Fluctuation in the diversity of mayflies (Insecta, Ephemerida) as documented in the fossil record
Language English Country Great Britain, England Media electronic
Document type Journal Article, Research Support, Non-U.S. Gov't
PubMed
37749134
PubMed Central
PMC10519997
DOI
10.1038/s41598-023-42571-7
PII: 10.1038/s41598-023-42571-7
Knihovny.cz E-resources
- MeSH
- Bayes Theorem MeSH
- Ephemeroptera * MeSH
- Insecta MeSH
- Larva MeSH
- Fossils MeSH
- Animals MeSH
- Check Tag
- Animals MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
Due to their aquatic larvae, the evolution of mayflies is intricately tied to environmental changes affecting lakes and rivers. Despite a rich fossil record, little is known about the factors shaping the pattern of diversification of mayflies in deep time. We assemble an unprecedented dataset encompassing all fossil occurrences of mayflies and perform a Bayesian analysis to identify periods of increased origination or extinction. We provide strong evidence for a major extinction of mayflies in the mid-Cretaceous. This extinction and subsequent faunal turnover were probably connected with the rise of angiosperms. Their dominance caused increased nutrient input and changed the chemistry of the freshwater environments, a trend detrimental mainly to lacustrine insects. Mayflies underwent a habitat shift from hypotrophic lakes to running waters, where most of their diversity has been concentrated from the Late Cretaceous to the present.
Department of Zoology Faculty of Science Charles University Viničná 7 128 00 Prague 2 Czech Republic
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Prokop J, Nel A, Tenny A. On the phylogenetic position of the palaeopteran Syntonopteroidea (Insecta: Ephemeroptera), with a new species from the upper Carboniferous of England. Org. Divers. Evol. 2010;10(4):331–340. doi: 10.1007/s13127-010-0022-2. DOI
Béthoux O. The late Carboniferous Triplosoba pulchella is not a fly in the ointment but a stem-mayfly. Syst. Entomol. 2014;40(2):1–15. doi: 10.1111/syen.12103. DOI
Kukalová-Peck J. Ephemeroid wing venation based upon new gigantic Carboniferous mayflies and basis morphological phylogeny and metamorphosis of pterygopte insects (Insecta, Ephemerida) Can. J. Zool. 1985;63:933–955. doi: 10.1139/z85-139. DOI
Rasnitsyn AP. 2.2.1.1. Cohors Libelluliformes Laircharting, 1781 (= Subulicornes Latreille, 1807, = Hydropalaeopaloptera Rohdendorf, 1968) In: Rasnitsyn AP, Quicke DLJ, editors. History of insects. Kluwer Academic Publishers; 2002. pp. 85–89.
Sartori M, Brittain J. Order Ephemeroptera. 873–891. In: Thorp J, Rodgers DC, editors. Freshwater Invertebrates: Ecology and General Biology. 4. Academic Press; 2015. p. 1118.
Wootton RJ. The historical ecology of aquatic insects: an overview. Palaeogeogr. Palaeoclimatol. Palaeoecol. 1988;62:477–492. doi: 10.1016/0031-0182(88)90068-5. DOI
Benton MJ, Wilf P, Saquet H. The angiosperm terrestrial revolution and the origins of modern biodiversity. New Phytol. 2022;233:2017–2035. doi: 10.1111/nph.17822. PubMed DOI
Labandeira CC, Sepkoski JJ. Insect diversity in the fossil record. Science. 1993;261:310–315. doi: 10.1126/science.11536548. PubMed DOI
Schachat SR, Labandeira CC. Are insects heading toward their first mass extinction? Distinguishing turnover from crises in their fossil record. Ann. Entomol. Soc. Am. 2021;114(2):99–118. doi: 10.1093/aesa/saaa042. DOI
Sinitshenkova ND. Ecological history of the aquatic insects. 388–426. In: Rasnitsyn AP, Quicke DLJ, editors. History of Insects. Kluwer Academic Publishers; 2002. p. 517.
Sinitshenkova ND. Main ecological events in aquatic insects history. Acta Zool. Crac. 2003;46:381–392.
