Biogeographical implications of a molecular phylogeny of ...

Mitt. Dtsch. Ges. allG. anGew. ent. 18halle (saale) 2012

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Biogeographical implications of a molecular phylogeny of the Raphidiidae (Raphidioptera)

Ulrike Aspöck 1,2, Elisabeth Haring 1,2 & Horst Aspöck 3

1 Natural History Museum Vienna; 2 Department of Evolutionary Biology, University of Vienna

3 Institute of Specific Prophylaxis and Tropical Medicine, Medical Parasitology, Medical University of Vienna

Abstract: Biogeographische Implikationen einer molekularen Phylogenie der Raphidiidae (Raphidioptera) Der jüngsten molekulargenetischen Analyse der Raphidiidae entsprangen sechs Kladen: (1) das nearktische Genus Agulla navás, 1914, als Schwestergruppe zum Rest, (2) das neark-tisch/zentralamerikanische Genus Alena navás, 1916, als Schwestergruppe zur großen Klade aller paläarktischen Raphidiidae, die (3) das zentral- und ostasiatische Genus Mongoloraphidia U. aspöck & h. aspöck, 1968, (4) die westpaläarktische Phaeostigma-Klade, (5) die west-paläarktische Puncha-Klade und (6) die westmediterrane Ohmella-Klade umfasst.Die rezenten Raphidiidae sind auf arboreale Teile der Holarktis (einschließlich südlicher Trans-gressionszonen) beschränkt, aber sie fehlen im Norden und Osten von Nordamerika. Rezente Raphidioptera brauchen eine kühle Periode – einen Kältereiz (Winter) – für eine erfolgreiche Entwicklung. Die üppige mesozoische Raphidiopteren-Fauna ist auch aus tropischem Ambiente nachgewiesen. Diese Fauna starb zum Ende der Kreide – vermutlich wegen klimatischer Ver-änderungen im Gefolge des K/T Impakts – aus. Offensichtlich überlebten nur jene (nördlichen) mesozoischen Linien den Impakt, die bereits kälteadaptiert waren. Die für das Verständnis der Verbreitung der rezenten Raphidiidae vordringlichen Fragen lauten: Welche Isolationsmechanis-men führten zur Entstehung der beiden amerikanischen Kladen, der asiatischen Mongoloraphidia-Klade und der drei westpaläarktischen Kladen?Gegenwärtig erscheint als plausibelste Hypothese die Annahme einer im Norden lebenden (end-kreidezeitlichen) Stammart, von der sich – vermutlich vor dem K/T Impakt – die Stammarten von Agulla und Alena jeweils unabhängig abspalteten und durch Ausbreitung oder Arealverschie-bungen durch Kontinentaldrift nearktisch wurden. Das heutige Fehlen von Kamelhalsfliegen im Norden Nordamerikas beruht vermutlich schlicht auf der geringen Expansivität dieser Insekten. Das große Epikontinental-Meer (105 – 60 MJ), das Nordamerika bis zum Ende der Kreide teilte, könnte Ursache für das heutige Fehlen von Raphidiopteren im Osten von Nordamerika sein. Die Turgaj-Senke (160 – 30 MJ), ein Epikontinental-Meer, das die Ostpaläarktis lange isolierte, könnte die Entstehung von Mongoloraphidia ausgelöst haben. Die Westpaläarktis war keineswegs ein geschlossener Kontinent, sondern – in ihren südlichen Bereichen – ein Archipel, dessen Inseln die Isolationsfaktoren zur Entstehung der Puncha- und der Phaeostigma-Klade lieferten. Die Iberische Halbinsel repräsentiert eine alte isolierte Landmasse – ein plausibler Faktor für die Entstehung der Ohmella-Klade.

Key Words: Raphidioptera, Raphidiidae, distribution, biogeography, K/T impact, epicontinental seas, European archipelago, Holarctic arboreal, Agulla, Alena, Mongoloraphidia, Palaearctic clades

Mitt. Dtsch. Ges. allG. anGew. ent. 18 halle (saale) 2012

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Ulrike Aspöck, Natural History Museum Vienna, Burgring 7, 1010 Wien, Austria, E-Mail: [email protected];Department of Evolutionary Biology, University of Vienna, Althanstraße 14, 1090 Vienna, Austria, E-Mail: [email protected]

Elisabeth Haring, Natural History Museum Vienna, Burgring 7, 1010 Vienna, E-Mail: [email protected], Department of Evolutionary Biology, University of Vienna, Althanstraße 14, 1090 Vienna, Austria, E-Mail: [email protected]

Horst Aspöck, Institute of Specific Prophylaxis and Tropical Medicine, Medical Parasitology, Medical University of Vienna, Kinderspitalgasse 15, 1095 Vienna, Austria,E-Mail: [email protected]

Point of departure and basic facts The family Raphidiidae (Fig. 1) comprising about 200 known species together with 31 described species of the family Inocelliidae constitutes the order Raphidioptera, which, associated with Megaloptera + Neuroptera, represent the triple superorder Neuropterida. In several aspects, e.g. the pharate adult and the primitive male genital sclerites, they contribute essentially to our understanding of Endopterygota (kristensen 1999).

