Proceedings of the Royal Society B: Biological Sciences
Restricted access Research articles

Not an ancient relic: the endemic Livistona palms of arid central Australia could have been introduced by humans

Toshiaki Kondo

Toshiaki Kondo

Graduate School for International Development and Cooperation, Hiroshima University, Higashi-Hiroshima 739-8529, Japan

[email protected]

Google Scholar

Find this author on PubMed

,
Michael D. Crisp

Michael D. Crisp

Research School of Biology, The Australian National University, Canberra, Australian Capital Territory 0200, Australia

Google Scholar

Find this author on PubMed

,
Celeste Linde

Celeste Linde

Research School of Biology, The Australian National University, Canberra, Australian Capital Territory 0200, Australia

Google Scholar

Find this author on PubMed

,
David M. J. S. Bowman

David M. J. S. Bowman

School of Plant Science, The University of Tasmania, Private Bag 55, Hobart, Tasmania 7001, Australia

Google Scholar

Find this author on PubMed

,
Kensuke Kawamura

Kensuke Kawamura

Graduate School for International Development and Cooperation, Hiroshima University, Higashi-Hiroshima 739-8529, Japan

Google Scholar

Find this author on PubMed

,
Shingo Kaneko

Shingo Kaneko

Graduate School of Agriculture, Kyoto University, Kyoto 606-8502, Japan

Google Scholar

Find this author on PubMed

and
Yuji Isagi

Yuji Isagi

Graduate School of Agriculture, Kyoto University, Kyoto 606-8502, Japan

Google Scholar

Find this author on PubMed

    Livistona mariae is an endemic palm localized in arid central Australia. This species is separated by about 1000 km from its congener L. rigida, which grows distantly in the Roper River and Nicholson–Gregory River catchments in northern Australia. Such an isolated distribution of L. mariae has been assumed to have resulted from contraction of ancestral populations as Australia aridified from the Mid-Miocene (ca 15 Ma). To test this hypothesis at the population level, we examined the genetic relationships among 14 populations of L. mariae and L. rigida using eight nuclear microsatellite loci. Our population tree and Bayesian clustering revealed that these populations comprised two genetically distinct groups that did not correspond to the current classification at species rank, and L. mariae showed closest affinity with L. rigida from Roper River. Furthermore, coalescent divergence-time estimations suggested that the disjunction between the northern populations (within L. rigida) could have originated by intermittent colonization along an ancient river that has been drowned repeatedly by marine transgression. During that time, L. mariae populations could have been established by opportunistic immigrants from Roper River about 15 000 years ago, concurrently with the settlement of indigenous Australians in central Australia, who are thus plausible vectors. Thus, our results rule out the ancient relic hypothesis for the origin of L. mariae.

