Molecular phylogeny and systematics of leaf-mining flies (Diptera: Agromyzidae): delimitation of Phytomyza FallEn sensu lato and included species groups, with new insights on morphological and host-use evolution

Phytomyza FallEn is the largest genus of leaf-mining flies (Agromyzidae), with over 530 described species. Species of the superficially similar genus Chromatomyia Hardy have been included in Phytomyza by some authors and the status of the genus remains uncertain. Using 3076 bp of DNA sequence from three genes [cytochrome oxidase I (COI), CAD (rudimentary), phosphogluconate dehydrogenase (PGD)] and 113 exemplar species, we identified and tested the monophyly of host-associated species groups in Phytomyza and Chromatomyia and investigated the phylogenetic relationships among these groups. Chromatomyia is polyphyletic and nested largely within Phytomyza; two small groups of species, however, are related more closely to Ptochomyza and Napomyza. Therefore, we synonymize Chromatomyia syn.n., Ptochomyza syn.n., and Napomyza syn.n. with Phytomyza, recognizing Ptochomyza, Napomyza and Phytomyza sensu stricto as subgenera of Phytomyza. We recognize five major clades within Phytomyza sensu stricto that comprise the majority of species ascribed previously to Chromatomyia and Phytomyza. Many species groups recognized previously were recovered as monophyletic, or virtually so, but some (e.g. robustella and atomaria groups) required emendation. On the basis of the proposed phylogeny and recent taxonomic literature, we present a preliminary revision of 24 species groups within Phytomyza, but leave many species unplaced. Evolution of internal pupariation (within the host's tissue), regarded as a defining character of the former Chromatomyia, is discussed with regard to the new phylogeny, and we suggest a correlation with stem or leaf midrib mining. The large size of the Phytomyza lineage and an inferred pattern of host family-specific species radiations make it a promising candidate for the study of macroevolutionary patterns of host shift and diversification in phytophagous insects. The proposed generic synonymies necessitate a number of new combinations. The following 46 species described in Chromatomyia are transferred to Phytomyza: P. actinidiae (Sasakawa) comb.n., P. alopecuri (Griffiths) comb.n., P. arctagrostidis (Griffiths) comb.n., P. beigerae (Griffiths) comb.n., P. blackstoniae (Spencer) comb.n., P. centaurii (Spencer) comb.n., P. chamaemetabola (Griffiths) comb.n., P. cinnae (Griffiths) comb.n., P. compta (Spencer) comb.n., P. cygnicollina (Griffiths) comb.n., P. doolittlei (Spencer) comb.n., P. elgonensis (Spencer) comb.n., P. eriodictyi (Spencer) comb.n., P. flavida (Spencer) comb.n., P. fricki (Griffiths) comb.n., P. furcata (Griffiths) comb.n., P. griffithsiana (Beiger) comb.n., P. hoppiella (Spencer) comb.n., P. ixeridopsis (Griffiths) comb.n., P. kluanensis (Griffiths) comb.n., P. leptargyreae (Griffiths) comb.n., P. linnaeae (Griffiths) comb.n., P. luzulivora (Spencer) comb.n., P. mimuli (Spencer) comb.n., P. mitchelli (Spencer) comb.n., P. montella (Spencer) comb.n., P. nigrilineata (Griffiths) comb.n., P. nigrissima (Spencer) comb.n., P. orbitella (Spencer) comb.n., P. paraciliata (Godfray) comb.n., P. poae (Griffiths) comb.n., P. pseudomilii (Griffiths) comb.n., P. qinghaiensis (Gu) comb.n., P. rhaetica (Griffiths) comb.n., P. scabiosella (Beiger) comb.n., P. seneciophila (Spencer) comb.n., P. shepherdiana (Griffiths) comb.n., P. spenceriana (Griffiths) comb.n., P. styriaca (Griffiths) comb.n., P. subnigra (Spencer) comb.n., P. suikazurae (Sasakawa) comb.n., P. symphoricarpi (Griffiths) comb.n., P. syngenesiae (Hardy) comb.n., P. thermarum (Griffiths) comb.n., P. torrentium (Griffiths) comb.n. and P. tschirnhausi (Griffiths) comb.n. Furthermore, we transfer all species of Napomyza to Phytomyza, resulting in the following new combinations: P. achilleanella (Tschirnhaus) comb.n., P. acutiventris (Zlobin) comb.n., P. angulata (Zlobin) comb.n., P. arcticola (Spencer) comb.n., P. bellidis (Griffiths) comb.n., P. carotae (Spencer) comb.n., P. cichorii (Spencer) comb.n., P. curvipes (Zlobin) comb.n., P. dubia (Zlobin) comb.n., P. filipenduliphila (Zlobin) comb.n., P. flavivertex (Zlobin) comb.n., P. flavohumeralis (Zlobin) comb.n., P. genualis (Zlobin) comb.n., P. grandella (Spencer) comb.n., P. humeralis (Zlobin) comb.n., P. immanis (Spencer) comb.n., P. immerita (Spencer) comb.n., P. inquilina (Kock) comb.n., P. kandybinae (Zlobin) comb.n., P. lacustris (Zlobin) comb.n., P. laterella (Zlobin) comb.n., P. manni (Spencer) comb.n., P. maritima (Tschirnhaus) comb.n., P. merita (Zlobin) comb.n., P. mimula (Spencer) comb.n., P. minuta (Spencer) comb.n., P. montanoides (Spencer) comb.n., P. neglecta (Zlobin) comb.n., P. nigriceps (van der Wulp) comb.n., P. nugax (Spencer) comb.n., P. pallens (Spencer) comb.n., P. paratripolii (Chen & Wang) comb.n., P. plumea (Spencer) comb.n., P. plumigera (Zlobin) comb.n., P. prima (Zlobin) comb.n., P. pubescens (Zlobin) comb.n., P. schusteri (Spencer) comb.n., P. scrophulariae (Spencer) comb.n., P. suda (Spencer) comb.n., P. tanaitica (Zlobin) comb.n., P. tenuifrons (Zlobin) comb.n., P. vivida (Spencer) comb.n., P. xizangensis (Chen & Wang) comb.n. and P. zimini (Zlobin) comb.n. Phytomyza asparagi (Hering) comb.n. and P. asparagivora (Spencer) comb.n. are transferred from Ptochomyza. In Phytomyza ten new names are proposed for secondary homonyms created by generic synonymy: P. echo Winkler nom.n. for P. manni Spencer, 1986; P. californiensis Winkler nom.n. for C. montana Spencer, 1981; P. griffithsella Winkler nom.n. for C. griffithsi Spencer, 1986; P. vockerothi Winkler nom.n. for C. nigrella Spencer, 1986; P. kerzhneri Winkler nom.n. for N. nigricoxa Zlobin, 1993; P. asteroide Winkler nom.n. for N. tripolii Spencer, 1966; P. minimoides Winkler nom.n. for N. minima Zlobin, 1994; P. nana Winkler nom.n. for N. minutissima Zlobin, 1994; P. ussuriensis Winkler nom.n. for N. mimica Zlobin, 1994 and P. zlobini Winkler nom.n. for N. hirta Zlobin, 1994.