Advertisement

Conservation Genetics

, Volume 11, Issue 4, pp 1283–1298 | Cite as

Stepping stone speciation in Hawaii’s flycatchers: molecular divergence supports new island endemics within the elepaio

  • Eric A. VanderWerf
  • Lindsay C. Young
  • Norine W. Yeung
  • David B. Carlon
Research Article

Abstract

The elepaio (Chasiempis sandwichensis) is a monarch flycatcher endemic to the Hawaiian Islands of Kauai, Oahu, and Hawaii. Elepaio vary in morphology among and within islands, and five subspecies are currently recognized. We investigated phylogeography of elepaio using mitochondrial (ND2) and nuclear (LDH) markers and population structure within Hawaii using ND2 and microsatellites. Phylogenetic analyses revealed elepaio on each island formed reciprocally monophyletic groups, with Kauai ancestral to other elepaio. Sequence divergence in ND2 among islands (3.02–2.21%) was similar to that in other avian sibling species. Estimation of divergence times using relaxed molecular clock models indicated elepaio colonized Kauai 2.33 million years ago (95% CI 0.92–3.87 myr), Oahu 0.69 (0.29–1.19) myr ago, and Hawaii 0.49 (0.21–0.84) myr ago. LDH showed less variation than ND2 and was not phylogenetically informative. Analysis of molecular variance within Hawaii showed structure at ND2 (fixation index = 0.31), but microsatellites showed no population structure. Genetic, morphological, and behavioral evidence supports splitting elepaio into three species, one on each island, but does not support recognition of subspecies within Hawaii or other islands. Morphological variation in elepaio has evolved at small geographic scales within islands due to short dispersal distances and steep climatic gradients. Divergence has been limited by lack of dispersal barriers in the extensive forest that once covered each island, but anthropogenic habitat fragmentation and declines in elepaio population size are likely to decrease gene flow and accelerate differentiation, especially on Oahu.

Keywords

Chasiempis Elepaio Hawaii Phylogeography Population structure Relaxed clock 

Notes

Acknowledgments

For assistance in mist-netting elepaio, we thank Joby Rohrer, Matthew Burt, Kapua Kawelo, John Polhemus, Stephen Mosher, Phil Taylor, Keith Swindle, Dan Sailer, Ethan Shiinoki, Amy Tsuneyoshi, Marcos Gorresen, Pauline Roberts, Jeremy Russell, and Lucas Behnke. Permits to capture elepaio and collect blood samples were provided by the U.S. Fish and Wildlife Service and the Hawaii Division of Forestry and Wildlife. Access was provided by the U.S. Fish and Wildlife Service, the Hawaii Natural Area Reserves System, the Hawaii Division of Forestry and Wildlife, The Nature Conservancy of Hawaii, the U.S. Army, the Damon Estate, and the City and County of Honolulu Board of Water Supply. Permission to capture and collect blood samples from the Tinian monarch was provided by the Commonwealth of the Northern Marianas Division of Fish and Wildlife. We thank Catherine Lippe and Joanna Kobayashi for lab assistance, Chris Filardi for discussion and advice, and Ken Hayes for technical assistance and comments on the manuscript. This work was supported in part by the Hawaii Division of Forestry and Wildlife, the U.S. Fish and Wildlife Service, and the University of Hawaii Ecology, Evolution, and Conservation Biology Program.

