Evolutionary Biology: Genome Evolution, Speciation, Coevolution and Origin of Life pp 261-299 | Cite as
Why Did Terrestrial Insect Diversity Not Increase During the Angiosperm Radiation? Mid-Mesozoic, Plant-Associated Insect Lineages Harbor Clues
- 7 Citations
- 2.3k Downloads
Abstract
Several studies provided evidence that family-level insect diversity remained flat throughout the initial mid-Cretaceous angiosperm radiation 125–90 million years ago. As this result has engendered considerable commentary, a reanalysis was done of a new dataset of 280 plant-associated insect families spanning the 174 million year interval of the Jurassic–Paleogene periods from 201 to 23 million years ago. Lineage geochronologic ranges were determined, and feeding attributes were characterized by: (i) dominant feeding guild (herbivore, pollinator, herbivore–pollinator, pollinator–mimic, xylophage); (ii) membership in one of eight functional feeding groups; and (iii) dominant plant host or host transition (cryptogam/fern only, cryptogam/fern → angiosperm, gymnosperm only, gymnosperm → angiosperm, angiosperm only). A time-series plot of insect lineages and their dominant plant–host affiliations resulted in four conclusions. First, insect lineages with dominant gymnosperm hosts reached a level of 95 families in the 35 million years preceding the initial angiosperm radiation. Second, earlier insect lineages with gymnosperm → angiosperm host transitions and newly originated insect lineages that developed dominant associations with emerging angiosperms rapidly diversified during the angiosperm radiation, later establishing a plateau of 110 families during a 20 million year interval after the initial angiosperm radiation. Third, these two diversity maxima were separated during the angiosperm radiation by a diversity minimum, the Aptian–Albian gap, indicating major turnover and time-lag effects associated with the extirpation and acquisition of plant associations. Last, insect lineages most affected during this interval were herbivores and pollinators, exophagous feeders, and those hosting gymnosperms, angiosperms and gymnosperm → angiosperm transitions. These data largely explain the flat or even decreased level of insect diversity immediately before, during, and after the initial angiosperm radiation.
Keywords
Aptian–albian gap Cretaceous Feeding guild Fern Functional feeding group Gymnosperm Host–plant preference Plant–insect interactions Stasis Time lagsNotes
Acknowledgments
Thanks go to Pierre Pontarotti for inviting CCL to attend the Seventeenth Evolutionary Biology meeting in Marseille France. Finnegan Marsh adroitly crafted the figures. We are grateful for the Missouri Botanical Garden (St. Louis, Missouri), Wang Chen (Capital Normal University, Beijing), and Enrique Peñalver (Museo Geominero, Madrid) for use of images in Fig. 13.4. An anonymous reviewer improved the manuscript. Use of the online Paleobiology Data Base (PBDB) is acknowledged. This is contribution 263 to the Evolution of Terrestrial Ecosystems consortium at the National Museum of Natural History, in Washington, D.C.
