Investigation of species boundaries and relationships in the Asplenium paleaceum complex (Aspleniaceae) using AFLP fingerprinting and chloroplast and nuclear DNA sequences
Daniel J. Ohlsen A , Leon R. Perrie B , Lara D. Shepherd B , Patrick J. Brownsey B and Michael J. Bayly A C
+ Author Affiliations
- Author Affiliations
A School of Botany, The University of Melbourne, Parkville, Vic. 3010, Australia.
B Museum of New Zealand Te Papa Tongarewa, PO Box 467, Wellington 6140, New Zealand.
C Corresponding author. Email: mbayly@unimelb.edu.au
Australian Systematic Botany 27(6) 378-394 https://doi.org/10.1071/SB14024
Submitted: 13 August 2014 Accepted: 5 May 2015 Published: 29 June 2015
Abstract
Species boundaries and relationships were investigated in the Asplenium paleaceum (Aspleniaceae) species complex from eastern Australia, using AFLP fingerprinting and chloroplast trnL–trnF and rps4–trnS and nuclear pgiC DNA sequences. Phenetic analyses of AFLP data resulted in the following five distinct groups: (1) A. carnarvonense, (2) A. bicentenniale (including nearby collections originally identified as A. paleaceum), (3) A. paleaceum with both aborted and normal spores, (4) one population of putative tetraploid A. attenuatum var. indivisum from south Queensland, and (5) remaining octoploid A. attenuatum populations and several putative hybrids. Taxonomic revision of this complex will require morphological re-circumscription of the current species and recognition of a new species if these AFLP groups are taken to represent separate species. The chloroplast regions, morphology and pgiC together provide good evidence that an Asplenium of unconfirmed identity, A. sp. ‘Kroombit Tops’, is an allopolyploid with a species of the A. paleaceum chloroplast clade, probably A. paleaceum, and distantly related A. polyodon as parents. Further study is required to determine the complete ancestry of the other species of the A. paleaceum complex.
Additional keywords: allopolyploidy, Asplenium attenuatum, A. bicentenniale, A. carnarvonense, gapCp, hybrids, low-copy nuclear genes, pgiC, taxonomy.
References
Andrews SB (1990) Asplenium. In ‘Ferns of Queensland, a Handbook to the Ferns and Fern Allies’. (Ed. SB Andrews) pp. 47–70. (Queensland Department of Primary Industries: Brisbane)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 |
Barrington DS, Haufler CH, Werth CR (1989) Hybridization, reticulation and species concepts in the ferns. American Fern Journal 79, 55–64.
| Hybridization, reticulation and species concepts in the ferns.Crossref | GoogleScholarGoogle Scholar |
Blears MJ, De Grandis SA, Lee H, Trevors JT (1998) Amplified fragment length polymorphism (AFLP): a review of the procedure and its application. Journal of Industrial Microbiology & Biotechnology 21, 99–114.
| Amplified fragment length polymorphism (AFLP): a review of the procedure and its application.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXitFWksg%3D%3D&md5=d7284adab7b09632d64f284add0014f9CAS |
Bonin A, Ehrich D, Manel S (2007) Statistical analysis of amplified fragment length polymorphism data: a toolbox for molecular ecologists and evolutionists. Molecular Ecology 16, 3737–3758.
| Statistical analysis of amplified fragment length polymorphism data: a toolbox for molecular ecologists and evolutionists.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD2srjs1Cnug%3D%3D&md5=ed2ad4381feb2ffefa816200a401868dCAS | 17850542PubMed |
Brownsey PJ (1977) Asplenium hybrids in the New Zealand flora. New Zealand Journal of Botany 15, 601–637.
| Asplenium hybrids in the New Zealand flora.Crossref | GoogleScholarGoogle Scholar |
Brownsey PJ (1998) Aspleniaceae. In ‘Flora of Australia, 48: Ferns, Gymnosperms and Allied Groups’ (Ed. PM McCarthy) pp. 295–327. (ABRS: Canberra; and CSIRO: Melbourne)
Chang Y, Li J, Lu S, Schneider H (2013) Species diversity and reticulate evolution in the Asplenium normale complex (Aspleniaceae) in China and adjacent areas. Taxon 62, 673–687.
| Species diversity and reticulate evolution in the Asplenium normale complex (Aspleniaceae) in China and adjacent areas.Crossref | GoogleScholarGoogle Scholar |
Dice LR (1945) Measures of the amount of ecologic association between species. Ecology 26, 297–302.
| Measures of the amount of ecologic association between species.Crossref | GoogleScholarGoogle Scholar |
Doyle JJ, Doyle JL (1990) Isolation of plant DNA from fresh tissue. Focus 12, 13–15.