Extant Raphidiidae, just as the whole order Raphidioptera, are restricted to arboreal parts of the Holarctic (including transgression zones) (h. aspöck & al. 1991, h. aspöck 1998), but do not occur in the northern and eastern parts of North America (Fig. 2). Fossil Raphidioptera, however, are known also from South America and eastern parts of North America (enGel 2002, Jepson & al. 2008).

To understand the distribution patterns of present-day Raphidioptera it is essential to know that extant Raphidioptera need a cool period (winter) for proper development. It is additionally important to bear in mind that the rich Mesozoic snakefly fauna is also known from a tropical ambience. This fauna died out at the end of the Cretaceous, probably due to the climatic consequences of the K/T impact (h. aspöck 1998). Apparently only those lines of the Mesozoic snakefly fauna that were already adapted to cold climates survived. It is worth mentioning that all fossil Raphidioptera from the Tertiary belong to the two extant families and are known from regions where Raphidioptera occur today.

A most recent molecular phylogeny of the family Raphidiidae (harinG & al. 2011) included representatives of 21 of the 26 genera and used sequences from the nuclear gene for the large subunit ribosomal RNA (28S rRNA) and the mitochondrial cytochrome c oxidase subunit 3 gene (cox3). This analysis ended in a big surprise: Six geographically assigned clades (Figs. 3, 4) emerged in the trees within the raphidiid family. However, not the eccentric Nearctic genus Alena (eccentric with respect to the bizarre male genital sclerites) appeared as sister group to the rest – as hitherto assumed (h. aspöck & al. 1991)

– instead the inconspicuous (inconspicuous with respect to male genital sclerites) Nearctic genus Agulla (lineage 1; Fig. 3) assumed this possition. The Nearctic Alena (2) turned up as the sister group of the huge Palaearctic clade comprising the central and eastern Asian genus Mongoloraphidia (3), which is the sister group to a clade containing the mainly western Palaearctic Phaeostigma clade (4), the mainly western Palaearctic Puncha clade (5), and the western Mediterranean Ohmella clade (6).

All 26 extant raphidiid genera are listed below. Genera which were not included in the molecular analysis (harinG & al. 2011) due to lack of appropriate material are marked with an asterisk *. On the basis of the morphology of the male genital sclerites, Iranoraphidia and Tauroraphidia can be clearly assigned to the Phaeostigma clade and Africoraphidia to the Ohmella clade. The systematic position of Tadshikoraphida (occurring in Central Asia) and Mauroraphidia (Morocco) remains unknown.


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Genera of the family Raphidiidae latreille, 1810Alena navás, 1916Africoraphidia* U. aspöck & h. aspöck, 1969Agulla navás, 1914 Atlantoraphidia h. aspöck & U. aspöck, 1968Calabroraphidia raUsch, h. aspöck & U. aspöck, 2004Dichrostigma navás, 1909Harraphidia steinMann, 1963Hispanoraphidia h. aspöck & U. aspöck, 1968Iranoraphidia* H. aspöck & U. aspöck, 1975Italoraphidia H. aspöck & U. aspöck, 1968 Mauroraphidia* H. aspöck , U. aspöck & raUsch, 1983Mongoloraphidia H. aspöck & U. aspöck, 1968Ohmella H. aspöck & U. aspöck, 1968Ornatoraphidia H. aspöck & U. aspöck, 1968Parvoraphidia H. aspöck & U. aspöck, 1968Phaeostigma navás, 1909Puncha navás, 1915Raphidia linnaeUs, 1758Subilla navás, 1916Tadshikoraphidia* H. aspöck & U. aspöck, 1968Tauroraphidia* H. aspöck , U. aspöck & raUsch, 1982Tjederiraphidia H. aspöck, U. aspöck & raUsch, 1985Turcoraphidia H. aspöck & U. aspöck, 1968Ulrike H. aspöck, 1968 Venustoraphidia H. aspöck & U. aspöck, 1968Xanthostigma navás, 1909

Questions surrounding the distribution patternsThe distribution areas of the clades obtained in the molecular analysis raise three essential questions:

1) Which processes can be evoked to explain the basal split of the two Nearctic clades? 2) Which biogeographic scenario could explain the origin of Mongoloraphidia?3) Which phenomena (vicariance/dispersal) induced the western Palaearctic clades?

