Molecular Phylogeny of Cimicoidea (Heteroptera: Cimicomorpha) Revisited: Increased Taxon Sampling Reveals Evolution of Traumatic Insemination and Paragenitalia

. 2023 Mar 08 ; 14 (3) : . [epub] 20230308

Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid36975952

Grantová podpora
2018002270005 Korea Environment Industry & Technology Institute (KEITI) through Exotic Invasive Species Management Program, funded by Korea Ministry of Environment (MOE)

The molecular phylogeny of the Cimicoidea was reconstructed from an expanded sampling based on mitochondrial (16S, COI) and nuclear (18S, 28SD3) genes. The data were analyzed using maximum likelihood (ML), maximum parsimony (MP), and Bayesian inference (BI) phylogenetic frameworks. The phylogenetic relationships inferred by the model-based analyses (ML and BI) were largely congruent with those inferred by the MP analysis in terms of the monophyly of most of the higher taxonomic groups and the species-level relationships. The following clades were recovered in all analyses: Cimiciformes; Nabidae: Prostemmatinae; Nabidae: Nabinae; Plokiophilidae; Microphysidae; Lasiochilidae; Cimicidae: Cacodminae; Cimicidae; Lyctocoridae; Anthocoridae s. str.; Cardiastethini excluding Amphiareus; Almeidini; Scolopini; Anthocorini; Oriini; Curaliidae + Lasiochilidae; Almeidini + Xylocorini; Oriini + Cardiastethini; and Anthocorini + Amphiareus. Reconstructions of ancestral copulation states based on Bayesian and parsimony inference indicated that at least one shift from standard insemination (SI) to traumatic insemination (TI) occurred within Cimicoidea, and an investigation of the evolutionary correlation between TI and paragenitalia (PG) revealed that the acquisition of PG in cimicoid females was correlated with the TI habit. Additionally, our morphological examination of various types of PG suggested that even the same PG type may not constitute a homologous feature at various taxonomic levels, indicating the convergent evolution of female morphology to adapt to TI.

Zobrazit více v PubMed

Schuh R.T., Slater J.A. True Bugs of the World (Hemiptera: Heteroptera), Classification and Natural History. Comstock Publishing Associates, Cornell University Press; Ithaca, NY, USA: London, UK: 1995.

Schuh R.T., Weirauch C., Wheeler W.C. Phylogenetic relationships within the Cimicomorpha (Hemiptera: Heteroptera): A total-evidence analysis. Syst. Entomol. 2009;34:15–48. doi: 10.1111/j.1365-3113.2008.00436.x. DOI

Jung S., Kim H., Yamada K., Lee S. Molecular phylogeny and evolutionary habitat transition of the flower bugs (Heteroptera: Anthocoridae) Mol. Phylogenet. Evol. 2010;57:1173–1183. doi: 10.1016/j.ympev.2010.09.013. PubMed DOI

Usinger R.L. Monograph of the Cimicidae (Hemiptera–Heteroptera) Entomological Society of America; College Park, MD, USA: 1966.

Weirauch C., Schuh R.T. Systematics and evolution of Heteroptera: 25 Years of Progress. Annu. Rev. Entomol. 2011;56:487–510. doi: 10.1146/annurev-ento-120709-144833. PubMed DOI

Ford L.J. Master’s Thesis. University of Connecticut; Storrs, CT, USA: 1979. The Phylogeny and Biogeography of the Cimicoidea (Insecta, Hemiptera)

Schuh R.T., Štys P. Phylogenetic analysis of cimicomorphan family relationships (Heteroptera) J. N.Y. Entomol. Soc. 1991;99:298–350.

Carayon J. Insemination traumatique heterosexuelle et homosexuelle chez Xylocoris maculipennis (Hemiptera: Anthocoridae) C. R. Acad. Sci. 1974;278:2803–2806.

Carayon J. Insémination extra-génitale traumatique. In: Grassé P.P., editor. Traité de Zoologie. Volume 8. Masson; Paris, France: 1977. pp. 351–390.

Arnqvist G., Rowe L. Sexual Conflict. Monographs in Behaviour and Ecology. Princeton University Press; Princeton, NJ, USA: 2005.

