Invertebrate Systematics Invertebrate Systematics Society
Systematics, phylogeny and biogeography
RESEARCH ARTICLE

A complete species phylogeny of the marine midge Pontomyia (Diptera : Chironomidae) reveals a cosmopolitan species and a new synonym

Danwei Huang A B C E , Peter S. Cranston D and Lanna Cheng B
+ Author Affliations
- Author Affliations

A Department of Earth and Environmental Sciences, University of Iowa, Iowa City, IA 52242, USA.

B Scripps Institution of Oceanography, University of California, San Diego, La Jolla, CA 92093, USA.

C Department of Biological Sciences, National University of Singapore, Singapore 117543, Singapore.

D Evolution, Ecology and Genetics, Research School of Biology, The Australian National University, Canberra ACT 0200, Australia.

E Corresponding author. Email: huangdanwei@nus.edu.sg

Invertebrate Systematics 28(3) 277-286 https://doi.org/10.1071/IS13059
Submitted: 23 November 2013  Accepted: 4 February 2014   Published: 30 June 2014

Abstract

Pontomyia (Diptera : Chironomidae) is an exclusively marine and flightless insect genus with four described species from the Indo-Pacific and one undescribed taxon known only by its larvae, pupal skins and females from the western Atlantic. A previous study of relationships among three of the Indo-Pacific species reported each of them to be monophyletic, with high genetic diversity within P. natans Edwards, 1926, the type species, and P. pacifica Tokunaga, 1932. The evolutionary affinities of the Australian endemic P. cottoni Womersley, 1937, which resembles P. natans, as well as the putative Atlantic species are hitherto undetermined. A complete molecular phylogeny of the genus based on two nuclear and two mitochondrial DNA markers indicates that P. cottoni and a Puerto Rican (Atlantic) larval population are nested within the P. natans clade. Furthermore, P. natans and P. cottoni are inseparable in all morphological characters used previously to distinguish them. Therefore, we synonymise P. cottoni with P. natans, syn. nov., whose known range now encompasses all three ocean basins after including the Puerto Rican population. This distribution warrants further investigation into the life history of Pontomyia, a midge with one of the shortest known adult lifespans among insects.

Additional keywords: biogeography, Chironominae, Insecta, phylogenetics, Tanytarsini, taxonomy, tide pools.


References

Armitage, P. D., Cranston, P. S., and Pinder, L. C. V. (1995). ‘The Chironomidae: Biology and Ecology of Non-Biting Midges.’ (Chapman and Hall: London, UK.)

Ashe, P., Murray, D. A., and Reiss, F. (1987). The zoogeographical distribution of Chironomidae (Insecta: Diptera). Annales de Limnologie – International. Journal of Limnology 23, 27–60.
The zoogeographical distribution of Chironomidae (Insecta: Diptera). Annales de Limnologie – International.CrossRef | open url image1

Bretschko, G. (1982). Pontomyia Edwards (Diptera: Chironomidae), a member of the coral reef community at Carrie Bow Cay, Belize. Smithsonian Contributions to the Marine Sciences 12, 381–385. open url image1

Brodin, Y., and Andersson, M. H. (2009). The marine splash midge Telmatogon japonicus (Diptera: Chironomidae) – extreme and alien? Biological Invasions 11, 1311–1317.
The marine splash midge Telmatogon japonicus (Diptera: Chironomidae) – extreme and alien?CrossRef | open url image1

Buxton, P. A. (1926). The colonization of the sea by insects: with an account of the habits of Pontomyia, the only known submarine insect. Proceedings of the Zoological Society of London 96, 807–814.
The colonization of the sea by insects: with an account of the habits of Pontomyia, the only known submarine insect.CrossRef | open url image1

Cheng, L. (2004). The flightless marine midge Pontomyia (Diptera: Chironomidae) with a first record from the Republic of the Maldives, Indian Ocean. In ‘Contemporary Trends in Insect Science’. (Ed. G. T. Gujar.) pp. 52–59. (Campus Books International: New Delhi, India.)

