Hidden diversity in the Brazilian Atlantic rainforest: the discovery of Jurasaidae, a new beetle family (Coleoptera, Elateroidea) with neotenic females
Jazyk angličtina Země Velká Británie, Anglie Médium electronic
Typ dokumentu časopisecké články, práce podpořená grantem
PubMed
32005908
PubMed Central
PMC6994542
DOI
10.1038/s41598-020-58416-6
PII: 10.1038/s41598-020-58416-6
Knihovny.cz E-zdroje
- MeSH
- brouci genetika MeSH
- deštný prales MeSH
- ekosystém MeSH
- fylogeneze MeSH
- genetická variace MeSH
- sekvenční analýza DNA MeSH
- zvířata MeSH
- Check Tag
- mužské pohlaví MeSH
- ženské pohlaví MeSH
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Geografické názvy
- Brazílie MeSH
Beetles are the most species-rich animal radiation and are among the historically most intensively studied insect groups. Consequently, the vast majority of their higher-level taxa had already been described about a century ago. In the 21st century, thus far, only three beetle families have been described de novo based on newly collected material. Here, we report the discovery of a completely new lineage of soft-bodied neotenic beetles from the Brazilian Atlantic rainforest, which is one of the most diverse and also most endangered biomes on the planet. We identified three species in two genera, which differ in morphology of all life stages and exhibit different degrees of neoteny in females. We provide a formal description of this lineage for which we propose the new family Jurasaidae. Molecular phylogeny recovered Jurasaidae within the basal grade in Elateroidea, sister to the well-sclerotized rare click beetles, Cerophytidae. This placement is supported by several larval characters including the modified mouthparts. The discovery of a new beetle family, which is due to the limited dispersal capability and cryptic lifestyle of its wingless females bound to long-term stable habitats, highlights the importance of the Brazilian Atlantic rainforest as a top priority area for nature conservation.
Museu de Zoologia Universidade de São Paulo Avenida Nazaré 481 04263 000 São Paulo SP Brazil
Senckenberg Deutsches Entomologisches Institut Eberswalder Strasse 90 15374 Müncheberg Germany
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Ślipiński, S. A., Leschen, R. A. B., Lawrence, J. F. Order Coleoptera Linnaeus, 1758 in Animal Biodiversity: An Outline of Higher-Level Classification and Survey of Taxonomic Richness (ed. Zhang, Z. Q.). Zootaxa3148, 203–208 (2011). PubMed
Lord NP, et al. Phylogenetic analysis of the minute brown scavenger beetles (Coleoptera: Latridiidae), and recognition of a new beetle family, Akalyptoischiidae fam.n. (Coleoptera: Cucujoidea) Syst. Entomol. 2010;35:753–763. doi: 10.1111/j.1365-3113.2010.00532.x. DOI
Robertson JA, et al. Phylogeny and classification of Cucujoidea and the recognition of a new superfamily Coccinelloidea (Coleoptera: Cucujiformia) Syst. Entomol. 2015;40:745–778. doi: 10.1111/syen.12138. DOI
Shin S, et al. Phylogenomic data yield new and robust insights into the phylogeny and evolution of weevils. Mol. Biol. Evol. 2018;35:823–836. doi: 10.1093/molbev/msx324. PubMed DOI
Gimmel ML, Bocakova M, Gunter NL, Leschen RAB. Comprehensive phylogeny of the Cleroidea (Coleoptera: Cucujiformia) Syst. Entomol. 2019;44:527–558. doi: 10.1111/syen.12338. DOI
Ribera I, Beutel RG, Balke M, Vogler AP. Discovery of Aspidytidae, a new family of aquatic Coleoptera. Proc. R. Soc. B. 2002;269:2351–2356. doi: 10.1098/rspb.2002.2157. PubMed DOI PMC
Balke, M., Ribera, I. & Beutel, R. G. Aspidytidae: on the discovery of a new family of beetles and a key to fossil and extant adephagan families in Water Beetles of China, Vol. III (ed. Jäch, M. A. & Ji, L.) 53–66 (Zoologisch-Botanische Gesellschaft in Österreich and Wiener Coleopterologenverein 2003).
