Genetic variation and phylogeography of the Australian and New Zealand fern Asplenium flabellifolium (Aspleniaceae)
Daniel J. Ohlsen A D , Lara D. Shepherd B , Leon R. Perrie B , Patrick J. Brownsey B and Michael J. Bayly CA Royal Botanic Gardens, Private Bag 2000, Birdwood Avenue, South Yarra, Vic. 3141, Australia.
B Museum of New Zealand Te Papa Tongarewa, PO Box 467, 55 Cable Street, Wellington, 6140, New Zealand.
C School of BioSciences, The University of Melbourne, Royal Parade, Parkville, Vic. 3010, Australia.
D Corresponding author. Email: ohlsend@gmail.com
Australian Systematic Botany 33(4) 412-426 https://doi.org/10.1071/SB20001
Submitted: 9 January 2020 Accepted: 8 April 2020 Published: 1 June 2020
Abstract
Asplenium flabellifolium Cav. is a cytologically variable Australian and New Zealand fern. Here, we sequence chloroplast trnL-trnF and rps4-trnS from samples throughout its range to provide the first phylogeographic investigation of a fern common in both countries. Twenty-three haplotypes were detected, which formed six haplogroups in a network. Australian specimens were placed in all haplogroups. The placement of New Zealand haplotypes in five of the haplogroups suggests that this species has dispersed across the Tasman Sea at least five times. Sexually reproducing plants of lower ploidy, detected only in south-eastern Australia, contained haplotypes from the two haplogroups that are successive sisters to the remaining diversity in the phylogeny. This likely suggests that A. flabellifolium was originally a sexually reproducing species in south-eastern Australia and spread to the rest of its distribution where apomictic plants dominate. More than one haplogroup was detected in several areas across its distribution, suggesting that these areas were colonised several times. Other areas harboured several haplotypes from a single haplogroup or haplogroups not recovered elsewhere, indicating possible long-term persistence in these areas. Haplotypes and morphological features were not found to be exclusive to either breeding system or ploidy and no taxonomic revision is proposed.
Additional keywords: apomixis, long-distance dispersal, refugia, taxonomy, trans-Tasman dispersal.
References
Arjen de Groot G, Verduyn B, Wubs ERJ, Erkens RHJ, During HJ (2012) Inter- and intraspecific variation in fern mating systems after long-distance colonization: the importance of selfing. BMC Plant Biology 12,| Inter- and intraspecific variation in fern mating systems after long-distance colonization: the importance of selfing.Crossref | GoogleScholarGoogle Scholar |
Bai W-N, Liao W-J, Zhang D-Y (2010) Nuclear and chloroplast DNA phylogeography reveal two refuge areas with asymmetrical gene flow in a temperate walnut tree from East Asia. New Phytologist 188, 892–901.
| Nuclear and chloroplast DNA phylogeography reveal two refuge areas with asymmetrical gene flow in a temperate walnut tree from East Asia.Crossref | GoogleScholarGoogle Scholar | 20723077PubMed |
Barrington DS, Paris CA (1986) Systematic inferences from spore and stomata size in the ferns. American Fern Journal 76, 149–159.
| Systematic inferences from spore and stomata size in the ferns.Crossref | GoogleScholarGoogle Scholar |
Beck JB, Allison JR, Pryer KM, Windham MD (2012) Identifying multiple origins of polyploid taxa: a multilocus study of the hybrid cloak fern (Astrolepis integerrima; Pteridaceae). American Journal of Botany 99, 1857–1865.
| Identifying multiple origins of polyploid taxa: a multilocus study of the hybrid cloak fern (Astrolepis integerrima; Pteridaceae).Crossref | GoogleScholarGoogle Scholar | 23108464PubMed |
Bloomfield JA, Nevill P, Potts BM, Vaillancourt RE, Steane DA (2011) Molecular genetic variation in a widespread forest tree species Eucalyptus obliqua (Myrtaceae) on the island of Tasmania. Australian Journal of Botany 59, 226–237.
| Molecular genetic variation in a widespread forest tree species Eucalyptus obliqua (Myrtaceae) on the island of Tasmania.Crossref | GoogleScholarGoogle Scholar |
Brownsey PJ (1977) A taxonomic revision of the New Zealand species of Asplenium. New Zealand Journal of Botany 15, 39–86.