1) In an earlier approach based on the hypothesis of a sister group relationship of the Nearctic Agulla with the western Mediterranean Ohmella and a sister group relationship of the Nearctic Alena with western Mediterranean Hispanoraphidia and Harraphidia (U. aspöck & h. aspöck 2007) the idea of two independent colonisations of North America previous to the formation of the Atlantic (about 100 My) via northern Africa and South America was discussed. Among the alternative routes, either via Laurasia or via Eastern Asia, the latter one appears more plausible as snakeflies are restricted to the western parts of North America. Considering this distribution gap, a colonisation of western North America via East Asia would be more likely. The dispersal of selected dinosaurs (skelton 2006) could serve as a pattern for analogous routes of Raphidioptera (Fig. 5). It is unnecessary to say that a migration of the stem species of Agulla and Alena via Beringia during the Pleistocene would have been much too late for the evolution of these groups. In the light of the results of the molecular analysis, however, any scenario involving colonisation of the Nearctic would require two independent dispersal events and therefore is not the most parsimonious interpretation.

An alternative and presently preferred hypothesis assumes the existence of a stem species with an extensive northern, possibly circumpolar distribution (Fig. 6). The two basal splits in the tree (Fig. 3) led to the stem species of Agulla (lineage 1), Alena (2), and the Palearctic taxa (the clade combining 3–6), whereby the Nearctic and Palearctic lineages were separated in the course of the continental drift.


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An epicontinental sea crossing North America from about 105 My up to 60 My (skelton 2006, sMith & al. 1995) (Fig. 5) represented an initial effective barrier which would have served as a plausible explanation for the lack of Raphidioptera in eastern North America (although it cannot be ruled out that this absence might be a consequence of the K/T impact). The general lack of Raphidioptera in the northern parts of North America (north of its current distribution) may simply be due to the low expansion capacity of these insects.

Fig. 1a: Raphidia ariadne H.A. & U.A, male (Crete, Christos).Length of forewing: 8.1 mm.

(Orig., H. Bruckner phot.)

Fig. 1b: Phaeostigma (Superboraphidia) rauschi H.A. & U.A, female (Greece, Simos).Length of forewing: 12.2 mm.

(Orig., H. Bruckner phot.).

Fig. 2: World distribution of the family Raphidiidae


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The molecular analysis signalized a quick differentiation of the Palaearctic clade after the split of the Agulla and Alena lineages, but we still lack a reliable calibration to estimate substitution rates.

2) The origin and isolation of the central and eastern Asian Mongoloraphidia clade (lineage 3, Fig. 3) can be ascribed to an enormous vicariance phenomenon: the epicontinental Turgaj sea, which persisted approximately from 160 to 30 My and dried up as recently as in the Oligocene (Brown & loMolino 1998, skelton 2006, sMith & al. 1995). According to our hypothesis this barrier led to the separation of Mongoloraphidia from the remaining Palearctic lineage. Mongoloraphidia comprises 63 extremely heterogeneous species, partly belonging to species groups on the subgeneric level. Evolutionary subcentres are not yet understood and probably overlap with more recent Pleistocene refugial centres, which themselves are still cryptic. Nevertheless, the high genetic distances among species of the genus Mongoloraphidia imply that they originated much earlier.

Fig. 3: Phylogenetic tree of the Raphidiidae based on a molecular analysis (after harinG & al. 2011). Six geographically assigned clades represent either genera or groups of genera, namely: The Nearctic genus Agulla, the Nearctic/Central American genus Alena, the Central Asiatic and Eastern Palaearctic genus Mongoloraphidia, the Palaearctic Phaeostigma clade (comprising 11 genera, including Iranoraphidia* and Tauroraphidia*, see list on page 577), the Palaearctic Puncha clade (comprising 5 genera) and the western Mediterranean Ohmella clade (comprising 5 genera, including Africoraphidia*, see list on page 577).


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3) The western Palaearctic clades (4–6, Fig. 3) represent bewildering complexes, but their origins can be explained by a conjoint causation: The archipelago character of Europe, which persisted over considerable amounts of time comprising Mesozoic and Tertiary periods (sMith & al. 1995, popov & al. 2005). The mosaic of islands is a reasonable background for isolation phenomena causing the divergence of the widely distributed Phaeostigma and Puncha clades on one hand, and the western Mediterranean Ohmella clade on the other, as well as for diversifications within these clades and the resulting distribution areas. Surprisingly, the Phaeostigma and the Puncha clades have superficially similar patterns, nevertheless, the origins of the genera constituting them are still not yet understood.

