Cretaceous environmental changes led to high extinction rates in a hyperdiverse beetle family

BMC Evolutionary Biology

Fabien L Condamine⁵  Laurent Soldati¹  Gwenaelle Genson¹  Roula Jabbour-Zahab³  Hervé Jourdan²  Jessica L Abbate³  Anne-Laure Clamens¹  Patrice Bouchard⁴  Gael J Kergoat¹ 

[1] INRA - UMR 1062 CBGP (INRA, IRD, CIRAD, Montpellier SupAgro), Campus de Baillarguet, Montferrier-sur-Lez, 34988, France;IRD, UMR 237 IMBE (IRD, Aix-Marseille Université, CNRS, Université d’Avignon et des pays de Vaucluse), Centre IRD de Nouméa, Nouméa, 98848, Nouvelle-Calédonie, France;CNRS - UMR 5175 CEFE (CNRS, Université Montpellier 2), 1919 Route de Mende, Montpellier, 34293, France;Canadian National Collection of Insects, Arachnids and Nematodes, Agriculture and Agri-Food Canada, 960 Carling Avenue, Ottawa K1A 0C6, ON, Canada;Department of Biological and Environmental Sciences, University of Gothenburg, Göteborg, SE-405 30, Sweden

关键词: Tenebrionidae;    Palaeoclimates;    Environmental changes;    Diversification analyses;    Dating analyses;    Cretaceous terrestrial revolution;    Cretaceous-palaeogene mass extinction;   

Others  :  1117879
DOI  :  10.1186/s12862-014-0220-1

 received in 2014-08-08, accepted in 2014-10-06,  发布年份 2014

【 摘 要 】

Background

As attested by the fossil record, Cretaceous environmental changes have significantly impacted the diversification dynamics of several groups of organisms. A major biome turnover that occurred during this period was the rise of angiosperms starting ca. 125 million years ago. Though there is evidence that the latter promoted the diversification of phytophagous insects, the response of other insect groups to Cretaceous environmental changes is still largely unknown. To gain novel insights on this issue, we assess the diversification dynamics of a hyperdiverse family of detritivorous beetles (Tenebrionidae) using molecular dating and diversification analyses.

Results

Age estimates reveal an origin after the Triassic-Jurassic mass extinction (older than previously thought), followed by the diversification of major lineages during Pangaean and Gondwanan breakups. Dating analyses indicate that arid-adapted species diversified early, while most of the lineages that are adapted to more humid conditions diversified much later. Contrary to other insect groups, we found no support for a positive shift in diversification rates during the Cretaceous; instead there is evidence for an 8.5-fold increase in extinction rates that was not compensated by a joint increase in speciation rates.

Conclusions

We hypothesize that this pattern is better explained by the concomitant reduction of arid environments starting in the mid-Cretaceous, which likely negatively impacted the diversification of arid-adapted species that were predominant at that time.

【 授权许可】

   
2014 Kergoat et al.; licensee BioMed Central Ltd.

【 图 表 】

Figure 1.

Figure 2.

Figure 3.

