Miltogramma manouchehrii Szpila and Pape, 2024

Szpila, Krzysztof, Walczak, Kinga, Grzywacz, Andrzej, Akbarzadeh, Agnieszka Soszyńska Kamran, Bystrowski, Cezary & Pape, Thomas, 2024, Underexplored diversity in Palaearctic Miltogramma Meigen, 1803 (Diptera: Sarcophagidae), Zoological Journal of the Linnean Society 201, pp. 1-21 : 14-19

Miltogramma manouchehrii Szpila and Pape , sp. nov.

( Figs 1C , 3G , 9A–K )

Zoobank registration: urn:lsid:zoobank.org:pub:C60CE24C-BCFF-4A7C-B481-ABF84EC230EF .

Type material. Holotype: 1M, Iran, Kerman, Sirch road, 6 May 2017, 30.1949 57.4614, leg. KEiB Iran Expedition IV . Paratypes: 1M, Iran, North Khorasan, Sarcheshmeh, 16 May 2014, 37.6333 57.4070, leg. KEiB Iran Expedition; 1M, Iran, North Khorasan, Kotalli, 17 June 2016, 37.3217 57.0211, leg. KEiB Iran Expedition III; 1M , Iran, North Khorasan, Chehar Bid, 19 June 2016, 37.8106 56.9002, leg. KEiB Iran Expedition III; 1M , Iran, Sevaldi , North Khorasan, 21 June 2016, 37.7186 57.7621, leg. KEiB Iran Expedition III (barcoded, KEIB _DIP_01228); 1M , Iran, Kerman, Sirch road, 8 May 2017, 30.1949 57.4614, leg. KEiB Iran Expedition IV; 1M , Iran, Kerman, Hinaman I, 9 May 2017, 30.5426 57.2818, leg. KEiB Iran Expedition IV .

Male. Body length 5–7 mm (N = 6). Head. Parafacial plate pale whitish, broad, slightly narrowed downward, with the width at level of vibrissal angles 0.7 of the width at the base of antenna. Frons broad, slightly widened posteriorly, 0.32 head width at the ocellar triangle and 0.29 head width at the base of antenna. Fronto-orbital plates yellowish except the posteriormost part, which is dark grey. Frontal viưa 1.5× broader than fronto-orbital plate at vertex, widened posteriorly, width at lunule 0.5 width at anterior ocellus, with yellow microtrichosity. Scape, pedicel, first flagellomere and arista black. Ocellar setae directed anterolaterally. Two pairs of postocellar setae. Inner vertical seta strong, slightly curved, outer vertical seta also curved and 0.7× as long as inner vertical seta; 11–14 pairs of long frontal setae, setae crossed over the frontal viưa. Frontal viưa and vertex bare, one pair of paravertical setae present. Four to seven proclinate orbital setae and one reclinate orbital seta, both strong. Upper part of fronto-orbital plate with a numerous long setulae distributed around orbital setae. Parafacial plate with sparse, yellow setulae. Lunule bare. Scape and pedicel with short setulae. Gena and postgena with sparse white setulae. Postcranium with black setulae. Antenna inserted distinctly above level of middle of eye. Antenna short, first flagellomere 1.9× as long as pedicel and with the same length as distance between tip of first flagellomere and lower margin of facial plate. Arista micropubescent, aristomere 1 shorter than their greatest diameter and aristomere 2 as slightly longer than their greatest diameter, aristomere 3 widened in basal 0.5. Facial plate with low keel below antennal insertion. Supravibrissal and subvibrissal seta numerous, long. Vibrissa distinctly longer than supravibrissal and subvibrissal seta. Vibrissal angles situated above lower margin of facial plate. Height of gena 0.4× length of first flagellomere and 0.1× eye height. Proboscis long, labellum 0.45× as long as prementum, palpus yellow.

Thorax. Black ground colour; covered with dense grey microtrichosity; scutum with unclear median stripes, presutural area with five stripes: a pair of broad lateral stripes flank three narrow inner stripes, postsutural area with three stripes: the continuation of the broad lateral stripes and the narrow median stripe. Entire surface of the thorax with long setulae.

Legs. Foreleg tarsomeres 1–5 with length proportions 1–0.6– 0.5–0.3–0.6. Fore tarsus with claws shorter than tarsomere 5. The anterior margin of the tarsomere 4 with elongated anterior, anterodorsal, posterodorsal and posterior setae. These setae 1.5–1.2× as long as the length of the tarsomere 5. Mid-tibia with two strong and one to two weak anterodorsal setae. Other legs without particular modifications.

Wing. Tegula brown, basicosta yellow, veins yellow; costal spine not developed; base of vein R 4 * 5 without setulae; distal part of vein M bent at right angle, M cell r 4 * 5 open.

Abdomen. Black, covered with grey microtrichosity. Syntergite 1 * 2 and tergites 3–5 with a black band across posterior margin. Black bands occupy 0.3–0.4 of the tergite length. In dorsal view each segment with median black spot separated from the lateral bands by area covered with grey microtrichosity.