The Phaeostigma clade has a predominately western Palaearctic distribution, however, one species, Raphidia ophiopsis linnaeUs, 1758, is an outlier ranging far into the east (Fig. 4). This outlier most probably represents a young Pleistocene expansion and is not relevant for the present discussion of early diversifications. The clade comprises 11 genera (genera not included in the molecular study can be ascribed to the clade on the basis of the morphology of the male genital sclerites and are marked with an asterisk *): Phaeostigma, Subilla, Dichrostigma, Turcoraphidia, Iranoraphidia *, Tauroraphidia *, Ornatoraphidia, Raphidia, and three enigmatic endemic taxa, Tjederiraphidia, at the southern tip of Italy, Parvoraphidia on the Balkan peninsula, and Ulrike with a disjunct distribution in Greece and the eastern Mediterranean region. A specific centre of diversification of the clade within the mosaic of islands constituting the European Archipelago cannot be identified with certainty. However, considering the fact that most of the extant species occur on the Balkan Peninsula, the geological precursors of this region – or more generally the eastern Mediterranean region – might have represented the centre of diversification of this group.

The Puncha clade (5) equally is predominately distributed in the western Palaearctic, again there is one species, Xanthostigma xanthostigma (schUMMel, 1832) representing a young outlier with a distribution range extended far to the east. The clade comprises five genera, Puncha, Xanthostigma, Venustoraphidia and the enigmatic genera Italoraphidia and Calabroraphidia (H. aspöck & U. aspöck 2007). Both are monotypic genera and endemic to the southern Apennine Peninsula. Again we ask (but are not yet able to answer), which territory of the mosaic of islands could have harboured the stem species of the clade. At least the endemic genera Tjederiraphidia (Phaeostigma clade), Italoraphidia and Calabroraphidia (Puncha clade) suggest an origin on an old core area in the Apennines.

The Ohmella clade (6) comprises five genera, Ohmella, Harraphidia, Hispanoraphidia, Atlantoraphidia and Africoraphidia *. The distribution ranges of the taxa constituting this clade circumscribe a geographically compact region in the western Mediterranean with a centre on the Iberian Peninsula. The origin as well as the diversification of the Ohmella clade on this old and formerly isolated land mass is a plausible hypothesis. For Harraphidia, which is known from the Iberian Peninsula and from northern Africa, the expansion from Europe to northern Africa seems more parsimonious than the converse pathway. Also for the exclusively African genus Africoraphidia *, which clearly can be assigned to the Ohmella clade based on morphological characters, dispersal from Europe to the African continent can be assumed. This assumption cannot be brought forward to the enigmatic Mauroraphidia * from Morocco, because this is an isolated genus which cannot be associated with any other taxon (see introduction).

The Raphidiidae are a group of insects characterized by high diversity of rather old lineages with a partially patchy distribution. An early diversification prior to the K/T impact is suggested by the predominantly isolated taxa, whose sister groups already died out long ago. To summarize our hypotheses, the main factors responsible for the present day patterns are (1) two epicontinental seas acting as long lasting global barriers, (2) a mosaic of isolated islands in the south-western Palaearctic facilitating divergence of many distinct lineages, and (3) the low expansion capacity of most species of Raphidiidae enforcing these diversification processes.

AcknowledgementsOur cordial thanks are due to Harald Bruckner for graphical assistance, to Wilhelm Pinsker for critically reading the manuscript, and to John Plant for linguistic improvement.


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Fig. 5: Schematic graph of the late Cretaceous territories (about 65 My), and of the epicontinental seas dividing North America on one hand and Europe and Asia on the other. Arrows indicating dispersal routes of selected dinosaurs (after skelton 2006). Possible analogous routes of the Raphidiidae from Eastern Asia to western North America are symbolised by a snakefly facing the corresponding direction.

Fig. 4: Distribution patterns of the clades obtained in the molecular analysis of the Raphidiidae (after harinG & al. 2011).

Fig. 6: Schematic graph of the northern hemisphere about 65 My (modified after schettino & scotese 2001) symbolising the stem species of present day Raphidiidae (fully black) and the stem species of the 6 clades (netted wings) discussed in the text: (1) Agulla, (2) Alena, (3) Mongoloraphidia, (4) Phaeostigma clade, (5) Puncha clade, and (6) Ohmella clade.


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