    References

    • 1
      Burbidge N. T. . 1960 The phytogeography of the Australian region. Aust. J. Bot. 8, 75–209.doi: 10.1071/BT9600075 (doi:10.1071/BT9600075). CrossrefGoogle Scholar
    • 2
      Barlow B. A. . 1981 The Australian flora: its origin and evolution. Flora of Australia, vol. 1 (ed. & George A. S. ), pp. 25–75. Canberra, Australia: Australian Government Public Service. Google Scholar
    • 3
      Keast A. . 1981 Ecological biogeography of Australia. The Hague, The Netherlands: Dr W. Junk Publishers. CrossrefGoogle Scholar
    • 4
      Crisp M. D., Cook L.& Steane D. . 2004 Radiation of the Australian flora: What can comparisons of molecular phylogenies across multiple taxa tell us about the evolution of diversity in present-day communities? Phil. Trans. R. Soc. Lond. B 359, 1551–1571.doi: 10.1098/rstb.2004.1528 (doi:10.1098/rstb.2004.1528). Link, ISIGoogle Scholar
    • 5
      Byrne M., et al. 2008 Birth of a biome: insight into the assembly and maintenance of the Australian arid zone biota. Mol. Ecol. 17, 4398–4417.doi: 10.1111/j.1365-294X.2008.03899.x (doi:10.1111/j.1365-294X.2008.03899.x). Crossref, PubMed, ISIGoogle Scholar
    • 6
      Byrne M., et al. 2011 Decline of a biome: evolution, contraction, fragmentation, extinction and invasion of the Australian mesic zone biota. J. Biogeogr. (doi:10.1111/j.1365-2699.2011.02535.x). Crossref, ISIGoogle Scholar
    • 7
      Bowman D. M. J. S., et al. 2010 Biogeography of the Australian monsoon tropics. J. Biogeogr. 37, 201–216.doi: 10.1111/j.1365-2699.2009.02210.x (doi:10.1111/j.1365-2699.2009.02210.x). Crossref, ISIGoogle Scholar
    • 8
      Chippendale G. M. . 1963 The relic nature of some central Australian plants. Trans. R. Soc. Aust. 86, 31–34. Google Scholar
    • 9
      Latz P. K. . 1996 Knowledge of relict plants in central Australia: a measure of botanical research during the last 100 years. Exploring central Australia: society, the environment and the 1984 Horn expedition (eds , Morton S. R.& Mulvaney D. J. ), pp. 225–229. Chipping Norton, Oxfordshire, UK: Surrey Beatty and Sons. Google Scholar
    • 10
      Box J. B., Duguid A., Read R. E., Kimber R. G., Knapton A., Davis J.& Bowland A. E. . 2008 Central Australian waterbodies: the importance of permanence in a desert landscape. J. Arid Environ. 72, 1395–1413.doi: 10.1016/j.jaridenv.2008.02.022 (doi:10.1016/j.jaridenv.2008.02.022). Crossref, ISIGoogle Scholar
    • 11
      Rodd A. N. . 1998 Revision of Livistona (Arecaceae) in Australia. Telopea 8, 49–153. CrossrefGoogle Scholar
    • 12
      Dowe J. L. . 2009 A taxonomic account of Livistona R.Br. (Arecaceae). Gard. Bull. Singapore 60, 185–344. Google Scholar
    • 13
      Latz P. K. . 1975 Notes on the relict palm Livistona mariae in central Australia. Trans. R. Soc. South. Aust. 99, 189–196. Google Scholar
    • 14
      Kerrigan R.& Albrecht D. . 2006 Threatened species of the Northern Territory: Palm Valley Palm, Red Cabbage Palm, central Australian Cabbage Palm Livistona mariae subsp. mariae. Threatened species profile. See http://www.nt.gov.au/nreta/wildlife/animals/threatened/pdf/plants/Livistona_mariae_mariae_VU.pdf. Google Scholar
    • 15
      Dowe J. L. . 1995 A preliminary review of the biogeography of Australian palms. Mooreana 2, 7–22. Google Scholar
    • 16
      Crisp M. D., Isagi Y., Kato Y., Cook L. G.& Bowman D. M. J. S. . 2010 Livistona palms in Australia: ancient relics or opportunistic immigrants? Mol. Phylogenet. Evol. 54, 512–523.doi: 10.1016/j.ympev.2009.09.020 (doi:10.1016/j.ympev.2009.09.020). Crossref, PubMed, ISIGoogle Scholar
    • 17
      Langford R. P., Wilford G. E., Truswell E. M.& Isern A. R. . 1995 Palaeogeographic atlas of Australia, vol. 10. Cainozoic. Canberra, Australia: Australian Geological Survey Organization. Google Scholar
    • 18
      Chivas A. R., et al. 2001 Sea-level and environmental changes since the last interglacial in the Gulf of Carpentaria, Australia: an overview. Quat. Int. 83–85, 19–46.doi: 10.1016/S1040-6182(01)00029-5 (doi:10.1016/S1040-6182(01)00029-5). Crossref, ISIGoogle Scholar
