Enhanced: How Old Is the Flower and the Fly?

Conrad C. Labandeira

Science 1998; 280: 57-59.

The first book that Charles Darwin wrote after publication of The Origin of Species (1859) was On the Various Contrivances by Which British and Foreign Orchids Are Fertilised by Insects, and on the Good Effects of Intercrossing (1862) [HN1], an intellectual forerunner to modern work on pollination biology. In this volume, Darwin applied a tradition of careful observation with principles such as reciprocal adaptation toward understanding pollination--one of the most pervasive and diverse of mutualisms known in nature. Orchids [HN2], although fascinating in their own right and the premiere group of plants renowned for their intimate and intricate coevolutionary associations with pollinating insects (1) [HN3], nevertheless represent a relatively recent (Cenozoic) event in the geologic history [HN4] of pollination. Recently, Friis (2) and others have produced anatomical evidence from spectacularly preserved floral structures and have elucidated the first occurrences of pollinator-associated floral features during the mid-Cretaceous. These angiosperm-[HN5]centered discoveries have pinpointed some of the earliest known fossil occurrences of particular pollination syndromes. [Pollination syndromes are morphologically convergent adaptive trends exhibited by both the floral features of pollinated plants and the mouthpart structure [HN6] and other flower-interactive features of their respective pollinators (1).] Nevertheless, the earlier Mesozoic history of insect pollination is considerably more ambiguous. At present, there are few clues regarding the pollination biology of "preangiospermous" Mesozoic insects. Most inferences come from modern associations between primitive lineages of insects and their gymnospermous [HN7] seed plant hosts, especially cycads (3), and from fossil gut contents and coprolites of pollen-consuming insects (4). Diagnostic mouthpart structures (4, 5) are rarely observed, which is now remedied by the discoveries reported by Ren on page 85 of this issue (6). This impressive documentation now places three lineages of lower brachyceran flies [HN8] [see figure, panel (B)] as pollinators in China during the Upper Jurassic. However, as explored below, the group of plants that these external fluid feeders were pollinating is as intriguing as the presence of the pollination itself.

Pollen consumption (pollinivory) has generally been the evolutionary precursor to pollination [HN9]. Pollinivory can become a mutualism (that is, pollination) if the pollinivore can deliver unconsumed pollen to the female reproductive organs of its host plant more efficiently than alternative dispersal by wind, splashing rain, or gravity. Pollination mutualisms require a plant to sacrifice pollen for improved access and efficiency in the fertilization of conspecific ovules. Even pollinivory is a derived feeding strategy, because it is temporally preceded by spore consumption (sporivory) in the fossil record. The earliest terrestrial sporivory occurs in Late Silurian to Early Devonian terrestrial ecosystems, indicated by distinctive coprolites, produced probably by myriapods [HN10] or insects, with abundant to occasional spore contents from primitive land plants (7) [see assemblage 1 in panel (A) of the figure]. During the Carboniferous, a younger assemblage has been documented [assemblage 2 in panel (A) of figure], represented by insects. By the end of the period, pollen consumption was established, evidenced both by well-preserved, dispersed coprolites [panels (D) and (E) of figure] and gut contents of hemipteroid and orthopteroid insects (8) [HN11] [panels (F) and (G) of figure]. Coeval pollination mutualisms have been inferred from the reproductive biology of certain seed ferns, such as anomalously large pollen grains, investitures of secretory glands adjacent to reproductive structures, and the presence of pollination drop mechanisms for attracting pollen and potentially insects (4). Curiously, elongate mouthparts are known from the Permian (4, 8, 9), probably representing feeding on surface fluids. The lineages displaying these mutualisms undoubtedly were extinguished during the late Permian; substantial evidence for pollinivory and pollination does not reappear until the Jurassic.

