Phylogenetic systematics of the Milichiidae

Summarized from Brake (2000)

The Milichiidae are a monophyletic family (Click here for phylogenetic tree).

Apomorphic characters for the Milichiidae are:

upper orbital seta lateroclinate (C1-1),
middle orbital seta lateroclinate (C2-1),
lower orbital seta lateroclinate (C3-1),
two medioclinate frontal setae present (C4-1),
proclinate setula between supra-antennal seta and eye margin present (C6-1),
a pair of setulae present on the lunule (C7-1),
four pseudotracheae (C16-1),
postgonites lost (C39-1).

The Milichiidae can be divided into three subgroups: Phyllomyzinae, Madizinae, and Milichiinae. The Phyllomyzinae is the first to branch off. The Madizinae and Milichiinae are sister-groups. Apomorphies for the Madizinae+Milichiinae are:

upper orbital seta medio-reclinate (C1-2),
postocellar setae parallel to slightly converging (C5-2),
basisternum large and V-shaped (C20-2),
phallapodemic sclerite fused with bases of pregonites and hypandrium (C40-2),
median part of hypandrium lost (C41-1).

A further apomorphy of the Madizinae+Milichiinae is probably the presence of a secondary ovipositor (C49), though it must have been subsequently reduced several times within the Milichiinae and the Madizinae. The following character states, which are all correlated with the presence of the secondary ovipositor in my opinion, are also apomorphic for the Milichiinae+Madizinae:

S8 forming two strips, each with a row of setulae (C47-4),
ring of barbed spines between S7 and S8 (C48-2),
secondary ovipositor present (C49-1),
ovipositor short (C50-1),
supra-anal plate bare (C51-1),
cerci short (C52-1).

Phyllomyzinae

Phyllomyzinae include the genera Aldrichiomyza, Borneomyia, Costalima, Microsimus, Neophyllomyza, Paramyia, Phyllomyza, Stomosis, and Xenophyllomyza. These genera are excluded from the Madizinae because the remaining genera of the Madizinae are more closely related to the Milichiinae than to those forming the Phyllomyzinae. The Phyllomyzinae are characterised by the following apomorphies:

the two medial pseudotracheae converging at tips (C17-1),
proepimeral seta present (C21-1),
first tarsomere of hind leg with a row of setae posteroventrally (C33-1),
the ring of barbed spines between segments 7 and 8 in females lost (C48-1).

A feature hypothesised to be an apomorphy of stem-species C is the notched surstylus (C38-5). This character state is present in Phyllomyza and Borneomyia, but needs to be checked for Costalima and Microsimus.

I tentatively suggest that the monotypic genera Costalima and Microsimus are closely related to Phyllomyza, based on the enlargement of the first flagellomere in males (C9-1). An apomorphy for Microsimus+Phyllomyza could be the presence of long and thick palpi (C14-2). To verify this relationship, the labella, male genitalia and ovipositor of Microsimus and Costalima need to be studied. An additional apomorphy for stem-species D could be myrmecophily, because all three genera are known to share this behaviour: Phyllomyza species have been found in the nests of Lasius and Formica ants, while Costalima was found in an Azteca nest and Microsimus in a Crematogaster nest. In the light of their relationship, the geographic distribution of these three genera is of interest. Phyllomyza is known from the Nearctic, Palaearctic, Afrotropical, Oriental, and Australasian-Oceanian Regions, but not from South America. However, although Phyllomyza is widely distributed, its association with ants is only known from Europe. Microsimus and Costalima are only known from South America. As all three genera are myrmecophilous, the distribution pattern of the flies could well reflect the distribution of the ants: Formica is distributed in the Nearctic and Palaearctic Regions, and Lasius additionally in the Oriental Region. Azteca is only known from the Neotropics, but Crematogaster is worldwide in distribution (Hölldobler & Wilson 1990). Neither the Phyllomyza flies nor the ants Formica and Lasius, with which they are associated, are found in South America. However, neither are these ant genera found in the Afrotropical, Australasian, and Oceanian regions. The question thus arises: with which ants are the flies associated in these regions?