Cheng, L., and Collins, J. D. (1980). Observations on behavior, emergence and reproduction of the marine midges Pontomyia (Diptera: Chironomidae). Marine Biology 58, 1–5.
Observations on behavior, emergence and reproduction of the marine midges Pontomyia (Diptera: Chironomidae).CrossRef | open url image1

Cheng, L., and Hashimoto, H. (1978). The marine midge Pontomyia (Chironomidae) with a description of females of P. oceana Tokunaga. Systematic Entomology 3, 189–196.
The marine midge Pontomyia (Chironomidae) with a description of females of P. oceana Tokunaga.CrossRef | open url image1

Cheng, L., and Huang, D. (). Discovery of the flightless marine midge Pontomyia (Diptera: Chironomidae) at Christmas Island, Australia. The Raffles Bulletin of Zoology , . open url image1

Colgan, D. J., McLauchlan, A., Wilson, G. D. F., Livingston, S. P., Edgecombe, G. D., Macaranas, J., Cassis, G., and Gray, M. R. (1998). Histone H3 and U2 snRNA DNA sequences and arthropod molecular evolution. Australian Journal of Zoology 46, 419–437.
Histone H3 and U2 snRNA DNA sequences and arthropod molecular evolution.CrossRef | open url image1

Cranston, P. S., Dillon, M. E., Pinder, L. C. V., and Reiss, F. (1989). Keys and diagnoses of the adult males of the subfamily Chironominae (Diptera, Chironomidae). Entomologica Scandinavica 34, 353–502. open url image1

Credland, P. F. (1973). The taxonomic status of Chironomus riparius Meigen and Chironomus thummi Kieffer (Diptera: Chironomidae). Journal of Natural History 7, 209–216.
The taxonomic status of Chironomus riparius Meigen and Chironomus thummi Kieffer (Diptera: Chironomidae).CrossRef | open url image1

Darriba, D., Taboada, G. L., Doallo, R., and Posada, D. (2012). jModelTest 2: more models, new heuristics and parallel computing. Nature Methods 9, 772.
jModelTest 2: more models, new heuristics and parallel computing.CrossRef | open url image1

Edgar, R. C. (2004a). MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinformatics 5, 113.
MUSCLE: a multiple sequence alignment method with reduced time and space complexity.CrossRef | open url image1

Edgar, R. C. (2004b). MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research 32, 1792–1797.
MUSCLE: multiple sequence alignment with high accuracy and high throughput.CrossRef | open url image1

Edwards, F. W. (1926). On marine Chironomidae (Diptera); with descriptions of a new genus and four new species from Samoa. Proceedings of the Zoological Society of London 96, 779–806.
On marine Chironomidae (Diptera); with descriptions of a new genus and four new species from Samoa.CrossRef | open url image1

Epler, J. H., Ekrem, T., and Cranston, P. S. (2013). The larvae of Chironominae (Diptera: Chironomidae) of the Holarctic region – keys and diagnoses. In ‘Chironomidae of the Holarctic Region: Keys and Diagnoses, Part 1: Larvae’. (Eds T. Andersen, P. S. Cranston and J. H. Epler.) pp. 387–556. Insect Systematics and Evolution Supplements 66, 1–571.

Felsenstein, J. (1978). Cases in which parsimony or compatibility methods will be positively misleading. Systematic Zoology 27, 401–410.
Cases in which parsimony or compatibility methods will be positively misleading.CrossRef | open url image1

Folmer, O., Black, M., Hoeh, W. R., Lutz, R., and Vrijenhoek, R. C. (1994). DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology 3, 294–299. open url image1

Glover, B. (1973). The Tanytarsini (Diptera: Chironomidae) of Australia. Australian Journal of Zoology 21, 403–478.
The Tanytarsini (Diptera: Chironomidae) of Australia.CrossRef | open url image1

Guindon, S., and Gascuel, O. (2003). A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Systematic Biology 52, 696–704.
A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood.CrossRef | open url image1

