Dong Ren

Science 1998; 280: 85-88.

Science 1998; 280: 85-88.

Pollinating insects played a decisive role in the origin and early evolution of the angiosperms. Pollinating orthorrhaphous Brachycera fossils (short-horned flies) collected from Late Jurassic rocks in Liaoning Province of northeast China provide evidence for a pre-Cretaceous origin of angiosperms. Functional morphology and comparison with modern confamilial taxa show that the orthorrhaphous Brachycera were some of the most ancient pollinators. These data thus imply that angiosperms originated during the Late Jurassic and were represented by at least two floral types.

National Geological Museum of China, Xisi, Beijing 100034, China.

The ancestors and time of appearance of angiosperms remain obscure (1-5). The earliest fossil evidence of nectar secretory tissue is provided by the Santonian-Campanian flowers from Sweden (6). The oldest angiosperm pollen grains have been found in Israel, in strata of Early Cretaceous time (Late Valanginian to Early Hauterivian) (7). The earliest recognized angiosperm inflorescences have been recovered from rocks of Late Hauterivian Age at Jixi, China (8).

The origin and early evolution of flowering plants are probably related to the coevolution of insect pollinators (9-11). Cretaceous and Tertiary flower-visiting insects were diverse and include an impressive variety of Coleoptera (beetles), Diptera (true flies), Lepidoptera (moths), Hymenoptera (wasps and bees), and other less diverse taxa, such as Thysanoptera (thrips). Some highly faithful pollinators such as butterflies and cyclorraphan flies appeared in the middle Tertiary (12). Few pre-Cretaceous pollinating insects are known. Small insects, especially flies and parasitoid wasps, may have been important then and thus in the origin and evolution of angiosperm pollination (13). Here I describe Late Jurassic pollinating orthorrhaphous Brachycera with well-preserved nectaring mouthparts.

Early pollinating insects have long tubular mouthparts designed for feeding on or extracting nectar from long tubular flowers (9-11). Other examples of Jurassic insects having this type of mouthpart include nemonychid weevils, which probably fed on bennettitaleans or cycads (14), and a monotrysian Lepidopteran with a siphonate proboscis (15, 16).

I collected the fossil Brachycera at a locality near Beipiao City, Liaoning Province, China, from nonmarine sedimentary rocks of the Yixian Formation (17). These rocks contain abdundant remains of insects (18, 19), fishes, conchostracans, reptiles, birds, and mammals of Late Jurassic (approximately Tithonian) age (20).

Extant Brachycera comprise a wide variety of flower visitors (9, 10). Most orthorrhaphous Brachycera feed on flowers as adults. The new fossil orthorrhaphous Brachycera (19) include deer flies (Pangoniinae of Tabanidae), flower-loving flies (Apioceridae), and tangleveined flies (Nemestrinidae).

Most extant pangoniines are exclusively flower feeders (21). They often hover over flowers on the borders of dense vegetation (9, 10). Both males and females subsist on nectar and on the juice of flowers. The female proboscis of some species is flexible and suitable only for imbibation of nectar (22, 23), and is three or four times the length of the body. One of the Jurassic fossils, described as Palaepangonius eupterus Ren, 1998, includes a complete body and an associated well-developed long proboscis (Fig. 1) (19). These fossils provide direct evidence for the mid-Mesozoic diversification within Tabanidae of subclades with nectaring mouthparts. Palaepangonius not only provides evidence for the extraction of nectar from flowers or flowerlike structures but also demostrates that the Pangoniinae have existed since the Late Jurassic. Another brachyceran clade, the Nemestrinidae, are important pollinators of flowers (9, 10). Modern members are often collected when feeding on blossoms or hovering over them while imbibing nectar (24). Many Late Juriassic examples were collected and were described as Protonemestrius jurassicus Ren, 1998. These had a proboscis about 5.2 mm long, which would have been especially suitable for visiting long tubular flowers (Fig. 2). Florinemestrius pulcherrimus was also an important flower visitor. Its long stout proboscis seems to have been suited to extracting nectar from open or short tubular flowers (Fig. 3). Similar proboscides have been reported from the Late Jurassic of Karatau, Kazakhstan (25).

  
Fig. 1. Palaepangonius eupterus Ren, 1998. (A) Camera lucida drawing of specimen LB97017. (B) Photograph of body, LB97017. (C) Photograph of proboscis, LB97017. Abbreviations: e, compound eye; Pr, proboscis

 
Fig. 2. Protonemestrius jurassicus Ren, 1998. (A) Camera lucida drawing of specimen LB97005. (B) Photograph, LB97005. (C) Photograph of proboscis, LB97005.

 
Fig. 3. Florinemestrius pulcherrimus Ren, 1998. (A) Camera lucida drawing of specimen LB97009. (B) Photograph, LB97009. (C) Photograph of proboscis, LB97009. Abbreviations: a, antenna; pal, palpus.

A representative of the stem group of the Apioceridae has also been found (Fig. 4) and called Protapiocera megista Ren, 1998. Its body bears dense hairs, a feature used in confamilial modern taxa for collecting pollen. Extant members are attracted to flowers (9, 10) and feed on pollen and nectar. These attributes support the conclusion that this fossil short-horned fly was also a pollinator (Fig. 4).

 
Fig. 4. Protapiocera megista Ren, 1998. (A) Camera lucida drawing of specimen LB97001. (B) Photograph, LB97002 (counterpart of LB97001).