| A taxonomic revision of the New Zealand species of Asplenium.Crossref | GoogleScholarGoogle Scholar |
Brownsey PJ (1998) Aspleniaceae. In ‘Flora of Australia. Ferns, Gymnosperms and Allied Groups. Vol. 48’. (Ed. PM McCarthy) pp. 295–327. (ABRS: Canberra, ACT, Australia; and CSIRO: Melbourne, Vic., Australia)
Brownsey PJ (2001) New Zealand’s pteridophyte flora-plants of ancient lineage but recent arrival? Brittonia 53, 284–303.
| New Zealand’s pteridophyte flora-plants of ancient lineage but recent arrival?Crossref | GoogleScholarGoogle Scholar |
Brownsey PJ, Perrie LR (2018) Aspleniaceae. In ‘Flora of New Zealand: Ferns and Lycophytes.’ (Eds I Breitwieser, AD Wilton) Fascicle 18. (Manaaki Whenua Press: Lincoln, New Zealand)
Byrne M, Hines B (2004) Phylogeographical analysis of cpDNA variation in Eucalyptus loxophleba (Myrtaceae). Australian Journal of Botany 52, 459–470.
| Phylogeographical analysis of cpDNA variation in Eucalyptus loxophleba (Myrtaceae).Crossref | GoogleScholarGoogle Scholar |
Byrne M, Hopper SD (2008) Granite outcrops as ancient islands in old landscapes: evidence from the phylogeography and population genetics of Eucalyptus caesia (Myrtaceae) in Western Australia. Biological Journal of the Linnean Society. Linnean Society of London 93, 177–188.
| Granite outcrops as ancient islands in old landscapes: evidence from the phylogeography and population genetics of Eucalyptus caesia (Myrtaceae) in Western Australia.Crossref | GoogleScholarGoogle Scholar |
Byrne M, Macdonald B, Coates D (1999) Divergence in the chloroplast genome and nuclear rDNA of the rare Western Australian plant Lambertia orbifolia Gardner (Proteaceae). Molecular Ecology 8, 1789–1796.
| Divergence in the chloroplast genome and nuclear rDNA of the rare Western Australian plant Lambertia orbifolia Gardner (Proteaceae).Crossref | GoogleScholarGoogle Scholar | 10620223PubMed |
Byrne M, Macdonald B, Coates D (2002) Phylogeographical patterns in chloroplast DNA variation within the Acacia acuminata (Leguminosae: Mimosoideae) complex in Western Australia. Journal of Evolutionary Biology 15, 576–587.
| Phylogeographical patterns in chloroplast DNA variation within the Acacia acuminata (Leguminosae: Mimosoideae) complex in Western Australia.Crossref | GoogleScholarGoogle Scholar |
Byrne M, Macdonald B, Brand J (2003) Phylogeography and divergence in the chloroplast genome in Western Australian sandalwood (Santalum spicatum). Heredity 91, 389–395.
| Phylogeography and divergence in the chloroplast genome in Western Australian sandalwood (Santalum spicatum).Crossref | GoogleScholarGoogle Scholar | 14512954PubMed |
Conolly JR, von der Borch CC (1967) Sedimentation and physiography of the sea floor south of Australia. Sedimentary Geology 1, 181–220.
| Sedimentation and physiography of the sea floor south of Australia.Crossref | GoogleScholarGoogle Scholar |
Crisp MD, Cook LG (2007) A congruent molecular signature of vicariance across multiple plant lineages. Molecular Phylogenetics and Evolution 43, 1106–1117.
| A congruent molecular signature of vicariance across multiple plant lineages.Crossref | GoogleScholarGoogle Scholar | 17434758PubMed |
Dyer RJ, Savolainen V, Schneider H (2012) Apomixis and reticulate evolution in the Asplenium monanthes fern complex. Annals of Botany 110, 1515–1529.
| Apomixis and reticulate evolution in the Asplenium monanthes fern complex.Crossref | GoogleScholarGoogle Scholar | 22984165PubMed |
Elshire RJ, Glaubitz JC, Sun Q, Poland JA, Kawamoto K, Bucler ES, Mitchell SE (2011) A robust, simple genotyping-by-sequencing (GBS) approach for high diversity species. PLoS One 6, e19379
| A robust, simple genotyping-by-sequencing (GBS) approach for high diversity species.Crossref | GoogleScholarGoogle Scholar | 21573248PubMed |
Frahm J-P (2008) Diversity, dispersal and biogeography of bryophytes (mosses). Biodiversity and Conservation 17, 277–284.