Spangler PJ, Steiner WE. A new aquatic beetle family, Meruidae, from Venezuela (Coleoptera: Adephaga) Syst. Entomol. 2005;30:339–357. doi: 10.1111/j.1365-3113.2005.00288.x. DOI
Bocak L, Kundrata R, Andújar-Fernández C, Vogler AP. The discovery of Iberobaeniidae (Coleoptera: Elateroidea), a new family of beetles from Spain, with immatures detected by environmental DNA sequencing. Proc. R. Soc. B. 2016;283:20152350. doi: 10.1098/rspb.2015.2350. PubMed DOI PMC
Kundrata R, Baena M, Bocak L. Iberobaenia andujari sp. nov., the third species of Iberobaeniidae (Coleoptera: Elateroidea) from southern Spain. Ann Zool. 2017;67:121–129. doi: 10.3161/00034541ANZ2017.67.1.014. DOI
McKenna DD, et al. The beetle tree of life reveals that Coleoptera survived end-Permian mass extinction to diversify during the Cretaceous terrestrial revolution. Syst. Entomol. 2015;40:835–880. doi: 10.1111/syen.12132. DOI
Zhang SQ, et al. Evolutionary history of Coleoptera revealed by extensive sampling of genes and species. Nat. Comm. 2018;9:205. doi: 10.1038/s41467-017-02644-4. PubMed DOI PMC
Kundrata R, Bocakova M, Bocak L. The comprehensive phylogeny of the superfamily Elateroidea (Coleoptera: Elateriformia) Mol. Phylogenet. Evol. 2014;76:162–171. doi: 10.1016/j.ympev.2014.03.012. PubMed DOI
Bocak L, Motyka M, Bocek M, Bocakova M. Incomplete sclerotization and phylogeny: The phylogenetic classification of Plastocerus (Coleoptera: Elateroidea) PLoS One. 2018;13:e0194026. doi: 10.1371/journal.pone.0194026. PubMed DOI PMC
Kusy D, et al. Genome sequencing of Rhinorhipus Lawrence exposes an early branch of the Coleoptera. Front. Zool. 2018;15:21. doi: 10.1186/s12983-018-0262-0. PubMed DOI PMC
Kusy D, Motyka M, Bocek M, Vogler AP, Bocak L. Genome sequences identify three families of Coleoptera as morphologically derived click beetles (Elateridae) Sci. Rep. 2018;8:17084. doi: 10.1038/s41598-018-35328-0. PubMed DOI PMC
Lawrence JF. Rhinorhipidae, a new beetle family from Australia, with comments on the phylogeny of the Elateriformia. Invertebr. Taxon. 1988;2:1–53. doi: 10.1071/IT9880001. DOI
Gould SJ. Ontogeny and Phylogeny. Cambridge: Harvard University Press; 1977.
Cicero JM. Ontophylogenetics of cantharoid larviforms (Coleoptera: Cantharoidea) Coleopt. Bull. 1988;42:105–151.
Bocak L, Bocakova M, Hunt T, Vogler AP. Multiple ancient origins of neoteny in Lycidae (Coleoptera): consequences for ecology and macroevolution. Proc. R. Soc. B. 2008;275:2015–2023. doi: 10.1098/rspb.2008.0476. PubMed DOI PMC
Crowson RA. A review of the classification of Cantharoidea (Coleoptera), with the definition of two new families Cneoglossidae and Omethidae. Rev. Univ. Madrid. 1972;21:35–77.
