The family Dolichopodidae forms two of the four largest evolutionary radiations in the Hawaiian Islands across all flies: Campsicnemus (183 spp) and the Eurynogaster complex (66 spp). They also include a small radiation of Conchopus (6 spp). A handful of other dolichopodid species are native to the islands in singleton lineages or small radiations. This study provides a phylogenetic perspective on the colonization history of the dolichopodid fauna in the islands. We generated a multi-gene data set including representatives from 11 of the 14 endemic Hawaiian dolichopodid genera to examine the history of colonization to the islands, and analyzed it using Bayesian and maximum likelihood phylogenetic methods. We used a subset of the data that included Conchopus and the eight genera comprising the Eurynogaster complex to estimate the first phylogenetic hypothesis for these endemic groups, then used Beast to estimate their age of arrival to the archipelago. The Eurynogaster complex, Campsicnemus and Conchopus are clearly the result of independent colonizations. The results strongly support the Eurynogaster complex as a monophyletic group, and also supports the monophyly of 4 of the 8 described genera within the complex (Adachia, Arciellia, Uropachys and Eurynogaster). Members of the family Dolichopodidae have been dispersing over vast distances to colonize the Hawaiian Archipelago for millions of years, leading to multiple independent evolutionary diversification events. The Eurynogaster complex arrived in the Hawaiian Archipelago 11.8 Ma, well before the arrival of Campsicnemus (4.5 Ma), and the even more recent Conchopus (1.8 Ma). Data presented here demonstrate that the Hawaiian Dolichopodidae both disperse and diversify easily, a rare combination that lays the groundwork for field studies on the reproductive isolating mechanisms and ecological partitioning of this group.

Department of Environmental Science Policy and Management University of California Berkeley CA United States

Department of Natural Sciences Bernice P Bishop Museum Honolulu HI United States

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

See more in PubMed

Bellemain E, Ricklefs RE. Are islands the end of the colonization road? Trends in Ecology and Evolution. 2008;23:461–468. doi: 10.1016/j.tree.2008.05.001. PubMed DOI

Bennett GM, O’Grady PM. Review of the native Hawaiian leafhopper genus Nesophrosyne(Hemiptera: Cicadellidae: Deltocephalinae) with descriptions of eight new species associated with Broussaisia arguta. Zootaxa. 2011;2805:1–25.

Bennett GM, O’Grady PM. Historical biogeography and ecological opportunity in the adaptive radiation of native Hawaiian leafhoppers (Cicadellidae: Nesophrosyne) Journal of Biogeography. 2013;40(8):1512–1523. doi: 10.1111/jbi.12099. DOI

Bernasconi MV, Pollet M, Ward PI. Molecular systematics of Dolichopodidae (Diptera) inferred from COI and 12S rDNA gene sequences based on European exemplars. Invertebrate Systematics. 2007;21:453–470. doi: 10.1071/IS06043. DOI

Bess EC, Catanach TA, Johnson KP. The importance of molecular dating analyses for inferring Hawaiian biogeographical history: a case study with bark lice (Psocidae: Ptycta) Journal of Biogeography. 2013;41:158–167. doi: 10.1111/jbi.12191. DOI

Bonacum J, DeSalle R, O’Grady PM, Olivera DSCG, Wintermute J, Zilversmit M. New nuclear and mitochondrial primers for systematics and comparative genomics in Drosophilidae. Drosophila Information Service. 2001;84:201–204.

Bonacum J, O’Grady PM, Kambysellis M, DeSalle R. Phylogeny and age of diversification of the planitibia species group of the Hawaiian Drosophila. Molecular Phylogenetics and Evolution. 2005;37:73–82. doi: 10.1016/j.ympev.2005.03.008. PubMed DOI

Carlton JT, Eldredge LG. Bishop Museum Bulletin in Cultural and Environmental Studies 4. Bernice P. Bishop Museum; Honolulu: 2009. Marine bioinvasions of hawai‘i: the introduced and cryptogenic marine and estuarine animals and plants of the hawaiian archipelago; p. pp. 202.

Carson HL. Evolution of Drosophila on the newer Hawaiian volcanoes. Heredity. 1982;48:3–25. doi: 10.1038/hdy.1982.2. PubMed DOI

Carson HL, Clague DA. Geology and biogeography of the Hawaiian Islands. In: Wagner WL, Funk VA, editors. Hawaiian biogeography: evolution on a hotspot archipelago. Smithsonian Institution Press; Washington, D.C.: 1995. pp. 14–29.

