), and with lower part to Sphaerophoria, but with no close relationship with Baccha. Thus, of face either receding, produced forwards or downwards. Vocke- Allograpta and Sphaerophoria were shown to be closely related roth (1969, 1973a) defined the current concept of Allograpta and based on separate studies on adult morphology, immature charac- discussed the great variation in size, body shape, colour pattern, ters and DNA sequences. Results of Mengual et al. (2008) resolved and head shape within the genus. He was the first to recognize that Allograpta + Sphaerophoria as sister group to genera ((Episyr- Old World species belonged to the genus described from the New phus + Meliscaeva)+Asarkina). As a sister group of this grouping World. Allograpta flower flies are distributed almost worldwide, were placed some genera like Toxomerus, Ocyptamus, Paragus and except not known from the northern areas of the Nearctic region Allobaccha. and in the Palaearctic region distributed only in its south-eastern portion (Vockeroth, 1969). 1.2. Aims of the study The total number of described species reaches 106 divided in six subgenera (from Thompson, 2006; Mengual et al., unpublished; To explore the monophyly of and the relationships between the summarized in Table 1). Highest diversity of species and subgenera subgenera of Allograpta are the major aims of this study. We also is found in Neotropics, with 56 species and all six subgenera pres- attempted to anwser if phytophagy has evolved several times ent. The subgenera are Allograpta s. str. Osten Sacken, 1875, Antillus within the group. Additionally, we were interested to re-address (Vockeroth, 1969), Claraplumula (Shannon, 1927), Fazia (Shannon, the phylogenetic relationships between Allograpta, Sphaerophoria 1927), Rhinoprosopa (Hull, 1942), and a new subgenus found only and Exallandra found by Mengual et al. (2008). Thus, a fragment in Costa Rica referenced here as subgenus CR, described by Men- of 18S rRNA gene (approx. 350 nucleotides) was used, in addition gual et al. (unpublished). All these subgenera have had generic sta- to the mitochondrial protein-coding gene cytochrome c oxidase tus in the past, but with a described close relationship with subunit I (COI) and the nuclear D2-3 28S previously used by Men- Allograpta. Consequently, Neotropical specimens are the most gual et al. (2008). Especially the two latter gene regions have abundant in our study. Only the subgenus Allograpta, rather uni- proved to be informative for species-level and genus-level analy- form except Australian and New Zealander species, is distributed ses, as demonstrated in a large number of studies of insect evolu- outside the Neotropical region. tionary relationships (e.g. Caterino et al., 2001; Ståhls et al., 2003, A first indication of genus Allograpta as being not obligatory 2004; Arevalo et al., 2004; Kjer, 2004; Mengual et al., 2006; Ståhls, predatory was Davidson (1922) observation of larvae of Allograpta 2006; Brammer and von Dohlen, 2007; Milankov et al., 2007). obliqua being able to sustain themselves on plant food. The signif- icant finding of Nishida et al. (2002) reported the first clear case in 2. Materials and methods which a reared syrphine species, Allograpta centropogonis Nishida, 2002, was shown to feed on live plant tissue, mining the leaves 2.1. Taxon sampling of four species of Centropogon (Campanulaceae). This species be- longs to subgenus Fazia and there are three additional undescribed The taxon sampling was done trying to cover as much taxo- species differing only in the details of the male genitalia (Nishida nomic diversity as possible, particularly of the genera Allograpta et al., 2002). Recently, another non-predacious Allograpta (classi- and Sphaerophoria. We included representatives of five subgenera fied into the same subgenus) was discovered at high elevations of Allograpta (specimens of the sixth sg. Claraplumula could not in Costa Rica when the larvae of A. (Fazia) micrura (Osten Sacken, be obtained for molecular analysis), and most included species 1877) were found to feed on pollen of Castilleja (Scrophulariaceae) have Neotropical or Afrotropical distributions (see Table 1). Finally, flowers (Weng and Rotheray, unpublished). 37 specimens of the genus Allograpta were included in the analysis Van Zuijen and Nishida (unpublished) found Allograpta zumba- representing 34 putative species (32.1% of known species) (Table doi Thompson, 2000 boring the stems of Centropogon plants. This 2). The highest diversity in number of species and subgenera is species is placed in a new subgenus (Mengual et al., unpublished) found in the Neotropical region, and it was represented in
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