Chloroplast DNA phylogeography reveals the island colonisation route of Eucalyptus urophylla (Myrtaceae)
Kitt G. Payn A B C , William S. Dvorak B and Alexander A. Myburg AA Forest Molecular Genetics Programme, Department of Genetics, Forestry and Agricultural Biotechnology Institute (FABI), University of Pretoria, Pretoria 0002, South Africa.
B Camcore, North Carolina State University, PO Box 7626, Raleigh, NC 27695, USA.
C Corresponding author. Email: kitt.payn@fabi.up.ac.za
Australian Journal of Botany 55(7) 673-683 https://doi.org/10.1071/BT07056
Submitted: 29 March 2007 Accepted: 5 June 2007 Published: 15 November 2007
Abstract
We present a study of the colonisation patterns of a tropical tree species among an island archipelago. Eucalyptus urophylla (S.T.Blake) is an economically important plantation species endemic to the volcanic slopes of seven islands in eastern Indonesia. In the present study, we investigated the geographical distribution of chloroplast DNA sequence variation in E. urophylla to gain insight into its historical seed-migration routes. DNA sequence data were obtained from 198 plants from which 20 haplotypes were identified. A moderate to high level of chloroplast genetic differentiation (GST = 0.581, NST = 0.724) and significant phylogeographic structure (NST > GST; P < 0.01) were observed, suggesting low levels of recurrent seed-mediated gene flow among the islands. The highest levels of haplotype diversity were observed on the eastern islands of Wetar and Timor. The two most westerly islands, Flores and Lomblen, were fixed for what appeared to be the ancestral haplotype. Chloroplast haplotype diversity therefore exhibited a decreasing trend from east to west in the species’ range, consistent with an east-to-west colonisation route across the seven islands. Environmental factors that may have contributed to the contemporary spatial distribution of chloroplast DNA haplotypes include island paleogeology, ocean currents, fluctuations in sea levels and possible hybridisation events.
Acknowledgements
The authors thank G. E. McKinnon for valuable comments on the manuscript and D. Posada for the review of the nested clade design. We are grateful to PT Sumalindo Lestari Jaya for the seed collections, Camcore for locality and reference information, Mondi Business Paper South Africa for maintenance of the plant materials, Sappi Forestry South Africa for providing the E. alba plant material, and F. Maleka for technical assistance. Financial support for this work was provided by Mondi Business Paper South Africa through the Wood and Fibre Molecular Genetics Programme and by Camcore, Raleigh, NC, USA. Additional funding was provided by the Technology and Human Resources for Industry Programme (THRIP) in South Africa.
Audley-Charles MG
(2004) Ocean trench blocked and obliterated by Banda forearc collision with Australian proximal continental slope. Tectonophysics 389, 65–79.
| Crossref | GoogleScholarGoogle Scholar |
Avise J
(1998) The history and purview of phylogeography: a personal reflection. Molecular Ecology 7, 371–379.
| Crossref | GoogleScholarGoogle Scholar |
Birky CW
(1995) Uniparental inheritance of mitochondrial and chloroplast genes: mechanisms and evolution. Proceedings of the National Academy of Sciences USA 92, 11331–11338.
| Crossref | GoogleScholarGoogle Scholar |
Bottin L,
Tassin J,
Nasi R, Bouvet JM
(2007) Molecular, quantitative and abiotic variables for the delineation of evolutionary significant units: case of sandalwood (Santalum austrocaledonicum Vieillard) in New Caledonia. Conservation Genetics 8, 99–109.
| Crossref | GoogleScholarGoogle Scholar |
Brown P,
Sutikna T,
Morwood MJ,
Soejono RP,
Jatmiko
,
Saptomo EW, Due RA
(2004) A new small-bodied hominin from the late Pleistocene of Flores, Indonesia. Nature 431, 1055–1061.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Byrne M,
Moran GF, Tibbits WN
(1993) Restriction map and maternal inheritance of chloroplast DNA in Eucalyptus nitens. Journal of Heredity 84, 218–220.
Byrne M, Moran GF
(1994) Population divergence in the chloroplast genome of Eucalyptus nitens. Heredity 73, 18–28.
Castelloe J, Templeton AR
(1994) Root probabilities for intraspecific gene trees under neutral coalescent theory. Molecular Phylogenetics and Evolution 3, 102–113.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Cavers S,
Navarro C, Lowe AJ
(2003) Chloroplast DNA phylogeography reveals colonization history of Neotropical tree, Cedrela odorata L., in Mesoamerica. Molecular Ecology 12, 1451–1460.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Clement M,
Posada D, Crandall KA
(2000) tcs: a computer program to estimate gene genealogies. Molecular Ecology 9, 1657–1659.
| Crossref | tcs: a computer program to estimate gene genealogies.&journal=Molecular Ecology&volume=9&pages=1657-1659&publication_year=2000&author=KA%20Crandall&hl=en&doi=10.1046/j.1365-294x.2000.01020.x" target="_blank" rel="nofollow noopener noreferrer" class="reftools">GoogleScholarGoogle Scholar | PubMed |
Corriveau JL, Coleman AW
(1988) Rapid screening method to detect potential biparental inheritance of plastid DNA and results for over 200 angiosperm species. American Journal of Botany 75, 1443–1458.