The sister-species of stem-species C is stem-species E. Stem-species E is characterised by several apomorphic characters: long labella (C18-1) with two pseudotracheae (C16-3), apically rounded surstyli (C38-1), and a large, "sock-shaped" distiphallus (C42-3). Furthermore, T7 of the female ovipositor is longitudinally divided in almost all the species which descended from stem-species E (C44-1). Only in Aldrichiomyza is T7 not divided. This division of T7 may either have evolved once in stem-species E and have been reversed in Aldrichiomyza, or it evolved convergently in Neophyllomyza+Paramyia, in Stomosis, and in Xenophyllomyza.

An apomorphy for the stem-species of Neophyllomyza+Paramyia is the basisternum forming a narrow triangle (C20-1). Additional apomorphies may be the shapes of S8 and T8 (C45-2, 47-2). These last two characters are uncertain, because there are species with differently shaped S8 and T8 in Neophyllomyza and Paramyia. To support these characters, the stem-species pattern of the genera Neophyllomyza and Paramyia should be checked.

In stem-species F there is apomorphically a long seta on the hind femur (C31-1), S5 in males is either very short or absent (C36-1), and the phallapodemic sclerite is fused with the median part of the hypandrium (C40-1).

Aldrichiomyza+Xenophyllomyza are apomorphically characterised by an absent upper, a reclinate middle, and a proclinate lower orbital seta (C1-3, 2-0, 3-2), by a bare lunule (C7-0), by long and narrow palpi (C14-1), by two katepisternal setae (C24-1), by the costa extending only to R4+5 (C26-1), by diverging R4+5 and M1 (C27-2), by the absence of the comb on the first tarsomere of the hind leg (C33-0), and by two sclerotised stripes on the distiphallus (C43-2). Of these character states, C14-1 (long and narrow palpi) is the only one which evolved only once within the Milichiidae. The other character states evolved more than once: for example, C26-1 (costa extending only to R4+5) and C27-2 (diverging R4+5 and M1) are also present in Paramyia, and C43-2 (two sclerotised stripes on the distiphallus) is present in Neophyllomyza. The character states which evolved convergently in Aldrichiomyza+Xenophyllomyza and in Paramyia, C26-1 and C27-2, and the character which evolved convergently in Xenophyllomyza and Paramyia, C28-1 (crossvein dm-cu lost), are all connected with the costalisation of the wing, which took place in the stem-species of Aldrichiomyza+Xenophyllomyza and in Paramyia convergently (see section 4.3.3). The costalisation must have evolved convergently in these two groups because the sister-group relationship between Aldrichiomyza+Xenophyllomyza and Stomosis (stem-species F) is well supported and it is unlikely that the costalisation was then reversed in Stomosis. In contrast with my results, Papp (1993) wrote that Xenophyllomyza and Paramyia seem to be related or even congeneric (he does not state why, but it is probably because crossvein dm-cu is missing, C28-1) and that Aldrichiomyza and Paramyia are related because they share the costa extending to R4+5, diverging R4+5 and M1, a very long proboscis, and because they have no vibrissa. However, Papp did not include Stomosis and Neophyllomyza in his considerations, nor did he make any phylogenetic analysis. According to my studies, which are based on many more characters, there is more support for the hypothesis that Aldrichiomyza and Xenophyllomyza are sister-groups and that they are not closely related to Paramyia.

Madizinae

The newly defined subfamily Madizinae, which now comprises only the genera Desmometopa, Madiza, Leptometopa, and Litometopa, is characterised by the shape of the distiphallus, which is apomorphically a membraneous tube with a widened part in the middle (C42-2). In addition, there is posteriorly a sclerotised stripe at the base of the distiphallus (C43-1), but this stripe is also present in Ulia and Milichia, which belong to the Milichiinae. This character may therefore be plesiomorphic for the Madizinae and may have evolved in the stem-species of the Madizinae+Milichiinae.

The sister-group relationship between Desmometopa and Litometopa is supported by two characters: the ring tips at the distal end of the medial pseudotrachea in females are longer than the other ring tips (C19-1), and the spermathecal ducts are loosely coiled (C53-1). In addition, the male genitalia (shapes of hypandrial complex, surstyli, and cerci) are very similar in Desmometopa and Litometopa. However, Litometopa shares even more characters with the subgenus Platophrymia of Desmometopa. Litometopa resembles several Platophrymia species in the shining black vibrissal angle and concave face, in the cheeks being about 0.1x the height of an eye, in the yellow colour of fore coxae (D. flavicoxa species-group), and in the fore legs, which are raptorial in appearance (D. melanderi, D. meridionalis, D. saguaro). Furthermore, the shape of the precoxal bridge in D. saguaro could be an early stage of the shape of the precoxal bridge found in Litometopa. Litometopa has been synonymized with Desmometopa by Brake & Freidberg (2003).