References

  1. Amadon D (1949) The seventy-five per cent rule for subspecies. Condor 51:250–258CrossRefGoogle Scholar
  2. American Ornithologists’ Union (1998) Check-list of North American Birds, 7th edn. American Ornithologists’ Union, Washington, DCGoogle Scholar
  3. American Ornithologists’ Union (2000) Forty-second supplement to the American Ornithologists’ Union Check-list of North American birds. Auk 117:847–858Google Scholar
  4. Arbogast BS, Slowinski JB (1998) Pleistocene speciation and the mitochondrial DNA clock. Science 282:1955aCrossRefGoogle Scholar
  5. Avise JC (2004) Molecular markers, natural history, and evolution, 2nd edn. Sinauer Associates, SunderlandGoogle Scholar
  6. Avise JC, Zink RM (1988) Molecular genetic divergence between avian sibling species: king and clapper rails, long-billed and short-billed dowitchers, boat-tailed and great-tailed grackles, and tufted and black-crested titmice. Auk 105:516–528Google Scholar
  7. Badyaev AV, Hill GE (2003) Avian sexual dichromatism in relation to phylogeny and ecology. Annu Rev Ecol Syst 34:27–49CrossRefGoogle Scholar
  8. Baldwin BG (1997) Adaptive radiation of the Hawaiian Silversword alliance: congruence and conflict of phylogenetic evidence from molecular and non-molecular investigations. In: Givnish TJ, Sytsma KJ (eds) Molecular evolution and adaptive radiation. Cambridge University Press, New York, pp 104–128Google Scholar
  9. Bryan EH Jr, Greenway JC Jr (1944) Check-list of the birds of the Hawaiian Islands. Bull Mus Comp Zool 94:92–140Google Scholar
  10. Burgess SL, Fleischer RC (2006) Isolation and characterization of polymorphic microsatellite loci in the Hawaiian flycatcher, the elepaio (Chasiempis sandwichensis). Mol Ecol Notes 6:14–16CrossRefGoogle Scholar
  11. Burney DA, James HF, Burney LP et al (2001) Fossil evidence for a diverse biota from Kaua`i and its transformation since human arrival. Ecol Monogr 71:615–641Google Scholar
  12. Burtt EH, Ichida JM (2004) Gloger’s rule, feather-degrading bacteria, and color variation among song sparrows. Condor 106:681–686CrossRefGoogle Scholar
  13. Carson H (1987) Tracing ancestry with chromosomal sequences. Trends Ecol Evol 2:203–207CrossRefGoogle Scholar
  14. Case TJ, Taper ML (2000) Interspecific competition, environmental gradients, gene flow, and the coevolution of species borders. Am Nat 155:583–605CrossRefPubMedGoogle Scholar
  15. Cibois A, Thibault J-C, Pasquet E (2004) Biogeography of eastern Polynesian monarchs (Pomarea): an endemic genus close to extinction. Condor 106:837–851CrossRefGoogle Scholar
  16. Cicero C (2004) Barriers to sympatry between avian sibling species (Paridae: Baeolophus) in local secondary contact. Evolution 58:1573–1587PubMedGoogle Scholar
  17. Clement M, Posada D, Crandall KA (2000) TCS: a computer program to estimate gene genealogies. Mol Ecol 9:1657–1659CrossRefPubMedGoogle Scholar
  18. Conant S, Pratt HD, Shallenberger RJ (1998) Reflections on a 1975 expedition to the lost world of the Alaka`i and other notes on the natural history, systematics, and conservation of Kaua`i birds. Wilson Bull 110:1–22Google Scholar
  19. Cowie RH, Holland BS (2008) Molecular biogeography and diversification of the endemic terrestrial fauna on the Hawaiian Islands. Philos Trans R Soc B 363:3363–3376CrossRefGoogle Scholar
  20. Delaney KS, Wayne RK (2005) Adaptive units for conservation: population distinction and historic extinctions in the island scrub-jay. Conserv Biol 19:523–533CrossRefGoogle Scholar