| Diversity, dispersal and biogeography of bryophytes (mosses).Crossref | GoogleScholarGoogle Scholar |
Freeman JS, Jackson HD, Steane DA, McKinnon GE, Potts BM, Vaillancourt RE (2001) Chloroplast DNA phylogeography of Eucalyptus globulus. Australian Journal of Botany 49, 585–596.
| Chloroplast DNA phylogeography of Eucalyptus globulus.Crossref | GoogleScholarGoogle Scholar |
Gastony GJ, Haufler CH (1976) Chromosome numbers and apomixis in the fern genus Bommeria (Gymnogrammaceae). Biotropica 8, 1–11.
| Chromosome numbers and apomixis in the fern genus Bommeria (Gymnogrammaceae).Crossref | GoogleScholarGoogle Scholar |
Gastony GJ, Windham MD (1989) Species concepts in pteridophytes: the treatment and definition of agamosporous species. American Fern Journal 79, 65–77.
| Species concepts in pteridophytes: the treatment and definition of agamosporous species.Crossref | GoogleScholarGoogle Scholar |
Grusz AL (2016) A current perspective on apomixes in ferns. Journal of Systematics and Evolution 54, 656–665.
| A current perspective on apomixes in ferns.Crossref | GoogleScholarGoogle Scholar |
Grusz AL, Windham MD, Pryer KM (2009) Deciphering the origins of apomictic polyploids in the Cheilanthes yavapensis complex (Pteridaceae). American Journal of Botany 96, 1636–1645.
| Deciphering the origins of apomictic polyploids in the Cheilanthes yavapensis complex (Pteridaceae).Crossref | GoogleScholarGoogle Scholar | 21622350PubMed |
Grusz AL, Windham MD, Yatskievych G, Huiet L, Gastony GJ, Pryer KM (2014) Patterns of diversification in the xeric-adapted fern genus Myriopteris (Pteridaceae). Systematic Botany 39, 698–714.
| Patterns of diversification in the xeric-adapted fern genus Myriopteris (Pteridaceae).Crossref | GoogleScholarGoogle Scholar |
Guindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W, Gascuel O (2010) New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Systematic Biology 59, 307–321.
| New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0.Crossref | GoogleScholarGoogle Scholar | 20525638PubMed |
Heenan PB, McGlone MS (2019) Cenozoic formation and colonization history of the New Zealand vascular flora based on molecular clock dating of the plastid rbcL gene. New Zealand Journal of Botany 57, 204–226.
| Cenozoic formation and colonization history of the New Zealand vascular flora based on molecular clock dating of the plastid rbcL gene.Crossref | GoogleScholarGoogle Scholar |
Hickok LG, Klekowski EJ (1974) Inchoate speciation in Ceratopteris: an analysis of the synthesized hybrid C. richardii × C. pteridoides. Evolution 28, 439–446.
| Inchoate speciation in Ceratopteris: an analysis of the synthesized hybrid C. richardii × C. pteridoides.Crossref | GoogleScholarGoogle Scholar | 28564836PubMed |
Hori K, Tono A, Fujimoto K, Kato J, Ebihara A, Watano Y, Murakami N (2014) Reticulate evolution in the apogamous Dryopteris varia complex (Dryopteridaceae, subg. Erythrovariae, sect. Variae) and its related sexual species in Japan. Journal of Plant Research 127, 661–684.
| Reticulate evolution in the apogamous Dryopteris varia complex (Dryopteridaceae, subg. Erythrovariae, sect. Variae) and its related sexual species in Japan.Crossref | GoogleScholarGoogle Scholar | 25064510PubMed |
Huelsenbeck JP, Ronquist FR (2001) MrBayes: Bayesian inference of phylogeny. Biometrics 17, 754–755.
