Conserved ancestral tropical niche but different continental histories explain the latitudinal diversity gradient in brush-footed butterflies

. 2021 Sep 29 ; 12 (1) : 5717. [epub] 20210929

Jazyk angličtina Země Anglie, Velká Británie Médium electronic

Typ dokumentu časopisecké články, práce podpořená grantem, Research Support, U.S. Gov't, Non-P.H.S.

Perzistentní odkaz   https://www.medvik.cz/link/pmid34588433
Odkazy

PubMed 34588433
PubMed Central PMC8481491
DOI 10.1038/s41467-021-25906-8
PII: 10.1038/s41467-021-25906-8
Knihovny.cz E-zdroje

The global increase in species richness toward the tropics across continents and taxonomic groups, referred to as the latitudinal diversity gradient, stimulated the formulation of many hypotheses to explain the underlying mechanisms of this pattern. We evaluate several of these hypotheses to explain spatial diversity patterns in a butterfly family, the Nymphalidae, by assessing the contributions of speciation, extinction, and dispersal, and also the extent to which these processes differ among regions at the same latitude. We generate a time-calibrated phylogeny containing 2,866 nymphalid species (~45% of extant diversity). Neither speciation nor extinction rate variations consistently explain the latitudinal diversity gradient among regions because temporal diversification dynamics differ greatly across longitude. The Neotropical diversity results from low extinction rates, not high speciation rates, and biotic interchanges with other regions are rare. Southeast Asia is also characterized by a low speciation rate but, unlike the Neotropics, is the main source of dispersal events through time. Our results suggest that global climate change throughout the Cenozoic, combined with tropical niche conservatism, played a major role in generating the modern latitudinal diversity gradient of nymphalid butterflies.

Australian Museum 6 College Street Sydney NSW 2010 Australia

Biology Centre of the Czech Academy of Sciences Institute of Entomology České Budějovice Czech Republic

City College of New York and Graduate Center CUNY New York NY USA

CNRS UMR 5554 Institut des Sciences de l'Evolution de Montpellier Place Eugene Bataillon 34095 Montpellier France

Cummington Street Department of Biology Boston University Boston MA 02215 USA

Departamento de Biologia Animal Instituto de Biologia Universidade Estadual de Campinas 13083 862 Campinas SP Brazil

Departamento de Química y Biología Universidad del Norte Barranquilla Colombia

Department of Biological Sciences University of New Orleans New Orleans LA USA

Department of Ecology Swedish University of Agricultural Sciences Ulls väg 16 75651 Uppsala Sweden

Department of Life and Earth Sciences Perimeter College Georgia State University 33 Gilmer Street Atlanta GA 30303 USA

Department of Life Sciences Natural History Museum London SW7 5BD UK

Department of Zoology Stockholm University 10691 Stockholm Sweden

Department of Zoology University of Cambridge Downing St Cambridge CB2 3EJ UK

Durrell Institute of Conservation and Ecology University of Kent Canterbury CT2 7NR UK

Gothenburg Global Biodiversity Centre Gothenburg Sweden

IISER TVM Centre for Research and Education in Ecology and Evolution School of Biology Indian Institute of Science Education and Research Thiruvananthapuram Thiruvananthapuram India

Institut de Biologia Evolutiva Barcelona Spain

ISYEB CNRS MNHN Sorbonne Université EPHE Université des Antilles 57 rue Cuvier Paris 75005 France

McGuire Center for Lepidoptera and Biodiversity Florida Museum of Natural History University of Florida Gainesville FL 32611 USA

Museo de Historia Natural Universidad Nacional Mayor de San Marcos Lima Peru

National Museum of Natural History Manila Philippines

Nature Education Centre Jagiellonian University ul Gronostajowa 5 30 387 Kraków Poland

Smithsonian Tropical Research Institute Gamboa Panama

Systematic Biology Group Department of Biology Lund University Lund Sweden

Universidade Estadual de Campinas Centro de Biologia Molecular e Engenharia Genética Av Candido Rondom 400 13083 875 Campinas SP Brazil

Vaccine and Infectious Disease Division Fred Hutchinson Cancer Research Center Seattle WA USA