Evolving together. The fossil history of associations between insects and reproductive structures of vascular plants. (A) The four distinctive assemblages of fossils (see text for description) representing consumption of spores, pollen, or nectar, based on a variety of evidence, such as the examples at right. The presence and intensity of background shading indicate the probable duration and pervasiveness of pollination. Dots in Late Jurassic denote suites of insects (5, 6) that could be assigned to either assemblages 3 or 4 or both. (B) (Top) Cladogram of major subgroups of the lower Brachycera [after (16)], showing three fly lineages inferred by Ren (6) to have been Late Jurassic angiosperm pollinators. (Bottom) The head and proboscis of an extant Australian member of the Tabanomorpha (17). (C) Ellipsoidal spore-bearing coprolites from Late Silurian (left) and Early Devonian (right) floras (7). The left specimen consists of plant cuticle with occasional spores; the right specimen comprises mostly spores. (D) Late Carboniferous insect coprolite from the Illinois Basin, USA, consisting of pollen from a cordaitalean gymnosperm, enlarged in (E). (F) A Lower Permian hypeperlid insect from Russia, with rectal contents illustrated in (G), containing pollen grains from glossopterid and conifer gymnosperms (8). (H) The snout weevil Rhopalotria mollis, pollinivore and pollinator of the extant cycad Zamia furfuracea (3).

F. Marsh/Smithsonian Institution; (C) Nature 377, 329 (1995); (F, G) Lethaia 29, 369 (1997); (H) Organization for Tropical Studies

Three diverse lines of evidence currently indicate that basal lineages of modern insect pollinators originated during the Jurassic, probably as generalists on seed plants [assemblage 3 in panel (A) of figure] (4, 8). First, although recently viewed as exclusively wind-pollinated, modern cycads [HN12] are now considered overwhelmingly insect-pollinated (3). Studies now demonstrate beetle pollinivory in 7 of the 10 extant genera of modern cycads, and apparently faithful pollination occurs in those species that have been extensively investigated. These cycad-inhabiting beetle lineages are extant representatives of basal lineages of the Curculionoidea (weevils and relatives) that originated during the Late Jurassic (10). This shift in received wisdom has also been demonstrated for a second clade of advanced seed plants, the Ephedrales, of which Gnetum and Ephedra [HN13] are now known to be insect-pollinated as well, especially by moths (11, 12). A second line of evidence is fossil evidence for plant damage, including fecal pellets in chambers evacuated within bennettitalean strobili [HN14], and coniferalean and ephedralean pollen in the gut contents of orthopteran and holometabolous insects (4, 8) [HN15]. Last, there has been limited evidence for pollen- and nectar-imbibing insect mouthparts that are difficult to explain otherwise. Examples include nemonychid weevils, glossatan moths, and nemestrinid flies (5) [HN16]. To this Jurassic list, Ren (6) adds evidence of elongate mouthparts and body hair patterns from tabanid, protapiocerid, and additional nemestrinid flies [HN17]. Although Ren indicates that these findings provide evidence for Late Jurassic angiosperms [initiating assemblage 4 in panel (A) of figure], it is equally likely that basal brachyceran lineages of flies were pollinating anthophytes other than angiosperms, lured by exposed sugary fluids secreted by nectaries located on vegetative or reproductive structures, pollination drop exudates, or even secondarily produced substances such as honeydew from sap-sucking insects (4, 12, 13). Seed plant candidates include ephedraleans and cycads and extinct clades such as bennettitaleans, corystosperms, and caytonialeans (1) [HN18].

Ren's (6) documentation of elongated mouthparts and other pollinator-associated features of Late Jurassic brachyceran flies, bolstered by recent advances in cycad-weevil pollination biology and the record of mid-Mesozoic plant-insect interactions, supports the above hypothesis that the origin of modern lineages of pollinating insects resides amid Jurassic gymnospermous seed plants. If we accept literally the earliest convincing record of angiosperms [HN19], well into the Early Cretaceous (11), then those lineages of pollinating insects that existed during the later Jurassic may have had their mutualisms subsequently co-opted and fine-tuned by angiosperms. The earliest evidence for fly pollination in angiosperms is during the mid-Cretaceous, among several early lineages of angiosperms bearing small, exposed flowers with relatively accessible floral rewards; however, their floral morphology indicates that their pollinators possessed short, sponging (labellate) mouthparts (1, 14) and that they were well established within assemblage 4 [panel (A) of figure]. Deeper throated flowers that require elongate, probing proboscides are relatively derived in angiosperms (15) and appeared later during the Cretaceous (2). One instructive counterexample to the above pattern of angiosperm co-optation is beetle pollinators and their cycad hosts, which represent an independent and parallel development that has persisted to the present (10). Consequently, investigations of the origins of basal groups of modern pollinating insects must explore more completely assemblage 3 [panel (A) of figure], of which there is tantalizing but still incomplete evidence. These investigations will require extensive examination of Middle Jurassic to earliest Cretaceous compression deposits. Although there has been considerable effort toward characterizing the insect constituents of Cretaceous amber, the oldest insect-bearing amber is about 125 million years old and thus too recent to address the origin of the basal clades of modern insect pollinators.