【 参考文献 】

• [1]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 R Soc B 2008, 275:2483-2490.
• [2]Coiffard C, Gomez B, Daviero-Gomez V, Dilcher DL: Rise to dominance of angiosperm pioneers in European Cretaceous environments. Proc Natl Acad Sci U S A 2012, 109:20955-20959.
• [3]Spicer RA, Chapman JL: Climate change and the evolution of high-latitude terrestrial vegetation and floras. Trends Ecol Evol 1990, 5:279-284.
• [4]Vakhrameev VA: Jurassic and Cretaceous floras and climates of the Earth. Cambridge University Press, Cambridge; 1991.
• [5]Morley RJ: Cretaceous and Tertiary Climate Change and the Past Distribution of Megathermal Rainforests. In Tropical Rainforest Responses to Climatic Changes. Edited by Bush MB, Flenley J. Praxis Publishing, Chichester; 2007:1-31.
• [6]Hallam A: Continental humid and arid zones during the Jurassic and Cretaceous. Palaeogeogr Palaeoclim Palaeoecol 1984, 47:195-223.
• [7]Föllmi KB: Early Cretaceous life, climate and anoxia. Cretaceous Res 2011, 35:230-257.
• [8]Labandeira CC: A paleobiologic perspective on plant-insect interactions. Curr Opin Plant Biol 2013, 16:414-421.
• [9]Benton MJ: The origins of modern biodiversity on land. Phil Trans R Soc B 2010, 365:3667-3679.
• [10]Farrell BD: “Inordinate fondness” explained: why are there so many beetles? Science 1998, 281:555-559.
• [11]Moreau CS, Bell CD, Vila R, Archibald SB, Pierce NE: Phylogeny of the ants: diversification in the age of angiosperms. Science 2006, 312:101-104.
• [12]McKenna DD, Sequeira AS, Marvaldi AE, Farrell BD: Temporal lags and overlap in the diversification of weevils and flowering plants. Proc Natl Acad Sci U S A 2009, 106:7083-7088.
• [13]Wahlberg N, Wheat CW, Peña C: Timing and patterns in the taxonomic diversification of Lepidoptera (butterflies and moths). PLoS One 2013, 8:e80875.
• [14]Meredith RW, Janečka JE, Gatesy J, Ryder OA, Fisher CA, Teeling EC, Goodbla A, Eizirik E, Simao TLL, Stadler T, Rabosky DL, Honeycutt RL, Flynn JJ, Ingram CM, Steiner C, Williams TL, Robinson TJ, Burk-Herrick A, Westerman M, Ayoub NA, Springer MS, Murphy WJ: Impacts of the Cretaceous terrestrial revolution and KPg extinction on mammal diversification. Science 2011, 334:521-524.
• [15]Jetz W, Thomas GH, Joy JB, Hartmann K, Mooers AO: The global diversity of birds in space and time. Nature 2012, 491:444-448.
• [16]Roelants K, Gower DJ, Wilkinson M, Loader SP, Biju SD, Guillaume K, Moriau L, Bossuyt F: Global patterns of diversification in the history of modern amphibians. Proc Natl Acad Sci U S A 2007, 104:887-892.
• [17]Grimaldi D, Engel MS: Evolution of the insects. Cambridge University Press, Cambridge; 2005.
• [18]Stadler T: Mammalian phylogeny reveals recent diversification rate shifts. Proc Natl Acad Sci U S A 2011, 108:6187-6192.
• [19]Pyron RA, Burbrink FT: Phylogenetic estimates of speciation and extinction rate for testing ecological and evolutionary hypotheses. Trends Ecol Evol 2013, 28:729-736.
• [20]Moreau CS, Bell CD: Testing the museum versus cradle tropical biological diversity hypothesis: phylogeny, diversification, and ancestral biogeographic range evolution of the ants. Evolution 2013, 67:2240-2257.
• [21]Rehan SM, Leys R, Schwarz MP: First evidence of a massive extinction event affecting bees close to the K-T boundary. PLoS One 2013, 8:e76683.
• [22]Hunt T, Bergsten J, Levkaničova Z, Papadopoulou A, St John O, Wild R, Hammond PM, Ahrens D, Balke M, Caterino MS, Gómez-Zurita J, Ribera I, Barraclough TG, Bocakova M, Bocak L, Vogler AP: A comprehensive phylogeny of beetles reveals the evolutionary origins of a superradiation. Science 2007, 318:1913-1916.
• [23]Wang B, Zhang H, Jarzembowski EA: Early Cretaceous angiosperms and beetle evolution. Front Plant Sci 2013, 4:360.
• [24]Ślipiński SA, Leschen RAB, Lawrence JF: Order coleoptera linnaeus, 1758. Zootaxa 2011, 3148:203-208.
• [25]Matthews EG, Lawrence JF, Bouchard P, Steiner WE, Slipiński SA: 11.14. Tenebrionidae Latreille, 1802. In Handbook of Zoology. A Natural History of the Phyla of the Animal Kingdom. Volume IV - Arthropoda: Insecta. Part 38. Coleoptera, Beetles. Volume 2: Systematics (Part 2). Edited by Leschen RAB, Beutel RG, Lawrence JF. Walter de Gruyter, Berlin; 2010:574-659.