Guryev, V., Makarevitch, I., Blinov, A., and Martin, J. (2001). Phylogeny of the genus Chironomus (Diptera) inferred from DNA sequences of mitochondrial cytochrome b and cytochrome oxidase I. Molecular Phylogenetics and Evolution 19, 9–21.
Phylogeny of the genus Chironomus (Diptera) inferred from DNA sequences of mitochondrial cytochrome b and cytochrome oxidase I.CrossRef | open url image1

Hashimoto, H. (1959). Notes on Pontomyia natans from Sada (Diptera, Chironomidae). Science Reports of the Tokyo Kyoiku Daigaku B 9, 57–64. open url image1

Hashimoto, H. (1962). Ecological significance of the sexual dimorphism in marine chironomids. Science Reports of the Tokyo Kyoiku Daigaku B 10, 221–252. open url image1

Hashimoto, H. (1973). Marine chironomids from Australia, with description of a new species of the genus Clunio (Diptera: Chironomidae). Bulletin of the Faculty of Education, Shizuoka University. Natural Science Series 24, 1–17. open url image1

Henriques-Oliveira, A. L., Silva, R. A., and Nessimian, J. L. (2009). First recorded of Pontomyia Edwards, 1926 (Diptera: Chironomidae: Tanytarsini) in Brazil. Biota Neotropica 9, 271–273.
First recorded of Pontomyia Edwards, 1926 (Diptera: Chironomidae: Tanytarsini) in Brazil.CrossRef | open url image1

Huang, D., and Cheng, L. (2011). The flightless marine midge Pontomyia (Diptera: Chironomidae): ecology, distribution, and molecular phylogeny. Zoological Journal of the Linnean Society 162, 443–456.
The flightless marine midge Pontomyia (Diptera: Chironomidae): ecology, distribution, and molecular phylogeny.CrossRef | open url image1

Huelsenbeck, J. P. (1997). Is the Felsenstein zone a fly trap? Systematic Biology 46, 69–74.
Is the Felsenstein zone a fly trap?CrossRef | open url image1

Huelsenbeck, J. P., and Hillis, D. M. (1993). Success of phylogenetic methods in the four-taxon case. Systematic Biology 42, 247–264.
Success of phylogenetic methods in the four-taxon case.CrossRef | open url image1

Huelsenbeck, J. P., and Ronquist, F. (2001). MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17, 754–755.
MRBAYES: Bayesian inference of phylogenetic trees.CrossRef | open url image1

Kao, C.-C., Chen, J., Chen, G.-F., and Soong, K. (2010). Variable swarming time of an intertidal midge (Pontomyia oceana Tokunaga, 1964) controlled by a circadian clock and temperature. Marine and Freshwater Behaviour and Physiology 43, 1–9.
Variable swarming time of an intertidal midge (Pontomyia oceana Tokunaga, 1964) controlled by a circadian clock and temperature.CrossRef | open url image1

Kerckhof, F., Haelters, J., and Gollasch, S. (2007). Alien species in the marine and brackish ecosystem: the situation in Belgian waters. Aquatic Invasions 2, 243–257.
Alien species in the marine and brackish ecosystem: the situation in Belgian waters.CrossRef | open url image1

Kerckhof, F., Rumes, B., Norro, A., Jacques, T. G., and Degraer, S. (2010). Seasonal variation and vertical zonation of the marine biofouling on a concrete offshore windmill foundation on the Thornton Bank (southern North Sea). In ‘Offshore Wind Farms in the Belgian Part of the North Sea: Early Environmental Impact Assessment and Spatio-Temporal Variability’. (Eds S. Degraer, R. Brabant and B. Rumes.) pp. 53–68. (Royal Belgian Institute of Natural Sciences: Bruxelles, Belgium.)

