Skip to main content Skip to main navigation menu Skip to site footer
Type: Article
Published: 2023-10-30
Page range: 472–481
Abstract views: 130
PDF downloaded: 94

Evolution of Insect Diversity in the Permian and Triassic

State Key Laboratory of Biogeology and Environmental Geology, China University of Geosciences (Wuhan), Wuhan 430074, China
State Key Laboratory of Biogeology and Environmental Geology, China University of Geosciences (Wuhan), Wuhan 430074, China
State Key Laboratory of Biogeology and Environmental Geology, China University of Geosciences (Wuhan), Wuhan 430074, China
Diversity change subsampling extinction terrestrial ecosystem fossil record

Abstract

The global warming that occurred during the Permo-Triassic transition, following the end of the Late Paleozoic glaciation, and the resulting responses of the biota to the changing environment, are considered important analogs for understanding rapid future warming scenarios. While there has been extensive research on the patterns and extent of diversity in plants, tetrapods, and marine invertebrates during the Permo-Triassic, the study of insect diversity and the evolution of their faunal composition has been relatively limited. The question of whether there were insect extinctions during this period continues to be a subject of debate. Here, we present a statistical study on taxonomic diversity of insects—at specific, generic and familial levels—throughout the Permian and Triassic, with subsampled context on the reported global occurrences. Our result show that more than one insect extinction events, accompanied by significant diversity drop and turnovers of faunal compositional, occurred in the Permian and Triassic. All the uncovered insect diversity crises exhibit strong correspondence with the well-known marine mass extinction events in the Middle Permian, Permo-Triassic transition, Carnian, and Rhaetian, whilst the marine correspondence with the Early Permian insect crisis is less pronounced. Insects, being a major component of terrestrial ecosystems, demonstrate varied diversity responses to climatic changes in Permian and Triassic. Our study sheds new light on the intricate interplay between insect diversity evolution and the changing environmental conditions during these critical geohistorical periods.

References

  1. Allen, B.J., Wignall, P.B., Hill, D.J., Saupe, E.E. & Dunhill, A.M. (2020) The latitudinal diversity gradient of tetrapods across the Permo-Triassic mass extinction and recovery interval. Proceedings of the Royal Society B, 287 (1929), 20201125. https://doi.org/10.1098/rspb.2020.1125
    Alroy, J. (2010a) Geographic, environmental and intrinsic biotic controls on Phanerozoic marine diversification. Palaeontology, 53 (6), 1211–1235. https://doi.org/10.1111/j.1475-4983.2010.01011.x
    Alroy, J. (2010b) The shifting balance of diversity among major marine animal groups. Science, 329 (5996), 1191–1194. https://doi.org/10.1126/science.1189910
    Alroy, J. (2010c) Fair sampling of taxonomic richness and unbiased estimation of origination and extinction rates. The Paleontological Society Papers, 16, 55–80. https://doi.org/10.1017/S1089332600001819
    Alroy, J., Marshall, C.R., Bambach, R.K., Bezusko, K., Foote, M., Fürsich, F.T., Hansen, T.A., Holland, S.M., Ivany, L.C., Jablonski, D., Jacobs, D.K., Jones, D.C., Kosnik, M.A., Lidgard, S., Low, S., Miller, A.I., Novack-Gottshall, P.M., Olszewski, T.D., Patzkowsky, M.E., Raup, D.M., Roy, K., Sepkoski, J.J., Jr., Sommers, M.G., Wagner, P.J. & Webber, A. (2001) Effects of sampling standardization on estimates of Phanerozoic marine diversification. Proceedings of the National Academy of Sciences, 98 (11), 6261–6266. https://doi.org/10.1073/pnas.111144698
    Aristov, D.S., Bashkuev, A.S., Golubev, V.K., Gorochov, A.V., Karasev, E.V., Kopylov, D.S., Ponomarenko, A.G., Rasnitsyn, A.P., Rasnitsyn, D.A., Sinitshenkova, N.D., Sukatsheva, I.D. & Vassilenko, D.V. (2013) Fossil insects of the middle and upper Permian of European Russia. Paleontological Journal, 47, 641–832. https://doi.org/10.1134/S0031030113070010