| Crossref | GoogleScholarGoogle Scholar |
Crandall KA, Templeton AR
(1993) Empirical tests of some predictions from coalescent theory with applications to intraspecific phylogeny reconstruction. Genetics 134, 959–969.
| PubMed |
Demesure B,
Comps B, Petit RJ
(1996) Chloroplast DNA phylogeography of the common beech (Fagus sylvatica L.) in Europe. Evolution 50, 2515–2520.
| Crossref | GoogleScholarGoogle Scholar |
Dumolin-Lapegue S,
Demesure B,
Fineschi S,
Le Corre V, Petit RJ
(1997) Phylogeographic structure of white oaks throughout the European continent. Genetics 146, 1475–1487.
| PubMed |
Excoffier L,
Smouse P, Quattro JM
(1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131, 479–491.
| PubMed |
Ferris C,
King RA,
Vainola R, Hewitt GM
(1998) Chloroplast DNA recognizes three refugial sources of European oaks and suggests independent eastern and western immigrations to Finland. Heredity 80, 584–594.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Freeman JS,
Jackson HD,
Steane DA,
McKinnon GE,
Dutkowski GW,
Potts BM, Vaillancourt RE
(2001) Chloroplast phylogeography of Eucalyptus globulus. Australian Journal of Botany 49, 585–596.
| Crossref | GoogleScholarGoogle Scholar |
Gordon AL, Fine RA
(1996) Pathways of water between the Pacific and Indian oceans in the Indonesian seas. Nature 379, 146–149.
| Crossref | GoogleScholarGoogle Scholar |
Goulding SE,
Olmstead RG,
Morden CW, Wolfe KH
(1996) Ebb and flow of the chloroplast inverted repeat. Molecular & General Genetics 252, 195–206.
Heaney LR
(1991) A synopsis of climatic and vegetational change in southeast Asia. Climatic Change 19, 53–61.
| Crossref | GoogleScholarGoogle Scholar |
House APN, Bell JC
(1994) Isozyme variation and mating system in Eucalyptus urophylla S.T.Blake. Silvae Genetica 43, 167–176.
How RA,
Schmitt LH, Suyanto A
(1996) Geographical variation in the morphology of four snake species from the Lesser Sunda Islands, eastern Indonesia. Biological Journal of the Linnean Society 59, 439–456.
| Crossref | GoogleScholarGoogle Scholar |
Jackson HD,
Steane DA,
Potts BM, Vaillancourt RE
(1999) Chloroplast DNA evidence for reticulate evolution in Eucalyptus (Myrtaceae). Molecular Ecology 8, 739–751.
| Crossref | GoogleScholarGoogle Scholar |
Jones ME,
Shepherd M,
Henry RJ, Delves A
(2006) Chloroplast DNA variation and population structure in the widespread forest tree, Eucalyptus grandis. Conservation Genetics 7, 691–703.
| Crossref | GoogleScholarGoogle Scholar |
King RA, Ferris C
(1998) Chloroplast DNA phylogeography of Alnus glutinosa (L.) Gaertn. Molecular Ecology 7, 1151–1161.
| Crossref | GoogleScholarGoogle Scholar |
Ladiges PY,
Udovicic F, Nelson G
(2003) Australian biogeographical connections and the phylogeny of large genera in the plant family Myrtaceae. Journal of Biogeography 30, 989–998.
Marchelli P,
Gallo L,
Scholz F, Ziegenhagen B
(1998) Chloroplast DNA markers reveal a geographical divide across Argentinean southern beech Nothofagus nervosa (Phil.) Dim. et Mil. distribution area. Theoretical and Applied Genetics 97, 642–646.
| Crossref | GoogleScholarGoogle Scholar |
Martin B, Cossalter C
(1976) Les eucalyptus des iles de la Sonde. Bois et Foréts des Tropiques 164, 3–14.
McCauley DE
(1995) The use of chloroplast DNA polymorphism in studies of gene flow in plants. Trends in Ecology & Evolution 10, 198–202.
| Crossref | GoogleScholarGoogle Scholar |
McKinnon GE,
Steane DA,
Potts BM, Vaillancourt RE
(1999) Incongruence between chloroplast and species phylogenies in Eucalyptus subgenus Monocalyptus (Myrtaceae). American Journal of Botany 86, 1038–1046.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
McKinnon GE,
Vaillancourt RE,
Tilyard PA, Potts BM
(2001a) Maternal inheritance of the chloroplast genome in Eucalyptus globulus and interspecific hybrids. Genome 44, 831–835.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
McKinnon GE,
Vaillancourt RE,
Jackson HD, Potts BM
(2001b) Chloroplast sharing in the Tasmanian eucalypts. Evolution 55, 703–711.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Michaux B
(1991) Distributional patterns and tectonic development in Indonesia. Australian Systematic Botany 4, 25–36.
| Crossref | GoogleScholarGoogle Scholar |
Molcard R,
Fieux M, Syamsudin F
(2001) The throughflow within Ombai Strait. Deep-sea Research. Part I. Oceanographic Research Papers 48, 1237–1253.
| Crossref | GoogleScholarGoogle Scholar |
Myers N,
Mittermeier RA,
Mittermeier CG,
da Fonseca GAB, Kent J
(2000) Biodiversity hotspots for conservation priorities. Nature 403, 853–858.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Norvick MS
(1979) The tectonic history of the Banda Arcs, eastern Indonesia: a review. Journal of the Geological Society London 136, 519–527.