Silvestro D, Salamin N, Schnitzler J. PyRate: A new program to estimate speciation and extinction rates from incomplete fossil record. Methods Ecol. Evol. 2014;5:1126–1131. doi: 10.1111/2041-210X.12263. DOI
Silvestro D, Schnitzler J, Liow LH, Antonelli A, Salamin N. Bayesian estimation of speciation and extinction from incomplete fossil occurrence data. Syst. Biol. 2014;63:349–367. doi: 10.1093/sysbio/syu006. PubMed DOI PMC
Silvestro D, Salamin N, Antonelli A, Meyer X. Improved estimation of macroevolutionary rates from fossil data using a Bayesian framework. Paleobiology. 2019;45:546–570. doi: 10.1017/pab.2019.23. DOI
Lehtonen S, Silvestro D, Karger DN, Scotese C, Tuomisto H, Kessler M, Peña C, Wahlberg N, Antonelli A. Environmentally driven extinction and opportunistic origination explain fern diversification patterns. Sci. Rep. 2017;7:4831. doi: 10.1093/sysbio/syu006. PubMed DOI PMC
Jouault C, Nel A, Legendre F, Condamine FL. Estimating the drivers of diversification of stoneflies through time and the limits of their fossil record. Insect Syst. Divers. 2022;6(4):1–14. doi: 10.1093/isd/ixac017. DOI
Schmedtje, U. & Colling, M. Ökologische Typisierung der aquatischen Makrofauna. Informationsberichte des Bayerischen Landesamtes für Wasserwirtschaft, 4196 (1996).
Merrit RW, Cummins KW. An Introduction to the Aquatic Insects of North America. Kendall/Hunt; 1996.
Müller RD, Cannon J, Qin X, Watson RJ, Gurnis M, Williams S, et al. GPlates: Building a virtual earth through deep time. Geochem. Geophys. Geosyst. 2018 doi: 10.1029/2018GC007584. PubMed DOI
Scotese, C. R. PALEOMAP PaleoAtlas for GPlates and the PaleoData Plotter Program, PALEOMAP Project. http://www.earthbyte.org/paleomap--‐paleoatlas--‐for--‐gplates/ (2016).
Alfonso-Rojas A, Cadena E-A. The first benthic insects (Ephemeroptera and Coleoptera) from the upper cretaceous of Colombia. Cretac. Res. 2022;132:105116. doi: 10.1016/j.cretres.2021.105116. DOI
Martínez-Delclòs X, Briggs DEG, Peñalver E. Taphonomy of insects in carbonates and amber. Palaeogeogr. Palaeoclimatol. Palaeoecol. 2004;203:19–64. doi: 10.1016/S0031-0182(03)00643-6. DOI
Jablonski D. Extinctions in the fossil record. Philos. Trans. R. Soc. B. 1994;344:11–17. doi: 10.1098/rstb.1994.0045. DOI
Raup DM. The role of extinction in evolution. PNAS. 1994;91:6758–6763. doi: 10.1073/pnas.91.15.6758. PubMed DOI PMC
Jouault C, Nel A, Perrichot V, Legendre F, Condamine FL. Multiple drivers and lineage-specific insect extinctions during the Permo-Triassic. Nat. Commun. 2022;13(1):7512. doi: 10.1038/s41467-022-35284-4. PubMed DOI PMC
Labandeira CC. The fossil record of insect extinction: New approaches and future directions. Am. Entomol. 2005;54(1):14–29. doi: 10.1093/ae/51.1.14. DOI
Vermeij GJ. The mesozoic marine revolution: Evidence from snails, predators and grazers. Paleobiology. 1977;3(3):245–258. doi: 10.1017/S0094837300005352. DOI
Lloyd GT, Davis KE, Pisani D, Tarver JE, Ruta M, Sakamoto M, Hone DW, Jennings R, Benton MJ. Dinosaurs and the cretaceous terrestrial revolution. Proc. Biol. Sci. 2008;275(1650):2483–2490. doi: 10.1098/rspb.2008.0715. PubMed DOI PMC
Buatois LA, Labandeira CC, Mángano MG, Cohen A, Voigt S. The mesozoic lacustrine revolution. In: Mángano MG, Buatois LA, editors. The Trace-Fossil Record of Major Evolutionary Events, Topics in Geobiology. Springer Netherlands; 2016. pp. 179–263.
Sukatsheva ID. The late cretaceous stage in the history of the caddisfles (Trichoptera) Acta Hydroentomol. Latv. 1991;1:68–85.
Zherikin VV, Kalugina NS. Landscapes and communities. In: Rasnitsyn AP, editor. Yurskie Continental’nye Biotsenozy Yuzhnoi Sibiri i sopredel’nykh Territorii (Jurassic Continental Biocoenoses of South Siberia and Adjacent Territories) Nauka; 1985. pp. 140–183.
Sinitshenkova ND, Zherikhin VV. Mesozoic lacustrine biota: Extinction and persistence of communities. Paleontol. J. 1996;30(6):710–715.
Berendse F, Scheffer M. The angiosperm radiation revisited, an ecological explanation for Darwin’s ‘abominable mystery‘. Ecol. Lett. 2009;12:865–872. doi: 10.1111/j.1461-0248.2009.01342.x. PubMed DOI PMC
Zherikin VV. 1.4 pattern of insect burial and conservation. 17–63. In: Rasnitsyn AP, Quicke DLJ, editors. History of Insects. Kluwer Academic Publishers; 2002. p. 517.