Jaarola M, Tegelstrom H (1995) Colonization history of north European field voles (Microtus agrestis) revealed by mitochondrial DNA. Molecular Ecology 4, 299–310.
| Colonization history of north European field voles (Microtus agrestis) revealed by mitochondrial DNA.Crossref | GoogleScholarGoogle Scholar | 7663749PubMed |
Jordan GJ (2001) An investigation of long-distance dispersal based on species native to both Tasmania and New Zealand. Australian Journal of Botany 49, 333–340.
| An investigation of long-distance dispersal based on species native to both Tasmania and New Zealand.Crossref | GoogleScholarGoogle Scholar |
Keppel G, Van Niel KP, Wardell-Johnson GW, Yates CJ, Byrne M, Mucina L, Schut AGT, Hopper SD, Franklin SE (2012) Refugia: identifying and understanding safe havens for biodiversity under climate change. Global Ecology and Biogeography 21, 393–404.
| Refugia: identifying and understanding safe havens for biodiversity under climate change.Crossref | GoogleScholarGoogle Scholar |
Korall P, Schuettpelz E, Pryer KM (2010) Abrupt deceleration of molecular evolution linked to the origin of arborescence in ferns. Evolution 64, 2786–2792.
| Abrupt deceleration of molecular evolution linked to the origin of arborescence in ferns.Crossref | GoogleScholarGoogle Scholar | 20394660PubMed |
Lovis JD (1973) A biosystematic approach to phylogenetic problems and its application to the Aspleniaceae. Botanical Journal of the Linnean Society 67, 211–228.
Manton I (1950) ‘Problems of Cytology and Evolution in the Pteridophyte.’ (Cambridge University Press: London, UK)
McCarthy PM (Ed.) (1998) ‘Flora of Australia. Ferns, Gymnosperms and Allied Groups. Vol. 4.’ (ABRS: Canberra, ACT, Australia; and CSIRO: Melbourne, Vic., Australia)
McDaniel SF, Shaw AJ (2003) Phylogeographic structure and cryptic speciation in the trans-Antarctic moss Pyrrhobryum mnioides. Evolution 57, 205–215.
| Phylogeographic structure and cryptic speciation in the trans-Antarctic moss Pyrrhobryum mnioides.Crossref | GoogleScholarGoogle Scholar | 12683518PubMed |
McKinnon GE, Jordan GJ, Vaillancourt RE, Steane DA, Potts BM (2004) Glacial refugia and reticulate evolution: the case of the Tasmanian eucalypts. Philosophical Transactions of the Royal Society of London – B. Biological Sciences 359, 275–284.
| Glacial refugia and reticulate evolution: the case of the Tasmanian eucalypts.Crossref | GoogleScholarGoogle Scholar | 15101583PubMed |
Meudt HM, Bayly MJ (2008) Phylogeographic patterns in the Australasian genus Chionohebe (Veronica s.l., Plataginaceae) based on AFLP and chloroplast DNA sequences. Molecular Phylogenetics and Evolution 47, 319–338.
| Phylogeographic patterns in the Australasian genus Chionohebe (Veronica s.l., Plataginaceae) based on AFLP and chloroplast DNA sequences.Crossref | GoogleScholarGoogle Scholar | 18299210PubMed |
Milner ML, Rossetto M, Crisp MD, Weston PH (2012) The impact of multiple biogeographic barriers and hybridization on species-level differentiation. American Journal of Botany 99, 2045–2057.
| The impact of multiple biogeographic barriers and hybridization on species-level differentiation.Crossref | GoogleScholarGoogle Scholar | 23221499PubMed |
Nelson CE (1981) Phytogeography of southern Australia. In ‘Ecological Biogeography of Australia’. (Ed. A Keast) pp. 31–50. (Junk: The Hague, Netherlands)
Nevill PG, Bossinger G, Ades PK (2010) Phylogeography of the world’s tallest angiosperm, Eucalyptus regnans: evidence for multiple isolated Quaternary refugia. Journal of Biogeography 37, 179–192.
| Phylogeography of the world’s tallest angiosperm, Eucalyptus regnans: evidence for multiple isolated Quaternary refugia.Crossref | GoogleScholarGoogle Scholar |
Nevill PG, Bradbury D, Williams A, Tomlinson S, Krauss SL (2014) Genetic and palaeo-climatic evidence for widespread persistence of the coastal tree species Eucalyptus gomphocephala (Myrtaceae) during the Last Glacial Maximum. Annals of Botany 113, 55–67.
| Genetic and palaeo-climatic evidence for widespread persistence of the coastal tree species Eucalyptus gomphocephala (Myrtaceae) during the Last Glacial Maximum.Crossref | GoogleScholarGoogle Scholar | 24284819PubMed |
Ohlsen D, Smith F, Meagher D (2012) Two significant bryophyte records from eastern Victoria. Australasian Bryological Newsletter 60, 8–9.