Pepe B,
Surata K,
Suhartono F,
Sipayung M,
Purwanto A, Dvorak WS
(2004) Conservation status of natural populations of Eucalyptus urophylla in Indonesia and international efforts to protect dwindling gene pools. Forest Genetic Resources [FAO: Rome] 31, 62–64.
Petit RJ,
Pineau E,
Demesure B,
Bacilierir R,
Ducousso A, Kremer A
(1997) Chloroplast DNA footprints of postglacial recolonization by oaks. Proceedings of the National Academy of Sciences USA 94, 9996–10001.
| Crossref | GoogleScholarGoogle Scholar |
Petit RJ,
Aguinagalde I,
de Beaulieu JL,
Bittkau C,
Brewer S,
Cheddadi R,
Ennos R,
Fineschi S,
Grivet D,
Lascoux M,
Mohanty A,
Müller-Starck G,
Demesure-Musch B,
Palmé A,
Martin JP,
Rendell S, Vendramin GG
(2003) Glacial refugia: hotspots but not melting pots of genetic diversity. Science 300, 1563–1565.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Petit RJ,
Duminil J,
Fineschi S,
Hampe A,
Salvini D, Vendramin GG
(2005) Comparative organisation of chloroplast, mitochondrial and nuclear diversity in plant populations. Molecular Ecology 14, 689–701.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Pons O, Petit RJ
(1996) Measuring and testing genetic differentiation with ordered vs. unodered alleles. Genetics 144, 1237–1245.
| PubMed |
Posada D,
Crandall KA, Templeton AR
(2000) Geodis: a program for cladistic nested analysis of the geographical distribution of genetic haplotypes. Molecular Ecology 9, 487–488.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Pryor LD,
Williams ER, Gunn BV
(1995) A morphometric analysis of Eucalyptus urophylla and some related taxa with descriptions of two new species. Australian Systematic Botany 8, 57–70.
| Crossref | GoogleScholarGoogle Scholar |
Rozas J,
Sánchez-DelBarrio JC,
Messeguer X, Rozas R
(2003) DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19, 2496–2497.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Sewell MM,
Parks CR, Chase MW
(1996) Intraspecific chloroplast DNA variation and biogeography of North American Liriodendron L. (Magnoliaceae). Evolution 50, 1147–1154.
| Crossref | GoogleScholarGoogle Scholar |
Steane DA,
Byrne M,
Vaillancourt RE, Potts BM
(1998) Chloroplast DNA polymorphism signals complex interspecific interactions in Eucalyptus (Myrtaceae). Australian Systematic Botany 11, 25–40.
| Crossref | GoogleScholarGoogle Scholar |
Templeton AR
(2004) Statistical phylogeography: methods of evaluating and minimizing inference errors. Molecular Ecology 13, 789–809.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Templeton AR, Sing CF
(1993) A cladistic analysis of phenotypic associations with haplotypes inferred from restriction endonuclease mapping. IV. Nested analysis with cladogram uncertainty and recombination. Genetics 134, 659–669.
| PubMed |
Templeton AR,
Boerwinkle E, Sing CF
(1987) A cladistic analysis of phenotypic associations with haplotypes inferred from restriction endonuclease mapping. I. Basic theory and an analysis of alcohol dehydrogenase activity in Drosophila. Genetics 117, 343–352.
| PubMed |
Templeton AR,
Crandall KA, Sing CF
(1992) A cladistic analysis of phenotypic associations with haplotypes inferred from restriction endonuclease mapping and DNA sequence data. III. Cladogram estimation. Genetics 132, 619–633.
| PubMed |
Vaillancourt RE, Jackson HD
(2000) A chloroplast DNA hypervariable region in eucalypts. Theory of Applied Genetics 101, 473–477.
| Crossref | GoogleScholarGoogle Scholar |
Voris HK
(2000) Maps of Pleistocene sea levels in Southeast Asia: shorelines, river systems and time durations. Journal of Biogeography 27, 1153–1167.
| Crossref | GoogleScholarGoogle Scholar |
Wallace AR
(1860) On the zoological geography of the Malay archipelago. Journal of the Linnean Society of London 4, 172–184.
van der Werff W
(1995) Cenozoic evolution of the Savu Basin, Indonesia: forearc basin response to arc-continent collision. Marine and Petroleum Geology 12, 247–262.
| Crossref | GoogleScholarGoogle Scholar |
Zhang AB,
Tan S, Sota T
(2006) Autoinfer 1.0: a computer program to infer biogeographical events automatically. Molecular Ecology Notes 6, 597–599.
| Crossref | GoogleScholarGoogle Scholar |