Reinhardt K., Siva-Jothy M.T. Biology of the Bed Bugs (Cimicidae) Annu. Rev. Entomol. 2006;52:151–374. doi: 10.1146/annurev.ento.52.040306.133913. PubMed DOI

Abele L.G., Gilchrist S. Homosexual rape and sexual selection in acanthocephalan worms. Science. 1977;197:81–83. doi: 10.1126/science.867055. PubMed DOI

Reinhardt K., Harney E., Naylor R., Gorb S., Siva-Jothy M.T. Female-Limited Polymorphism in the Copulatory Organ of a Traumatically Inseminating Insect. Am. Nat. 2007;170:931–935. doi: 10.1086/522844. PubMed DOI

Lange R., Reinhardt K., Michiels N.K., Anthes N. Functions, diversity, and evolution of traumatic mating. Biol. Rev. 2013;88:585–601. doi: 10.1111/brv.12018. PubMed DOI

Carayon J. Traumatic insemination and the paragenital system. In: Usinger R.L., editor. Monograph of Cimicidae (Hemiptera, Heteroptera) Entomological Society of America; College Park, MD, USA: 1966. pp. 81–166.

Tatarnic N.J., Cassis G., Hochuli D.F. Traumatic insemination in the plant bug genus Coridromius Signoret (Heteroptera: Miridae) Biol. Lett. 2006;2:58–61. doi: 10.1098/rsbl.2005.0394. PubMed DOI PMC

Yamada K. Blaptostethus aurivillus, a new flower bug (Heteroptera, Anthocoridae) from West Malaysia. Jpn. J. Syst. Entomol. 2008;14:7–11.

Yamada K., Hirowatari T. Two new species of the flower bug genus Scoloposcelis (Insecta: Heteroptera: Anthocoridae) from Japan. Species Divers. 2005;10:125–133. doi: 10.12782/specdiv.10.125. DOI

Yamada K., Yasunaga T., Nakatani Y., Hirowatari T. The minute pirate-bug genus Xylocoris dufour (Hemiptera: Heteroptera: Anthocoridae) from rice mills in Thailand. Proc. Entomol. Soc. Wash. 2006;108:525–533.

Yamada K., Yasunaga T. Species of the minute pirate bug genus Buchananiella Reuter from Thailand (Heteroptera: Anthocoridae) Nouv. Rev. Entomol. 2009;25:273–280.

Carayon J. Insémination par ‘spermalège’ et cordon conducteur de spermatozoids chez Stricticimex brevispinosus Usinger (Heteroptera, Cimicidae) Rev. Zool. Bot. Afr. 1959;60:81–104.

Reinhardt K., Naylor R., Siva–Jothy M.T. Reducing a cost of traumatic insemination: Female bedbugs evolve a unique organ. Proc. R. Soc. B Biol. Sci. 2003;270:2371–2375. doi: 10.1098/rspb.2003.2515. PubMed DOI PMC

Horton D.R., Lewis T.M. Variation in male and female genitalia among ten species of North American Anthocoris (Hemiptera: Heteroptera: Anthocoridae) Ann. Entomol. Soc. Am. 2011;104:1260–1278. doi: 10.1603/AN11087. DOI

Jung S., Lee S. Systematic and phylogenetic study of the Korean Orius species based on morphological and molecular data (Heteroptera: Anthocoridae) Appl. Entomol. Zool. 2011;46:153–164. doi: 10.1007/s13355-011-0024-3. DOI

Jung S., Lee S. Taxonomic review of the genus Amphiareus (Heteroptera: Anthocoridae) in the Korean Peninsula. J. Asia Pac. Entomol. 2011;14:335–340. doi: 10.1016/j.aspen.2011.04.005. DOI

Jung S., Lee S. Two new records of the tribe Cardiastethini (Hemiptera: Heteroptera: Anthocoridae) from the Korean Peninsula. Zootaxa. 2011;2931:59–64. doi: 10.11646/zootaxa.2931.1.5. DOI

Jung S., Yamada K., Lee S. A new species of Scoloposcelis Fieber (Hemiptera: Heteroptera: Anthocoridae: Scolopini) from the Korean Peninsula, with a key to the Palaearctic species. Zootaxa. 2011;2766:64–68.