The relationship between Leptometopa and Madiza, and the relationship between these two and Desmometopa+Litometopa, is uncertain. Apomorphies for Leptometopa+Madiza could be the apically rounded surstylus (C38-1) and the loss of the secondary ovipositor (C49-0, 50-0, 51-0, 52-0). However, these character states are also present in several other Milichiidae and may have evolved convergently in Leptometopa and Madiza. For the present I prefer to leave the relationship between Leptometopa and Madiza unresolved, with the possibility left open that either Leptometopa or Madiza is more closely related to Desmometopa+Litometopa.

There are two groups of species in Leptometopa, the L. niveipennis-group and the L. latipes-group. The L. latipes-group is characterised by an enlarged hind tibia in males (apomorphic) and one or two anepimeral setae (apomorphic). The L. niveipennis-group is characterised by a setose anepisternum (apomorphic) and a pair of strong prescutellar setae (apomorphic or plesiomorphic) (Papp 1984). The only character present in both groups is the epistoma which is warped forward and has a triangular shape. The tip of the triangle nearly meets the large lunule (pl. 3B). This character state is expressed in Madiza in a similar way, but is not as pronounced. I cannot rule out the possibility that Leptometopa is not monophyletic and that Madiza is closely related to the Leptometopa niveipennis-group.

Milichiinae

The subfamily Milichiinae comprises Enigmilichia, Eusiphona, the Milichia distinctipennis-group, the Milichia speciosa-group, Milichiella, Pholeomyia, Pseudomilichia, and Ulia. The Milichiinae are characterised by the following apomorphies:

middle orbital seta reclinate (C2-0),
lower orbital seta proclinate (C3-2),
vibrissal angle obsolescent and vibrissa above lower margin of eye (C8-1),
eyes enlarged (C10-1),
frons in males narrower than in females (C11-1),
R4+5 and M1 converging at tip (C27-1),
distal margin of anal cell meeting anal vein in a sharp angle (C29-1).

The position of the vibrissa above the lower margin of the eye is correlated with the enlargement of the eyes, and this enlargement and the narrow frons in males are probably adaptations to swarming behaviour in males.

Enigmilichia is the first genus to branch off in the Milichiinae. Apomorphies for stem-species H, the sister-group of Enigmilichia, are subcostal break in the costa developed into a notch (C25-1) and the triangular shape of the wing (C30-1). Additional apomorphies for stem-species H could be a pubescent outer surface of the labella (C15-1) and strongly bent tergites in males (C35-1). However, the proboscis of Enigmilichia has not been dissected, nor has the male abdomen been studied. It is therefore not known whether these characters evolved in the Milichiinae before or after the branching off of Enigmilichia. Further apomorphies of stem-species H could be the presence of more than one katepisternal seta (C24-1) and silvery microtomentose tergites in males (C34-1). In that case, however, these character states must have been reversed in several taxa.

According to my studies, the genus Milichia is para- or polyphyletic: the Milichia speciosa-group is more closely related to Pholeomyia than to the Milichia distinctipennis-group. Traditionally, the genus Milichia has been characterised only by plesiomorphic characters, for example by an entire posterior eye margin (in contrast to Milichiella and Ulia) and a bare anepisternum (in contrast to Pholeomyia). Consequently it is not surprising that the genus is not monophyletic. Apomorphies of stem-species I (Milichia speciosa-group and Pholeomyia) are the loss of the setula between supra-antennal seta and eye margin (C6-0), and parallel R4+5 and M1 (C27-0). Both character states are reversals, and so the group is not well supported.

The Milichia distinctipennis-group comprises M. distinctipennis, M. fumicostata, M. savannaticola, and M. sylvicola. An apomorphy for the M. distinctipennis-group is that the frontal and orbital setae in males are all reclinate except for the lower medioclinate frontal seta. An apomorphy for the M. speciosa-group, which comprises nearly all the other Milichia species, is the absence of frontal setae (C4-0) and perhaps also the tubular shape of the distiphallus (C42-4). The relationship to the M. speciosa-group of all those Milichia species in which frontal setae are present (for example M. ludens) should be checked.