Zobrazit více v PubMed

Mittelbach GG, et al. Evolution and the latitudinal diversity gradient: speciation, extinction and biogeography. Ecol. Lett. 2007;10:315–331. doi: 10.1111/j.1461-0248.2007.01020.x. PubMed DOI

Mannion PD, Upchurch P, Benson RBJ, Goswami A. The latitudinal biodiversity gradient through deep time. Trends Ecol. Evol. 2014;29:42–50. doi: 10.1016/j.tree.2013.09.012. PubMed DOI

Kinlock NL, et al. Explaining global variation in the latitudinal diversity gradient: meta‐analysis confirms known patterns and uncovers new ones. Glob. Ecol. Biogeogr. 2018;27:125–141. doi: 10.1111/geb.12665. DOI

Wiens JJ, Graham CH, Moen DS, Smith SA, Reeder TW. Evolutionary and ecological causes of the latitudinal diversity gradient in hylid frogs: treefrog trees unearth the roots of high tropical diversity. Am. Nat. 2006;168:579–596. doi: 10.1086/507882. PubMed DOI

Wiens JJ, Sukumaran J, Pyron RA, Brown RM. Evolutionary and biogeographic origins of high tropical diversity in old world frogs (Ranidae) Evolution. 2009;63:1217–1231. doi: 10.1111/j.1558-5646.2009.00610.x. PubMed DOI

Jansson R, Rodríguez-Castañeda G, Harding LE. What can multiple phylogenies say about the latitudinal diversity gradient? A new look at the tropical conservatism, out of the tropics, and diversification rate hypotheses: phylogenies and the latitudinal diversity gradient. Evolution. 2013;67:1741–1755. doi: 10.1111/evo.12089. PubMed DOI

Economo EP, Narula N, Friedman NR, Weiser MD, Guénard B. Macroecology and macroevolution of the latitudinal diversity gradient in ants. Nat. Commun. 2018;9:1778. doi: 10.1038/s41467-018-04218-4. PubMed DOI PMC

Stephens PR, Wiens JJ. Explaining species richness from continents to communities: the time‐for‐speciation effect in Emydid turtles. Am. Nat. 2003;161:112–128. doi: 10.1086/345091. PubMed DOI

Wiens JJ, Donoghue MJ. Historical biogeography, ecology and species richness. Trends Ecol. Evol. 2004;19:639–644. doi: 10.1016/j.tree.2004.09.011. PubMed DOI

Morley, R. J. Cretaceous and Tertiary climate change and the past distribution of megathermal rainforests. In Tropical Rainforest Responses to Climatic Change 1–31 (Springer Berlin Heidelberg, 2007). 10.1007/978-3-540-48842-2_1.

Jablonski D, Roy K, Valentine JW. Out of the tropics: evolutionary dynamics of the latitudinal diversity gradient. Science. 2006;314:102–106. doi: 10.1126/science.1130880. PubMed DOI

Condamine FL, Sperling FAH, Wahlberg N, Rasplus J-Y, Kergoat GJ. What causes latitudinal gradients in species diversity? Evolutionary processes and ecological constraints on swallowtail biodiversity: phylogeny and latitudinal diversity gradient. Ecol. Lett. 2012;15:267–277. doi: 10.1111/j.1461-0248.2011.01737.x. PubMed DOI

Rolland J, Condamine FL, Beeravolu CR, Jiguet F, Morlon H. Dispersal is a major driver of the latitudinal diversity gradient of Carnivora: dispersal and the latitudinal gradient of Carnivora. Glob. Ecol. Biogeogr. 2015;24:1059–1071. doi: 10.1111/geb.12354. DOI

Fischer AG. Latitudinal variations in organic diversity. Evolution. 1960;14:64. doi: 10.1111/j.1558-5646.1960.tb03057.x. DOI

Rolland J, Condamine FL, Jiguet F, Morlon H. Faster speciation and reduced extinction in the tropics contribute to the mammalian latitudinal diversity gradient. PLoS Biol. 2014;12:e1001775. doi: 10.1371/journal.pbio.1001775. PubMed DOI PMC

Rosenzweig, M. L. Species diversity in space and time. (Cambridge University Press, 1995). 10.1017/CBO9780511623387.

