Phylogenetic Position of Puyehuemyia and of Opetiidae

The genus Puyehuemyia is monobasic and P. chandleri is the only species of the family known for the Southern Hemisphere and the New World. Its closer relationship with Opetia, i.e., its inclusion in the Opetiidae, is based on a number of derived similarities, not just plesiomorphies. Some plesiomorphic traits in Puyehuemyia—such as the long, complete Sc, the long R₁ and R₂₊₃, and the complete medial fork—are indeed shared with Opetia. Features such as the absence of crossvein dm-m, the very basal origin of Rs and of R₂₊₃, the long medial stem, and the small size and the basal position of cells br, bm, and cua are apomorphic features shared by Puyehuemyia with lonchopterids, sciadocerines, and euphorids (see Brown et al., 2015). A strong M₄ is shared by Opetia and Puyehumyia, as well as the discrete r-m and the circumambient C (which is also known in the lonchopterids). A small maxillary palpus is widespread among the platypezoids, but the condition in Opetia is similar to that in Puyehumyia. The reduced abdominal segments 5–7 and a piercing-type ovipositor are clearly shared by P. chandleri with O. nigra (Chandler, 2001) and O. anomalipennis (Saigusa, 1963) (female unknown in O. alticola).

The differences between the Chilean species and the Palearctic species are not enough to justify a separate family, but are certainly enough for a distinct genus. The dark brown or black color of O. alticola and O. nigra (fig. 5A) is not seen in P. chandleri (fig. 1A), which is grayish ochre to light brown. The antenna in the Chilean genus has meaningful dissimilarities with that of Opetia. The longer antennal pedicel in Puyehuemyia, widening to the apex (fig. 1B), diverges from the remaining opetiid species (fig. 5B, C). The shape of the first flagellomere in Opetia is slightly wider at the base and tapered to the apex; in Puyehuemyia the first flagellomere is slightly wider midway to the apex. As will be discussed below, the condition of a 3-articled arista in Pueyhuemyia is noticeably divergent from Opetia, and particularly meaningful to the understanding of the evolution of the antennae among the Eremoneura. The 3-articled arista is the plesiomorphic condition in Platypezoidea, and Opetia is well known for its 2-articled arista, with a short basal aristomere (fig. 5B, C). The wing in Pueyhuemyia has dorsal setation on R₁ (fig. 2C), while in Opetia all veins are entirely bare of macrochaetae (fig. 6C). Finally, Opetia has four pairs of well-developed dorsocentrals, though in irregular rows, reaching the anterior third of the scutum (fig. 6A), while in Pueyehuemyia there is a single pair of dorsocentrals at the distal fifth of the scutum (fig. 2A). The male of P. chandleri is unknown, so features of the male terminalia cannot be compared between the two genera at this time. Similarities of the antenna with the Atelestidae, in which the antenna has more a stylus than an arista, would be plesiomorphic.

The question of the 2-articled arista in Opetia is an old issue in the discussion of the position of Opetia. Other features, such as the rotation of the male terminalia, the three sclerotized spermathecae, and the ejaculatory apodeme and sperm pump detached from the base of the phallus, join the “problem” of the 2-articled arista to produce what Chandler (2001) referred to as an enigma—which is now clarified with the description of Puyehuemyia. A many-articled arista is obviously the plesiomorphic condition for the antenna in flies, with many independent reductions. In the Stratiomyomorpha (James, 1981c; Woodley, 2009), the stylus has between five and eight flagellomeres, while in the Xylophagidae and in Xylomyidae its number varies between three and nine (James, 1981a, 1981b; Pechuman and Teskey, 1981; Webb, 1981; Stuckenberg, 1999). The Asilomorpha have a 2-articled stylus. The phylogenetic position of bombyliids, acrocerids, and nemestrinids relative to the asilomorphs and other higher brachycerans has been an issue, but the condition of the stylus in these families helps to clarify the discussion. The Nemestrinidae have a 3-articled stylus (Teskey, 1981), as do the Acroceridae (Schlinger, 1981). In the Bombyliidae this feature varies between one and three segments (Hall, 1981). Most Empidoidea have a 2-articled stylus. Cases of a 3-articled stylus in empidoids are hypothesized to be secondary, since they are deeply nested inside the group—e.g., in the genera Acarteroptera and Meghyperus—with the possible exception of the Atelestidae.