References
- Alekseev AC, Dmitriev VY, Ponomarenko AG (2001) The evolution of taxonomic diversity. Geos, MoscowGoogle Scholar
- Barreda VD, Cúneo NR, Wilf P, Currano ED, Scasso RA, Brinkhuis H (2012) Cretaceous/Paleogene floral turnover in Patagonia: drop in diversity, low extinction, and a Classopollis spike. PLoS ONE 7(12):e52455PubMedCentralPubMedCrossRefGoogle Scholar
- Bell CD, Soltis DE, Soltis PS (2010) The age and diversification of the angiosperms re-revisited. Am J Bot 97:1296–1303PubMedCrossRefGoogle Scholar
- Buatois LA, Labandeira CC, Cohen AC, Mángano G, Voigt S (2015) The fossil history of continental aquatic taxa and the Mesozoic lacustrine revolution. In: Buatois LA, Mángano G (eds) The trace-fossil record of major evolutionary events, in review. Springer, Berlin (in review)Google Scholar
- Carpenter FM (1992) Superclass Hexapoda. In: Moore RC, Kaesler RL, Brosius E, Keim J, Priesner J (eds) Treatise on invertebrate paleontology, part R Arthropoda 4, vol 3 and 4. Geological Society of America, Boulder, and University of Kansas, LawrenceGoogle Scholar
- Cocroft RB, Rodriguez RL, Hunt RE (2008) Host shifts, the evolution of communication, and speciation in the Enchenopa binotata species complex of treehoppers. In: Tillmon KJ (ed) Specialization, speciation, and radiation: the evolutionary biology of herbivorous insects. University of California Press, Berkeley, pp 88–100Google Scholar
- Crane PR (1987) Vegetational consequences of the angiosperm diversification. In: Friis EM, Chaloner WG, Crane PR (eds) The origins of angiosperms and their biological consequences. Cambridge, New York, p 107–144Google Scholar
- Crane PR, Friis EM, Pedersen KR (1995) The origin and early diversification of angiosperms. Nature 374:27–33CrossRefGoogle Scholar
- Currano ED, Labandeira CC, Wilf P (2009) Fossilized insect folivory tracks temperature for six million years. Ecol Mon 80:547–567CrossRefGoogle Scholar
- Davis RB, Baldauf SL, Mayhew PJ (2010) The origins of species richness in the Hymenoptera: insights from a family-level supertree. BMC Evol Biol 10:109PubMedCentralPubMedCrossRefGoogle Scholar
- Davis SR, Engel MS, Legalov A, Ren D (2013) Weevils of the Yixian Formation, China (Coleoptera: Curculionoidea): phylogenetic considerations and comparison with other Mesozoic faunas. Syst Entomol 11:399–429Google Scholar
- Ding Q, Labandeira CC, Ren D (2014) Distinctive insect leaf mines on Liaoningocladus boii (Coniferales) from the Early Cretaceous Yixian Formation of northeastern China. Arthro Syst Phylo (in review)Google Scholar
- Dmitriev VJ, Zherikhin VV (1988) Changes in the diversity of insect families from data of first and last occurrences. In: Ponomarenko AG (ed) The Mesozoic-Cenozoic crisis in the evolution of insects. Nauka, Moscow, pp 208–215 (in Russian)Google Scholar
- Dodd JR, Stanton (1990) Paleoecology: concepts and applications, 2nd edn. Wiley, New YorkGoogle Scholar
- Dolling WR (1991) The Hemiptera. Oxford, New YorkGoogle Scholar
- Dunne JA, Labandeira CC, Williams RJ (2014) Highly resolved middle Eocene food webs show early development of modern trophic structure after the end-Cretaceous extinction. Proc Roy Soc B 281. http://dx.doi.org/10.1098/rspb.2013.3280
- Engel MS (2000) A new interpretation of the oldest fossil bee (Hymenoptera: Apidae). Am Mus Novit 3296:1–11CrossRefGoogle Scholar