    Benton, M.J. (1986) More than one event in the late Triassic mass extinction. Nature, 321 (6073), 857–861. https://doi.org/10.1038/321857a0
    Benton, M.J. (2016) The Triassic. Current Biology, 26 (23), R1214–R1218. https://doi.org/10.1016/j.cub.2016.10.060
    Benton, M.J. (2018) Hyperthermal-driven mass extinctions: killing models during the Permian–Triassic mass extinction. Philosophical Transactions of the Royal Society A: Mathematical, Physical and Engineering Sciences, 376 (2130), 20170076. https://doi.org/10.1098/rsta.2017.0076
    Benton, M.J. & Newell, A.J. (2014) Impacts of global warming on Permo-Triassic terrestrial ecosystems. Gondwana Research, 25 (4), 1308–1337. https://doi.org/10.1016/j.gr.2012.12.010
    Benton, M.J. & Twitchett, R.J. (2003) How to kill (almost) all life: the end-Permian extinction event. Trends in Ecology & Evolution, 18 (7), 358–365. https://doi.org/10.1016/S0169-5347(03)00093-4
    Béthoux, O., Papier, F. & Nel, A. (2005) The Triassic radiation of the entomofauna. Comptes Rendus Palevol, 4 (6–7), 609–621. https://doi.org/10.1016/j.crpv.2005.06.005
    Burgess S.D., Burgess, S.D. & Bowring, S.A. (2015) High-precision geochronology confirms voluminous magmatism before, during, and after Earth’s most severe extinction. Science Advances, 1 (7), e1500470. https://doi.org/10.1126/sciadv.1500470
    Black, B.A., Hauri, E.H., Elkins-Tanton, L.T. & Brown, S.M. (2014) Sulfur isotopic evidence for sources of volatiles in Siberian Traps magmas. Earth and Planetary Science Letters, 394, 58–69. https://doi.org/10.1016/j.epsl.2014.02.057
    Bond, D.P., Hilton, J., Wignall, P.B., Ali, J.R., Stevens, L.G., Sun, Y.D. & Lai, X.L. (2010) The Middle Permian (Capitanian) mass extinction on land and in the oceans. Earth-Science Reviews, 102 (1–2), 100–116. https://doi.org/10.1016/j.earscirev.2010.07.004
    Bottjer, D.J., Clapham, M.E., Fraiser, M.L. & Powers, C.M. (2008) Understanding mechanisms for the end-Permian mass extinction and the protracted Early Triassic aftermath and recovery. GSA Today, 18 (9), 4. https://doi.org/10.1130/GSATG8A.1
    Burgess, S.D. & Bowring, S.A. (2015) High-precision geochronology confirms voluminous magmatism before, during, and after Earth’s most severe extinction. Science Advances, 1 (7), e1500470. https://doi.org/10.1126/sciadv.1500470
    Chao, A. & Jost, L. (2012) Coverage‐based rarefaction and extrapolation: standardizing samples by completeness rather than size. Ecology, 93 (12), 2533–2547. https://doi.org/10.1890/11-1952.1
    Clapham, M.E., Karr, J.A., Nicholson, D.B., Ross, A.J. & Mayhew, P.J. (2016) Ancient origin of high taxonomic richness among insects. Proceedings of the Royal Society B: Biological Sciences, 283 (1824), 20152476. https://doi.org/10.1098/rspb.2015.2476
    Condamine, F.L., Clapham, M.E. & Kergoat, G.J. (2016) Global patterns of insect diversification: towards a reconciliation of fossil and molecular evidence? Scientific Reports, 6 (1), 19208. https://doi.org/10.1038/srep19208
    Dal Corso, J., Song, H.J., Callegaro, S., Chu, D.L., Sun, Y.D., Hilton, J., Grasby, S.E., Joachimski, M.M. & Wignall, P.B. (2022) Environmental crises at the Permian–Triassic mass extinction. Nature Reviews Earth & Environment, 3 (3), 197–214. https://doi.org/10.1038/s43017-021-00259-4
    Economo, E.P., Narula, N., Friedman, N.R., Weiser, M.D. & Guénard, B. (2018) Macroecology and macroevolution of the latitudinal diversity gradient in ants. Nature Communications, 9 (1), 1778. https://doi.org/10.1038/s41467-018-04218-4
    Eggleton, P. (2020) The state of the world’s insects. Annual Review of Environment and Resources, 45, 61–82. https://doi.org/10.1146/annurev-environ-012420-050035
    Fattorini, S. (2022) Global patterns of earwig species richness. Diversity, 14 (10), 890. https://doi.org/10.3390/d14100890