Allen AP, Gillooly JF, Savage VM, Brown JH. Kinetic effects of temperature on rates of genetic divergence and speciation. Proc. Natl Acad. Sci. 2006;103:9130–9135. doi: 10.1073/pnas.0603587103. PubMed DOI PMC

Schemske, D. W. Ecological and evolutionary perspectives on the origins of tropical diversity. In Foundations of tropical forest biology (eds Chazdon, R. & Whitmore, T.) 163–173 (University of Chicago Press, Chicago, IL, 2002).

Janzen DH. Why mountain passes are higher in the tropics. Am. Nat. 1967;101:233–249. doi: 10.1086/282487. DOI

Wahlberg N, et al. Nymphalid butterflies diversify following near demise at the Cretaceous/Tertiary boundary. Proc. R. Soc. B. 2009;276:4295–4302. doi: 10.1098/rspb.2009.1303. PubMed DOI PMC

Aduse-Poku K, et al. Systematics and historical biogeography of the old world butterfly subtribe Mycalesina (Lepidoptera: Nymphalidae: Satyrinae) BMC Evol. Biol. 2015;15:167. doi: 10.1186/s12862-015-0449-3. PubMed DOI PMC

Kozak KM, et al. Multilocus species trees show the recent adaptive radiation of the mimetic Heliconius butterflies. Syst. Biol. 2015;64:505–524. doi: 10.1093/sysbio/syv007. PubMed DOI PMC

Chazot N, et al. Renewed diversification following Miocene landscape turnover in a Neotropical butterfly radiation. Glob. Ecol. Biogeogr. 2019;28:1118–1132. doi: 10.1111/geb.12919. DOI

Chazot N, et al. Priors and posteriors in Bayesian timing of divergence analyses: the age of butterflies revisited. Syst. Biol. 2019;68:797–813. doi: 10.1093/sysbio/syz002. PubMed DOI PMC

Wahlberg N, Wheat CW, Peña C. Timing and patterns in the taxonomic diversification of Lepidoptera (Butterflies and Moths) PLoS ONE. 2013;8:e80875. doi: 10.1371/journal.pone.0080875. PubMed DOI PMC

Heikkilä M, Kaila L, Mutanen M, Peña C, Wahlberg N. Cretaceous origin and repeated tertiary diversification of the redefined butterflies. Proc. R. Soc. B. 2012;279:1093–1099. doi: 10.1098/rspb.2011.1430. PubMed DOI PMC

Condamine FL, Nabholz B, Clamens A-L, Dupuis JR, Sperling FAH. Mitochondrial phylogenomics, the origin of swallowtail butterflies, and the impact of the number of clocks in Bayesian molecular dating: mito-phylogenomics of swallowtail butterflies. Syst. Entomol. 2018;43:460–480. doi: 10.1111/syen.12284. DOI

Espeland M, et al. A comprehensive and dated phylogenomic analysis of butterflies. Curr. Biol. 2018;28:770–778. doi: 10.1016/j.cub.2018.01.061. PubMed DOI

Ree RH, Smith SA. Maximum likelihood inference of geographic range evolution by dispersal, local extinction, and cladogenesis. Syst. Biol. 2008;57:4–14. doi: 10.1080/10635150701883881. PubMed DOI

Crisp M, Cook L. Do early branching lineages signify ancestral traits? Trends Ecol. Evol. 2005;20:122–128. doi: 10.1016/j.tree.2004.11.010. PubMed DOI

Meseguer AS, Condamine FL. Ancient tropical extinctions at high latitudes contributed to the latitudinal diversity gradient*. Evolution. 2020;74:1966–1987. doi: 10.1111/evo.13967. PubMed DOI

Ziegler A, et al. Tracing the tropics across land and sea: Permian to present. Lethaia. 2003;36:227–254. doi: 10.1080/00241160310004657. DOI

Meng J, McKenna MC. Faunal turnovers of Palaeogene mammals from the Mongolian Plateau. Nature. 1998;394:364–367. doi: 10.1038/28603. DOI

Archibald SB, Bossert WH, Greenwood DR, Farrell BD. Seasonality, the latitudinal gradient of diversity, and Eocene insects. Paleobiology. 2010;36:374–398. doi: 10.1666/09021.1. DOI