- Evenhuis NL (1994) Catalogue of the fossil flies of the world (Insecta: Diptera). Backhuys, LeidenGoogle Scholar
- Farrell BD (1998) “Inordinate fondness” explained: why are there so many beetles? Science 281:555–559PubMedCrossRefGoogle Scholar
- Friis EM, Pedersen KR, Crane PR (2010) Diversity in obscurity: fossil flowers and the early history of angiosperms. Phil Trans Roy Soc B 365:369–382CrossRefGoogle Scholar
- Friis EM, Crane PR, Pedersen KR (2011) Early flowers and angiosperm evolution. Cambridge, CambridgeCrossRefGoogle Scholar
- Gauld I, Bolton B (eds) (1988) The Hymenoptera. Oxford, New YorkGoogle Scholar
- Goulet H, Huber JT (eds) (1993) Hymenoptera of the world: an identification guide to families. Agriculture Canada, OttawaGoogle Scholar
- Gradstein FM, Ogg JG, Schmitz MD, Ogg G (2012) The geologic time scale 2012. Elsevier, BostonGoogle Scholar
- Grimaldi D, Engel MS (2005) Evolution of the insects. Cambridge, New YorkGoogle Scholar
- Harris TM (1942) Wonnacottia, a new Bennettitalean microsporophyll. Ann Bot 6:577–592Google Scholar
- Hartkopf-Fröder C, Rust J, Wappler T, Friis EM, Viehofen A (2011) Mid-Cretaceous charred flowers reveal direct observation of arthropod feeding strategies. Biol Lett 8:295–298PubMedCentralPubMedCrossRefGoogle Scholar
- Hill RS, Carpenter RJ (1999) Ginkgo leaves from Paleogene sediments in Tasmania. Austral J Bot 47:717–724CrossRefGoogle Scholar
- Hughes N (1994) The enigma of angiosperm origins. Cambridge University Press, CambridgeGoogle Scholar
- Imada Y, Kawakita A, Kato M (2011) Allopatric distribution and diversification without niche shift in a bryophyte-feeding basal moth lineage (Lepidoptera: Micropterigidae). Proc Roy Soc B 278:3026–3033CrossRefGoogle Scholar
- Jarzembowski EA, Ross AJ (1993) Time flies: the geological record of insects. Geol Today 9:218–223CrossRefGoogle Scholar
- Jarzembowski EA, Ross AJ (1996) Insect origination and extinction in the Phanerozoic. In: Hart MB (ed) Biotic recovery from mass extinction events. Geol Soc Spec Publ 102:65–78Google Scholar
- Krassilov VA, Rasnitsyn AP, Afonin SA (2007) Pollen eaters and pollen morphology: co-evolution through the Permian and Mesozoic. Afr Invert 48:3–11Google Scholar
- Labandeira CC (1994) A compendium of fossil insect families. Milwaukee Publ Mus Contrib Biol Geol 88:1–71Google Scholar
- Labandeira CC (1997) Insect mouthparts: ascertaining the paleobiology of insect feeding strategies. Annu Rev Ecol Syst 28:153–193CrossRefGoogle Scholar
- Labandeira CC (1998) Early history of arthropod and vascular plant associations. Annu Rev Earth Planet Sci 26:329–377CrossRefGoogle Scholar
- Labandeira CC (2002) The paleobiology of predators, parasitoids, and parasites: accommodation and death in the fossil record of terrestrial invertebrates. In: Kowalewski M, Kelley PH (eds) The fossil record of predation. Paleontol Soc Pap 8:211–250Google Scholar
- Labandeira CC (2005) Fossil history and evolutionary ecology of Diptera and their associations with plants. In: Yeates DK, Wiegmann BM (eds) The evolutionary biology of flies. Columbia, New York, pp 217–273Google Scholar
- Labandeira CC (2006) Silurian to Triassic plant and insect clades and their associations: new data, a review, and interpretations. Arth Syst Phylo 64:53–94Google Scholar