  21. Drovetski SV, Zink RM, Rohwer S, Fadeev IV, Nesterov EV, Karagodin I, Koblik EA, Red’kin YA (2004) Complex biogeographic history of a Holarctic passerine. Proc R Soc Lond Ser B 271:545–551CrossRefGoogle Scholar
  22. Drummond AJ, Rambaut A (2007) BEAST: Bayesian evolutionary analysis sampling trees. BMC Evol Biol 7:214CrossRefPubMedGoogle Scholar
  23. Endler JA (1977) Geographic variation, speciation, and clines. Princeton University Press, PrincetonGoogle Scholar
  24. Excoffier L, Laval G, Schneider S (2005) Arlequin version 3.0—an integrated software package for population genetics data analysis. Evol Bioinform Online 1:47–50PubMedGoogle Scholar
  25. Falush D, Stephens M, Pritchard JK (2007) Inference of population structure using multilocus genotype data: dominant markers and null alleles. Mol Ecol Notes. doi: 10.1111/j.1471-8286.2007.01758.x
  26. Filardi CE, Moyle RG (2005) Single origin of a pan-Pacific bird group and upstream colonization of Australasia. Nature 438:216–219CrossRefPubMedGoogle Scholar
  27. Filardi CE, Smith CE (2005) Molecular phylogenetics of monarch flycatchers (genus Monarcha) with emphasis on Solomon Island endemics. Mol Phylogenet Evol. doi: 10.1016/j.ympev.2005.02.007
  28. Filardi CE, Smith CE (2008) Social selection and geographic variation in two monarch flycatchers from the Solomon Islands. Condor 110:24–34CrossRefGoogle Scholar
  29. Fleischer RC, McIntosh CE (2001) Molecular systematics and biogeography of the Hawaiian avifauna. Stud Avian Biol 22:51–60Google Scholar
  30. Fleischer RC, McIntosh CE, Tarr CL (1998) Evolution on a volcanic conveyor belt: using phylogeographic reconstructions and K–Ar-based ages of the Hawaiian Islands to estimate molecular evolutionary rates. Mol Ecol 7:533–545CrossRefPubMedGoogle Scholar
  31. Foster JT, Tweed EJ, Camp RJ, Woodworth BL, Adler CD, Telfer T (2004) Long-term population changes of native and introduced birds in the Alaka`i Swamp, Kaua`i. Conserv Biol 18:716–725CrossRefGoogle Scholar
  32. Foster JT, Woodworth BL, Eggert LE et al (2007) Genetic structure and evolved malaria resistance in Hawaiian honeycreepers. Mol Ecol 16:4738–4746CrossRefPubMedGoogle Scholar
  33. Freed LA, Conant S, Fleischer RC (1987) Evolutionary ecology and radiation of Hawaiian passerine birds. Trends Ecol Evol 2:196–203CrossRefGoogle Scholar
  34. Friesen VL, Congdon BC, Kidd MG, Birt TP (1999) Polymerase chain reaction (PCR) primers for the amplification of five nuclear introns in vertebrates. Mol Ecol 8:2147–2149CrossRefPubMedGoogle Scholar
  35. Friesen VL, Anderson DJ, Steeves TE, Jones H, Schreiber EA (2002) Molecular support for species status of the Nazca booby (Sula granti). Auk 119:820–826CrossRefGoogle Scholar
  36. Garcia-Moreno J (2004) Is there a universal mtDNA clock for birds? J Avian Biol 35:465–468CrossRefGoogle Scholar
  37. Givnish TJ, Millam KC, Mast AR et al (2008) Origin, adaptive radiation and diversification of the Hawaiian lobeliads (Asterales: Campanulaceae). Proc R Soc. doi: 10.1098/rspb.2008.1204
  38. Gorresen PM, Camp RJ, Pratt TK, Woodworth BL (2005) Status of forest birds in the central windward region of Hawai`i Island. U.S. Geological Survey, Biological Resources Discipline, Open-File Report 2005-1441, 85 ppGoogle Scholar
  39. Gorresen PM, Camp RJ, Pratt TK, Woodworth BL (2006) Status of forest birds in the Ka`ū Region of Hawai`i Island: population distribution and trends. U.S. Geological Survey, Biological Resources Discipline, Open-File reportGoogle Scholar
  40. Grant PR (2001) Reconstructing the evolution of birds on islands: 100 years of research. Oikos 92:385–403CrossRefGoogle Scholar