References and Notes

1. M. Proctor, P. Yeo, A. Lack, The Natural History of Pollination (Timber, Portland, OR, 1996).
2. E. M. Friis, P. R. Crane, K. R. Pedersen, Nature 320, 163 (1986) [GEOREF]; W. L. Crepet, Rev. Palaeobot. Palynol. 90, 339 (1996) [GEOREF].
3. K. J. Norstog, D. W. Stevenson, K. J. Niklas, Biotropica 18, 300 (1986); A. P. Vovides, N. Ogata, V. Sosa, E. Peña-García, Bot. J. Linn. Soc. 125, 201 (1997).
4. C. C. Labandeira, Annu. Rev. Ecol. Syst. 28, 153 (1997).
5. B. B. Rohdendorf, Ed., Jurassic Insects of Karatau (Izdatelstvo "Nauka," Moscow, 1968) (in Russian); L. V. Arnol'di, V. V. Zherikhin, L. M. Nikritin, A. G. Ponomarenko, Eds., Trans. Paleontol. Inst. 161, 1 (1977) (in Russian) [GEOREF]; M. V. Kozlov, Paleont. Zhur. 1989 (no. 4), 37 (1989) (in Russian).
6. D. Ren, Science 280, 85 (1998).
7. D. Edwards, P. A. Selden, J. B. Richardson, L. Axe, Nature 377, 329 (1995) [GEOREF].
8. V. A. Krassilov and A. P. Rasnitsyn, Lethaia 29, 369 (1997).
9. V. G. Novokshonov, Paleontol. Zhur. 1997 (no. 1), 65 (1997) (in Russian).
10. R. A. Crowson, in Advances in Coleopterology, M. Zunino, X. BellÇs, M. Blas, Eds. (European Association of Coleopterology, Barcelona, Spain, 1991), pp. 13-28; R. S. Anderson, Mem. Entomol.Soc. Wash. 14, 103 (1995).
11. P. R. Crane, E. M. Friis, K. R. Pedersen, Nature 374, 27 (1995) [GEOREF].
12. A. D. J. Meeuse, A. H. DeMeijer, O. W. P. Mohr, S. M. Wellinga, Isr. J. Bot. 39, 113 (1990); M. Kato and T. Inoue, Nature 368, 195 (1994).
13. W. L. Downes and G. A. Dahlem, Environ. Entomol. 16, 847 (1987).
14. S. C. Willemstein, Leiden Bot. Ser. 10, 1 (1987).
15. D. L. Dilcher, Monogr. Syst. Bot. 53, 187 (1995).
16. B. J. Sinclair, J. M. Cumming, D. M. Wood, Entomol. Scand. 24, 407 (1994).
17. I. M. Mackerras, Aust. J. Zool. 3, 439 (1955).
18. I thank P. R. Crane, W. A. DiMichele, B. D. Farrell, F. C. Thompson, B. M. Wiegmann, and D. K. Yeates for their comments. This is contribution 39 of the Evolution of Terrestrial Ecosystems consortium at the National Museum of Natural History.

The author [HN20] is in the Department of Paleobiology, National Museum of Natural History, Smithsonian Institution, Washington, DC 20560, USA; and the Department of Entomology, University of Maryland, College Park, MD 20742, USA. E-mail: labandec@nmnh.si.edu

HyperNotes
Related Resources on the World Wide Web

General Hypernotes

 

The University of California Museum of Paleontology (UCMP) at Berkeley presents extensive Web exhibits about the phylogeny of living and fossil organisms, geology and geologic time, and evolutionary theory; the UCMP Subway offers links to other Internet resources.