Terminalia ( Fig. 9I–K ). Cuticle black, with grey microtrichosity. Cercus (c) black, slightly curved (lateral view) and gradually tapering into a pointed tip (lateral and posterior view). Cercus with scaưered setae and short setulae in basal half, almost bare in distal half. Gonostylus (gst) brown, straight, shorter than cercus, evenly rounded apically and with setulae along whole length. Pregonite (prg) broad, slightly curved anteriorly with pointed tip; postgonite (pog) curved, with rounded tip and strong anterior seta. Basiphallus (bp), ventral plate (vp) and dorsal plate (dp) strongly sclerotized; dorsal plate shallowly bifid apically (posterior view); ventral plate much shorter than dorsal plate. Membranous part of phallus broad, with numerous denticles, acrophallus (ac) widened at tip.

Female. Unknown.

Biology. Specimens were collected around noon perching on stones along dry stream beds and on gravel roads in mountainous habitat.

Barcoding. Barcoded specimen (male) was grouped as sister to species Miltogramma punctata ( Table 2 ; Fig. 4 ).

Etomologo. Species is named in honour of recently deceased, eminent Iranian entomologist, Dr Abdolvahab Manouchehri.

Remarks. Identifying specimens of M. manouchehrii sp. nov. using keys provided by Rohdendorf (1930, 1935) and Verves (1994) leads to species belonging to their subgenera Miltogramma s.s. or Pseudomiltogramma Rohdendorf. The slightly differentiated vibrissa, the fore tarsus chaetotaxy and abdominal colour

paưern provide a unique combination among known species of Miltogramma .

Barcode gap analysis

Analysis of COI sequences with ABGD ( Table 2 ) revealed the interspecific distance between all putative species above the proposed 3% minimum threshold for interspecific gene diversity in DNA barcoding (Hebert et al. 2003). The smallest interspecific distance was observed between M. rognesi sp. nov. and M. vera (5.19%), while the greatest between M. angustissons and M. margiana (22.97%). For other newly described species the distance to the nearest interspecific neighbour was 5.82% between M. mikolajczoki sp. nov. and M. aurissons , 10.22% between M. soszonskii sp. nov. and M. aurissons , 8.05% between M. vervesi sp. nov. and M. brevipila , 9.91% between M. manoucherhii sp. nov. and M. punctata , and 6.92% between M. thompsoni sp. nov. and M. turanica .

D I SC USSI O N

More than 70% of the currently recognized species of Miltogramma were described by B.B. Rohdendorf and Yu.G. Verves, either separately or by these authors together ( Pape 1996). Rohdendorf may be recognized as one of the pioneers in flesh fly systematics by his extensive implementation of the morphology of male terminalia to resolve taxonomy ( Rohdendorf, 1937) and phylogenetic relationships ( Rohdendorf, 1967). Unfortunately, the historical descriptions of new species of Miltogramma suffer from a lack of detail and few or no illustrations. In his early works on Miltogramma, Rohdendorf (1925 , 1926, 1927, 1930, 1934, 1935) ossen omiưed information about male fore tarsal chaetotaxy, which appeared later to be the key character in the taxonomy of the genus( Verves 1979, 1982, 1990, Pape 1987b, Zhang et al. 2021). One benefit from the dominance of Rohdendorf and Verves in the α-taxonomy of Miltogramma has been their consistent use of the same characters for species delimitation and their access to comparative material. This has resulted in high taxonomic accuracy with a low number of subsequent synonymizations ( Pape 1996), but the lack of proper documentation of relevant type material has impeded further progress. Recent reconnaissance surveys in Iran (Kerman and North Khorasan provinces) and Uzbekistan (Bukhara and Samarkanda regions), undertaken in the past decade by K.S. and K.A., have revealed a high number (~30) of potentially new species of Miltogramma , despite thorough taxonomic work focused on this area in the past ( Verves and Khrokalo 2018). Most of these species will have to await detailed revisionary work, including studies of type specimens and application of methods of integrative taxonomy, but the most distinctive are described in the present paper in order to present the wide range of modifications of male foreleg morphology found in the genus Miltogramma . Secondary sexual dimorphism in foreleg morphology is present also in some other groups of schizophoran flies, like Sepsidae ( Puniamoorthy et al. 2008) , Muscidae (Grzywacz et al. 2017) , Calliphoridae ( Jones et al. 2014) , and Drosophilidae ( Kopp and Barmina 2022), where the modifications are related to chemoreception of pheromones ( Kopp and Barmina 2022) or to clasping females during mating ( Puniamoorthy et al. 2008). In Miltogramminae , including species of Miltogramma , modifications usually involve only chaetotaxy and length of tarsomeres of the fore tarsus ( Verves 1990, Pape 1996, Povolný and Verves 1997) or, more rarely, the loss of a single tarsal claw ( Johnston et al. 2020b, c). This form of sexual dimorphism appears in all main lineages of the subfamily ( Verves 1989, Buenaventura et al. 2020) and seems to be related to different types of courtship behaviour ( Spofford and Kurczewski 1985), although this topic has remained practically unstudied. Even small details in the length and position of the modified setae on the particular tarsomeres may be species-specific, as confirmed by the application of barcoding on M. rognesi sp. nov. and M. vera . In contrast to species with extreme elongation of numerous tarsal setae, we describe also M. thompsoni sp. nov. with unmodified male fore tarsal chaetotaxy. This is the first species showing a lack of secondary sexual dimorphism among a large set of species grouped by Rohdendorf (1935) and Verves (1990) in the subgenus Miltogrammidium . The lack in M. thompsoni sp. nov. of the structures thought to be crucial for courtship opens the question of what other mechanisms of sexual selection are at work in this group and, in particular, as the morphology of male terminalia of M. thompsoni sp. nov. remain without any specific modification and are similar to the terminalia of other species of Miltogrammidium ( Rohdendorf 1935, Verves 1990, Povolný and Verves 1997). Similar paưerns of male foreleg chaetotaxy may occur in different lineages of Miltogramma ( Rohdendorf 1930, 1935, Verves 1979, 1984, 1990, Povolný and Verves 1997). A good example is the modification of setae on the ventral surface of the fourth tarsomere in the subgenera Dichiracantha and Rohdendorfiella ( Rohdendorf 1930, Verves 1979). Miltogramma mikolajczoki sp. nov. has elongated setae on the anterior surface of the fissh tarsomere, which resembles the condition in the Afrotropical species M. maculigera Speiser and M. hargreavesi Pape , and the Asiatic M. rohdendorfi Tscharykuliev. However , without a comprehensive phylogenetic hypothesis for species of the genus Miltogramma ( Piwczyński et al. 2017, Buenaventura et al. 2020), it is premature to decide about relative character polarity or cases of convergence for these tarsal modifications.