    Feng, Z., Wei, H.B., Guo, Y., He, X.Y., Sui, Q., Zhou, Y., Liu, H.Y., Gou, X.D. & Lü, Y. (2020) From rainforest to herbland: New insights into land plant responses to the end-Permian mass extinction. Earth-Science Reviews, 204, 103153. https://doi.org/10.1016/j.earscirev.2020.103153
    Fielding, C.R., Frank, T.D., McLoughlin, S., Vajda, V., Mays, C., Tevyaw, A.P., Winguth, A., Winguth, C., Nicoll, R.S., Bocking, M. & Crowley, J.L. (2019) Age and pattern of the southern high-latitude continental end-Permian extinction constrained by multiproxy analysis. Nature Communications, 10 (1), 385. https://doi.org/10.1038/s41467-018-07934-z
    Gastaldo R.A. (2019) Ancient plants escaped the end-Permian mass extinction. Nature, 567, 38–39. https://doi.org/10.1038/d41586-019-00744-3
    Grimaldi, D., Engel, M.S., Engel, M.S. & Engel, M.S. (2005) Evolution of the Insects. Cambridge University Press, Cambridge, 755 pp.
    Jarzembowski, E.A. & Ross, A.J. (1996) Insect origination and extinction in the Phanerozoic. Geological Society, London, Special Publications, 102 (1), 65–78. https://doi.org/10.1144/GSL.SP.1996.001.01.05
    Jouault, C., Nel, A., Perrichot, V., Legendre, F. & Condamine, F.L. (2022) Multiple drivers and lineage-specific insect extinctions during the Permo–Triassic. Nature Communications, 13 (1), 7512. https://doi.org/10.1038/s41467-022-35284-4
    Kristensen, N.P. (1999) Phylogeny of Endopterygota insects, the most successful lineage of living organisms. European Journal of Entomology, 96 (3), 237–254.
    Kusnezov, N. (1957) Numbers of species of ants in faunae of different latitudes. Evolution, 11 (3), 298–299. https://doi.org/10.1111/j.1558-5646.1957.tb02898.x
    Labandeira, C.C. (1997) Insect mouthparts: ascertaining the paleobiology of insect feeding strategies. Annual Review of Ecology and Systematics, 28 (1), 153–193. https://doi.org/10.1146/annurev.ecolsys.28.1.153
    Labandeira, C.C. (2005) The fossil record of insect extinction: new approaches and future directions. American Entomologist, 51 (1), 14–29. https://doi.org/10.1093/ae/51.1.14
    Labandeira, C.C. (2006) Silurian to Triassic plant and insect clades and their associations: new data, a review, and interpretations. Arthropod Systematics & Phylogeny, 64, 53–94.
    Labandeira, C.C. (2013) A paleobiologic perspective on plant–insect interactions. Current Opinion in Plant Biology, 16 (4), 414–421. https://doi.org/10.1016/j.pbi.2013.06.003
    Labandeira, C.C. & Sepkoski Jr, J.J. (1993) Insect diversity in the fossil record. Science, 261 (5119), 310–315. https://doi.org/10.1126/science.11536548
    Liu, H.Y., Wei, H.B., Chen, J., Guo, Y., Zhou, Y., Gou, X.D., Yang, S.L., Labandeira, C. & Feng, Z. (2020) A latitudinal gradient of plant–insect interactions during the late Permian in terrestrial ecosystems? New evidence from Southwest China. Global and Planetary Change, 192, 103248. https://doi.org/10.1016/j.gloplacha.2020.103248
    Mayhew, P.J. (2007) Why are there so many insect species? Perspectives from fossils and phylogenies. Biological Reviews, 82 (3), 425–454. https://doi.org/10.1111/j.1469-185X.2007.00018.x
    McKenna, D.D. & Farrell, B.D. (2006) Tropical forests are both evolutionary cradles and museums of leaf beetle diversity. Proceedings of the National Academy of Sciences, 103 (29), 10947–10951. https://doi.org/10.1073/pnas.0602712103
    Miller, A.I. & Foote, M. (1996) Calibrating the Ordovician radiation of marine life: implications for Phanerozoic diversity trends. Paleobiology, 22 (2), 304–309. https://doi.org/10.1017/S0094837300016237
    Montagna, M., Tong, K.J., Magoga, G., Strada, L., Tintori, A., Ho, S.Y. & Lo, N. (2019) Recalibration of the insect evolutionary time scale using Monte San Giorgio fossils suggests survival of key lineages through the End-Permian Extinction. Proceedings of the Royal Society B, 286 (1912), 20191854. https://doi.org/10.1098/rspb.2019.1854