Ohlsen D, Perrie LR, Shepherd LD, Brownsey PJ, Bayly MJ (2014) Phylogeny of the fern family Aspleniaceae in Australasia and the south-west Pacific. Australian Systematic Botany 27, 355–371.
| Phylogeny of the fern family Aspleniaceae in Australasia and the south-west Pacific.Crossref | GoogleScholarGoogle Scholar |
Parsons RF (1969) Distribution and palaeogeography of two mallee species of Eucalyptus in southern Australia. Australian Journal of Botany 17, 323–330.
| Distribution and palaeogeography of two mallee species of Eucalyptus in southern Australia.Crossref | GoogleScholarGoogle Scholar |
Peck JH, Peck CJ, Farrar DR (1990) Influences of life history attributes on formation of local and distant fern populations. American Fern Journal 80, 126–142.
| Influences of life history attributes on formation of local and distant fern populations.Crossref | GoogleScholarGoogle Scholar |
Perrie LR, Brownsey PJ (2005) Insights into the biogeography and polyploid evolution of New Zealand Asplenium from chloroplast DNA sequence data. American Fern Journal 95, 1–21.
| Insights into the biogeography and polyploid evolution of New Zealand Asplenium from chloroplast DNA sequence data.Crossref | GoogleScholarGoogle Scholar |
Perrie LR, Brownsey PJ (2007) Molecular evidence for long-distance dispersal in the New Zealand pteridophyte flora. Journal of Biogeography 34, 2028–2038.
| Molecular evidence for long-distance dispersal in the New Zealand pteridophyte flora.Crossref | GoogleScholarGoogle Scholar |
Perrie LR, Parris BS (2012) Chloroplast DNA sequences indicate the grammitid ferns (Polypodiaceae) in New Zealand belong to a single clade, Notogrammitis gen. nov. New Zealand Journal of Botany 50, 457–472.
| Chloroplast DNA sequences indicate the grammitid ferns (Polypodiaceae) in New Zealand belong to a single clade, Notogrammitis gen. nov.Crossref | GoogleScholarGoogle Scholar |
Perrie LR, Brownsey PJ, Lockhart PJ, Brown EA, Large MF (2003) Biogeography of temperate Australasian Polystichum ferns as inferred from chloroplast sequence and AFLP. Journal of Biogeography 30, 1729–1736.
| Biogeography of temperate Australasian Polystichum ferns as inferred from chloroplast sequence and AFLP.Crossref | GoogleScholarGoogle Scholar |
Perrie LR, Bayly MJ, Lehnebach CA, Brownsey PJ (2007) Molecular phylogenetics and molecular dating of the New Zealand Gleicheniaceae. Brittonia 59, 129–141.
| Molecular phylogenetics and molecular dating of the New Zealand Gleicheniaceae.Crossref | GoogleScholarGoogle Scholar |
Perrie LR, Ohlsen DJ, Shepherd LD, Garrett M, Brownsey PJ, Bayly MJ (2010a) Tasmanian and Victorian populations of the Australasian fern Asplenium hookerianum result from independent dispersals from New Zealand. Australian Systematic Botany 23, 387–392.
| Tasmanian and Victorian populations of the Australasian fern Asplenium hookerianum result from independent dispersals from New Zealand.Crossref | GoogleScholarGoogle Scholar |
Perrie LR, Shepherd LD, de Lange PJ, Brownsey PJ (2010b) Parallel polyploidy speciation: distinct sympatric gene-pools of recurrently derived allo-octoploid Asplenium ferns. Molecular Ecology 19, 2916–2932.
| Parallel polyploidy speciation: distinct sympatric gene-pools of recurrently derived allo-octoploid Asplenium ferns.Crossref | GoogleScholarGoogle Scholar | 20579287PubMed |
Pryer KM, Schuettpelz E, Wolf PG, Schneider H, Smith AR, Cranfill R (2004) Phylogeny and evolution of ferns (monilophytes) with a focus on the early leptosporangiate divergences. American Journal of Botany 91, 1582–1598.
| Phylogeny and evolution of ferns (monilophytes) with a focus on the early leptosporangiate divergences.Crossref | GoogleScholarGoogle Scholar | 21652310PubMed |
Ranker TA, Floyd SK, Trapp PG (1994) Multiple colonizations of Asplenium adiantum-nigrum onto the Hawaiian archipelago. Evolution 48, 1364–1370.