The pioneering contribution to taxonomy and phylogeny of Miltogramma by Rohdendorf and Verves needs to be revised following modern standards of integrative taxonomy along the lines of the recent revision of Australian species of Protomiltogramma Townsend , where a combination of morphological and molecular data led to the removal of two nominal species through synonymy and the addition of another eight new species ( Johnston et al. 2021). Achieving a comprehensive revision of Palaearctic Miltogramma would require substantial additional material from the Middle East and Central Asia. The politically fraught conditions in many of the countries of this area pose obvious difficulties for this task. We hope to successfully overcome all obstacles and accelerate the work by involving local researchers and their students.

SUPPLEMENTARY DATA

Supplementary data are available at Zoological Journal of the Linnean Societo online.

Figures

Figure 1. Male fore tarsus of Miltogramma spp. A, M.vervesi sp. nov., right tarsus, tarsomeres 2–5, anterior view. B, M.mikolajczyki sp. nov., right tarsus, tarsomeres 4 and 5, dorsal view.C, M.manouchehrii sp. nov., less tarsus, tarsomeres 4 and 5, dorsal view.D, M.soszynskii sp.nov., right tarsus, tarsomeres 1–5, anterior lateral view.E, M. rognesi sp. nov., right tarsus, tarsomeres 1–5, anterior lateral view.

Figure 3. Male fore tarsus of Miltogramma spp.A, M.vervesi sp. nov., right tarsus, anterior lateral view. B, M.mikolajczyki sp. nov., right tarsus, dorsal view. C, M. soszynskii sp. nov., right tarsus, anterior lateral view. D, M.thompsoni sp. nov., right tarsus, anterior lateral view. E, M.rognesi sp.nov., right tarsus, anterior lateral view.F, M.vera, right tarsus, anterior lateral view. G, M. manouchehrii sp. nov., right tarsus, dorsal view. Scale bars:0.2 mm.

Figure 4. Neighbour-joining phylogenetic tree based on COI gene sequences of Miltogramma species.Numbers at branch nodes represent bootstrap support values as a percentage of 1000 replicates. The scale bar, measured in 0.2 substitutions per nucleotide position, indicates the genetic distance between the species. The asterisk (*) in Miltogramma efflatouni indicates a specimen that was misidentified as Miltogramma nuda in Kuưy et al. (2010).

Figure 9. Miltogramma manouchehrii sp. nov. (male paratype:Iran, North Khorasan, Sarcheshmeh, 16 May 2014, 37.6333 57.4070, leg. KEiB Iran Expedition, NHMD: male genital apparatus: paratype Iran, Kerman, Sirch road, 8 May 2017, 30.1949 57.4614, leg.KEiB Iran Expedition IV, NHMD). A, habitus, lateral view.B, habitus, dorsal view.C, abdomen, dorsal view.D, head, lateral view.E, head, frontal view. F, head, dorsal view. G, right fore tarsus, anterior lateral view.H, right fore tarsus, dorsal view. I, epandrial complex, dorsal view.J, epandrial complex, lateral, view. K, phallus, pre- and postgonites, ejaculatory sclerite, hypandrium.