Bocakova M, Bocak L, Hunt T, Teraväinen M, Vogler AP. Molecular phylogenetics of Elateriformia (Coleoptera): evolution of bioluminescence and neoteny. Cladistics. 2007;23:477–496. doi: 10.1111/j.1096-0031.2007.00164.x. DOI
Kundrata R, Bocak L. The phylogeny and limits of Elateridae (Insecta, Coleoptera): is there a common tendency of click beetles to soft-bodiedness and neoteny? Zool. Scr. 2011;40:364–378. doi: 10.1111/j.1463-6409.2011.00476.x. DOI
Myers N, Mittermeier RA, Mittermeier CG, da Fonseca GAB, Kent J. Biodiversity hotspots for conservation priorities. Nature. 2000;403:853–885. doi: 10.1038/35002501. PubMed DOI
Ribeiro MC, Metzger JP, Martensen AC, Ponzoni FJ, Hirota MM. The Brazilian Atlantic Forest: how much is left, and how is the remaining forest distributed? Implications for conservation. Biol. Conserv. 2009;142:1141–1153. doi: 10.1016/j.biocon.2009.02.021. DOI
Dias, D. S., Rosa, S. P. & Silveira, L. F. L. Diversidade de vagalumes Lampyridae (Coleoptera) da Reserva Biológica Municipal da Serra dos Toledos, Itajubá-MG in Caderno de Resumos da XXIV Jornada de Iniciação Científica da UNIFEI (ed. Canuto, J. G.) 699–701 (Universidade Federal de Itajubá 2017).
Amaral DT, Mitani Y, Ohmiya Y, Viviani VR. Organization and comparative analysis of the mitochondrial genomes of bioluminescent Elateroidea (Coleoptera: Polyphaga) Gene. 2016;586:254–262. doi: 10.1016/j.gene.2016.04.009. PubMed DOI
Fallon TR, et al. Firefly genomes illuminate parallel origins of bioluminescence in beetles. eLife. 2018;7:e36495. doi: 10.7554/eLife.36495. PubMed DOI PMC
Kundrata R, Bocak L. Molecular phylogeny reveals the gradual evolutionary transition to soft-bodiedness in click-beetles and identifies Sub-Saharan Africa as a cradle of diversity for Drilini (Coleoptera: Elateridae) Zool. J. Linn. Soc. 2019;187:413–452. doi: 10.1093/zoolinnean/zlz033. DOI
Zaragoza-Caballero S, Zurita-García ML. A preliminary study on the phylogeny of the family Phengodidae (Insecta: Coleoptera) Zootaxa. 2015;3947:527–542. doi: 10.11646/zootaxa.3947.4.4. PubMed DOI
Rosa, S. P., Costa C. & Lopes, A. C. C. Discovery of a new genus and species of Penicillophorinae (Phengodidae) from Southeastern Brazil: description of larva, pupa, neotenic female and male in Abstracts of the Immature Beetles Meeting 2017 October 5−6, Prague, Czech Republic (ed. Seidel, M., Arriaga-Varela, E. & Vondráček, D.). Acta Entomol. Mus. Nat. Pragae57, 852–853 (2017).
Beutel RG. Phylogenetic analysis of Elateriformia (Coleoptera: Polyphaga) based on larval characters. J. Zool. Syst. Evol. Res. 1995;33:145–171. doi: 10.1111/j.1439-0469.1995.tb00222.x. DOI
Lawrence JF, et al. Phylogeny of the Coleoptera based on morphological characters of adults and larvae. Ann. Zool. 2011;61:1–217. doi: 10.3161/000345411X576725. DOI
Kawashima, I., Lawrence, J. F. & Branham, M. A. Rhagophthalmidae Olivier, 1907 in Coleoptera, Beetles; Volume 2: Morphology and Systematics (Elateroidea, Bostrichiformia, Cucujiformia partim) (eds. Leschen, R. A. B., Beutel, R. G. & Lawrence, J. F) in Handbook of Zoology, Arthropoda: Insecta (eds. Kristensen, N. P. & Beutel, R. G.) 135–140 (Berlin/New York: Walter de Gruyter GmbH & Co. 2010).
Malohlava V, Bocak L. Evidence of extreme habitat stability in a Southeast Asian biodiversity hotspot based on the evolutionary analysis of neotenic net-winged beetles. Mol. Ecol. 2010;19:4800–4811. doi: 10.1111/j.1365-294X.2010.04850.x. PubMed DOI
Bray TC, Bocak L. Slowly dispersing neotenic beetles can speciate on a penny coin and generate space-limited diversity in the tropical mountains. Sci. Rep. 2016;6:33579. doi: 10.1038/srep33579. PubMed DOI PMC
Mateos, E., Guix, J. C., Serra, A. & Pisciotta, K. Censuses of vertebrates in a Brazilian Atlantic rainforest area: The Paranapiacaba fragment. Centre de Recursos de Biodiversitat Animal Divisió III, Universitat de Barcelona (2002).