FIGURE 6.

Opetia nigra Meigen, male: A, thorax, dorsal view; B, thorax, lateral view; C, wing. Black arrow points to the short displacement of the katepisternum under the mesepimeron, white arrows points to the partial suture between mesopleurotrochantim and meron.

In most syrphids, the arista has two segments (Vockeroth and Thompson, 1987), while the Pipunculidae have a 3-articled arista (Hardy, 1987). The question of the antennal arista in the Schizophora is also complex. Both 2- and 3-articled conditions are present in various schizophoran families, although this information is not always clear. The 3-articled condition is known, among other families, in Micropezidae, Tanypezidae, Syringogastridae, Lonchaeidae, Ulidiidae, Pyrgotidae, Tephritidae, Richardiidae, in all Sciomyzoidea, all Lauxanioidea, Clusiidae, Agromyzidae, Heleomyzidae, Scatophagidae, Muscidae, Sarcophagidae, Tachinidae, and Calliphoridae. Inferences about the ground-plan condition at different levels within the brachycerans depend on optimization over a phylogeny—presently under heavy dispute. It is quite straightforward, however, independent of the disagreements about the phylogeny of the Muscomorpha, that the 3-articled arista is plesiomorphic and that reductions from three to two segments must have occurred many times independently in the group.

In the Platypezoidea, Ironomyia, Lonchoptera, most platypezids, and most phorids have 3-articled arista—phorids also have species with 2- and 1-articled arista (McAlpine, 2011). The Cretaceous amber platypezid Electrosania cretica Grimaldi and Cumming has a 2-articled arista (Grimaldi and Cumming, 1999). In other Cretaceous platypezids (some being described now, D. Grimaldi, personal commun.), ironomyiids, and sciadocerines, the arista is usually 3-articled. In this scenario the condition of the 3-articled arista in Puyehuemyia (fig. 2B, C) is instructive. It shares the plesiomorphic condition for most other Platypezoidea and elucidates that the 2-articled condition in Opetia is probably secondary. Indeed, the condition in O. nigra, with a first aristomere much shorter than the second, seems to be more modified than in O. anomalipennis, where the second aristomere is only slightly less than half the length of the third aristomere (see, e.g., Sinclair and Cumming, 2006: figs. 45–46). This scenario reinforces the opinion that the condition in acrocerids and nemestrinids, some bombyliids, most platypezids, pipunculids, and many schizophorans is indeed plesiomorphic, with independent reductions in the history of the Muscomorpha.

The evolution of the thoracic pleural sclerites in Phoridae has been addressed in great detail in Brown et al. (2015). Thoracic pleural sclerites show a number of different modifications along the evolution of phorids, particularly in the size and position of the meron relatively to the mesepimeron. The condition seen in sciadocerines is relatively plesiomorphic within the phorids, in many senses similar to the condition in Platypezidae or even outside the Platypezoidea. The condition in Lonchoptera is highly distinctive, apparently with a dorsoposterior displacement of the posterior spiracle, stretching the shape of the meron. In Puyehuemyia the shape of the katepisternum is puzzling, since it only slightly projects posteriorly over the meron. The considerable projection of the katepisternum over the meron is widespread in brachycerans, seen, e.g., in Therevidae, schizophorans, Platypezidae, Lonchopteridae, and Phoridae (see Brown et al., 2015: figs. 1–4). In this sense, the short katepisternum in Puyehuemyia, also seen in Opetia (seta respectively in figs. 2B and 6B), should be seen as apomorphic in relation to the condition in platypezids or sciadocerines. On the other hand, the size and placement of the anterior spiracle relative to the anepisternum and to the proepimeron, and the elongated shape of the anterior basalare, at the dorsoposterior corner of the anepisternum, show considerable similarity with the pattern seen in other nonphorid platypezoids, corroborating its inclusion in the clade. The shape of the mesopleurotrochantin in Puyehuemyia (fig. 6B), with an incomplete suture separating it from meron, is similar to Opetia (fig. 6B), but also to other platypezids (Brown et al., 2015: fig. 2), when comparing the complete mesopleurotrochantin, e.g., in Therevidae (Brown et al., 2015: fig. 1). Another helpful feature in this context concerns the abdominal plaques seen in tergites and sternites of different fly families. These structures have been found in all nematoceran clades, besides basal brachycerans (including Empidoidea), assumed to be the site of attachment of muscles used by the pupa for abdominal movements and for éclosion of the adult (Stoffolano et al., 1988). These structures are missing in all Cyclorrhapha (including Opetia), which does not have mobile pupae (Wiegmann et al., 1993, Cumming et al., 1995, Sinclair and Cumming, 2006), and are not seen as well in Puyehuemyia.