• [26]Watt JC: A revised subfamily classification of Tenebrionidae (Coleoptera). New Zealand J Zool 1974, 1:381-452.
• [27]Geisthardt M: Tenebrionidae (Insecta, Coleoptera) as an indicator for climatic changes on the Cape Verde Islands. Spec Bull Jap Soc Coleopt 2003, 6:331-337.
• [28]Kirejtshuk AG, Merkl O, Kernegger F: A new species of the genus Pentaphyllus Dejean, 1821 (Coleoptera: Tenebrionidae, Diaperinae) from the Baltic amber and checklist of the fossil Tenebrionidae. Zoosyst Ross 2008, 17:131-137.
• [29]Matthews EG: Classification, phylogeny and biogeography of the genera of Adeliini (Coleoptera: Tenebrionidae). Inver Taxon 1998, 12:685-824.
• [30]Matthews EG, Bouchard P: Tenebrionid Beetles of Australia: Description of Tribes, Keys to Genera, Catalogue of Species. Australian Biological Resources Study, Canberra; 2008.
• [31]McKenna DD, Farrell BD: Beetles (Coleoptera). In The Timetree of Life. Edited by Hedges SB, Kumar S. Oxford University Press, New York; 2009:278-289.
• [32]Crisp MD, Arroyo MTK, Cook LG, Gandolfo MA, Jordan GJ, McGlone MS, Weston PH, Westoby M, Wilf P, Linder HP: Phylogenetic biome conservatism on a global scale. Nature 2009, 458:754-756.
• [33]Chandler MA, Rind D, Ruedy R: Pangaean during the Early Jurassic: GCM simulations and the sedimentary record of paleoclimate. Geol Soc Am Bull 1992, 104:543-559.
• [34]Parrish JT: Climate of the supercontinent Pangea. J Geol 1993, 101:215-233.
• [35]Byrne M, Yeates DK, Joseph L, Kearney M, Bowler J, Williams MAJ, Cooper S, Donnellan SC, Keogh JS, Leys R, Melville J, Murphy DJ, Porch N, Wyrwoll KH: Birth of a biome: insights into the assembly and maintenance of the Australian arid zone biota. Mol Ecol 2008, 17:4398-4417.
• [36]Byrne M, Steane DA, Joseph L, Yeates DK, Jordan GJ, Crayn D, Aplin K, Cantrill DJ, Cook LG, Crisp MD, Keogh JS, Melville J, Moritz C, Porch N, Sniderman JMK, Sunnucks P, Weston PH: Decline of a biome: evolution, contraction, fragmentation, extinction and invasion of the Australian mesic zone biota. J Biogeogr 2011, 38:1635-1656.
• [37]Matthews EG: Origins of Australian arid-zone tenebrionid beetles. Invert Syst 2000, 14:941-951.
• [38]Zachos JC, Dickens GR, Zeebe RE: An early Cenozoic perspective on greenhouse warming and carbon-cycle dynamics. Nature 2008, 451:279-283.
• [39]Veizer J, Godderis Y, François LM: Evidence for decoupling of atmospheric CO2 and global climate during the Phanerozoic eon. Nature 2000, 408:698-701.
• [40]Prokoph A, Shields GA, Veizer J: Compilation and time-series analysis of a marine carbonate δ18O, δ13C,87Sr/86Sr and δ34S database through Earth history.Earth-Sci Rev 2008, 87:113–133.
• [41]Blakey RC: Gondwana Paleogeography From Assembly to Breakup – A 500 Million Year Odyssey. In Resolving the Late Paleozoic Ice Age in Time and Space. Edited by Fielding CR, Frank TD, Isbell JL. Geological Society of America Special Paper 441. Geological Society of America, Boulder, CO; 2008:1-28.
• [42]Mitterboeck TF, Adamowicz SJ: Flight loss linked to faster molecular evolution in insects. Proc R Soc B 2013, 280:20131128.
• [43]Parmesan C: Ecological and evolutionary responses to recent climate change. Annu Rev Ecol Evol Syst 2006, 37:637-669.
• [44]Ikeda H, Nishikawa M, Sota T: Loss of flight promotes beetle diversification. Nat Commun 2012, 3:648.
• [45]Cornell HV: Is regional species diversity bounded or unbounded? Biol Rev 2013, 88:140-165.
• [46]Erwin DH: Climate as a driver of evolutionary change. Curr Biol 2009, 19:R575-R583.
• [47]Mayhew PJ, Jenkins GN, Benton TG: A long-term association between global temperature and biodiversity, origination and extinction in the fossil record. Proc R Soc Lond B 2009, 275:47-53.
• [48]Condamine FL, Rolland J, Morlon H: Macroevolutionary perspectives to environmental change. Ecol Lett 2013, 16(Suppl 1):72-85.
• [49]Kergoat GJ, Soldati L, Clamens A-L, Jourdan H, Jabbour-Zahab R, Genson G, Bouchard P, Condamine FL: Higher-level molecular phylogeny of darkling beetles (Coleoptera, Tenebrionoidea, Tenebrionidae).Syst Entomol. in press.
• [50]Drummond AJ, Suchard MA, Xie D, Rambaut A: Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol Biol Evol 2012, 29:1969-1973.
