Molecular Phylogeny of Cimicoidea (Heteroptera: Cimicomorpha) Revisited: Increased Taxon Sampling Reveals Evolution of Traumatic Insemination and Paragenitalia
Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic
Typ dokumentu časopisecké články
Grantová podpora
2018002270005
Korea Environment Industry & Technology Institute (KEITI) through Exotic Invasive Species Management Program, funded by Korea Ministry of Environment (MOE)
PubMed
36975952
PubMed Central
PMC10051671
DOI
10.3390/insects14030267
PII: insects14030267
Knihovny.cz E-zdroje
- Klíčová slova
- Cimicoidea, Heteroptera, evolution, paragenitalia, phylogeny, traumatic insemination,
- Publikační typ
- časopisecké články MeSH
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