A long Sc, reaching at least the middle of the wing, is the plesiomorphic condition in Brachycera, also seen in some platypezid genera (fig. 8A), as well as in Ironomyia (fig. 8B). In Lonchoptera (fig. 8C), Opetia (fig. 6C), and in most phorids, Sc does not reach the middle of the wing. A reduction of Sc also has occurred independently within the Platypezidae. The evolution of the length of R₁ is slightly different: a strong reduction occurred independently in Lonchoptera and in the Euphorida (Brown et al., 2015). The only noticeable change in R₂₊₃ in platypezoids is, by contrast, the extension of the vein in Lonchoptera, ending close to the wing tip. The extension of R₄₊₅ shows no significant changes in the Platypezoidea except for the major reduction (with various stages) that has occurred in the evolution of the Phoridae. The extension of the costa has some variation. In different species of Platypezidae (fig. 8A) C reaches M₁. Sinclair and Cumming (2006) infer that the circumambient costa would be the ground-plan condition within the Empidoidea, with many changes within the clade, stating that this feature is variable and hard to code. For the time being, it is difficult to say whether the condition in Opetia and Puyehuemyia is homolog to that of empidoids, or whether it is a secondary development within the Platypezoidea. A reduction of the costa to R₄₊₅ is shared by Ironomyia and nearly all phorids. The condition in Lonchoptera is puzzling, since there is a wide costa clearly extending to R₄₊₅, but a slender circumambient costa along the posterior margin of the wing.

The origin of Rs in all platypezoids seems to be closer to the wing base than in most empidoids (fig. 7C), maybe with the exception of the Dolichopodidae (fig. 7D), and other cyclorraphans (fig. 9B–C). This feature, however, is hard to quantify and to transform into an objective character. The displacement to the base of the fork between R₁ and Rs may have occurred in parallel with the displacement of the closed posterior cells to the base of the wing (see below). The transverse vein r-m is conservative in the Platypezoidea. It acquires a longitudinal position in Lonchoptera and is lost in the Euphorida (r-m is tiny in Sciadocera, but still present). Perhaps the position of r-m is slightly more displaced to the base in the platypezoids, but the differences are subtle and this is a variable feature. In Lonchoptera and sciadocerines the origin of r-m at Rs is much closer to the fork of the radial sector, i.e., the origin of R₂₊₃. The medial fork appears to have undergone different changes in the evolution of the Platypezoidea. In Platypezina the medial fork is at the level of m-m+M₃. Other platypezids have a complete loss of M₂ (as in Agathomyia and Callomyia) or displacement of the medial fork close to the tip of the wing (as in Lindneromyia, in which M₂ does not reach the wing margin). The medial fork in Lonchoptera is possibly at its plesiomorphic position, slightly beyond the middle of the wing, as is also seen in Opetia and in Puyehuemyia. The main difference of the medial fork in Opetiidae and Lonchopteridae, when compared with Ironomyia or the platypezids, is that the distal crossvein (that closes the discal-medial cell) is clearly absent. Surprisingly in Sciadocerinae (fig. 13) there is a tiny dm cell near the base of the wing, with the crossvein still present. The displacement of the closed posterior wing cells—d, br, bm, and cua—to a basal position in the wing and their reduction in size in higher platypezoids is one of the most characteristic features of a clade including Opetiidae (fig. 12A–B), Lonchopteridae (fig. 11B), and Phoridae (fig. 13). These cells are considerably larger in Ironomyia (fig. 8B) and all platypezid genera (e.g., fig. 8A)—and even larger in some empidoids (fig. 10B) or pipunculids (fig. 9B), and schizophorans (fig. 9C).