Synapomorphies for the two Pholeomyia species studied by me are the presence of three frontal setae (C4-2), of more than one postpronotal seta (C22-1), and of three or four strong anepisternal setae (C23-3). The generic position of one of these two Pholeomyia species, Pholeomyia nigricosta, has been disputed. It was described as type-species of the genus Macromilichia by Hendel (1932). According to Hendel, Macromilichia is similar to Pseudomilichia Becker, 1907, and Pholeomyia Bilimek, 1867. In the same paper, Hendel synonymised Pseudomilichia with Pholeomyia because he convincingly argued that the character which separated Pseudomilichia from Pholeomyia, an emargination of the posterior eye margin, was not suitable for the differentiation of genera. Hennig (1939) did not follow Hendel's synonymy, but gave no reasons for this. Instead, he synonymised Macromilichia with Pseudomilichia and suggested that Macromilichia nigricosta might be synonymous with Pseudomilichia schnusei. However, Hennig had not seen M. nigricosta. I have only seen the type-specimen of M. nigricosta, but from the description of P. schnusei I conclude that both species are valid. In my opinion, Macromilichia and Pseudomilichia are both synonyms of Pholeomyia, because there are no good grounds for separating these taxa and because all three genera are characterised by the apomorphies of Pholeomyia.

The relationship between the other taxa of the Milichiinae (Eusiphona, Milichia distinctipennis-group, Milichiella, and Ulia) could not be resolved in the present study. However, I believe that the relationships within the Milichiinae can be resolved through a comparative study of the male genitalia of all available species. This study should also resolve the monophyly of the genera.

Phylogenetic position of the Milichiidae within the Schizophora

Since the position of the Milichiidae within the system of Acalyptratae is still uncertain, I will first describe the sister-group relationship of the Milichiidae. I will then work my way up to the family-group level.

The sister-group of the Milichiidae is the Chloropidae. The following characters evolved in their common stem-species B:

ventral appendage of stipes lost and lacinia of maxillae strongly reduced (C13-1),
proboscis slightly elongate and geniculate,
anepisternum without setae (C23-1),
distiphallus short and glabrous (C42-1),
pocket-like ventral receptacle.

The short distiphallus and the pocket-like ventral receptacle are valuable characters because, according to Griffiths (1972) and Sturtevant (1925-1926), they are present only in the Milichiidae and Chloropidae. The other characters evolved convergently among some other Schizophora: in particular, a bare anepisternum is widespread within the Schizophora. An additional apomorphy could be the strongly converging to cruciate postocellar setae (C5-1). However, as the postocellar setae have differing inclinations in the Acartophthalmidae and Carnidae and since the sister-group of the Chloropidae family-group is unknown, converging postocellar setae may be plesiomorphic for the Chloropidae family-group.

The sister-group of the Milichiidae+Chloropidae is the Acartophthalmidae. In their common stem-species A the following characters evolved:

spermathecal ducts elongated and rolled into a single coil distally,
S7/8 symmetrical (male).

The first character is very important, because this situation is not known in other Schizophora. The second character occurs convergently in other Schizophora, for example in the Tethinidae and Canacidae. However, the presence of a symmetrical S7/8 could also be an indication that the Tethinidae/Canacidae complex is the sister-group of stem-species A.

The sister-group of the (Milichiidae+Chloropidae)+Acartophthalmidae is probably the Carnidae. This group of four families was called the Chloropidae family-group by Griffiths (1972). According to Andersson (1977), the only valuable apomorphic character for the Chloropidae family-group is the presence of a phallapodemic sclerite. Support for the inclusion of the Carnidae in the Chloropidae family-group is therefore rather weak.

The sister-group relationship between Milichiidae and Chloropidae is supported by the molecular analysis of Winkler et al. (2010). However, no close relationship of these two families with either Acartophthalmidae or Carnidae could be found and the position of Milichiidae+Chloropidae within Acalyptratae could not be determined.