  41. Grant PR, Grant BR (2007) How and why species multiply: the radiation of Darwin’s finches. Princeton University Press, PrincetonGoogle Scholar
  42. Hackett J (1996) Molecular phylogenetics and biogeography of tanagers in the genus Ramphocelus (Aves). Mol Phylogen Evol 5:368–382CrossRefGoogle Scholar
  43. Haldane JBS (1956) The relation between density regulation and natural selection. Proc R Soc Lond B Biol Sci 145:306–308CrossRefPubMedGoogle Scholar
  44. Henshaw HW (1902) The elepaio of Hawaii. Auk 19:221–232Google Scholar
  45. Ho SYW (2007) Calibrating molecular estimates of substitution rates and divergence times in birds. J Avian Biol 38:409–414Google Scholar
  46. Ho SYW, Phillips MJ, Cooper A, Drummond AJ (2005) Time dependency of molecular rate estimates and systematic overestimation of recent divergence times. Mol Biol Evol 22:1561–1568CrossRefPubMedGoogle Scholar
  47. Holland BS, Hadfield MG (2004) Origin and diversification of the endemic Hawaiian tree snails (Achatinellinae: Achatinellidae) based on molecular evidence. Mol Phylogen Evol 32:588–600CrossRefGoogle Scholar
  48. Huelsenbeck JP, Ronquist F (2001) MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17:754–755CrossRefPubMedGoogle Scholar
  49. International Union for the Conservation of Nature (2007) 2007 IUCN Red list of threatened species. www.iucnredlist.org. Accessed 18 June 2008
  50. Johnson NK, Cicero C (2002) The role of ecologic diversification in sibling speciation of Empidonax flycatchers (Tyrannidae): multigene evidence from mtDNA. Mol Ecol 11:2065–2081CrossRefPubMedGoogle Scholar
  51. Kaneshiro KY, Boake CRB (1987) Sexual selection and speciation: issues raised by Hawaiian Drosophila. Trends Ecol Evol 2:207–212CrossRefGoogle Scholar
  52. Keller I, Largiadèr C (2003) Recent habitat fragmentation caused by major roads leads to reduction of gene flow and loss of genetic variability in ground beetles. Proc R Soc Lond Ser B 270:417–423CrossRefGoogle Scholar
  53. Kirch PV (1982) The impact of prehistoric Polynesians on the Hawaiian ecosystem. Pac Sci 36:1–14Google Scholar
  54. Lack D (1976) Island biology illustrated by the land birds of Jamaica. Blackwell, OxfordGoogle Scholar
  55. Lovette IJ (2004) Mitochondrial dating and mixed support for the “2%” rule in birds. Auk 121:1–6CrossRefGoogle Scholar
  56. Martinez-Cruz B, Godoy JA, Negro JJ (2007) Population fragmentation leads to spatial and temporal genetic structure in the endangered Spanish imperial eagle. Mol Ecol 16:477–486CrossRefPubMedGoogle Scholar
  57. Mayr E (1982) Of what use are subspecies? Auk 99:593–595Google Scholar
  58. Mayr E, Diamond J (2001) The birds of northern Melanesia. Oxford University Press, OxfordGoogle Scholar
  59. Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New YorkGoogle Scholar
  60. Newton A (1892) Ornithology of the Sandwich Islands. Nature 45:465–469CrossRefGoogle Scholar
  61. Olson SL (1989) Two overlooked holotypes of the Hawaiian Flycatcher Chasiempis described by Leonhard Stejneger (Aves: Myiagrinae). Proc Biol Soc Washington 102:555–558Google Scholar
  62. Olson SL, James HF (1982) Prodromus of the fossil avifauna of the Hawaiian Islands. Smithson Contrib Zool 365:1–59Google Scholar
  63. Omland KE, Lanyon SM (2000) Reconstructing plumage evolution in orioles (Icterus): repeated convergence and reversal in patterns. Evolution 54:2119–2133PubMedGoogle Scholar
  64. Patten MA, Unitt P (2002) Diagnosability versus mean differences of sage sparrow subspecies. Auk 119:26–35CrossRefGoogle Scholar