    Nel, P., Bertrand, S. & Nel, A. (2018) Diversification of insects since the Devonian: a new approach based on morphological disparity of mouthparts. Scientific Reports, 8 (1), 3516. https://doi.org/10.1038/s41598-018-21938-1
    Novotny, V., Drozd, P., Miller, S.E., Kulfan, M., Janda, M., Basset, Y. & Weiblen, G.D. (2006) Why are there so many species of herbivorous insects in tropical rainforests? Science, 313 (5790), 1115–1118. https://doi.org/10.1126/science.1129237
    Nowak, H., Schneebeli-Hermann, E. & Kustatscher, E. (2019) No mass extinction for land plants at the Permian–Triassic transition. Nature communications, 10 (1), 384. https://doi.org/10.1038/s41467-018-07945-w
    Pinheiro, E.R., Iannuzzi, R. & Duarte, L.D. (2016) Insect herbivory fluctuations through geological time. Ecology, 97 (9), 2501–2510. https://doi.org/10.1002/ecy.1476
    Ponomarenko, A.G. (2006) Changes in terrestrial biota before the Permian-Triassic ecological crisis. Paleontological Journal, 40 (4), S468–S474. https://doi.org/10.1134/S0031030106100066
    Ponomarenko, A.G. (2016) Insects during the time around the Permian—Triassic crisis. Paleontological Journal, 50 (2), 174–186. https://doi.org/10.1134/S0031030116020052
    Retallack, G.J. (2013) Permian and Triassic greenhouse crises. Gondwana Research, 24 (1), 90–103. https://doi.org/10.1016/j.gr.2012.03.003
    Retallack, G.J., Sheldon, N.D., Carr, P.F., Fanning, M., Thompson, C.A., Williams, M.L., Jones, B.G. & Hutton, A. (2011) Multiple Early Triassic greenhouse crises impeded recovery from Late Permian mass extinction. Palaeogeography, Palaeoclimatology, Palaeoecology, 308 (1–2), 233–251. https://doi.org/10.1016/j.palaeo.2010.09.022
    Retallack, G.J., Veevers, J.J. & Morante, R. (1996) Global coal gap between Permian–Triassic extinction and Middle Triassic recovery of peat-forming plants. Geological Society of America Bulletin, 108 (2), 195–207. https://doi.org/10.1130/0016-7606(1996)108<0195:GCGBPT>2.3.CO;2
    Romano, M., Bernardi, M., Petti, F.M., Rubidge, B., Hancox, J. & Benton, M.J. (2020) Early Triassic terrestrial tetrapod fauna: a review. Earth-Science Reviews, 210, 103331. https://doi.org/10.1016/j.earscirev.2020.103331
    Schachat, S.R. & Labandeira, C.C. (2015) Evolution of a complex behavior: the origin and initial diversification of foliar galling by Permian insects. The Science of Nature, 102, 1–8. https://doi.org/10.1007/s00114-015-1266-7
    Schachat, S.R. & Labandeira, C.C. (2021) Are insects heading toward their first mass extinction? Distinguishing turnover from crises in their fossil record. Annals of the Entomological Society of America, 114 (2), 99–118. https://doi.org/10.1093/aesa/saaa042
    Scotese, C.R., Song, H., Mills, B.J. & van der Meer, D.G. (2021) Phanerozoic paleotemperatures: The earth’s changing climate during the last 540 million years. Earth-Science Reviews, 215, 103503. https://doi.org/10.1016/j.earscirev.2021.103503
    Sepkoski, J.J. (1984) A kinetic model of Phanerozoic taxonomic diversity. III. Post-Paleozoic families and mass extinctions. Paleobiology, 10 (2), 246–267. https://doi.org/10.1017/S0094837300008186
    Shu, W.C., Tong, J.N., Yu, J.X., Hilton, J., Benton, M.J., Shi, X., Diez, J.B., Wignall, P.B., Chu, D.L., Tian, L., Yi, Z.X. & Mao, Y.D. (2023) Permian-Middle Triassic flora succession in North China and implications for the great transition of continental ecosystems. GSA Bulletin, 135, 1747–1767. https://doi.org/10.1130/B36316.1
    Signor, P.W. & Lipps, J.H. (1982) Sampling bias, gradual extinction patterns, and catastrophes in the fossil record. In: Silver, L.T. & Schultz, P.H. (Eds), Geological implications of impacts of large asteroid and comets on the Earth. Geological Society of America Press, Boulder, pp. 291–296. https://doi.org/10.1130/SPE190-p291
    Shcherbakov, D.E. (2008) Insect recovery after the Permian/Triassic crisis. Alavesia, 2, 125–131.