| Multiple colonizations of Asplenium adiantum-nigrum onto the Hawaiian archipelago.Crossref | GoogleScholarGoogle Scholar | 28564453PubMed |
Remington CL (1968) Suture-zones of hybrid interaction between recently joined biotas. In ‘Evolutionary Biology’. (Eds T Dobzhansky, MK Hecht, WC Steere) pp. 321–428. (Plenum: New York, NY, USA)
Rowe HC, Renaut S, Guggisberg A (2011) RAD in the realm of next-generation sequencing technologies. Molecular Ecology 20, 3499–3502.
| RAD in the realm of next-generation sequencing technologies.Crossref | GoogleScholarGoogle Scholar | 21991593PubMed |
Salzburger W, Ewing GB, Von Haeseler A (2011) The performance of phylogenetic algorithms in estimating haplotype genealogies with migration. Molecular Ecology 20, 1952–1963.
| The performance of phylogenetic algorithms in estimating haplotype genealogies with migration.Crossref | GoogleScholarGoogle Scholar | 21457168PubMed |
Schneider H, Russell SJ, Cox CJ, Bakker F, Henderson S, Rumsey F, Barrett J, Gibby M, Vogel JC (2004) Chloroplast phylogeny of asplenioid ferns based on rbcL and trnL–F spacer sequences (Polypodiidae, Aspleniaceae) and its implications for biogeography. Systematic Botany 29, 260–274.
| Chloroplast phylogeny of asplenioid ferns based on rbcL and trnL–F spacer sequences (Polypodiidae, Aspleniaceae) and its implications for biogeography.Crossref | GoogleScholarGoogle Scholar |
Schneider H, Ranker TA, Russell SJ, Cranfill R, Geiger JM, Aguraiuja R, Wood KR, Grundmann M, Kloberdanz K, Vogel JC (2005) Origin of the endemic fern genus Diella coincides with the renewal of Hawaiian terrestrial life in the Miocene. Proceedings. Biological Sciences 272, 455–460.
| Origin of the endemic fern genus Diella coincides with the renewal of Hawaiian terrestrial life in the Miocene.Crossref | GoogleScholarGoogle Scholar | 15734701PubMed |
Schönberger I, Wilton AD, Brownsey P, Perrie L, Boardman KF, Breitwieser I, Cochrane M, de Pauw B, Fife AJ, Ford KA, Gibb ES, Glenny DS, Korver MA, Novis PM, Prebble JM, Redmond DN, Smissen RD, Tawiri K (2019) ‘Checklist of the New Zealand Flora – Ferns and Lycophytes.’ (Manaaki Whenua-Landcare Research: Lincoln, New Zealand)
Sheffield E (2008) Alternation of generations. In ‘Biology and Evolution of Ferns and Lycophytes’. (Eds TA Ranker, CH Haufler) pp. 49–74. (Cambridge University Press: Cambridge, UK)
Shepherd LD, Perrie LR, Brownsey PJ (2007) Fire and Ice: volcanic and glacial impacts on the phylogeography of the New Zealand forest fern Asplenium hookerianum. Molecular Ecology 16, 4536–4549.
| Fire and Ice: volcanic and glacial impacts on the phylogeography of the New Zealand forest fern Asplenium hookerianum.Crossref | GoogleScholarGoogle Scholar | 17877716PubMed |
Shepherd LD, de Lange PJ, Perrie LR (2009) Multiple colonizations of a remote oceanic archipelago by one species: how common is long-distance dispersal? Journal of Biogeography 36, 1972–1977.
| Multiple colonizations of a remote oceanic archipelago by one species: how common is long-distance dispersal?Crossref | GoogleScholarGoogle Scholar |
Smith AR (1972) Comparison of fern flowering plant distributions with some evolutionary interpretations for ferns. Biotropica 4, 4–9.
| Comparison of fern flowering plant distributions with some evolutionary interpretations for ferns.Crossref | GoogleScholarGoogle Scholar |
Smith AR (1974) Taxonomic and cytological notes on ferns from California and Arizona. Madroño 22, 376–378.
Su Y-J, Wang T, Zheng B, Jiang Y, Chen G-P, Ouyang P-Y, Sun Y-F (2005) Genetic differentiation of relictual populations of Alsophila spinulosa in southern China inferred from cpDNA trnL–F noncoding sequences. Molecular Phylogenetics and Evolution 34, 323–333.
| Genetic differentiation of relictual populations of Alsophila spinulosa in southern China inferred from cpDNA trnL–F noncoding sequences.Crossref | GoogleScholarGoogle Scholar | 15619445PubMed |
Sutter G (2010) National Recovery Plan for the Maidenhair Spleenwort Asplenium hookerianum. Arthur Rylah Institute for Environmental Research, Department of Sustainability and Environment, National Recovery Plan, Melbourne, Vic., Australia.