A collection of links to evolution information on the Web is maintained by the Biological Laboratories of Harvard University for the World Wide Web Virtual Library. The PaleoNet Pages are maintained by N. MacLeod. PaleoNet is a system of listservers, Web pages, and ftp sites designed to enhance electronic communication among paleontologists. There is a mirror site at the Natural History Museum in London.

D. Rand, Department of Biology of Brown University (Providence, RI) provides lecture notes for a course on evolutionary biology that includes a discussion of coevolution.

D. Bogler, Division of Biological Sciences, University of Texas at Austin, maintains a Web site with extensive lecture notes and Internet links for a course on ecology and evolutionary biology.

K.-P. Kelber, Mineralogisches Institut, Universitä Würzburg, Germany, maintains a Web page with annotated Internet links for paleobotanists.

The Tree of Life is a project under the direction of D. Maddison, University of Arizona, that contains information about the phylogenetic relationships and characteristics of all organisms and provides a map with links to other biological information on the Internet.

Numbered Hypernotes

1. The text of The Origin of Species is available from the Online Literature Library. J. Wilkins at the The Walter and Eliza Hall Institute of Medical Research, Victoria, Australia, maintains a Web page with links to evolution and Darwin-related Internet resources. The University of South Carolina Library Department of Rare Books and Special Collections describes Darwin's book on orchids and insects that it has in its C. Warren Irvin Jr. Collection of Darwin and Darwinana.
2. Orchids and related plants are discussed in the presentation on Orchidales from the UCMP. The Department of Botany, University of Hawaii, provides an introduction to the Orchidaceae that includes a collection of photographs. A collection of orchid images is available from the Vascular Plant Image Gallery provided by the Texas A&M University Bioinformatics Working Group. Texas A&M University's Flowering Plant Gateway provides links to scientific and other Web resources about the family Orchidaceae.
3. The Program in Plant Biology, University of Maryland, College Park, presents lecture notes on pollination and pollinators from a course on general botany. The Insects on WWW page has collected links to Web sites with information about insects and pollination. M. McIntosh, Department of Entomology, University of Arizona, provides lecture notes on pollen use in bees and other insects from a course on insect diversity. A page about flower flies is available on the Diptera Web site from the Systematic Entomology Laboratory of the U.S. Department of Agriculture. S. Buchmann of the Forgotten Pollinators Campaign, Arizona-Sonora Desert Museum, Tucson, AZ, presents a pollination lesson for children.
4. The Department of Geology and Geophysics, University of Alaska Fairbanks, displays a Geologic Time Scale. The UCMP presents a discussion of geologic time that includes a hyperlinked geologic time scale.
5. The Garden Web Glossary of Botanical Terms defines angiosperm. R. Volkwyn, Botany Department, University of the Western Cape, South Africa, discusses angiosperm anatomy. The Department of Plant Biology, University of Maryland, offers lecture notes on angiosperms from a course on general botany. A review article titled "Present state of Angiospermae phylogeny" by R. Spichiger and V. Savolainen is available from the Web site of the Conservatoire et Jardin Botaniques de la Ville de Genève, Switzerland.
6. The mouthparts of an insect are illustrated and described in the insect anatomy section of Gordon's Entomological Home Page. J. Pinto, Entomology Department, University of California, Riverside, offers lecture notes on mouthpart diversity in insects.
7. The Garden Web Glossary of Botanical Terms defines gymnosperm. M. Knee, Department of Horticulture and Crop Science, Ohio State University, Columbus, offers lecture notes about gymnosperms from a course on general plant biology. J. Reveal, Norton-Brown Herbarium, University of Maryland, provides a section about gymnosperms that includes extensive Web links in his lecture notes for a course in plant taxonomy.
8. The Tree of Life Web site's entry for Diptera describes the suborder Brachycera.
