Diptera

Yeates, David K., Wiegmann, Brian M., Courtney, Greg W., Meier, Rudolf, Lambkin, Christine & Pape, Thomas, 2007, Phylogeny and systematics of Diptera: Two decades of progress and prospects *, Zootaxa 1668, pp. 565-590 : 569-571

Lower Diptera

The paraphyly of this assemblage (=”Nematocera”) was suspected for three decades ( Hennig 1968, 1973, 1981, Wood and Borkent 1989) and demonstrated in recent cladistic analyses ( Sinclair 1992, Oosterbroek and Courtney 1995, Blagoderov et al. 2007). A classification of Diptera that avoided the use of the paraphyletic “Nematocera” was proposed recently ( Amorim and Yeates 2006). While there have been a few modern phylogenetic analyses of the relationships between the Lower dipteran families, both using morphological ( Wood and Borkent 1989, Oosterbroek and Courtney 1995) and molecular (Friedrick and Tautz 1997b) data, there is little consensus of relationships ( Yeates and Wiegmann 1999). However, the supertree is well resolved in the Lower Diptera , largely reflecting Oosterbroek and Courtney’s (1995) tree. Detailed examination of the male genital tract and aedeagus found a character uniting the Bibionomorpha, Ptychopteromorpha and Culicomorpha, and a character uniting the Blephariceromorpha, Psychodomorpha and the Brachycera ( Sinclair et al. 2007). In contrast to Osterbroek and Courtney’s (1995) results, both Sinclair et al. (2007) and Blagoderov et al. (2007) found the Tipulomorpha to be sister to the remaining Diptera .

Some of the traditionally recognized Lower Dipteran infraorders near the origin of the Brachycera are not monophyletic in the supertree—Psychodomorpha and Tipulomorpha form paraphyletic groupings, and the superfamily Tipuloidea is placed as sister-group to the Brachycera. This arrangement of Tipulomorpha and Psychodomorpha reflects conflict between the trees of Wood and Borkent (1989) and Oosterbroek and Courtney (1995). The Culicomorpha and Ptychopteromorpha form a monophyletic group that is the sister lineage to all other Diptera , and the Culicomorpha contains two sister superfamilies, Culicoidea and Chironomoidea.

Culicomorpha are a well-supported clade containing most bloodsucking lower dipterans. This group includes the families Culicidae (mosquitoes), Dixidae , Corethrellidae , Chaoboridae , together comprising Culicoidea, and families Thaumaleidae , Simuliidae (black flies), Ceratopogonidae (biting midges) and Chironomidae (midges), together comprising Chironomoidea ( Hennig 1981). Most recent phylogenetic studies in Lower Diptera have focused molecular sequence data on issues within the Culicomorpha, especially the Culicidae . A number of studies have examined the relationship between Culicomorpha using sequence data from ribosomal genes ( Pawlowski et al. 1996, Miller et al. 1997). The latter results generally did not support the morphology-based tree of Oosterbroek and Courtney (1995). Saether (2000a) reexamined culicomorph relationships using 81 morphological characters, including a number of new characters not considered by previous authors. Results varied depending on specific weights and transformation models applied to characters, suggesting that support for critical nodes may be weak for this dataset. In Saether’s tree, Thaumaleidae or ( Thaumaleidae + Nymphomyiidae ) were the sister to all other culicomorph families. Chironomidae and Simuliidae formed a sister clade to the remaining families in the infraorder, and this clade sometimes included the Ceratopogonidae . The Chironomoidea were paraphyletic with respect to the Culicoidea. Beckenbach and Borkent (2003) used mtDNA to resolve the phylogeny of Ceratopogonidae and in so doing addressed the position of the family within the infraorder. Their results are congruent with earlier morphological analyses of the family and infraorder in suggesting that the Ceratopogonidae is sister to the Chironomidae , and that Simuliidae is sister to this combination. It appears that the mtDNA evolves at a higher rate in Ceratopogonidae and Chironomidae than in the other families sequenced.

More recent studies have examined relationships of and within the Culicidae , using both mitochondrial ( Beebe et al. 2000, Krzywinski et al. 2001a, Sallum et al. 2002, Mitchell et al. 2002) and single copy nuclear genes ( Besansky and Fahey 1997, Krzywinski et al. 2001b), combinations of molecular data classes ( Foley et al. 2007) and morphological data ( Anthony et al. 1999, Harbach and Kitching 1998, Sallum et al. 2000, Harbach and Kitching 2005). Subfamily relationships of Chironomidae were articulated using a matrix of 89 morphological characters ( Saether 2000b), compiled from previous studies. Results of this quantitative study were broadly comparable to previous, nonquantitative approaches. Simultaneous phylogenetic analysis of 28S, elongation factor-1alpha, PEPCK (phosphoenolpyruvate carboxykinase) and DDC (dopa decarboxylase) sequences yielded concordant results with morphological studies for the oldest divergences in the Simuliidae ( Moulton 2000) .

Blephariceromorpha comprise three families, Blephariceridae , Deuterophlebiidae and Nymphomyiidae , united by a number of morphological characteristics generally associated with their larval habitat preference for swift-flowing streams ( Wood and Borkent 1989, Courtney 1990ab, 1991, Oosterbroek and Courtney 1995, Arens 1995). The infraorder is also monophyletic in the current supertree analysis ( Fig. 1 ).