Swofford DL (2000). ‘PAUP* 4.0: Phylogenetic Analysis using Parsimony (*and Other Methods).’. (Sinauer Associates: Sunderland, MA, USA)
Taberlet P, Gielly L, Pautou G, Bouvet J (1991) Universal primers for amplification of three non-coding regions of chloroplast DNA. Plant Molecular Biology 17, 1105–1109.
| Universal primers for amplification of three non-coding regions of chloroplast DNA.Crossref | GoogleScholarGoogle Scholar | 1932684PubMed |
Taberlet P, Fumagalli L, Wust-Saucy A-G, Cosson J-F (1998) Comparative phylogeography and postglacial colonization routes in Europe. Molecular Ecology 7, 453–464.
| Comparative phylogeography and postglacial colonization routes in Europe.Crossref | GoogleScholarGoogle Scholar | 9628000PubMed |
Tay ML, Meudt HM, Garnock-Jones PJ, Ritchie PA (2010) Erratum to: DNA sequences reveal multiple long-distance dispersals and non-monophyly of sections in Australasian Plantago (Plantaginaceae). Australian Systematic Botany 23, 306–308.
| Erratum to: DNA sequences reveal multiple long-distance dispersals and non-monophyly of sections in Australasian Plantago (Plantaginaceae).Crossref | GoogleScholarGoogle Scholar |
Tindale MD, Roy SK (2002) A cytotaxonomic survey of the Pteridophyta of Australia. Australian Systematic Botany 15, 839–937.
| A cytotaxonomic survey of the Pteridophyta of Australia.Crossref | GoogleScholarGoogle Scholar |
Trewick SA, Morgan-Richards M, Russell SJ, Henderson S, Rumsey FJ, Pinter I, Barrett JA, Gibby M, Vogel JC (2002) Polyploidy, phylogeography and Pleistocene refugia of the rockfern Asplenium ceterach: evidence from chloroplast DNA. Molecular Ecology 11, 2003–2012.
| Polyploidy, phylogeography and Pleistocene refugia of the rockfern Asplenium ceterach: evidence from chloroplast DNA.Crossref | GoogleScholarGoogle Scholar | 12296944PubMed |
Tryon AF (1968) Comparisons of sexual and apogamous races in the fern genus Pellaea. Rhodora 70, 1–24.
Tryon R (1970) Development and evolution of fern floras of oceanic islands. Biotropica 2, 76–84.
| Development and evolution of fern floras of oceanic islands.Crossref | GoogleScholarGoogle Scholar |
Tryon R (1972) Endemic areas and geographic speciation in tropical American ferns. Biotropica 4, 121–131.
| Endemic areas and geographic speciation in tropical American ferns.Crossref | GoogleScholarGoogle Scholar |
Vida G, Page CN, Walker TG, Reichstein T (1970) Cytologie der Farn-Gattung Cheilanthes in Europa und auf den Canarischen Inseln. Bauhinia 4, 223–253.
Vogel JC, Rumsey FJ, Schneller JJ, Barrett JA, Gibby M (1999) Where are the glacial refugia in Europe? Evidence from pteridophytes. Biological Journal of the Linnean Society. Linnean Society of London 66, 23–37.
| Where are the glacial refugia in Europe? Evidence from pteridophytes.Crossref | GoogleScholarGoogle Scholar |
Wagner WH (1972) Disjunctions in homosporous vascular plants. Annals of the Missouri Botanical Garden 59, 203–217.
| Disjunctions in homosporous vascular plants.Crossref | GoogleScholarGoogle Scholar |
Wagner WH, Farrar DR, Chen KK (1965) A new sexual form of Pellaea glabella var. glabella from Missouri. American Fern Journal 55, 171–178.