Jung S., Yasunaga T., Lee S. Taxonomic review of the genus Orius (Heteroptera: Anthocoridae) in the Korean Peninsula. J. Asia Pac. Entomol. 2011;14:64–74. doi: 10.1016/j.aspen.2010.11.014. DOI

Jung S., Duwal R.K., Lee S. COI barcoding of true bugs (Insecta, Heteroptera) Mol. Ecol. Resour. 2011;11:266–270. doi: 10.1111/j.1755-0998.2010.02945.x. PubMed DOI

Jung S., Lee S. Correlated evolution and Bayesian divergence time estimates of the Cimicoidea (Heteroptera: Cimicomorpha) reveal the evolutionary history. Syst. Entomol. 2012;37:22–31. doi: 10.1111/j.1365-3113.2011.00596.x. DOI

Jung S., Lee S. Molecular phylogeny of the plant bugs (Heteroptera: Miridae) and the evolution of feeding habits. Cladistics. 2012;28:50–79. doi: 10.1111/j.1096-0031.2011.00365.x. PubMed DOI

Folmer O., Black M., Hoeh W., Lutz R., Vrijenhoek R. DNA primer for ampllification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol. Mar. Biol. Biotechnol. 1994;3:294–299. PubMed

Campbell B.C., Ross G.F., Woodward T.E. Paraphyly of Homoptera and Auchenorrhyncha inferred from 18S rDNA nucleotide sequences. Syst. Entomol. 1995;20:175–194. doi: 10.1111/j.1365-3113.1995.tb00090.x. DOI

Hillis D.M., Dixon M.T. Ribosomal DNA: Molecular evolution and phylogenetic inference. Q. Rev. Biol. 1991;66:411–453. doi: 10.1086/417338. PubMed DOI

Simon C., Frati F., Beckenbach A., Crespi B., Liu H., Flook P. Evolution, weighting, and phylogenetic utility of mitochondrial gene sequences and a compilation of conserved polymerase chain reaction primers. Ann. Entomol. Soc. Am. 1994;87:651–701. doi: 10.1093/aesa/87.6.651. DOI

Kambhampati S., Smith P.T. PCR primers for the amplification of four insect mitochondrial gene fragments. Insect Mol. Biol. 1995;4:233–236. doi: 10.1111/j.1365-2583.1995.tb00028.x. PubMed DOI

Rambaut A. Se–Al. Sequence Alignment Editor. University of Oxford, Department of Zoology; Oxford, UK: 2002. [(accessed on 8 December 2022)]. Version 2.0 Alpha 11. Available online: http://tree.bio.ed.ac.uk/software/seal/

Katoh K., Misawa K., Kuma K., Miyata T. MAFFT: A novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res. 2002;30:3059–3066. doi: 10.1093/nar/gkf436. PubMed DOI PMC

Katoh K., Kuma K., Toh H., Miyata T. MAFFT version 5: Improvement in accuracy of multiple sequence alignment. Nucleic Acids Res. 2005;33:511–518. doi: 10.1093/nar/gki198. PubMed DOI PMC

Katoh K., Asimenos G., Toh H. Multiple alignment of DNA sequences with MAFFT. In: Pasada D., editor. Bioinformatics for DNA Sequence Analysis. Humana Press; New York, NY, USA: 2009. pp. 39–64. PubMed

Castresana J. Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol. Biol. Evol. 2000;17:540–552. doi: 10.1093/oxfordjournals.molbev.a026334. PubMed DOI

Maddison D.R., Maddison W.P. MacClade 4: Analysis of Phylogeny and Character Evolution. Sinauer Associates; Sunderland, MA, USA: 2000.

Farris J.S., Källersjö M., Kluge A.G., Bult C. Testing significance of incongruence. Cladistics. 1994;10:315–319. doi: 10.1111/j.1096-0031.1994.tb00181.x. DOI

Swofford D.L. PAUP*: Phylogenetic Analysis Using Parsimony (*and Other Methods). (Version 4.0b10) Sinauer Associates; Sunderland, MA, USA: 2002.