    • 19
      Stewart C. N.& Via L. E. . 1993 A rapid CTAB DNA isolation technique useful for RAPD fingerprinting and other applications. Biotechniques 14, 748–750. PubMed, ISIGoogle Scholar
    • 20
      Kaneko S., Kondo T.& Isagi Y. . 2011 Development of microsatellite markers for the northern Australian endemic fan palm Livistona rigida (Arecaceae), with cross-amplification in the five related species. Conserv. Genet. Resour. 3, 697–699.doi: 10.1007/s12686-011-9436-1 (doi:10.1007/s12686-011-9436-1). Crossref, ISIGoogle Scholar
    • 21
      Van Oosterhout C., Hutchinson W. F., Wills D. P. M.& Shipley P. . 2004 Micro-Checker: software for identifying and correcting genotype errors in microsatellite data. Mol. Ecol. Notes 4, 535–538.doi: 10.1111/j.1471-8286.2004.00684.x (doi:10.1111/j.1471-8286.2004.00684.x). CrossrefGoogle Scholar
    • 22
      Cavalli-Sforza L. L.& Edwards A. W. F. . 1967 Phylogenetic analysis: models and estimation procedures. Evolution 32, 550–570.doi: 10.2307/2406616 (doi:10.2307/2406616). Crossref, ISIGoogle Scholar
    • 23
      Saitou N.& Nei M. . 1987 The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 4, 406–425. PubMed, ISIGoogle Scholar
    • 24
      Felsenstein J. . 2004 phylip: phylogeny inference package. Seattle, WA: Department of Genome Sciences and Department of Biology, University of Washington. Google Scholar
    • 25
      Takezaki N.& Nei M. . 1996 Genetic distances and reconstruction of phylogenetic trees from microsatellite DNA. Genetics 144, 389–399. Crossref, PubMed, ISIGoogle Scholar
    • 26
      Orscheg C. K.& Parsons R. F. . 1996 Ecology of Livistona australis (R. Br.) Martius at its southern limit, south-eastern Australia: I. Distribution and genetic variation. Mooreana 6, 8–17. Google Scholar
    • 27
      Evanno G., Regnaut S.& Goudet J. . 2005 Detecting the number of clusters of individuals using the software structure: a simulation study. Mol. Ecol. 14, 2611–2620.doi: 10.1111/j.1365-294X.2005.02553.x (doi:10.1111/j.1365-294X.2005.02553.x). Crossref, PubMed, ISIGoogle Scholar
    • 28
      Hey J.& Nielsen R. . 2004 Multilocus methods for estimating population sizes, migration rates and divergence time, with applications to the divergence of Drosophila pseudoobscura and D. persimilis. Genetics 167, 747–760.doi: 10.1534/genetics.103.024182 (doi:10.1534/genetics.103.024182). Crossref, PubMed, ISIGoogle Scholar
    • 29
      Estoup A., Jarne P.& Cornuet J. M. . 2002 Homoplasy and mutation model at microsatellite loci and their consequences for population genetics analysis. Mol. Ecol. 11, 1591–1604.doi: 10.1046/j.1365-294X.2002.01576.x (doi:10.1046/j.1365-294X.2002.01576.x). Crossref, PubMed, ISIGoogle Scholar
    • 30
      Sun J. X., Mullikin J. C., Patterson N.& Reich D. E. . 2009 Microsatellites are molecular clocks that support accurate inferences about history. Mol. Biol. Evol. 26, 1017–1027.doi: 10.1093/molbev/msp025 (doi:10.1093/molbev/msp025). Crossref, PubMed, ISIGoogle Scholar
    • 31
      Thuillet A.-C., Bru D., David J., Roumet P., Santoni S., Sourdille P.& Bataillon T. . 2002 Direct estimation of mutation rate for 10 microsatellite loci in durum wheat, Triticum turgidum (L.) Thell. ssp. durum Desf. Mol. Biol. Evol. 19, 122–125.doi: 10.1093/oxfordjournals.molbev.a003977 (doi:10.1093/oxfordjournals.molbev.a003977). Crossref, PubMed, ISIGoogle Scholar
    • 32
      Girod C., Vitalis R., Leblois R.& Fréville H. . 2011 Inferring population decline and expansion from microsatellite data: a simulation-based evaluation of the Msvar method. Genetics 188, 165–179.doi: 10.1534/genetics.110.121764 (doi:10.1534/genetics.110.121764). Crossref, PubMed, ISIGoogle Scholar
    • 33
      Weir B. S.& Cockerham C. C. . 1984 Estimating F-statistics for the analysis of population structure. Evolution 38, 1358–1370.doi: 10.2307/2408641 (doi:10.2307/2408641). Crossref, PubMed, ISIGoogle Scholar
    • 34