Carson HL, Kaneshiro KY. Drosophila of Hawaii—systematics and ecological genetics. Annual Review of Ecology and Systematics. 1976;7:311–345. doi: 10.1146/annurev.es.07.110176.001523. DOI

Casquet J, Bourgeois YX, Cruaud C, Gavory F, Gillespie RG, Thebaud C. Community assembly on remote islands: a comparison of Hawaiian and Mascarene spiders. Journal of Biogeography. 2015;42:39–50. doi: 10.1111/jbi.12391. DOI

Cibois A, Beadell JS, Graves GR, Pasquet E, Slikas B, Sonsthagen SA, Thibault J, Fleischer RC. Charting the course of reed-warblers across the Pacific islands. Journal of Biogeography. 2011;38:1963–1975. doi: 10.1111/j.1365-2699.2011.02542.x. DOI

Clague DA. The growth and subsidence of the Hawaiian-Emporer volcanic chain. In: Keast A, Miller SE, editors. The origin and evolution of Pacific island biotas, New Guinea to eastern Polynesia: patterns and processes. SPB Academic Publishing; Amsterdam: 1996. pp. pp. 35–50.

Clague DA, Dalrymple GB. The Hawaiian-Emperor volcanic chain: part 1. Geologic evolution. United States Geological Survey Professional Paper. 1987;1350:5–54.

Clary DO, Wolstenholme DR. The mitochondrial DNA molecule of Drosophila yakuba: nucleotide sequence, gene organization and genetic code. Journal of Molecular Evolution. 1985;22:252–271. doi: 10.1007/BF02099755. PubMed DOI

Collins KP, Wiegmann BM. Phylogenetic relationships and placement of the Empidoidea (Diptera: Brachycera) based on 28S rDNA and EF-1alpha sequences. Insect Systematics and Evolution. 2002;33:421–444. doi: 10.1163/187631202X00226. DOI

Costello A, Motley TJ. Molecular systematics of Tetraplasandra, Munroidendron and Reynoldsia sandwicensis (Araliaceae) and the evolution of superior ovaries in Tetraplasandra. Edinburgh Journal of Botany. 2001;58:229–242. doi: 10.1017/S0960428601000609. DOI

DeSalle R. The origin and possible time of divergence of the Hawaiian Drosophilidae—evidence from DNA-sequences. Molecular Biology and Evolution. 1992;9:905–915. PubMed

DeSalle R, Freedman R, Prager EM, Wilson AC. Tempo and mode of sequence evolution in mitochondrial DNA of Hawaiian Drosophila. Journal of Molecular Evolution. 1987;26:157–164. doi: 10.1007/BF02111289. PubMed DOI

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

Duncan RA, Keller RA. Radiometric ages for basement rocks from the Emperor Seamounts, ODP Leg 197. Geochemistry Geophysics Geosystems. 2004;5:Q08L03. doi: 10.1029/2004GC000704. DOI

Eldon J, Price JP, Magnacca K, Price DK. Patterns and processes in complex landscapes: testing alternative biogeographical hypotheses through intergrated analysis of phylogeography and community ecology in Hawaii. Molecular Ecology. 2013;22:3613–3628. doi: 10.1111/mec.12326. PubMed DOI

Evenhuis NL. A review of the genera comprising species of the genus Eurynogaster sensu Hardy & Kohn, 1964 in Hawaii (Diptera: Dolichopodidae) Zootaxa. 2005;1017:39–60.

Filardi CE, Moyle RG. Single origin of a pan-Pacific bird group and upstream colonization of Australasia. Nature. 2005;438:216–219. doi: 10.1038/nature04057. PubMed DOI

Gillespie RG, Baldwin BG, Waters JM, Fraser C, Nikula R, Roderick GK. Long-distance dispersal—a framework for hypothesis testing. Trends in Ecology & Evolution. 2012;27(1):47–56. doi: 10.1016/j.tree.2011.08.009. PubMed DOI

Gillespie RG, Roderick GK. Arthropods on islands: colonization, speciation, and conservation. Annual Review of Entomology. 2002;47:595–632. doi: 10.1146/annurev.ento.47.091201.145244. PubMed DOI