9. R. Koning, Biology Department, Eastern Connecticut State University, Willimantic, provides lecture notes from a course on plants and human affairs that includes a section on pollination adaptations. "The yucca plant and the yucca moth" by M. Ramsay and J. R. Schrock is an article from the The Kansas School Naturalist about coevolution of those two species available on the Web from Emporia State University, Emporia, KS. An article titled "Pollination Biology of Lapeirousia subgenus Lapeirousia (Iridaceae) in southern Africa; floral divergence and adaptation for long-tongued fly-pollination" by P. Goldblatt, J. Manning, and P. Bernhardt, is available on the Web site of the Missouri Botanical Garden, St. Louis. An article titled "Prosoeca peringueyi (Diptera: Nemestrinidae) pollination guild in southern Africa: long-tongued flies and their tubular flowers" by J. Manning and P. Goldblatt is also available at the Missouri Botanical Garden Web site.
10. Coprolite is defined in the 1913 Webster's Hypertext Dictionary. The Hypertext Webster Gateway has two entries for myriapod. The UCMP provides an introduction to the Myriapoda. Here is a photograph of a fossil myriapod from the Illinois State Museum's Mazon Creek fossil collection.
11. The Neoptera entry in the Tree of Life Web site discusses the hemipteroid assemblage of insects and the orthopteroid orders. A table of winged insects that lists the orthopteroid and hemipteroid orders is provided by A. R. Palmer, Department of Biological Science, University of Alberta, Canada. The Hemiptera and Orthoptera are described in the insect orders section of Gordon's Entomological Home Page. A classification of Insecta is available from the Kingdoms Project of the Illinois State Academy of Science.
12. A description and photographs of Cycadaceae are available on the Vascular Plant Family Access Page maintained by G. Carr, Department of Botany, University of Hawaii at Manoa. The Garden Web Glossary of Botanical Terms defines a cycad. The UCMP presents an introduction to the cycads. The Cycad Society is dedicated to the conservation of cycads through education and scientific research; its Web site includes a photo gallery.
13. Photographs of Ephedra and Gnetums are available on the Vascular Plant Family Access Page from the University of Hawaii Botany Department. The Hypertext Webster Gateway provides definitions of Ephedra and Gnetum. Entries for Ephreda and Gnetum are included in the Classification of Plants Web site from Manhattan College, Bronx, NY.
14. The Garden Web Glossary of Botanical Terms defines strobilus. Strobilus is defined in the WordNet database accessed from the Hypertext Webster Gateway.
15. A section on the insect order Orthoptera is available from the Tree of Life Web project. J. Meyer, Department of Entomology, North Carolina State University, Ralaigh provides a page about Orthoptera in the Compendium of Hexapod Classes and Orders. The online Merriam-Webster dictionary defines holometabolous. J. Pinto, Department of Entomology, University of California, Riverside, defines and describes holometabolous in the lecture notes on insect metamorphosis for a course on insect morphology.
16. The BIOSIS Web site provides the taxonomic hierarchy used in the Zoological Record for Lepidoptera, which lists the members of the suborder Glossata. The Nemonychidae is one of the families of Curculionoidea represented in the Coleoptera collection at the California Academy of Sciences Department of Entomology. Here is the UCMP page about Coleoptera, which includes the weevils.
17. The family Tabanidae is described on the Fossil Diptera Web site maintained by N. Evenhuis, Department of Natural Sciences, Bishop Museum, Honolulu. N. Evenhuis also provides the Australasian/Oceanian Diptera Catalog that includes a section about the Nemestrinidae and Tabanidae families of brachyceran flies. Photos of Tabinid flies are available from the Diptera Home Page of the Systematic Entomology Laboratory, U.S. Department of Agriculture. Gordon's Entomological Home Page includes a page devoted to the Tabanidae and other brachyceran flies.
18. On the UCMP Web site Bennettitalales, Corystospermales, and Caytoniales are grouped under the gymnosperms as nonflowering seed-plants. R. Taggart, Department of Botany and Department of Geological Sciences, Michigan State University, East Lansing, describes and illustrates the difference between Bennettitales (also called cycadeoids) and cycads. An entry for Bennettitophyta is included in the fossil plants division of the Classification of Plants Web site based on Whittaker's Five Kingdom System from the Department of Biology, Manhattan College.
19. K. Willis, Department of Plant Sciences, University of Cambridge, UK, offers a lecture on angiosperm origins from a course on the paleobiology and evolution of plants. The UCMP discusses the origin of Anthophyta (angiosperms) and the uncertainties and debates surrounding the topic. The UCMP site includes a chart of the first appearances of major groups of plants in the fossil record.
20. The author is at Department of Paleobiology, National Museum of Natural History, Smithsonian Institution, and the Department of Entomology, University of Maryland, College Park.