Baker WJ, Couvreur TLP. Global biogeography and diversification of palms sheds light on the evolution of tropical lineages. I. Historical biogeography. J. Biogeogr. 2013;40:274–285. doi: 10.1111/j.1365-2699.2012.02795.x. DOI

Liu Z, et al. Global cooling during the Eocene-Oligocene climate transition. Science. 2009;323:1187–1190. doi: 10.1126/science.1166368. PubMed DOI

Eldrett JS, Greenwood DR, Harding IC, Huber M. Increased seasonality through the Eocene to Oligocene transition in northern high latitudes. Nature. 2009;459:969–973. doi: 10.1038/nature08069. PubMed DOI

Saupe EE, et al. Climatic shifts drove major contractions in avian latitudinal distributions throughout the Cenozoic. Proc. Natl Acad. Sci. USA. 2019;116:12895–12900. doi: 10.1073/pnas.1903866116. PubMed DOI PMC

Hawkins BA, DeVries PJ. Tropical niche conservatism and the species richness gradient of North American butterflies. J. Biogeogr. 2009;36:1698–1711. doi: 10.1111/j.1365-2699.2009.02119.x. DOI

Mayr G. Two-phase extinction of “Southern Hemispheric” birds in the Cenozoic of Europe and the origin of the Neotropic avifauna. Palaeobio. Palaeoenv. 2011;91:325–333. doi: 10.1007/s12549-011-0062-4. DOI

Veizer J, Prokoph A. Temperatures and oxygen isotopic composition of Phanerozoic oceans. Earth-Sci. Rev. 2015;146:92–104. doi: 10.1016/j.earscirev.2015.03.008. DOI

Zhang Z, et al. Aridification of the Sahara desert caused by Tethys Sea shrinkage during the Late Miocene. Nature. 2014;513:401–404. doi: 10.1038/nature13705. PubMed DOI

Feakins SJ, et al. Northeast African vegetation change over 12 m.y. Geology. 2013;41:295–298. doi: 10.1130/G33845.1. DOI

Jacobs BF. Palaeobotanical studies from tropical Africa: relevance to the evolution of forest, woodland and savannah biomes. Philos. Trans. R. Soc. Lond. B. 2004;359:1573–1583. doi: 10.1098/rstb.2004.1533. PubMed DOI PMC

Jaramillo C. Cenozoic plant diversity in the Neotropics. Science. 2006;311:1893–1896. doi: 10.1126/science.1121380. PubMed DOI

Stebbins, G. L. Flowering plants: evolution above the species level. (Harvard University Press, 1974). 10.4159/harvard.9780674864856.

Wahlberg N, Wheat CW. Genomic outposts serve the phylogenomic pioneers: designing novel nuclear markers for genomic DNA extractions of Lepidoptera. Syst. Biol. 2008;57:231–242. doi: 10.1080/10635150802033006. PubMed DOI

Philippe H, et al. Resolving difficult phylogenetic questions: why more sequences are not enough. PLoS Biol. 2011;9:e1000602. doi: 10.1371/journal.pbio.1000602. PubMed DOI PMC

Nee S. Birth-Death models in macroevolution. Annu. Rev. Ecol. Evol. Syst. 2006;37:1–17. doi: 10.1146/annurev.ecolsys.37.091305.110035. DOI

Ricklefs RE. Estimating diversification rates from phylogenetic information. Trends Ecol. Evol. 2007;22:601–610. doi: 10.1016/j.tree.2007.06.013. PubMed DOI

Crisp MD, Cook LG. Explosive radiation or cryptic mass extinction? Interpreting signatures in molecular phylogenies. Evolution. 2009;63:2257–2265. doi: 10.1111/j.1558-5646.2009.00728.x. PubMed DOI

Lambert A, Stadler T. Birth–death models and coalescent point processes: the shape and probability of reconstructed phylogenies. Theor. Popul. Biol. 2013;90:113–128. doi: 10.1016/j.tpb.2013.10.002. PubMed DOI

Rabosky DL. Extinction rates should not be estimated from molecular phylogenies: estimating extinction from molecular phylogenies. Evolution. 2010;64:1816–1824. doi: 10.1111/j.1558-5646.2009.00926.x. PubMed DOI