- Labandeira CC (2007) The origin of herbivory on land: the initial pattern of live tissue consumption by arthropods. Ins Sci 14:259–274CrossRefGoogle Scholar
- Labandeira CC (2010) The pollination of mid Mesozoic seed plants and the early history of long-proboscid insects. Ann Missouri Bot Gard 97:469–513CrossRefGoogle Scholar
- Labandeira CC (2013) A paleobiological perspective on plant–insect interactions. Curr Opin Pl Biol 16:414–421CrossRefGoogle Scholar
- Labandeira CC, Allen EM (2007) Minimal insect herbivory for the lower Permian coprolite bone bed site of north-central Texas, USA, and comparison to other late Paleozoic floras. Palaeogeogr Palaeoclimatol Palaeoecol 247:197–219CrossRefGoogle Scholar
- Labandeira CC, Dilcher DL, Davis DR, Wagner DL (1994) Ninety-seven million years of angiosperm-insect association: paleobiological insights into the meaning of coevolution. Proc Natl Acad Sci USA 91:12278–12282PubMedCentralPubMedCrossRefGoogle Scholar
- Labandeira CC, Kvaček J, Mostovski MB (2007a) Pollination fluids, pollen, and insect pollination of Mesozoic gymnosperms. Taxon 56:663–695CrossRefGoogle Scholar
- Labandeira CC, Johnson KR, Wilf P (2002) Impact of the terminal Cretaceous event on plant–insect associations. Proc Natl Acad Sci USA 99:2061–2066PubMedCentralPubMedCrossRefGoogle Scholar
- Labandeira CC, Sepkoski JJ Jr (1993) Insect diversity in the fossil record. Science 261:310–315Google Scholar
- Labandeira CC, Wilf P, Johnson KR, Marsh F (2007b) Guide to insect (and other) damage types on compressed plant fossils. Version 3.0—Spring 2007). Smithsonian Institution, Washington. http://paleobilogy.si.edu/pdf:insectDamageGuide3.01.pdf
- Lawrence JF, Ślipiński A (2013) Australian beetles: Morphology, classification and keys, vol 1. CSIRO, CollingwoodGoogle Scholar
- Lewis T (1973) Thrips: their biology, ecology and economic importance. Academic Press, LondonGoogle Scholar
- López-Vaamonde C, Wikström N, Labandeira CC, Goodman S, Godfray HCJ, Cook JM (2006) Fossil-calibrated molecular phylogenies reveal that leaf-mining moths radiated millions of years after their host plants. J Evol Biol 19:1314–1326PubMedCrossRefGoogle Scholar
- Magallón S (2010) Using fossils to break long branches in molecular dating: a comparison of relaxed clocks applied to the origin of angiosperms. Syst Biol 59:384–399PubMedCrossRefGoogle Scholar
- Marshall SA (2012) Flies: the natural history and diversity of Diptera. Firefly, BuffaloGoogle Scholar
- McAlpine JF, Peterson BV, Shewell GE, Teskey HJ, Vockeroth JR, Wood DW (eds) (1981–1989) Manual of Nearctic Diptera vols 1–3. Canadian Government Publishing Centre, Hull, QuebecGoogle Scholar
- McKenna DD, Sequeira AS, Marvaldi AE, Farrell BD (2009) Temporal lags and overlap in the diversification of weevils and flowering plants. Proc Natl Acad Sci USA 106:7083–7088PubMedCentralPubMedCrossRefGoogle Scholar
- McLoughlin S, Carpenter RJ, Jordan GJ, Hill RS (2008) Seed ferns survived the end-Cretaceous extinction in Tasmania. Am J Bot 95:465–471PubMedCrossRefGoogle Scholar
- McLoughlin S, Carpenter RJ, Pott C (2011) Ptilophyllum muelleri (Ettingsh.) comb. nov. from the Oligocene of Australia: last of the Bennettitales? Int J Plant Si 172:574–585CrossRefGoogle Scholar
- Miller NCE (1956) The biology of the Heteroptera. Leonard Hill, LondonGoogle Scholar