Structural features such as long fluid-imbibing mouthparts and densely and appropriately positioned hairs on the body surface imply that the behavior of some Late Jurassic brachyceran flies was related to flower visiting and pollination. Insects with nectaring mouthparts would have been adapted to consume nectar from flowers, extrafloral nectaries, or flowerlike structures such as those documented from contemporaneous and fossil anthophytes. Such structures today are associated with cross-pollination (6).

Apart from the three fossil taxa mentioned above, many other short-horned flies, particularly the Stratiomyidae, Athericidae, Vermileonidae, Mydidae, Acroceridae, Mythicomyiidae, Bombyliidae, Empididae, and Dolichopodidae, are known to feed on modern flowers (9, 10, 26). Species from these taxa are primarily adapted to consume pollen and nectar and have an effective role in pollination. This interaction is particularly important because the fossil records of these flies also extend to the Late Jurassic and early Cretaceous (27, 28) (Fig. 5).

Fig. 5. Stratigraphic distribution of flower-associated orthorrhaphous Brachycera. Solid ellipses indicate the fossils of this study. Abbreviations: J, Jurassic; K, Cretaceous; N, Neogene; P, Paleogene; Q, Quaternary.

These paleoentomological records indicate that the oldest known anthophilous orthorrhaphous Brachycera existed during the Middle to Late Jurassic. During the Late Jurassic, the orthorrhaphous Brachycera underwent an explosive radiation (29, 30). Hitherto, about 46 genera and 58 species within 18 families have been reported (19, 27, 31, 32) (Table 1). Most of these fossils have been recovered from Late Jurassic rocks of Eurasia, principally from northeast China, Karatau, Baissa, and Siberia.

Table 1. Geographical distribution of Middle and Late Jurassic main orthorrhaphous Brachycera. Solid circles indicate locations where fossils were found. Family Genus (n) Species (n) Liaoning Shandong Siberia Karatau Solnhofen Protobrachycerontidae 1 1 + Archisargidae 2 5 + Kovalevisargidae 2 2 + Palaeostratiomyiidae 1 1 + Eomyiidae 1 1 + Xylomyidae 1 1 + Eostratiomyiidae 1 1 + Rhagionidae 16 16 + + + + Tabanidae 3 3 + Acroceridae 1 1 + Nemestrinidae 6 11 + + + + Bombyliidae 1 1 + Vermileonidae 1 1 + Eremochaetidae 4 5 + + Protempididae 2 4 + + Protomphralidae 1 1 + Protapioceridae 1 2 + Mythicomyiidae 1 1 +

Although anthophytes (including Bennettitales, Gnetales, and angiosperms) also have flowerlike reproductive structures, the flower is one of the defining characteristics of angiosperms. Insects probably visited the flowers of primitive angiosperms mainly because of their pollen and nectar (1, 10). I conclude that the presence of nectar-collecting Brachycera during the Late Jurassic provides direct evidence of the occurrence of nectariferous angiosperms during this time interval. This conclusion is supported by a tricarpous female angiosperm reproductive fossil (33) recently collected from the same bed that contains the Brachycera fossils. It is also possible that these pollinating short-horned flies were pollinators of nonangiospermous anthophytes. Comparative morphology of the mouthparts suggests that at least two types of general morphotypes of nectar-feeding proboscides of orthorrhaphous Brachycera existed during the Late Jurassic. One was a stout proboscis, typical of Palaepangoninius euptera and Florinemestrius pulcherrimus, suitable for feeding on open and short tubular structures that contained fluid. Another was a slender proboscis that was suited to extracting nectar from long tubular structures. In view of the presence of early (primitive) pollen feeders or pollinators with mandibulate mouthparts (14), the orthorrhaphous Brachycera pollinators with nectar-imbibing mouthparts seem to have been considerably advanced by the Late Jurassic. They were sufficiently diverse by the Late Jurassic that an earlier origin of angiosperms seems possible.

These fossils thus imply that either angiosperms originated during the Middle Jurassic and flourished in the Late Jurassic or, which is less likely, that other clades of anthophytes were responsible for the pollination syndromes exhibited by these orthorrhaphous Diptera. This possibility also can be supported by the final phase of mouthpart class expansion that occurred during the Late Jurassic and perhaps as early as the early Middle Jurassic, in which surface-fluid-feeding mouthpart classes evolved; these became important during the subsequent ecological expansion of angiosperms (12). The origin and diversification of the orthorrhaphous Brachycera during the Jurassic may offer support for either the hypothesis of a Middle Jurassic origin of angiosperms (preferred) or the existence of anthophyte seed plants with reproductive biologies that required pollinating insects, similar to those documented for extant cycads and gnetaleans (less likely). The paleogeographical distribution of anthophilous orthorrhaphous Brachycera fossils from the Late Jurassic (Table 1) and other fossil insects, such as scorpionflies of the family Bittacidae (20), indicate that central Asia (China and Siberia) split from Neopangea (Pangea without China and Siberia) not earlier than the Middle Jurassic (34). If angiosperms are monophyletic, they should have originated no later than the Middle Jurassic; otherwise, their ancestors could not have dispersed to the other continents. These paleogeographical patterns, together with the observation that most extant primitive angiosperms occur in the southwestern Pacific (5), imply that the earliest angiosperms originated in eastern Laurasia.

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28 October 1997; accepted 13 February 1998