Mittermeier, R. A. et al. Hotspots revisited: Earth’s biologically richest and most endangered terrestrial ecoregions. CEMEX/Agrupación Sierra Madre, Mexico City (2004).
Pie MR, Faircloth BC, Ribeiro LF, Bornschein MR, Mccormack JE. Phylogenomics of montane frogs of the Brazilian Atlantic Forest is consistent with isolation in sky islands followed by climatic stability. Biol. J. Linn. Soc. 2018;125:72–82.
Paviolo A, et al. A biodiversity hotspot losing its top predator: The challenge of jaguar conservation in the Atlantic Forest of South America. Sci. Rep. 2016;6:37147. doi: 10.1038/srep37147. PubMed DOI PMC
Morellato LPC, Haddad CFB. Introduction: The Brazilian Atlantic Forest. Biotropica. 2000;32:786–792. doi: 10.1111/j.1744-7429.2000.tb00618.x. DOI
Joly CA, Metzger JP, Tabarelli M. Experiences from the Brazilian Atlantic Forest: ecological findings and conservation initiatives. New Phytol. 2014;204:459–473. doi: 10.1111/nph.12989. PubMed DOI
Bornschein MR, et al. Three new species of phytotelm-breeding Melanophryniscus from the Atlantic Rainforest of southern Brazil (Anura: Bufonidae) PLoS One. 2015;10:e0142791. doi: 10.1371/journal.pone.0142791. PubMed DOI PMC
Lourenço-de-Moraes R, et al. Diversity of miniaturized frogs of the genus Adelophryne (Anura: Eleutherodactylidae): A new species from the Atlantic Forest of northeast Brazil. PLoS One. 2018;13:e0201781. doi: 10.1371/journal.pone.0201781. PubMed DOI PMC
Maciel AO, et al. Phylogenetic systematics of the Neotropical caecilian amphibian Luetkenotyphlus (Gymnophiona: Siphonopidae) including the description of a new species from the vulnerable Brazilian Atlantic Forest. Zool. Anz. 2019;281:76–83. doi: 10.1016/j.jcz.2019.07.001. DOI
Cezar LA, Fisher EM, Lamas CJ. Four new species of Oidardis Hermann, 1912 (Diptera, Asilidae, Laphriinae, Atomosiini) from two major faunistic surveys in the Atlantic Rainforest. ZooKeys. 2013;350:47–74. doi: 10.3897/zookeys.350.6096. PubMed DOI PMC
Magalhaes ILF, Fernandes LR, Ramirez MJ, Bonaldo AB. Phylogenetic position and taxonomic review of the Ianduba spiders (Araneae: Corinnidae) endemic to the Brazilian Atlantic rainforest. Arthropod Syst. Phyl. 2016;74:127–159.
Silveira L, et al. Integrative taxonomy of new firefly taxa from the Atlantic Rainforest. Syst. Biodivers. 2016;14:371–384. doi: 10.1080/14772000.2016.1153006. DOI
Roza AS, Quintino HYS, Mermudes JRM, Silveira LFL. Akamboja gen. nov., a new genus of railroad-worm beetle endemic to the Atlantic Rainforest, with five new species (Coleoptera: Phengodidae, Mastinocerinae) Zootaxa. 2017;4306:501–523. doi: 10.11646/zootaxa.4306.4.3. DOI
Campello-Gonçalves L, Souto PM, Mermudes JRM, Silveira LFL. Uanauna gen. nov., a new genus of fireflies endemic to the Brazilian Atlantic forest (Coleoptera: Lampyridae), with key to brazilian genera of Lucidotina. Zootaxa. 2019;4585:59–72. doi: 10.11646/zootaxa.4585.1.4. PubMed DOI
Falaschi RL, et al. Neoceroplatus betaryiensis nov. sp. (Diptera: Keroplatidae) is the first record of a bioluminescent fungus-gnat in South America. Sci. Rep. 2019;9:11291. doi: 10.1038/s41598-019-47753-w. PubMed DOI PMC
Melloni R, Guida EC, Andrade MR, Melloni EGP. Fungos micorrízicos arbusculares em solos da Reserva Biológica Municipal Serra dos Toledos, Itajubá/MG. Ciência Flor. 2011;21:799–809.