- Moran NA, Tran P, Gerardo NM (2005) Symbiosis and insect diversification: an ancient symbiont of sap-feeding insects from the bacterial phylum Bacteroidetes. Appl Environ Microbiol 71:8802–8810PubMedCentralPubMedCrossRefGoogle Scholar
- Naumann ID, Carne PB, Lawrence JF, Nielsen ES, Spradbery JP, Taylor RW, Whitten MJ, Littlejohn MJ (eds) (1991) The insects of Australia: A textbook for students and research workers, vols. 1, 2. Cornell, IthacaGoogle Scholar
- Nylin S, Wahlberg N (2008) Does plasticity drive speciation? Host-plant shifts and diversification in nymphaliine butterflies (Lepidoptera: Nymphalidae) during the Tertiary. Biol J Linn Soc 94:115–130CrossRefGoogle Scholar
- Paleobiology Database (2014) http://paleobiol.org. Last accessed 10 Feb 2014
- Pellmyr O, Seagraves K (2003) Pollinator divergence within an obligate mutualism: two yucca moth species (Lepidoptera: Prodoxidae: Tegeticula) on the Joshua tree (Yucca brevifolia; Agavaceae). Ann Entomol Soc Am 96:716–722CrossRefGoogle Scholar
- Peñalver E, Labandeira CC, Barrón E, Delclòs X, Nel A, Nel P, Taffoureau P, Soriano C (2012) Thrips pollination of Mesozoic gymnosperms. Proc Natl Acad Sci USA 109:8623–8628PubMedCentralPubMedCrossRefGoogle Scholar
- Rasnitsyn AP (1980) The origin and evolution of hymenopterous insects. Trans Paleontol Inst 174:1–192 (in Russian)Google Scholar
- Rasnitsyn AP (1988) Principles and methods of phylogenetic reconstruction. In: Ponomarenko AG (ed) The Mesozoic-Cenozoic crisis in the evolution of insects. Nauka, Moscow, pp 191–207 (in Russian)Google Scholar
- Rasnitsyn AP, Krassilov VA (2000) The first documented occurrence of phyllophagy in pre-Cretaceous insects: leaf tissues in the gut of Upper Jurassic insects from southern Kazakhstan. Paleontol J 34:301–309Google Scholar
- Rasnitsyn AP, Quicke DLJ (eds) (2002) History of insects. Kluwer, DordrechtGoogle Scholar
- Ratzel SR, Rothwell GW, Mapes G, Mapes RH, Doguzhaeva LA (2001) Pityostrobus hokodzensis, a new species of pinaceous cone from the Cretaceous of Russia. J Paleontol 75:895–900CrossRefGoogle Scholar
- Ren D (1998) Flower-associated Brachycera flies as fossil evidence for Jurassic angiosperm origins. Science 280:85–88PubMedCrossRefGoogle Scholar
- Ren D (ed) (2010) Current research on palaeoentomology. Acta Geol Sin 84(4):655–1010Google Scholar
- Ren D, Labandeira CC, Santiago-Blay JA, Rasnitsyn AP, Shih CK, Bashkuev A, Logan MAV, Hotton CL, Dilcher DL (2009) A probable pollination mode before angiosperms: Eurasian, long-proboscid scorpionflies. Science 326:840–847PubMedCentralPubMedCrossRefGoogle Scholar
- Ross AJ, Jarzembowski EA (1993) Arthropoda (Hexapoda; Insecta). In: Benton MJ (ed) The fossil record 2. Chapman & Hall, London, pp 363–426Google Scholar
- Schachat S, Labandeira CC, Gordon J, Chaney D, Levi S, Halthore MS, Alvarez J (2014) Plant–insect interactions from the Early Permian (Kungurian) Colwell Creek Pond, North-Central Texas: the early spread of herbivory in riparian environments. Int J Pl Sci 175: in pressGoogle Scholar
- Schuh RT, Slater JA (1995) True bugs of the world (Hemiptera: Heteroptera). Cornell, IthacaGoogle Scholar
- Sinitshenkova ND (2002) Ecological history of the aquatic insects. In: Rasnitsyn AP, Quicke DLJ (eds) History of insects. Kluwer, Dordrecht, pp 388–426Google Scholar