Comparison with traditional classifications

The Milichiidae, Chloropidae, and related families have been variously placed in two different superfamilies: Tephritoidea and Carnoidea, or Chloropoidea (Griffiths 1972, Hennig 1973, J. F. McAlpine 1989). J. F. McAlpine changed the name Chloropoidea to Carnoidea because the oldest family name is Carnidae.

According to Griffiths (1972), the Chloropidae family-group belongs to the superfamily Tephritoidea (his prefamily Tephritoinea), which he characterised mainly by an elongate, flexible and coiled distiphallus, bearing numerous fine cuticular processes. Apart from the Chloropidae family-group, the Tephritoidea contained for example the Conopidae, Odiniidae, Tephritidae, and Tethinidae. This superfamily in the sense of Griffiths is no longer recognised as several taxa have been removed to other superfamilies (D. K. McAlpine 1985, J. F. McAlpine 1989). This means that the shape of the distiphallus is homoplasious.

Hennig (1973) united the Milichiidae, Carnidae, and Chloropidae in the superfamily Chloropoidea, based on characters present in the Milichiidae and Chloropidae (spermathecal duct coil, reduced anal vein, presence of vibrissa, only one sclerite complex anterior to the male genitalia). He stated that the relationship between Carnidae and Milichiidae needed further study. Colless & McAlpine (1975) expanded the Chloropoidea to include the Tethinidae, Canacidae, and possibly Cryptochetidae, which were later placed near the Drosophiloidea (D. K. McAlpine 1976). D. K. McAlpine (1982) later excluded the Carnidae from the superfamily Chloropoidea because the family did not agree with the Chloropoidea in several characters.

A more recent discussion of the phylogeny of the Diptera was presented by J. F. McAlpine (1989). He placed the Milichiidae in the superfamily Carnoidea, consisting of the families Australimyzidae, ?Braulidae, Canacidae, Carnidae, Chloropidae, Cryptochetidae, Milichiidae, Risidae, and Tethinidae (fig. 11). The Acartophthalmidae were not included in the Carnoidea, but were placed in the Opomyzoidea. J. F. McAlpine lists the following apomorphies for the Carnoidea:

arista dorsal,
vibrissa weakly differentiated,
upper fronto-orbital setae ("orbital setae") lateroclinate,
postocellar setae weakened,
paravertical setae developed,
proepisternal seta developed,
proepimeral seta developed,
sc weakened apically, close to R1,
2 spermathecae.

In my opinion, the support for the Carnoidea is rather weak because it rests mainly on characters of the chaetotaxy, which are often variable even within families. Only the last character of two spermathecae is more substantial. However, it is a reduction, and two spermathecae are present in several other Schizophora families (Kotrba 1993) and may very well be plesiomorphic for the Carnoidea. Another character which is widespread in the Schizophora is the dorsal arista. A proepimeral seta is certainly not present in the stem-species pattern of Carnoidea, but evolved convergently within the Milichiidae and within the Tethinidae/Canacidae complex.

Two families have to be excluded from the Carnoidea: the Risidae belong to the Ephydridae (Freidberg, Mathis & Kotrba 1998), and the Cryptochetidae do not belong to the Carnoidea (D. K. McAlpine 1976, Wheeler 1994). It is possible that the Tethinidae/Canacidae complex (Freidberg 1995) is correctly placed in the Carnoidea because these flies have a similar habitus. However, support for the inclusion of the Tethinidae/Canacidae complex in the Carnoidea is rather weak. Reconstruction of the stem-species pattern of the Tethinidae/Canacidae complex may reveal the true position of this taxon within the Schizophora.

The only genus Australimyza of the Australimyzidae has been included in the Carnidae by Colless & D. K. McAlpine (1991) and Grimaldi (1997). However, I will neither discuss the position of the Australimyzidae nor the Braulidae because I have not studied these families. J. F. McAlpine (1989) placed the Acartophthalmidae next to the Clusiidae in the Opomyzoidea, but his three arguments are rather weak (anepisternum with one seta near middle of posterior margin, S6 in male reduced, and two spermathecae). In my opinion, the arguments for placing the Acartophthalmidae as the sister-group of the Milichiidae+Chloropidae (spermathecal duct coil and phallapodemic sclerite) are much stronger.

For a recent phylogenetic analysis of Carnoidea see Buck (2006).

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