  65. Percy DM, Garver AM, Wagner WL et al (2008) Progressive island colonization and ancient origin of Hawaiian Metrosideros (Myrtaceae). Proc R Soc 275:1479–1490CrossRefGoogle Scholar
  66. Pereira SL, Baker AJ (2006) A molecular timescale for galliform birds accounting for uncertainty in time estimates and heterogeneity of rates of DNA substitutions across lineages and sites. Mol Phylogen Evol 38:499–509CrossRefGoogle Scholar
  67. Peterson AT (2006) Application of molecular clocks in ornithology revisited. J Avian Biol 37:541–544CrossRefGoogle Scholar
  68. Phillimore AB, Owens IPF (2006) Are subspecies useful in evolutionary and conservation biology. Proc R Soc Ser B 273:1049–1053CrossRefGoogle Scholar
  69. Posada D, Crandall KA (1998) Modeltest: testing the model of DNA substitution. Bioinformatics 14:817–818CrossRefPubMedGoogle Scholar
  70. Pratt HD (1979) A new subspecies of the elepaio Chasiempis sandwichensis, from the island of Hawaii. Bull Brit Ornithol Club 99:105–108Google Scholar
  71. Pratt HD (1980) Intra-island variation in the `elepaio on the island of Hawaii. Condor 82:449–458CrossRefGoogle Scholar
  72. Pratt HD, Bruner PL, Berrett DG (1987) A field guide to the birds of Hawai`i and the tropical Pacific. Princeton University Press, PrincetonGoogle Scholar
  73. Price JP, Clague DA (2002) How old is the Hawaiian biota? Geology and phylogeny suggest recent divergence. Proc R Soc B 269:2429–2435CrossRefPubMedGoogle Scholar
  74. Rambaut A (2009) FigTree: tree figure drawing tool, v1.2.1. University of Edinburgh, UKGoogle Scholar
  75. Raymond M, Rousset F (1997) GENEPOP version 3.1b. An updated version of GENEPOP version 1.2: population genetics software for exact tests and ecumenicism. J Hered 86:248–249Google Scholar
  76. Roderick GK, Gillespie RG (1998) Speciation and phylogeography of Hawaiian terrestrial arthropods. Mol Ecol 7:519–531CrossRefPubMedGoogle Scholar
  77. Rozas J, Sanchez-Delbarrio JC, Messeguer X et al (2003) DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19:2496–2497CrossRefPubMedGoogle Scholar
  78. Sclater PL (1885) On the muscicapine genus Chasiempis. Ibis 3:17–19Google Scholar
  79. Scott JM, Mountainspring S, Ramsey FL et al (1986) Forest bird communities of the Hawaiian islands: their dynamics, ecology, and conservation. Stud Avian Biol 9:1–431Google Scholar
  80. Scott JM, Conant S, van Riper C III (2001) Evolution, ecology, conservation, and management of Hawaiian birds: a vanishing avifauna. Stud Avian Biol 22:1–428Google Scholar
  81. Seutin G, White BN, Boag PT (1991) Preservation of avian blood and tissue samples for DNA analyses. Can J Zool 69:82–90CrossRefGoogle Scholar
  82. Simon C (1987) Hawaiian evolutionary biology: an introduction. Trends Ecol Evol 2:175–178CrossRefGoogle Scholar
  83. Sorenson MD, Quinn TW (1998) Numts: a challenge for avian systematics and population biology. Auk 115:214–221Google Scholar
  84. Stejneger L (1887) Birds of Kauai Island, Hawaiian Archipelago, collected by Mr. Valdemar Knudsen, with descriptions of new species. Proc United States Natl Mus 10:75–102Google Scholar
  85. Swofford DL (2002) PAUP*. Phylogenetic analysis using parsimony (and other methods) 4.0 Beta for Macintosh. Sinnauer Associates, SunderlandGoogle Scholar
  86. Tajima F (1993) Simple methods for testing molecular clock hypothesis. Genetics 135:599–607PubMedGoogle Scholar
  87. Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599CrossRefPubMedGoogle Scholar
  88. Tarr CL, Fleischer RC (1993) Mitochondrial DNA variation and evolutionary relationships in the amakihi complex. Auk 110:825–831Google Scholar