| A new sexual form of Pellaea glabella var. glabella from Missouri.Crossref | GoogleScholarGoogle Scholar |
Wang L, Wu Z-Q, Bystriakova N, Ansell SW, Xiang Q-P, Heinrichs J, Schneider H, Zhang X-C (2011) Phylogeography of the Sino-Himalayan Fern Lepisorus clathratus on ‘the roof of the world’. PLoS One 6, e25896
| Phylogeography of the Sino-Himalayan Fern Lepisorus clathratus on ‘the roof of the world’.Crossref | GoogleScholarGoogle Scholar | 22216295PubMed |
Wang R, Shao W, Liu L (2014) Cytotaxonomic study of Hypodematium (Hypodematiaceae) from China. Phytotaxa 161, 101–110.
| Cytotaxonomic study of Hypodematium (Hypodematiaceae) from China.Crossref | GoogleScholarGoogle Scholar |
Weston PH, Carolin RC, Armstrong JA (1984) A cladistics analysis of Boronia Sm. and Boronella Baill. (Rutaceae). Australian Journal of Botany 32, 187–203.
| A cladistics analysis of Boronia Sm. and Boronella Baill. (Rutaceae).Crossref | GoogleScholarGoogle Scholar |
Wheeler MA, Byrne M (2006) Congruence between phylogeographic patterns in cpDNA variation in Eucalyptus marginata (Myrtaceae) and geomorphology of the Darling Plateau, south-west of Western Australia. Australian Journal of Botany 54, 17–26.
| Congruence between phylogeographic patterns in cpDNA variation in Eucalyptus marginata (Myrtaceae) and geomorphology of the Darling Plateau, south-west of Western Australia.Crossref | GoogleScholarGoogle Scholar |
Whittier DP (1970) The rate of gametophyte maturation in sexual and apogamous species of ferns. Phytomorphology 20, 30–35.
Winkworth RC, Wagstaff SJ, Glenny D, Lockhart PJ (2002) Plant dispersal NEWS from New Zealand. Trends in Ecology & Evolution 17, 514–520.
| Plant dispersal NEWS from New Zealand.Crossref | GoogleScholarGoogle Scholar |
Worth JR, Jordan GJ, McKinnon GE, Vaillancourt RE (2009) The major Australian cool temperate rainforest tree Nothofagus cunninghamii withstood Pleistocene glacial aridity within multiple regions: evidence from the chloroplast. New Phytologist 182, 519–532.
| The major Australian cool temperate rainforest tree Nothofagus cunninghamii withstood Pleistocene glacial aridity within multiple regions: evidence from the chloroplast.Crossref | GoogleScholarGoogle Scholar | 19210718PubMed |
Worth JR, Jordan GJ, Marthick JR, McKinnon GE, Vaillancourt RE (2010) Chloroplast evidence for geographic stasis of the Australian bird-dispersed shrub Tasmannia lanceolata (Winteraceae). Molecular Ecology 19, 2949–2963.
| Chloroplast evidence for geographic stasis of the Australian bird-dispersed shrub Tasmannia lanceolata (Winteraceae).Crossref | GoogleScholarGoogle Scholar | 20609080PubMed |
Worth JR, Marthick JR, Jordan GJ, Vaillancourt RE (2011) Low but structured chloroplast diversity in Atherspermum moschatum (Athermospermataceae) suggests bottlenecks in response to the Pleistocene glacials. Annals of Botany 108, 1247–1256.
| Low but structured chloroplast diversity in Atherspermum moschatum (Athermospermataceae) suggests bottlenecks in response to the Pleistocene glacials.Crossref | GoogleScholarGoogle Scholar | 21856633PubMed |
Wright IJ, Ladiges PY (1997) Geographic variation in Eucalyptus diversifolia (Myrtaceae) and recognition of new subspecies E. diversifolia subsp. hesperia and E. diversifolia subsp. megacarpa. Australian Systematic Botany 10, 651–680.
| Geographic variation in Eucalyptus diversifolia (Myrtaceae) and recognition of new subspecies E. diversifolia subsp. hesperia and E. diversifolia subsp. megacarpa.Crossref | GoogleScholarGoogle Scholar |
Xu K-W, Zhang L, Rothfels CJ, Smith AR, Viane R, Lorence D, Wood KR, Chen C-W, Knapp R, Zhou L, Lu NT, Zhou X-M, Wei H-J, Fan Q, Chen S-F, Cicuzza D, Gao X-F, Liao W-B, Zhang L-B (2020) A global plastid phylogeny of the fern genus Asplenium (Aspleniaceae). Cladistics 36, 22–71.
| A global plastid phylogeny of the fern genus Asplenium (Aspleniaceae).Crossref | GoogleScholarGoogle Scholar |