As mentioned above, a relatively wide M₄ is a newly proposed synapomorphy of the Opetiidae (figs. 2C, 6C). The fusion of CuA and CuP is apomorphic in all Eremoneura (with parallel developments in other brachycerans, as in some asilids, acrocerids, etc.). An elongated cell cua is the plesiomorphic condition shared, for example, by brachystomatids, pipunculids, and conopids (fig. 7A–C, 9B–C). The reduction of the size of cell cua has occurred independently at different times. In all Platypezoidea, cell cua is relatively short, but the condition in Platypezidae and Ironomyia is plesiomorphic when compared to that in Lonchopteridae, Opetiidae, and Phoridae, all of which have a very small cell cua. Different clades within the empidoids and the schizophorans developed an incomplete CuA+CuP, not reaching the wing margin. Within the Platypezoidea, only Opetia males (complete in females, fig. 2C) and some few phorids have an incomplete CuA+CuP.

An additional source of information in the discussion about the placement of Puyehuemyia and the position of the Opetiidae is the structure of abdominal segments—at this stage applicable only to females. Platypezids, ironomyids, and lonchopterids have a regular number of well-developed abdominal segments, i.e., from 1–7. Chandler (2001: 19) describes the female abdomen of Opetia as with “segments 1–3 normal, 4 at least a little longer than 3 (...) and 5 shorter,” with tergum and sternum fused basally, the remaining segments fused into the ovipositor, “strongly chitinised.” This condition, which is unique in the Platypezoidea (with some possible exceptions among strongly modified phorids), is extremely similar to that seen in Puyehuemyia (fig. 3C, D).

The set of features seen in Puyehuemyia, hence, supports the hypothesis (Chandler, 2001; Wiegmann et al., 2011) that the Opetiidae belongs to the Platypezoidea Cyclorrhapha. The 2-articled condition of the stylus in Opetia is a secondary, independent reduction, while the wing venation suggests a close connection of the Opetiidae with the higher Platypezoidea—all of which with cells small cells br, bm, and cua, displaced toward to wing base.

Fossils Associated with the Opetiidae

Evenhuis (1994) compiled five Mesozoic fossils in the world catalog of fossil Diptera assigned to Opetiidae: Palaeopetia Zhang, Pseudopetia Zhang, Mesopetia Zhang, Lithopetia Zhang—Sinolesta Hong and Wang was later considered a junior synonym of Palaeopetia—and their position was later discussed by Chandler (2001). He assumed that Pseudopetia Zhang belongs to the Rhagionidae, while Mesopetia Zhang could belong to Platypezidae. Palaeopetia Zhang was suggested by Mostovski (1996) to be related to the Ironomyiidae. Lithopetia Zhang also does not fit with other opetiids. The long medial fork and the origin of R₂₊₃ distant from the wing base clearly separates it from the Opetiidae crown group, as well as from the stem group. Zhang's (1987: fig. 5B) illustration of the wing is not very clear, because of a leg over the wing, but cell cua seems to be too long to fit into the clade including Opetiidae, Lonchopteridae, and Phoridae. Lithopetia might belong in Platypezoidea, but more certainty depends on the reexamining the holotype for a better understanding of the wing venation. Being a Jurassic fossil, it would be understandable if it fits slightly lower in the platypezoid phylogeny.

FIGURE 7.