  89. U.S. Fish and Wildlife Service (2000) Final rule to list as endangered the Oahu elepaio from the Hawaiian Islands and determination of whether designation of critical habitat is prudent. Federal Register 65:20760–20769Google Scholar
  90. U.S. Fish and Wildlife Service (2006) Final revised recovery plan for Hawaiian forest birds. U.S. Fish and Wildlife Service, Portland. 508 ppGoogle Scholar
  91. Vandergast AG, Gillespie RG, Roderick GK (2004) Influence of volcanic activity on the population genetic structure of Hawaiian Tetragnatha spiders: fragmentation, rapid population growth and the potential for accelerated evolution. Mol Ecol 13:1729–1743CrossRefPubMedGoogle Scholar
  92. VanderWerf EA (1998) Elepaio (Chasiempis sandwichensis). In: Poole A, Gill F (eds) The birds of North America. The Birds of North America Inc., Philadelphia, No. 344Google Scholar
  93. VanderWerf EA (2001) Two-year delay in plumage maturation of male and female elepaio. Condor 103:756–766CrossRefGoogle Scholar
  94. VanderWerf EA (2004) Demography of Hawai`i `elepaio: variation with habitat disturbance and population density. Ecology 85:770–783CrossRefGoogle Scholar
  95. VanderWerf EA (2007) Biogeography of elepaio: evidence from inter-island song playbacks. Wilson J Ornithol 119:325–333CrossRefGoogle Scholar
  96. VanderWerf EA (2008) Sources of variation in survival, recruitment, and natal dispersal of the Hawaii elepaio. Condor 110:241–250CrossRefGoogle Scholar
  97. VanderWerf EA (2009) Importance of nest predation by alien rodents and avian poxvirus in conservation of Oahu elepaio. J Wildl Manag 73:737–746CrossRefGoogle Scholar
  98. VanderWerf EA, Freed LA (2003) Elepaio subadult plumages reduce aggression through graded status signaling, not mimicry. J Field Ornithol 74:406–415Google Scholar
  99. VanderWerf EA, Smith DG (2002) Effects of alien rodent control on demography of the O`ahu `elepaio, an endangered Hawaiian forest bird. Pacific Conserv Biol 8:73–81Google Scholar
  100. VanderWerf EA, Rohrer JL, Smith DG et al (2001) Current distribution and abundance of the Oahu elepaio. Wilson Bull 113:10–16CrossRefGoogle Scholar
  101. VanderWerf EA, Burt MD, Rohrer JL et al (2006) Distribution and prevalence of mosquito-borne diseases in O`ahu `elepaio. Condor 108:770–777CrossRefGoogle Scholar
  102. Wagner WL, Funk VA (eds) (1995) Hawaiian biogeography: evolution on a hot spot archipelago. Smithsonian Institution Press, Washington, DCGoogle Scholar
  103. Wilson SB (1891) On the muscicapine genus Chasiempis, with a description of a new species. Proc Zool Soc Lond 1891:164–166Google Scholar
  104. Xia X, Xie Z (2001) DAMBE: software package for data analysis and molecular biology and evolution. J Heredity 92:371–373CrossRefGoogle Scholar
  105. Zink RM (2004) The role of subspecies in obscuring avian biological diversity and misleading conservation policy. Proc R Soc B 271:561–564CrossRefPubMedGoogle Scholar
  106. Zink RM, Barrowclough GF (2008) Mitochondrial DNA under siege avian phylogeography. Mol Ecol 17:2107–2121CrossRefPubMedGoogle Scholar
  107. Zink RM, Remsen JV Jr (1986) Evolutionary processes and patterns of geographic variation in birds. Curr Ornithol 4:1–69Google Scholar

Copyright information

© Springer Science+Business Media B.V. 2009

Authors and Affiliations

  • Eric A. VanderWerf
    • 1
  • Lindsay C. Young
    • 2
  • Norine W. Yeung
    • 2
  • David B. Carlon
    • 2
  1. 1.Pacific Rim ConservationHonoluluUSA
  2. 2.Ecology, Evolution and Conservation Biology Program, Department of ZoologyUniversity of Hawaii at ManoaHonoluluUSA

Personalised recommendations