Goloboff P.A., Farris J.S., Nixon K.C. TNT, a free program for phylogenetic analysis. Cladistics. 2008;24:774–786. doi: 10.1111/j.1096-0031.2008.00217.x. DOI

Goloboff P.A. Analyzing large data sets in reasonable times, solutions for composite optima. Cladistics. 1999;15:415–428. doi: 10.1111/j.1096-0031.1999.tb00278.x. PubMed DOI

Nixon K.C. The Parsimony Ratchet, a new method for rapid parsimony analysis. Cladistics. 1999;15:407–414. doi: 10.1111/j.1096-0031.1999.tb00277.x. PubMed DOI

Posada D., Crandall K.A. MODELTEST: Testing the model of DNA substitution. Bioinformatics. 1998;14:817–818. doi: 10.1093/bioinformatics/14.9.817. PubMed DOI

Ronquist F., Huelsenbeck J.P. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics. 2003;19:1572–1574. doi: 10.1093/bioinformatics/btg180. 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

Schuh R.T., Weirauch C., Henry T.J., Halbert S.E. Curaliidae, a new family of Heteroptera (Insecta: Hemiptera) from the eastern United States. Ann. Entomol. Soc. Am. 2008;101:20–29. doi: 10.1603/0013-8746(2008)101[20:CANFOH]2.0.CO;2. DOI

Schuh R.T. Heissophila macrotheleae, a new genus and new species of Plokiophilidae from Thailand (Hemiptera, Heteroptera), with comments on the family diagnosis. Denisia. 2006;19:637–645.

Pagel M., Meade A. BaysTrait Version 2.0–Draft Manual. [(accessed on 8 December 2022)]. Available online: http://www.evolution.reading.ac.uk/BayesTraitsV2.html.

Pagel M. Detecting correlated evolution on phylogenies: A general method for the comparative analysis of discrete characters. Proc. R. Soc. B Biol. Sci. 1994;255:37–45.

Pagel M., Meade A. Bayesian analysis of correlated evolution of discrete characters by reversible–jump Markov chain Monte Carlo. Am. Nat. 2006;167:808–825. doi: 10.1086/503444. PubMed DOI

Maddison D.R., Maddison W.P. Mesquite: A Modular System for Evolutionary Analysis. (Version 2.6) [(accessed on 8 December 2022)]. Available online: http://mesquiteproject.org.

Carayon J. Caractères systématiques et classification des Anthocoridae (Hemipt.) Ann. Soc. Entomol. Fr. 1972;7:737–770.

Barker D., Pagel M. Predicting functional gene links from phylogenetic-statistical analyses of whole genomes. PLoS Comput. Biol. 2005;1:24–31. doi: 10.1371/journal.pcbi.0010003. PubMed DOI PMC

Kim J., Roca-Cusachs M., Jung S. Molecular phylogeny of Nabidae (Hemiptera: Heteroptera: Cimicomorpha): Insight into relationships and reclassification with the proposal of the new tribe Stenonabini. Syst. Entomol. 2022;47:1–12. doi: 10.1111/syen.12512. DOI

Štys P., Kerzhner I.M. Rank and nomenclature of higher taxa in recent Heteroptera. Act. Entomol. Bohemos. 1975;72:65–79.

Cassis G., Gross G.F. Hemiptera: Heteroptera (Coleorrhyncha to Cimicomorpha) In: Houston W.W.K., Maynard G.V., editors. Zoological Catalogue of Australia. Volume 37 CSIRO; Melbourne, Australia: 1995.

Péricart J. Family Anthocoridae fieber, 1836-flower bugs, minute pirate bugs. In: Aukema B., Rieger C., editors. Catalogue of the Heteroptera of the Palaearctic Region. Vol. 2. Cimicomorpha I. Volume 2. The Netherlands Entomological Society; Amsterdam, The Netherlands: 1996. pp. 108–140.

Schuh R.T., Weirauch C. True Bugs of the World (Hemiptera: Heteroptera): Classification and Natural History. 2nd ed. Siri Scientific Press; Manchester, UK: 2020.

Tatarnic N.J., Cassis G. Sexual coevolution in the traumatically inseminating plant bug genus Coridromius. J. Evol. Biol. 2010;23:1321–1326. doi: 10.1111/j.1420-9101.2010.01991.x. PubMed DOI

Najít záznam

Citační ukazatele

Pouze přihlášení uživatelé

Možnosti archivace

Nahrávání dat ...