Wing of brachyceran families: A, Austroleptis sp. (Austroleptidae); B, Holcocephala calva (Loew 1872) (Asilidae) (photo kindly provided by Torsten Dikow); C, Brachystoma sp. (Brachystomatidae); D, Amblypsilopus sp. (Dolichopodidae).

FIGURE 8.

Wing of brachyceran families: A, Lindneromyia sp. (Platypezidae); B, Ironomyia sp. (Ironomyiidae); C, Lonchoptera bifurcata Fallén (Lonchopteridae).

FIGURE 9.

Wing ofbrachyceran families: A, Sciadocera rufomaculata (White 1916) (Phoridae); B, Protonephrocerus sp. (Pipunculidae); C, Physoconops sp. (Conopidae).

FIGURE 10.

Detail of venation at base of wing of Muscomorpha families: A, Holcocephala calva (Loew 1872) (Asilidae; photo, Torsten Dikow); B, Brachystoma sp. (Brachystomatidae).

FIGURE 11.

Detail of venation at base of wing of Muscomorpha families: A, Lindneromyia sp. (Platypezidae); B, Lonchoptera bifurcata Fallén.

FIGURE 12.

Detail of venation at base of wing of Muscomorpha families: A, Puehuemyia chandleri, gen. nov., sp. nov.; B, Opetia nigra Meigen.

FIGURE 13.

Detail of venation at base of wing of Muscomorpha families: Sciadocera rufomaculata (White 1916).

The Cretaceous New Jersey amber fossil Electrosania Grimaldi and Cumming was questionably assigned to the Platypezidae. Chandler (2001) agreed with its inclusion in the Platypezidae, observing that it “has a thoracic chaetotaxy and aristal structure as in Opetiidae.” The distal medial fork with an incomplete M₂ in Electrosania is a unique synapomorphy of a subgroup of Platypezidae. The setation of the scutum, as in Puyehuemyia, is a plesiomorphic trait, while the condition of two aristomeres in Electrosania is most certainly only an additional case of independent shift from three to two articles in the arista within the platypezoids. The results here help to fully support Grimaldi and Cummings (1999) and Chandler's (2001) association of Electrosania to the platypezids. More recently, Coram et al. (2000) described Opetiala from the Purbeck Limestone Early Cretaceous. The wing has a closed discal cell and there is no medial fork. It is beyond the scope of this paper to determine its position within the platypezoids, but Opetiala does not belong to the crown of Opetiidae or to its stem.

A relevant addition to the discussion of platypezoid fossils concerns the Neocomian early Cretaceous Lebanon amber Lonchopterites prisca Grimaldi and Cumming. Sc and R₁ in this fossil are shorter (apomorphic traits) than in the crown species of Opetiidae. R₂₊₃ and R₄₊₅ diverging at the very base of the wing, the shape of the medial fork, the absence of a closed discal cell, and the fact that cells bm, br, and cua are not at a more distal position in the wing— not represented in the original illustration (Grimaldi and Cumming, 1999: fig. 53)—produce a wing pattern like that of Opetia. Some features typical to the Lonchopteridae—the basal fusion of M₁₊₂ to M₄, the displacement of R₂₊₃ to the tip of the wing, and the strong reduction in the length of Sc and R—are not present and Lonchopterites does not properly fit into crown-group Lonchopteridae. Moreover, the antenna has a basal flagellomere widening midway to the apex and the arista has a terminal position with two aristomeres—features that we can better understand in light of the information brought up by Puyehuemyia. There is no other group within the eremoneurans with such a combination of features. In fact, Grimaldi and Cumming (1999) specifically discuss the similarities of Lonchopterites with Opetia. Nevertheless, the acute apex of the wing, vein C ending at R₄₊₅ (instead of circumambient), the bristly legs, a well-developed vibrissa, and robust head setae led them to suggest Lonchopterites to be a stem-group lonchopterid. Some features listed as present in the fossil and absent in Opetia are actually observable in Puyehuemyia, including the spinulose costa and R₄₊₅ longitudinally bisecting the wing. On the other hand, the abdomen of the female holotype has a “generalized structure, with small pair of terminal cerci closely adpressed to apex of abdomen” (Grimaldi and Cumming, 1999: 84) and the wing has a well-developed anal lobe in the female. These are plesiomorphic conditions compared to the recent species of Opetiidae of the genera Opetia and Puyehumyia. This combination of features suggests that Lonchopterites would be a good candidate to be sister to the clade with the recent members of the family.