Goodman KR, Evenhuis NL, Bartosoya-Sojkova P, O’Grady PM. Diversification in Hawaiian long-legged flies (Diptera: Dolichopodidae: Campsicnemus): biogeographic isolation and ecological adaptation. Molecular Phylogenetics and Evolution. 2014;81:232–241. doi: 10.1016/j.ympev.2014.07.015. PubMed DOI

Goodman KR, Kelley JP, Welter SC, Roderick GK, Elias DO. Rapid diversification of sexual signals in Hawaiian Nesosydne planthoppers (Hemiptera: Delphacidae): the relative role of neutral and selective forces. Journal of Evolutionary Biology. 2015;28(2):415–427. doi: 10.1111/jeb.12577. PubMed DOI

Goodman KR, O’Grady PM. Molecular phylogeny and biogeography of the Hawaiian craneflies Dicranomyia (Diptera: Limoniidae) PLoS ONE. 2013;8(9):e73019. doi: 10.1371/journal.pone.0073019. PubMed DOI PMC

Goodman KR, Welter SC, Roderick GK. Genetic divergence is decoupled from ecological diversification in the Hawaiian Nesosydne planthoppers. Evolution. 2012;66:2798–2813. doi: 10.1111/j.1558-5646.2012.01643.x. PubMed DOI

Grace JL, Shaw KL. Coevolution of male signal and female preference during early lineage divergence of the Hawaiian cricket, Laupala cerasina. Evolution. 2011;65:2184–2196. doi: 10.1111/j.1558-5646.2011.01278.x. PubMed DOI

Haines WP, Rubinoff D. Molecular phylogenetics of the moth genus Omiodes Guenee (Crambidae: Spilomelinae), and the origins of the Hawaiian lineage. Molecular Phylogenetics and Evolution. 2012;65:305–316. doi: 10.1016/j.ympev.2012.06.021. PubMed DOI

Haines WP, Schmitz P, Rubinoff D. Ancient diversification of Hyposmocoma moths in Hawaii. Nature Communications. 2014;5(3502):1–7. doi: 10.1038/ncomms4502. PubMed DOI

Harbaugh DT, Baldwin BG. Phylogeny and biogeography of the sandalwoods (Santalum, Santalaceace): repeated dispersals throughout the Pacific. American Journal of Botany. 2007;94:1028–1040. doi: 10.3732/ajb.94.6.1028. PubMed DOI

Hardin J. The competitive exclusion principle. Science. 1960;131:1292–1297. doi: 10.1126/science.131.3409.1292. PubMed DOI

Hardy DE, Kohn MA. Insects of Hawaii. Vol 11. University of Hawaii Press; Honolulu: 1964. Dolichopodidae; pp. 1–256.

Heads M. Dating nodes on molecular phylogenies: a critique of molecular biogeography. Cladistics. 2005;21:62–78. doi: 10.1111/j.1096-0031.2005.00052.x. PubMed DOI

Heaney LR. Is a new paradigm emerging for oceanic island biogeography? Journal of Biogeography. 2007;34:753–757. doi: 10.1111/j.1365-2699.2007.01692.x. DOI

Hembry DH, Kawakita A, Gurr NE, Schmaedick MA, Baldwin BG, Gillespie RG. Non-congruent colonizations and diversification in a coevolving pollination mutualism on oceanic islands. Proceedings of The Royal Society B. 2013;280:20130361. doi: 10.1098/rspb.2013.0361. PubMed DOI PMC

Hennig W. Phylogenetic systematics. University of Illinois Press; Urbana: 1966.

Huelsenbeck JP, Ronquist F. MrBayes: Bayesian inference of phylogenetic trees. Bioinformatics. 2001;17:754–755. PubMed

Jordan S, Simon C, Polhemus D. Molecular systematics and adaptive radiation of hawaii’s endemic damselfly genus Megalagrion (Odonata: coenagrionidae) Systematic Biology. 2003;52(1):89–109. doi: 10.1080/10635150390132803. PubMed DOI

Kaneshiro KY. Ethological isolation and phylogeny in the planitibia subgroup of Hawaiian Drosophila. Evolution. 1976;30(4):740–745. doi: 10.2307/2407814. PubMed DOI