• [51]Parham JF, Donoghue PC, Bell CJ, Calway TD, Head JJ, Holroyd PA, Inoue JG, Irmis RB, Joyce WG, Ksepka DT, Patané JSL, Smith ND, Tarver JE, van Tuinen M, Yang Z, Angielczyk KD, Greenwood JM, Hipsley CA, Jacobs L, Makovicky PJ, Müller J, Smith KT, Theodor JM, Warnock RCM, Benton MJ: Best practices for justifying fossil calibrations. Syst Biol 2012, 61:346-359.
• [52]Sauquet H, Ho SYW, Gandolfo MA, Jordan GJ, Wilf P, Cantrill DJ, Bayly MJ, Bromham L, Brown GK, Carpenter RJ, Lee DM, Murphy DJ, Sniderman JMK, Udovicic F: Testing the impact of calibration on molecular divergence times using a fossil-rich group: the case of Nothofagus (Fagales). Syst Biol 2012, 61:289-313.
• [53]Gradstein FM, Ogg JG, Schmitz M, Ogg G: The Geologic Time Scale 2012. Elsevier, Boston; 2012.
• [54]Condamine FL, Soldati L, Clamens A-L, Rasplus J-Y, Kergoat GJ: Diversification patterns and processes of wingless endemic insects in the Mediterranean Basin: historical biogeography of the genus Blaps (Coleoptera: Tenebrionidae). J Biogeogr 2013, 40:1899-1913.
• [55]Kergoat GJ, Le Ru BP, Genson G, Cruaud C, Couloux A, Delobel A: Phylogenetics, species boundaries and timing of resource tracking in a highly specialized group of seed beetles (Coleoptera: Chrysomelidae: Bruchinae). Mol Phylogenet Evol 2011, 59:746-760.
• [56]Fernández-Palacios JM, de Nascimento L, Otto R, Delgado JD, Garcia-del-Rey E, Arévalo JR, Whittaker RJ: A reconstruction of Palaeo-Macaronesia, with particular reference to the long-term biogeography of the Atlantic island laurel forest. J Biogeogr 2011, 38:226-246.
• [57]Lopez-Vaamonde C, Wikström N, Labandeira C, Godfray HCJ, Goodman SJ, Cook JM: Fossil-calibrated molecular phylogenies reveal that leaf-mining moths radiated millions of years after their host plants. J Evol Biol 2006, 19:1314-1326.
• [58]Biffin E, Hill RS, Lowe AJ: Did Kauri (Agathis: Araucariaceae) really survive the Oligocene drowning of New Zealand? Syst Biol 2010, 59:594-602.
• [59]Crisp MD, Cook LG: Cenozoic extinctions account for the low diversity of extant gymnosperms compared with angiosperms. New Phyt 2011, 192:997-1009.
• [60]Yang Z, Rannala B: Bayesian estimation of species divergence times under a molecular clock using multiple fossil calibrations with soft bounds. Mol Biol Evol 2006, 23:212-226.
• [61]Ho SYW, Phillips MJ: Accounting for calibration uncertainties in phylogenetic estimation of evolutionary divergence times. Syst Biol 2009, 58:367-380.
• [62]Lartillot N, Philippe H: Computing Bayes factors using thermodynamic integration. Syst Biol 2006, 55:195-207.
• [63]Baele G, Li WLS, Drummond AJ, Suchard MA, Lemey P: Accurate model selection of relaxed clocks in Bayesian phylogenetics. Mol Biol Evol 2013, 30:239-243.
• [64][http://beast.bio.ed.ac.uk/Tracer] webcite Rambaut A, Drummond AJ: Tracer v1.5..
• [65]Kass RE, Raftery AE: Bayes factors. J Am Stat Assoc 1995, 90:773-795.
• [66]Cusimano N, Renner SS: Slowdowns in diversification rates from real phylogenies may be not real. Syst Biol 2010, 59:458-464.
• [67]Davies MP, Midford PE, Maddison W: Exploring power and parameter estimation of the BiSSE method for analysing species diversification. BMC Evol Biol 2013, 13:38. BioMed Central Full Text
• [68]Goldberg EE, Kohn JR, Lande R, Robertson KA, Smith SA, Igic B: Species selection maintains self-incompatibility. Science 2010, 330:493-495.
• [69]Hugall AF, Stuart-Fox D: Accelerated speciation in colour-polymorphic birds. Nature 2012, 485:631-634.
• [70]Magallón S, Sanderson MJ: Absolute diversification rates in angiosperm clades. Evolution 2001, 55:1762-1780.
• [71]Lewis P: A likelihood approach to estimating phylogeny from discrete morphological character data. Syst Biol 2001, 50:913-925.
• [72][http://mesquiteproject.org] webcite Maddison WP, Maddison DR: Mesquite: A Modular System for Evolutionary Analysis, Version 2.75. Available at . 2011.
• [73]Schluter D, Price T, Mooers AO, Ludwig D: Likelihood of ancestor states in adaptive radiation. Evolution 1997, 51:1699-1711.
• [74]Ricklefs RE: Estimating diversification rates from phylogenetic information. Trends Ecol Evol 2007, 22:602-610.
• [75]Rabosky DL: Ecological limits and diversification rate: alternative paradigms to explain the variation in species richness among clades and regions. Ecol Lett 2009, 12:735-743.
• [76]Rabosky DL: Primary controls on species richness in higher taxa. Syst Biol 2010, 59:634-645.