ICMBIO. Plano de manejo do Parque Nacional da Serra dos Orgãos. Instituto Chico Mendes de Conservacão da Biodiversidade, Portaria ICMBio, Brasília (2008).
Kundrata R, et al. One less mystery in Coleoptera systematics: the position of Cydistinae (Elateriformia incertae sedis) resolved by multigene phylogenetic analysis. Zool. J. Linn. Soc. 2019 doi: 10.1093/zoolinnean/zlz104. DOI
Hunt T, et al. A comprehensive phylogeny of beetles reveals the evolutionary origins of a superradiation. Science. 2007;318:1913–1916. doi: 10.1126/science.1146954. PubMed DOI
Kundrata R, Jäch MA, Bocak L. Molecular phylogeny of the Byrrhoidea-Buprestoidea complex (Coleoptera, Elateriformia) Zool. Scr. 2017;46:150–164. doi: 10.1111/zsc.12196. DOI
Kearse M, et al. Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics. 2012;28:1647–1649. doi: 10.1093/bioinformatics/bts199. PubMed DOI PMC
Katoh K, Standley DM. MAFFT Multiple sequence alignment software version 7: improvements in performance and usability. Mol. Biol. Evol. 2013;30:772–780. doi: 10.1093/molbev/mst010. PubMed DOI PMC
Tamura K, Stecher G, Peterson D, Filipski A, Kumar S. MEGA6: Molecular evolutionary genetics analysis version 6.0. Mol. Biol. Evol. 2013;30:2725–2729. doi: 10.1093/molbev/mst197. PubMed DOI PMC
Lanfear R, Calcott B, Ho SYW, Guindon S. PartitionFinder: combined selection of partitioning schemes and substitution models for phylogenetic analyses. Mol. Biol. Evol. 2012;29:1695–1701. doi: 10.1093/molbev/mss020. PubMed DOI
Stamatakis A. RAxML-VI-HPC: Maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics. 2006;22:2688–2690. doi: 10.1093/bioinformatics/btl446. PubMed DOI
Stamatakis A, Hoover P, Rougemont J. A rapid bootstrap algorithm for the RAxML web servers. Syst. Biol. 2008;57:758–771. doi: 10.1080/10635150802429642. PubMed DOI
Huelsenbeck JP, Ronquist F. MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics. 2001;17:754–755. doi: 10.1093/bioinformatics/17.8.754. PubMed DOI
Rambaut A, Drummond AJ, Xie D, Baele G, Suchard MA. Posterior summarization in Bayesian phylogenetics using Tracer 1.7. Syst. Biol. 2018;67:901–904. doi: 10.1093/sysbio/syy032. PubMed DOI PMC
Miller, M. A., Pfeiffer, W. & Schwartz, T. Creating the CIPRES Science Gateway for inference of large phylogenetic trees in Proceedings of the Gateway Computing Environments Workshop (GCE), 14 Nov. 2010. New Orleans, LA (2010).
Xia X, Xie Z, Salemi M, Chen L, Wang Y. An index of substitution saturation and its application. Mol. Phylogenet. Evol. 2003;26:1–7. doi: 10.1016/S1055-7903(02)00326-3. PubMed DOI
Xia, X. & Lemey, P. Assessing substitution saturation with DAMBE in The Phylogenetic Handbook: A Practical Approach to DNA and Protein Phylogeny, 2nd Edition (eds. Lemey, P., Salemi, M. & Vandamme, A. M.) 615–630 (Cambridge: Cambridge University Press, 2009).
Lawrence, J. F., Beutel, R. G., Leschen, R. A. B. & Ślipiński, S. A. Glossary of morphological terms in Coleoptera, Beetles; Volume 2: Morphology and Systematics (Elateroidea, Bostrichiformia, Cucujiformia partim) (eds. Leschen, R. A. B., Beutel, R. G. & Lawrence, J. F) in Handbook of Zoology, Arthropoda: Insecta (eds. Kristensen, N. P. & Beutel, R. G.) 9–20 (Berlin/New York: Walter de Gruyter GmbH & Co., 2010).
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