Lanfear R, Calcott B, Ho SYW, Guindon S. PartitionFinder: combined selection of partitioning schemes and substitution models for phylogenetic analyses. Molecular Biology and Evolution. 2012;29:1695–1701. doi: 10.1093/molbev/mss020. PubMed DOI

Lapoint RT, Gidaya A, O’Grady PM. Phylogenetic relationships in the spoon tarsus subgroup of Hawaiian Drosophila; Conflict and concordance between gene trees. Molecular Phylogenetics and Evolution. 2011;58:492–501. doi: 10.1016/j.ympev.2010.12.015. PubMed DOI

Lapoint RT, Magnacca KN, O’Grady PM. Phylogenetics of the antopocerus-modified tarsus clade of Hawaiian Drosophila: diversification across the Hawaiian Islands. PLoS ONE. 2014;9(11):e113227. doi: 10.1371/journal.pone.0113227. PubMed DOI PMC

Lapoint RT, O’Grady PM, Whiteman NK. Diversification and dispersal of the hawaiian drosophilidae: the evolution of scaptomyza. Molecular Phylogenetics and Evolution. 2013;69(1):95–108. doi: 10.1016/j.ympev.2013.04.032. PubMed DOI PMC

Lerner HRL, Meyer M, James HF, Hofreiter M, Fleischer RC. Multilocus resolution of phylogeny and timescale in the extant adaptive radiation of Hawaiian honeycreepers. Current Biology. 2011;21:1–7. PubMed

Liebherr JK. The Mecyclothorax beetles (Coleoptera, Carabidae, Moriomorphini) of Haleakala, Maui: keystone of a hyperdiverse Hawaiian radiation. Zookeys. 2015;544:1–407. doi: 10.3897/zookeys.544.6074. PubMed DOI PMC

Lim GS, Hwang WS, Kutty SN, Meier R, Grootaert P. Mitochondrial and nuclear markers support the monophyly of Dolichopodidae and suggest a rapid origin of the subfamilies (Diptera: Empidoidea) Systematic Entomology. 2010;35:59–70. doi: 10.1111/j.1365-3113.2009.00481.x. DOI

MacArthur RH, Wilson EO. The theory of Island biogeography. Princeton University Press; Princeton: 1967. p. pp. 203.

Maddison WP, Maddison DR. Mesquite: a modular system for evolutionary analysis. 2009. Version 2.72. http://mesquiteproject.org .

Medeiros MJ, Davis D, Howarth FG, Gillespie RG. Evolution of cave living in Hawaiian Schrankia (Lepidoptera: Noctuidae) with description of a remarkable new cave species. Zoological Journal of the Linnean Society. 2009;156:114–139. doi: 10.1111/j.1096-3642.2008.00477.x. DOI

Medeiros MJ, Gillespie RG. Biogeography and the evolution of flightlessness in a radiation of Hawaiian moths (Xyloryctidae: Thyrocopa) Journal of Biogeography. 2011;38:101–111. doi: 10.1111/j.1365-2699.2010.02402.x. DOI

Mendelson TC, Shaw KL. Sexual behavior: rapid speciation in an arthropod. Nature. 2005;433:375–376. doi: 10.1038/433375a. PubMed DOI

Miller MA, Pfeiffer W, Schwartz T. Creating the CIPRES Science Gateway for inference of large phylogenetic trees. Proceedings of the gateway computing environments workshop (GCE); 2010. pp. pp. 1–8.

Moulton JK, Weigmann BM. Evolution and phylogenetic utility of cad (rudimentary) amond Mesozoic-aged Eremoneuran Diptera (Insecta) Molecular Phylogenetics and Evolution. 2004;31:363–378. doi: 10.1016/S1055-7903(03)00284-7. PubMed DOI

O’Grady PM, DeSalle R. Out of Hawaii: the biogeographic history of the genus Scaptomyza (Diptera: Drosophilidae) Biology Letters. 2008;4(2):195–199. doi: 10.1098/rsbl.2007.0575. PubMed DOI PMC

O’Grady PM, Lapoint RT, Bonacum J, Lasola J, Owen E, Wu Y, DeSalle R. Phylogenetic and ecological relationships of the Hawaiian Drosophila inferred by mitochondrial DNA analysis. Molecular Phylogenetics and Evolution. 2011;58:244–256. doi: 10.1016/j.ympev.2010.11.022. PubMed DOI

O’Grady PM, Magnacca KN, Lapoint RT. Drosophila. In: Gillespie RG, Clague DA, editors. Encyclopedia of Islands. Berkeley: University of California Press; 2009. pp. pp. 232–235.