- Sohn J-C, Labandeira CC, Davis D, Mitter C (2012) An annotated catalog of fossil and subfossil Lepidoptera (Insecta: Holometabola) of the world. Zootaxa 3286:1–132Google Scholar
- Sukatcheva ID (1991) The Late Cretaceous stage in the history of the caddisflies (Trichoptera). Acta Hydroentom Lat 1:68–85Google Scholar
- Taylor TN, Taylor EL, Krings M (2009) Paleobotany: the biology and evolution of fossil plants, 2nd edn. Elsevier, AmsterdamGoogle Scholar
- Wang B, Szwedo J, Zhang H (2012a) New Jurassic Cercopoidea from China and their evolutionary significance (Insecta: Hemiptera). Palaeontology 55:1223–1243CrossRefGoogle Scholar
- Wang B, Zhang H, Jarzembowski EA (2013) Early Cretaceous angiosperms and beetle evolution. Front Pl Sci 4:360Google Scholar
- Wang Y, Labandeira CC, Ding Q, Shih CK, Zhao Y, Ren D (2012b) An extraordinary Jurassic mimicry between a hangingfly and ginkgo from China. Proc Natl Acad Sci USA 109:20514–20519PubMedCentralPubMedCrossRefGoogle Scholar
- Wang Y, Liu Z, Wang X, Shih C, Zhao Y, Engel MS, Ren D (2010) Ancient pinnate leaf mimesis among lacewings. Proc Natl Acad Sci USA 107:16212–16215PubMedCentralPubMedCrossRefGoogle Scholar
- Wappler T, Labandeira CC, Rust J, Frankenhäuser H, Wilde V (2012) Testing for the effects and consequences of mid-Paleogene climate change on insect herbivory. PLoS ONE 7:e40744PubMedCentralPubMedCrossRefGoogle Scholar
- Watson J (1977) Some Lower Cretaceous conifers of the Cheirolepidiaceae from the U.S.A. and England. Palaeontology 20:715–749Google Scholar
- Weingartner E, Wahlberg N, Nylin S (2006) Dynamics of host plant use and species diversity in Polygonia butterflies (Nymphalidae). J Evol Biol 19:483–491PubMedCrossRefGoogle Scholar
- Wilf P, Labandeira CC, Johnson KR, Cúneo NR (2005) Richness of plant–insect associations in Eocene Patagonia: a legacy for South American biodiversity. Proc Natl Acad Sci USA 102:8944–8948PubMedCentralPubMedCrossRefGoogle Scholar
- Wilf P, Labandeira CC, Johnson KR, Ellis B (2006) Decoupled plant and insect diversity after the end-Cretaceous extinction. Science 313:1112–1115PubMedCrossRefGoogle Scholar
- Winkler IS, Labandeira CC, Wappler T, Wilf P (2010) Diptera (Agromyzidae) leaf mines from the Paleogene of North America and Germany: implications for host use evolution and an early origin for the Agromyzidae. J Paleontol 84:935–954CrossRefGoogle Scholar
- Yeates DK, Wiegmann BM (eds) (2005) The evolutionary biology of flies. Columbia, New YorkGoogle Scholar
- Zhang W, Shih CK, Labandeira CC, Sohn JC, Davis DR, Santiago-Blay JA, Flint O, Ren D (2013) New fossil Lepidoptera (Insecta: Amphiesmenoptera) from the Middle Jurassic Jiulongshan Formation of Northeastern China. PLoS ONE 8(11):e79500PubMedCentralPubMedCrossRefGoogle Scholar
- Zherikhin VV, Mostovski MB, Vršanský P, Blagoderov VA, Lukashevich ED (1999) The unique lower Cretaceous locality Baissa and other contemporaneous fossil insect sites in North and West Transbaikalia. In: Proceedings of 1st International Palaeoentom Conference (Moscow, 1998). AMBA Projects, Bratislava, p 185–191Google Scholar
- Zhou Z, Zhang B (1989) A sideritic Protocupressinoxylon with insect borings and frass from the Middle Jurassic, Henan, China. Rev Palaeobot Palynol 59:133–143CrossRefGoogle Scholar