Bibionomorpha include Bibionidae , Pachyneuridae , Mycetophilidae , Sciaridae and Cecidomyiidae ( Blaschke-Berthold 1994, Wood and Borkent 1989), and Axymyidae were added recently ( Oosterbroek and Courtney 1995). Evidence from 28S rDNA sequence ( Friedrich and Tautz 1997b) supported an expanded concept ( Hennig 1981) of Bibionomorpha that also contains the families Anisopodidae and Scatopsidae from Psychodomorpha. Chandler (2002) examined the relationships of Sciaridae , Mycetophilidae sensu stricto, and their relatives, discussing the distributions of 21 adult morphological characters. A number of extant genera normally placed in the Sciaridae or Diadocidiidae showed greater affinities with extinct Mesozoic families of Sciaroidea. Malaise trapping in New Zealand temperate forests revealed a new family-level lineage of sciaroids, the Rangomaramidae , or long-winged fungus gnats ( Jaschhof and Didham 2002). The small little – known family, Axymyidae, is placed as sister group to the remaining Bibionomorpha on the full supertree.

Psychodomorpha include the families Psychodidae , Perissommatidae , Anisopodidae , Scatopsidae and Synneuridae and were considered monophyletic based on synapomorphies of the larval mouthparts ( Krivosheina 1988, Wood and Borkent 1989). These synapomorphies have been criticized because of their widespread distribution in other infraorders ( Griffiths 1990). More recent morphological studies have found that Psychodomorpha are paraphyletic with respect to Tipulomorpha and Brachycera ( Oosterbroek and Courtney 1995). Molecular analyses have suggested that Psychodomorpha are polyphyletic, and Anisopodidae and Scatopsidae have closest relatives in Bibionomorpha ( Friedrich and Tautz 1997b). The relationships of the Synneuridae were examined using 59 adult morphological features ( Amorim 2000). The Canthyloscelidae are now recognized as a family-level taxonand is placed as sister group to the Scatopsidae ( Hutson 1977, Amorim 2000). The Valeseguyidae are considered sister to Canthyloscelidae + Synneuridae , known from the Cretaceous of Myanmar, Miocene of the Dominican Republic, and recent of Australia ( Amorim and Grimaldi 2006). A phylogeny of the genera of Mycetophilidae sensu stricto genera Soli (1997) did not support the three commonly recognized subfamilies. The relationships of families related to the Mycetophilidae were reviewed, and a new morphological phylogeny found Cecidomyiidae ( Sciaridae ( Rangomaramidae + Mycetophilidae sensu lato) ( Amorim and Rindal 2007), however other studies placed Sciaridae closer to Mycetophilidae sensu stricto ( Hippa and Vilkamaa 2006).

The Tipulomorpha are a traditionally problematic taxon, both in terms of their familial composition and their relationship to other Lower Diptera . A number of synapomorphies have been proposed for a Tipulomorpha containing both the Tipuloidea (= Tipulidae sensu lato, or Cylindrotomidae , Limoniidae , Pediciidae , and Tipulidae sensu stricto) and Trichoceridae ( Hennig 1954, 1973, 1981, Griffiths 1990, Oosterbroek and Courtney 1995). Hennig further hypothesized a sister-group relationship between Tipulomorpha and all remaining Diptera , an arrangement accepted by some authors (e.g., Krzeminski 1992a, Michelsen 1996b, Blagoderov et al. 2007) but only partly by Wood and Borkent (1989). Wood and Borkent’s concept of Tipulomorpha was restricted to the Tipuloidea, with this clade sister-group to all other Diptera and Trichoceridae assigned to Psychodomorpha. Larval characters were the primary basis for this rearrangement. Griffiths (1990) accepted the Psychodomorpha sensu Wood and Borkent but suggested tipuloids should be moved from the base of the tree to be nested within the Psychodomorpha. This shift of tipulomorph families from the basal-most lineage of Diptera to nested amongst psychodomorph families was suggested also by Oosterbroek and Courtney (1995). The Tipulomorpha were paraphyletic in an analysis of 28S rDNA sequence data ( Friedrich and Tautz 1997b). This group also is paraphyletic in our supertree analysis ( Fig. 1 ), with Trichoceridae nesting within the Psychodomorpha.

The search for the sister-group of Brachycera among subgroups of lower Diptera began relatively recently. The root of Brachycera has been localized within the Psychodomorpha in most studies ( Wood and Borkent 1989, Woodley 1989, Sinclair 1992, Michelsen 1996b), or is shared with the Psychodomorpha and Tipulomorpha together ( Oosterbroek and Courtney 1995). Some studies favor Anisopodidae , over other families of Psychodomorpha, as sister-group of Brachycera ( Krivosheina 1988, Woodley 1989, Oosterbroek and Courtney 1995, Blagoderov et al. 2007). Synapomorphies proposed to link Anisopodidae and Brachycera include the loss of mandibular prostheca in the larvae, larval head with membranous ventral region, larval anal papillae absent ( Oosterbroek and Courtney 1995), R4, M3 and discal cell present in the adult wings, and three spermathecae present in the adult females ( Woodley 1989).

Figures

FIGURE 1. Supertree for Diptera based on MRP coding of 313 nodes found in 12 primary trees listed in text. The MRP supertree matrix (available from the senior author) was analysed with PAUP * 4.0 B 10 (Swofford 2002) using Goloboff's weighting function, 10 random addition sequences and NNI branch swapping. The tree is stable to values of k ranging from 1 to 8. Figure 1 is a semi-strict consensus of 1879 trees (each cost - 295.34). Goloboff’s weighting scheme downweights characters with homoplasy during tree search, and k describes the shape of the weighting function, or the severity with which homoplasious characters are downweighted. Lower values of k discriminate most strongly against homoplasy, but the tree is insensitive to a range of different weighting functions. In terms of a MRP matrix, homoplasy can be interpreted as input tree nodes that are incongruent with other input tree nodes. This weighting scheme tends to prefer congruent nodes over incongruent ones.