      Goudet J. . 1995 fstat (version 1.2): a computer program to calculate F-statistics. J. Hered. 86, 485–486. Crossref, ISIGoogle Scholar
    • 35
      Peakall R.& Smouse P. E. . 2001 genalex (version 5.1): genetic analysis in Excel. Population genetic software for teaching and research. Canberra, Australia: Australian National University. See www.anu.edu.au/BoZo/GenAlEx/. Google Scholar
    • 36
      El Mousadik A.& Petit R. J. . 1996 Chloroplast DNA phylogeography of the Argan tree of Morocco. Mol. Ecol. 5, 547–555.doi: 10.1046/j.1365-294X.1996.00123.x (doi:10.1046/j.1365-294X.1996.00123.x). Crossref, PubMed, ISIGoogle Scholar
    • 37
      Nei M. . 1972 Genetic distance between populations. Am. Nat. 106, 283–292.doi: 10.1086/282771 (doi:10.1086/282771). Crossref, ISIGoogle Scholar
    • 38
      François O.& Durand E. . 2010 Spatially explicit Bayesian clustering models in population genetics. Mol. Ecol. Res. 10, 773–784.doi: 10.1111/j.1755-0998.2010.02868.x (doi:10.1111/j.1755-0998.2010.02868.x). Crossref, PubMed, ISIGoogle Scholar
    • 39
      Pritchard J. K., Stephens M.& Donnelly P. . 2000 Inference of population structure using multilocus genotype data. Genetics 155, 945–959. Crossref, PubMed, ISIGoogle Scholar
    • 40
      Excoffier L.& Schneider S. . 2005 Arlequin, version 3.0: an integrated software package for population genetics data analysis. Evol. Bioinform. Online 1, 47–50. Crossref, ISIGoogle Scholar
    • 41
      Hewitt G. M. . 1996 Some genetic consequences of ice ages, and their role in divergence and speciation. Biol. J. Linn. Soc. 58, 247–276.doi: 10.1006/bijl.1996.0035 (doi:10.1006/bijl.1996.0035). Crossref, ISIGoogle Scholar
    • 42
      Jones M. R.& Torgersen T. . 1988 Late Quaternary evolution of Lake Carpentaria on the Australia–New Guinea continental shelf. Aust. J. Earth Sci. 35, 313–324.doi: 10.1080/08120098808729450 (doi:10.1080/08120098808729450). Crossref, ISIGoogle Scholar
    • 43
      Harold K. V. . 2000 Maps of Pleistocene sea levels in Southeast Asia: shorelines, river systems and time durations. J. Biogeogr. 27, 1153–1167.doi: 10.1046/j.1365-2699.2000.00489.x (doi:10.1046/j.1365-2699.2000.00489.x). Crossref, ISIGoogle Scholar
    • 44
      Hewitt G. M. . 2000 The genetic legacy of the Quaternary ice ages. Nature 405, 907–913.doi: 10.1038/35016000 (doi:10.1038/35016000). Crossref, PubMed, ISIGoogle Scholar
    • 45
      Petit R. J., et al. 2003 Glacial refugia: hotspots but not melting pots of genetic diversity. Science 300, 1563–1565.doi: 10.1126/science.1083264 (doi:10.1126/science.1083264). Crossref, PubMed, ISIGoogle Scholar
    • 46
      Smith M. A. . 2009 Late Quaternary landscapes in Central Australia: sedimentary history and palaeoecology of Puritjarra rock shelter. J. Quat. Sci. 24, 747–760.doi: 10.1002/jqs.1249 (doi:10.1002/jqs.1249). Crossref, ISIGoogle Scholar
    • 47
      Balick M. J.& Beck H. C. . 1990 Useful palms of the world: a synoptic bibliography. New York, NY: Columbia University Press. Google Scholar
    • 48
      O'Connor S. . 2007 New evidence from East Timor contributes to our understanding of earliest modern human colonisation east of the Sunda Shelf. Antiquity 81, 523–535. Crossref, ISIGoogle Scholar
    • 49
      Veth P., Smith M. A., Bowler J., Fitzsimmons K. E., Williams A.& Hiscock P. . 2009 Excavations at Parnkupirti, Lake Gregory, Great Sandy Desert: OSL ages for occupation before the Last Glacial Maximum. Aust. Archaeol. 69, 1–10. CrossrefGoogle Scholar
    • 50
      Smith M. A. . 1987 Pleistocene occupation in arid Central Australia. Nature 328, 710–711.doi: 10.1038/328710a0 (doi:10.1038/328710a0). Crossref, ISIGoogle Scholar
    • 51
      O'Connor S., Veth P.& Campbell C. . 1998 Serpent's Glen rockshelter: report of the first Pleistocene-aged occupation sequence from the Western Desert. Aust. Archaeol. 46, 12–22. CrossrefGoogle Scholar
    • 52
      Thorley P. B. . 1998 Pleistocene settlement in the Australian arid zone: occupation of an inland riverine landscape in the central Australian ranges. Antiquity 72, 34–45. Crossref, ISIGoogle Scholar