Le, H. L. V., Lecointre, G., and Perasso, R. (1993). A 28S rRNA-based phylogeny of the gnathostomes: first steps in the analysis of conflict and congruence with morphologically based cladograms. Molecular Phylogenetics and Evolution 2, 31–51.
A 28S rRNA-based phylogeny of the gnathostomes: first steps in the analysis of conflict and congruence with morphologically based cladograms.CrossRef | open url image1

Lenaers, G., Maroteaux, L., Michot, B., and Herzog, M. (1989). Dinoflagellates in evolution. A molecular phylogenetic analysis of large subunit ribosomal RNA. Journal of Molecular Evolution 29, 40–51.
Dinoflagellates in evolution. A molecular phylogenetic analysis of large subunit ribosomal RNA.CrossRef | open url image1

Maddison, W. P., and Maddison, D. R. (2011). ‘Mesquite: A Modular System for Evolutionary Analysis. Version 2.75.’ Available at http://mesquiteproject.org

Neumann, D. (1986). Diel eclosion rhythm of a sublittoral population of the marine insect Pontomyia pacifica. Marine Biology 90, 461–465.
Diel eclosion rhythm of a sublittoral population of the marine insect Pontomyia pacifica.CrossRef | open url image1

Pinder, L. C. V., and Reiss, F. (1983). The larvae of Chironominae (Diptera: Chironomidae) of the Holarctic region – keys and diagnoses. Entomologica Scandinavica 19, 293–435. open url image1

Pinder, L. C. V., and Reiss, F. (1986). The pupae of Chironominae (Diptera: Chironomidae) of the Holarctic region – keys and diagnoses. Entomologica Scandinavica 28, 299–456. open url image1

Posada, D. (2008). jModelTest: Phylogenetic model averaging. Molecular Biology and Evolution 25, 1253–1256.
jModelTest: Phylogenetic model averaging.CrossRef | open url image1

Rambaut, A., and Drummond, A. J. (2009). ‘Tracer: MCMC Trace Analysis Tool. Version 1.5.’ Available at http://beast.bio.ed.ac.uk

Renema, W., Bellwood, D. R., Braga, J. C., Bromfield, K., Hall, R., Johnson, K. G., Lunt, P., Meyer, C. P., McMonagle, L. B., Morley, R. J., O’Dea, A., Todd, J. A., Wesselingh, F. P., Wilson, M. E. J., and Pandolfi, J. M. (2008). Hopping hotspots: global shifts in marine biodiversity. Science 321, 654–657.
Hopping hotspots: global shifts in marine biodiversity.CrossRef | open url image1

Rögl, F. (1998). Palaeogeographic considerations for Mediterranean and Paratethys seaways (Oligocene to Miocene). Annalen des Naturhistorischen Museums in Wien 99A, 279–310. open url image1

Rögl, F. (1999). Mediterranean and Paratethys. Facts and hypotheses of an Oligocene to Miocene paleogeography (short overview). Geologica Carpathica 50, 339–349. open url image1

Ronquist, F., and Huelsenbeck, J. P. (2003). MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19, 1572–1574.
MrBayes 3: Bayesian phylogenetic inference under mixed models.CrossRef | open url image1

Ronquist, F., Teslenko, M., van der Mark, P., Ayres, D. L., Darling, A., Höhna, S., Larget, B., Liu, L., Suchard, M. A., and Huelsenbeck, J. P. (2012). MrBayes 3.2: Efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology 61, 539–542.
MrBayes 3.2: Efficient Bayesian phylogenetic inference and model choice across a large model space.CrossRef | open url image1

Schärer, M. T., and Epler, J. H. (2007). Long-range dispersal possibilities via sea turtle – a case for Clunio and Pontomyia (Diptera: Chironomidae) in Puerto Rico. Entomological News 118, 273–277.
Long-range dispersal possibilities via sea turtle – a case for Clunio and Pontomyia (Diptera: Chironomidae) in Puerto Rico.CrossRef | open url image1

Soong, K., and Leu, Y. (2005). Adaptive mechanism of the bimodal emergence dates in the intertidal midge Pontomyia oceana. Marine Ecology Progress Series 286, 107–114.
Adaptive mechanism of the bimodal emergence dates in the intertidal midge Pontomyia oceana.CrossRef | open url image1

Soong, K., Chen, G. F., and Cao, J. R. (1999). Life history studies of the flightless marine midges Pontomyia spp. (Diptera: Chironomidae). Zoological Studies 38, 466–473. open url image1