Quental TB, Marshall CR. Diversity dynamics: molecular phylogenies need the fossil record. Trends Ecol. Evol. 2010;25:434–441. doi: 10.1016/j.tree.2010.05.002. PubMed DOI

Burin G, Alencar LRV, Chang J, Alfaro ME, Quental TB. How well can we estimate diversity dynamics for clades in diversity decline? Syst. Biol. 2019;68:47–62. doi: 10.1093/sysbio/syy037. PubMed DOI

Louca S, Pennell MW. Extant timetrees are consistent with a myriad of diversification histories. Nature. 2020;580:502–505. doi: 10.1038/s41586-020-2176-1. PubMed DOI

Sohn J-C, Labandeira CC, Davis DR. The fossil record and taphonomy of butterflies and moths (Insecta, Lepidoptera): implications for evolutionary diversity and divergence-time estimates. BMC Evol. Biol. 2015;15:12. doi: 10.1186/s12862-015-0290-8. PubMed DOI PMC

de Jong R. Fossil butterflies, calibration points and the molecular clock (Lepidoptera: Papilionoidea) Zootaxa. 2017;4270:1. doi: 10.11646/zootaxa.4270.1.1. PubMed DOI

Edger PP, et al. The butterfly plant arms-race escalated by gene and genome duplications. Proc. Natl Acad. Sci. USA. 2015;112:8362–8366. doi: 10.1073/pnas.1503926112. PubMed DOI PMC

Allio R, et al. Genome-wide macroevolutionary signatures of key innovations in butterflies colonizing new host plants. Nat. Commun. 2021;12:354. doi: 10.1038/s41467-020-20507-3. PubMed DOI PMC

Stamatakis A. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics. 2014;30:1312–1313. doi: 10.1093/bioinformatics/btu033. PubMed DOI PMC

Drummond AJ, Suchard MA, Xie D, Rambaut A. Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol. Biol. Evol. 2012;29:1969–1973. doi: 10.1093/molbev/mss075. PubMed DOI PMC

Lanfear, R., Frandsen, P. B., Wright, A. M., Senfeld, T. & Calcott, B. PartitionFinder 2: new methods for selecting partitioned models of evolution for molecular and morphological phylogenetic analyses. Mol. Biol. Evol.34, 772–773. 10.1093/molbev/msw260 (2016). PubMed

Smith SA. Taking into account phylogenetic and divergence-time uncertainty in a parametric biogeographical analysis of the Northern Hemisphere plant clade Caprifolieae. J. Biogeogr. 2009;36:2324–2337. doi: 10.1111/j.1365-2699.2009.02160.x. DOI

Beeravolu Reddy, C. & Condamine, F. An extended maximum likelihood inference of geographic range evolution by dispersal, local extinction and cladogenesis. bioRxiv.10.1101/038695 (2016). PubMed

Rabosky DL. Automatic detection of key innovations, rate shifts, and diversity-dependence on phylogenetic trees. PLoS ONE. 2014;9:e89543. doi: 10.1371/journal.pone.0089543. PubMed DOI PMC

Rabosky DL, et al. BAMMtools: an R package for the analysis of evolutionary dynamics on phylogenetic trees. Methods Ecol. Evol. 2014;5:701–707. doi: 10.1111/2041-210X.12199. DOI

Rabosky DL, Mitchell JS, Chang J. Is BAMM flawed? theoretical and practical concerns in the analysis of multi-rate diversification models. Syst. Biol. 2017;66:477–498. doi: 10.1093/sysbio/syx037. PubMed DOI PMC

Dudas G, et al. Virus genomes reveal factors that spread and sustained the Ebola epidemic. Nature. 2017;544:309–315. doi: 10.1038/nature22040. PubMed DOI PMC

Morlon H, Parsons TL, Plotkin JB. Reconciling molecular phylogenies with the fossil record. Proc. Natl Acad. Sci. 2011;108:16327–16332. doi: 10.1073/pnas.1102543108. PubMed DOI PMC

Morlon H, et al. RPANDA: an R package for macroevolutionary analyses on phylogenetic trees. Methods Ecol. Evol. 2016;7:589–597. doi: 10.1111/2041-210X.12526. DOI

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...