Pape T, Thompson FC, editors. 2013. [16 October 2014]. Systema dipterorum version 1.5. http://www.diptera.org/

Plunkett GM, Soltis DE, Soltis PS. Clarification of the relationship between Apiaceae and Araliaceae based on matK and rbcL sequence data. American Journal of Botany. 1997;84:565–580. doi: 10.2307/2446032. PubMed DOI

Price DK, Boake CRB. Behavioral reproductive isolation in Drosophila silvestris, D. heteroneura and their F1 hybrids (Diptera: Drosophilidae) Journal of Insect Behaviour. 1995;8:595–616. doi: 10.1007/BF01997233. DOI

Price JP, Clague DA. How old is the Hawaiian biota? Geology and phylogeny suggest recent divergence. Proceedings of the Royal Society of London, B. 2002;269:2429–2435. doi: 10.1098/rspb.2002.2175. PubMed DOI PMC

Price JP, Wagner WL. Speciation in Hawaiian angiosperm lineages: cause, consequence, and mode. Evolution. 2004;58:2185–2200. doi: 10.1111/j.0014-3820.2004.tb01597.x. PubMed DOI

Rambaut A, Drummond AJ. Tracer v1.7.2, obtained from the “Workshop on Molecular Evolution”, August 2011. 2012. Tracer v1.5. http://beastbioedacuk/Tracer .

Rubinoff D, Schmitz P. Multiple aquatic invations by an endemic, terrestrial Hawaiian moth radiation. Proceedings of the National Academy of Sciences of the United States of America. 2010;107:5903–5906. doi: 10.1073/pnas.0912501107. PubMed DOI PMC

Shapiro LH, Strazanac JS, Roderick GK. Molecular phylogeny of Banza (Orthoptera: Tettigoniidae), the endemic katydids of the Hawaiian Archipelago. Molecular Phylogenetics and Evolution. 2006;41:53–63. doi: 10.1016/j.ympev.2006.04.006. PubMed DOI

Sharp WD, Clague DA. 50-Ma initiation of Hawaiian-Emperor bend records major change in pacific plate motion. Science. 2006;313:1281–1284. doi: 10.1126/science.1128489. 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. Annals of the Entomological Society of America. 1994;86:651–701.

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

Sunose T, Sato M. Morphological and ecological studies on a marine shore dolichopodid fly, Conchopus borealis Takagi (Diptera, Dolichopodidae) Japanese Journal of Entomology. 1994;62(4):651–660.

Takagi S. A contribution to the knowledge of the marine shore dolichopodidae of Japan (Diptera) Insecta Matsumaurana. 1965;27(2):49–84.

Tenorio JM. Insects of Hawaii 11 (Supplement) Honolulu: University of Hawai’i Press; 1969. Diptera: Dolichopodidae. v + 73 pp.

Ulrich H. Predation by adult Dolichopodidae (Diptera): a review of literature with an annotated prey-predator list. Studia Dipterologica. 2005;11:369–403.

Wagner WL, Funk VA, editors. Hawaiian biogeography: evolution on a hot spot archipelago. Smithsonian Institution Press; Washington and London: 1995. p. 467.

Williams FX. Biological studies in Hawaiian water-loving insects part III, Diptera or flies B. Asteiidae, Syrphidae and Dolichopodidae. Proceedings of The Hawaiian Entomological Society. 1938;X:281–315.

Wilson JT. A possible origin of the Hawaiian islands. Canadian Journal of Physics. 1963;41:863–870. doi: 10.1139/p63-094. DOI

Yang D, Zhu Y, Wang M, Shang L. World catalog of dolichopodidae (Insecta: Diptera) China Agricultural University Press; Beijing: 2006.

Zimmer M, Diestelhorst O, Lunau K. Courtship in long-legged flies (Diptera: Dolichopodidae): function and evolution of signals. Behavioral Ecology. 2003;14:526–530. doi: 10.1093/beheco/arg028. DOI

Zimmerman EC. Insects of Hawaii, 1 (reissue) Honolulu: University of Hawai’i Press; 2001. Introduction, with a new preface and dedication. 206 pp.