Biogeographical and Evolutionary Implications

Anyone who might have sorted a Malaise trap sample from the southern island of New Zealand may have noticed the similarity of the final list of sampled families with the list of Cretaceous amber flies—basically species that belong to families that go “up” in the fly phylogeny to the phorids. Only a few schizophorans come into the traps. Malaise trap samples from southern Chile lowland temperate rainforests are similar, though the number of schizophorans may be slightly higher. Austral nonschizophoran elements shared by New Zealand and Chile include, for example, the ditomyiid genus Nervijuncta Marshall (also present in southern Brazil), the canthyloscelid genus Canthyloscelis, ceratomerines empodoids and the sciadocerine phorids Sciadocera rufomaculata (New Zealand and Australia) and Archiphora patagonica (Chile). The empidoid Gondwanamyia, though quite derived, also has one species known from Puyehue National Park and one species known from New Zealand (Sinclair et al., 2016). Canthyloscelis, Gondwanamyia, and Archiphora Schmitz were all collected at the collecting site of Puyehuemyia. There are a considerable number of other austral connections in tipulomorphs, bibionomorphs, and other flies, as well as in various insects (reviewed in Grimaldi and Engel, 2005).

Dominant floral elements in these forests, including certain clades of bryophytes, ferns, conifers, and early angiosperms, are well documented as fossils in Antarctica (Cantrill and Poole, 2005). Cases of disjunctions between Chile and Australia already include a number of modern elements, i.e., the schizophoran families Paraleucopidae, Pseudopomyzidae, Pallopteridae, Teratomyzidae, Helosciomyzidae, Helcomyzidae, and the quite diversified (and possibly paraphyletic) Heleomyzidae. This means that the shared elements between Chile and New Zealand are phylogenetically more restricted than those between Chile and Australia, i.e., probably limited to the fly diversity at the time of detachment between New Zealand and the rest of southern Gondwana.

Edwards (1929) based on extensive collecting in Chile already assumed a land connection between South America, New Zealand, and Australia, and in a period with limited information on geology, paleoclimatology, and phylogeny of flies, Hennig (1966) tried to explain the elements shared between these three areas. More recently, Almeida et al. (2012) demonstrated that the latest cladogeneses between South American and Australian elements of colletid bees occurred about 30 million years ago. This was later corroborated with results in scionini tabanid evolution (Lessard et al., 2013).

The fact that Opetia has been reared from rotting Fagus wood logs and that Puyehuemyia has been found in the Valdivian forest in Chile, dominated by Nothofagus, is also noteworthy. Fagus and Nothofagus are not sister genera, but belong to the same clade Fagales (Hilu et al., 2003). The age estimated for the cladogenesis separating the clades including Fagaceae and Nothofagaceae is close to 120 m.y. (Sauquet et al., 2012), which is about Aptian age. The divergence age for the Cyclorrhapha has been suggested to be about 150 m.y. (Wiegmann et al., 2011). This is also compatible with the age of the Lebanon amber fossil Lonchopterites, from the Neocomian. The combination of the data seen here including fossils, age of divergence of Cyclorrhapha and of Fagales, geology of the southern terranes of Gondwana, and biogeography suggests that the lowland temperate rain forest biota in Chile that includes Puyehuemyia belongs to a biogeographical layer (in the sense of Amorim et al., 2009) that typically encompasses the fly diversification that originated prior to the large schizophoran diversification. If the reasoning is correct we may still expect more cases of unnoticed higher brachyceran relicts in austral lowland forests in Chile and/or New Zealand, perhaps even species that would fit at the stem of the Schizophora. As in any case of negative evidence, this can be checked only with intense collecting in these environments.