Soong, K., Chen, J., and Tsao, C. J. (2006). Adaptation for accuracy or for precision? Diel emergence timing of the intertidal insect Pontomyia oceana (Chironomidae). Marine Biology 150, 173–181.
Adaptation for accuracy or for precision? Diel emergence timing of the intertidal insect Pontomyia oceana (Chironomidae).CrossRef | open url image1

Soong, K., Lee, Y.-J., and Chang, I.-H. (2011). Short-lived intertidal midge Pontomyia oceana have semilunar eclosion rhythm entrained by night light. Marine Ecology Progress Series 433, 121–130.
Short-lived intertidal midge Pontomyia oceana have semilunar eclosion rhythm entrained by night light.CrossRef | open url image1

Stamatakis, A. (2006). RAxML-VI-HPC: Maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22, 2688–2690.
RAxML-VI-HPC: Maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models.CrossRef | open url image1

Stamatakis, A., Hoover, P., and Rougemont, J. (2008). A rapid bootstrap algorithm for the RAxML web servers. Systematic Biology 57, 758–771.
A rapid bootstrap algorithm for the RAxML web servers.CrossRef | open url image1

Swofford, D. L. (2003). ‘PAUP*. Phylogenetic Analysis Using Parsimony (*and Other Methods). Version 4.’ Available at http://paup.csit.fsu.edu

Teske, P. R., Papadopoulos, I., Barker, N. P., McQuaid, C. D., and Beheregaray, L. B. (2014). Mitonuclear discordance in genetic structure across the Atlantic/Indian Ocean biogeographical transition zone. Journal of Biogeography 41, 392–401.
Mitonuclear discordance in genetic structure across the Atlantic/Indian Ocean biogeographical transition zone.CrossRef | open url image1

Tokunaga, M. (1932). Morphological and biological studies on a new marine chironomid fly, Pontomyia pacifica, from Japan. Part I. Morphology and taxonomy. Memoirs of the College of Agriculture. Kyoto Imperial University 19, 1–56. open url image1

Tokunaga, M. (1964). Diptera: Chironomidae. Insects of Micronesia 12, 485–628. open url image1

von der Heyden, S., Prochazka, K., and Bowie, R. C. K. (2008). Significant population structure and asymmetric gene flow patterns amidst expanding populations of Clinus cottoides (Perciformes, Clinidae): application of molecular data to marine conservation planning in South Africa. Molecular Ecology 17, 4812–4826.
Significant population structure and asymmetric gene flow patterns amidst expanding populations of Clinus cottoides (Perciformes, Clinidae): application of molecular data to marine conservation planning in South Africa.CrossRef | open url image1

Vonnemann, V., Schrodl, M., Klussmann-Kolb, A., and Wagele, H. (2005). Reconstruction of the phylogeny of the Opisthobranchia (Mollusca: Gastropoda) by means of 18S and 28S rRNA gene sequences. The Journal of Molluscan Studies 71, 113–125.
Reconstruction of the phylogeny of the Opisthobranchia (Mollusca: Gastropoda) by means of 18S and 28S rRNA gene sequences.CrossRef | open url image1

Womersley, H. (1937). A new marine chironomid from South Australia. Transactions and Proceedings of the Royal Society of South Australia 61, 102–103. open url image1

Xia, X. (2013). DAMBE5: a comprehensive software package for data analysis in molecular biology and evolution. Molecular Biology and Evolution 30, 1720–1728.
DAMBE5: a comprehensive software package for data analysis in molecular biology and evolution.CrossRef | open url image1

Xia, X., and Xie, Z. (2001). DAMBE: Software package for data analysis in molecular biology and evolution. The Journal of Heredity 92, 371–373.
DAMBE: Software package for data analysis in molecular biology and evolution.CrossRef | open url image1

Xia, X., Xie, Z., Salemi, M., Chen, L., and Wang, Y. (2003). An index of substitution saturation and its application. Molecular Phylogenetics and Evolution 26, 1–7.
An index of substitution saturation and its application.CrossRef | open url image1



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