    Shcherbakov, D.Y. (1984) Systematics and phylogeny of Permian Cicadomorpha (Cimicada and Cicadina). Paleontological Journal, 18 (2), 87–97.
    Song, H.J., Wignall, P.B., Chu, D.L., Tong, J.N., Sun, Y.D., Song, H.Y., He, W.H. & Tian, L. (2014) Anoxia/high temperature double whammy during the Permian-Triassic marine crisis and its aftermath. Scientific reports, 4 (1), 4132. https://doi.org/10.1038/srep04132
    Stork, N.E. (2018) How many species of insects and other terrestrial arthropods are there on Earth? Annual review of entomology, 63, 31–45. https://doi.org/10.1146/annurev-ento-020117-043348
    Stork, N.E., McBroom, J., Gely, C. & Hamilton, A.J. (2015) New approaches narrow global species estimates for beetles, insects, and terrestrial arthropods. Proceedings of the National Academy of Sciences, 112 (24), 7519–7523. https://doi.org/10.1073/pnas.1502408112
    Sun, Y.D., Joachimski, M.M., Wignall, P.B., Yan, C.B., Chen, Y.L., Jiang, H.S., Wang, L.N. & Lai, X.L. (2012) Lethally hot temperatures during the Early Triassic greenhouse. Science, 338 (6105), 366–370. https://doi.org/10.1126/science.1224126
    Uhl, D., Jasper, A., Hamad, A.M.A. & Montenari, M. (2008) Permian and Triassic wildfires and atmospheric oxygen levels. Ecosystems, 9, 179–187.
    Viglietti, P.A., Benson, R.B., Smith, R.M., Botha, J., Kammerer, C.F., Skosan, Z., Butler, E., Crean, A., Eloff, B., Kaal, S., Mohoi, J., Molehe, W., Mtalana, N., Mtungata, S., Ntheri, N., Ntsala, T., Nyaphuli, J., October, P., Skinner, G., Strong, M., Stummer, H., Wolvaardt, F.P. & Angielczyk, K.D. (2021) Evidence from South Africa for a protracted end-Permian extinction on land. Proceedings of the National Academy of Sciences, 118 (17), e2017045118. https://doi.org/10.1073/pnas.2017045118
    Vajda, V., McLoughlin, S., Mays, C., Frank, T.D., Fielding, C.R., Tevywa, A., Lehsten, V., Bocking, M. & Nicoll, R.S. (2020) End-Permian (252 Mya) deforestation, wildfires and flooding-An ancient biotic crisis with lessons for the present. Earth and Planetary Science Letter, 529, 115875. https://doi.org/10.1016/j.epsl.2019.115875
    Wappler, T., Kustatscher, E. & Dellantonio, E. (2015) Plant–insect interactions from Middle Triassic (late Ladinian) of Monte Agnello (Dolomites, N-Italy)—Initial pattern and response to abiotic environmental perturbations. PeerJ, 3, e921. https://doi.org/10.7717/peerj.921
    Wappler, T., Labandeira, C.C., Rust, J., Frankenhäuser, H. & Wilde, V. (2012) Testing for the effects and consequences of mid Paleogene climate change on insect herbivory. PLOS ONE, 7 (7), e40744. https://doi.org/10.1371/journal.pone.0040744
    Xiong, C.H. & Wang, Q. (2011) Permian–Triassic land-plant diversity in South China: Was there a mass extinction at the Permian/Triassic boundary? Paleobiology, 37 (1), 157–167. https://doi.org/10.1666/09029.1