Ponomarenko AG. Evolution of continental aquatic ecosystems. Palaeontomol. J. 1996;30(6):705–709.
Coiro M, Doyle JA, Hilton J. How deep is the conflict between molecular and fossil evidence on the age of angiosperms? New Phytol. 2019;223:83–99. doi: 10.1111/nph.15708. PubMed DOI
Donoghue P. Evolution: The flowering of land plant evolution. Curr. Biol. 2019;29:R738–R761. doi: 10.1016/j.cub.2019.06.021. PubMed DOI
Friis EM, Pedersen KR, Crane PR. Diversity in obscurity: Fossil flowers and the early history of angiosperms. Philos. Trans. R. Soc. Lond. B Biol. Sci. 2010;365:369–382. doi: 10.1098/rstb.2009.0227. PubMed DOI PMC
Barba-Montoya J, dos Reis M, Schneider H, Donoghue PCJ, Yang Z. Constraining uncertainty in the timescale of angiosperm evolution and the veracity of a Cretaceous terrestrial revolution. New Phytol. 2018;218:819–834. doi: 10.1111/nph.15011. PubMed DOI PMC
Herendeen PS, Friis EM, Pedersen KR, Crane PR. Palaeobotanical redux: Revisiting the age of the angiosperms. Nat. Plants. 2017;3(3):1–8. doi: 10.1038/nplants.2017.15. PubMed DOI
Lidgard S, Crane PR. Quantitative analyses of the early angiosperm radiation. Nature. 1988;331:344–346. doi: 10.1038/331344a0. DOI
Willis KJ, McElwain JC. The Evolution of Plants. Oxford University Press; 2002.
Mueller KE, Diefendorf AF, Freeman KH, Eissenstat DM. Appraising the roles of nutrient availability, global change, and functional traits during the angiosperm rise to dominance. Ecol. Lett. 2010;13:E1–E6. doi: 10.1111/j.1461-0248.2010.01455.x. PubMed DOI
Augusto L, Davies TJ, Delzon S, De Schrijver A. The enigma of the rise of angiosperms: Can we untie the knot? Ecol. Lett. 2014;17:1326–1338. doi: 10.1111/ele.12323. PubMed DOI
Brodribb TJ, Feild TS. Leaf hydraulic evolution led a surge in leaf photosynthetic capacity during early angiosperm diversification. Ecol. Lett. 2010;13:175–183. doi: 10.1111/j.1461-0248.2009.01410.x. PubMed DOI
Comas LH, Eissenstat DM. Patterns in root trait variation among 25 co-existing North American forest species. New Phytol. 2009;182:919–928. doi: 10.1111/j.1469-8137.2009.02799.x. PubMed DOI
Smith VH, Tilman GD, Nekola JC. Eutrophication: Impacts of excess nutrient inputs on freshwater, marine, and terrestrial ecosystems. Environ. Pollut. 1999;100:179–196. doi: 10.1016/s0269-7491(99)00091-3. PubMed DOI
Nessel MP, Konnovitch T, Romero GQ, Gonzáles AL. Decline of insects and arachnids driven by nutrient enrichment: A meta-analysis. Ecology. 2022;104:e3897. doi: 10.1002/ecy.3897. PubMed DOI PMC
Kleinman PJ, Sharpley AN. Eutrophication of lakes and rivers. Encycl. Life Sci. 2001 doi: 10.1038/npg.els.0003249. DOI
Rasnitsyn AP, Zherikin VV. 4.1 impression fossils. 437–444. In: Rasnitsyn AP, Quicke DLJ, editors. History of Insects. Kluwer Academic Publishers; 2002. p. 517.
Sroka P, Staniczek AH, Bechly G. Revision of the giant pterygote insect Bojophlebia prokopi Kukalová-Peck, 1985 (Hydropalaeoptera: Bojophlebiidae) from the Carboniferous of the Czech Republic, with the first cladistic analysis of fossil palaeopterous insects. J. Syst. Paleontol. 2015;13:963–982. doi: 10.1080/14772019.2014.987958. DOI
Sroka P, Staniczek AH. Evolution of filter-feeding in aquatic insects dates back to the Middle Triassic: New evidence from stem-group mayflies (Insecta, Ephemerida) from Grès à Voltzia, Vosges, France. Pap. Palaeontol. 2022 doi: 10.1002/spp2.14561. DOI
R Core Team. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/ (2022).
Bayesian modelling of the fossil record enlightens the evolutionary history of Hemiptera