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 | 1:CAS:528:DC%2BC3MXmtVKru7Y%3D&md5=0a8b844aea41137d35ce2ae4213c176fCAS | 21573248PubMed |
Gastony GJ, Haufler CH (1976) Chromosome numbers and apomixis in the fern genus Bommeria. Biotropica 8, 1–11.
| Chromosome numbers and apomixis in the fern genus Bommeria.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, 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 | 1:CAS:528:DC%2BD1MXhtF2jtLvO&md5=40ebe7ebbb097047a551fa43922f5ea0CAS | 21622350PubMed |
Hennipman E (1977) ‘A Monograph of the Fern Genus Bolbitis (Lomariopsidaceae)’, Leiden Botanical Series 2. (Leiden University Press: Leiden, Netherlands)
Herrero A, Pajaron S, Prada C (2001) Isozyme variation and genetic relationships among taxa in the Asplenium obovatum group (Aspleniaceae, Pteridophyta). American Journal of Botany 88, 2040–2050.
| Isozyme variation and genetic relationships among taxa in the Asplenium obovatum group (Aspleniaceae, Pteridophyta).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XktFyn&md5=f2279af2d9d5f75cf4460e00a9117546CAS | 21669636PubMed |
Hunt HV, Ansell SW, Russell SJ, Schneider H, Vogel JC (2011) Dynamics of polyploidy formation and establishment in the allotetraploid rock fern Asplenium majoricum. Annals of Botany 108, 143–157.
| Dynamics of polyploidy formation and establishment in the allotetraploid rock fern Asplenium majoricum.Crossref | GoogleScholarGoogle Scholar | 21593062PubMed |
Ishikawa H, Watano Y, Kano K, Ito M, Kurita S (2002) Development of primer sets for PCR amplification of the pgiC gene in ferns. Journal of Plant Research 115, 65–70.
| Development of primer sets for PCR amplification of the pgiC gene in ferns.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XjsVKgt7w%3D&md5=6e135bb563581e6b21181560d56c9131CAS | 12884051PubMed |
Koenemann DM, Maisonpierre JA, Barrington DS (2011) Broad-scale integrity and local divergence in the fiddlehead fern Matteuccia struthiopteris (L.) Todaro (Onocleaceae). American Fern Journal 101, 213–230.
| Broad-scale integrity and local divergence in the fiddlehead fern Matteuccia struthiopteris (L.) Todaro (Onocleaceae).Crossref | GoogleScholarGoogle Scholar |
Kramer KU, Viane R (1990) Aspleniaceae. In ‘The Families and Genera of Vascular Plants Pteridophytes and Gymnosperms 1’. (Eds KU Kramer, PS Green) pp. 52–56. (Springer-Verlag: Berlin)
Kreier H-P, Rex M, Weising K, Kessler M, Smith AR, Schneider H (2008) Inferring the diversification of the epiphytic fern genus Serpocaulon (Polypodiaceae) in South America using chloroplast sequences and amplified fragment length polymorphisms. Plant Systematics and Evolution 274, 1–16.
| Inferring the diversification of the epiphytic fern genus Serpocaulon (Polypodiaceae) in South America using chloroplast sequences and amplified fragment length polymorphisms.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXpsVCmtLs%3D&md5=47cd469a47a677d5cf7ec9e589e103dbCAS |
Lovis JD (1973) A biosystematic approach to phylo-genetic problems and its application to the Aspleniaceae. In ‘The Phylogeny and Classification of the Ferns’. (Eds AC Jermy, JA Crabbe, BA Thomas) pp. 211–228. (Academic Press: London)
Manton I (1950) ‘Problems of Cytology and Evolution in the Pteridophyta.’ (Cambridge University Press: London)
Meudt HM, Clarke AC (2007) Almost forgotten or latest practice? AFLP applications, analyses and advances. Trends in Plant Science 12, 106–117.
| Almost forgotten or latest practice? AFLP applications, analyses and advances.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXivVShsbY%3D&md5=701cec49cec928a05a148ee4baf0aa15CAS | 17303467PubMed |
Mueller UG, Wolfenbarger LL (1999) AFLP genotyping and fingerprinting. Trends in Ecology & Evolution 14, 389–394.
| AFLP genotyping and fingerprinting.Crossref | GoogleScholarGoogle Scholar |
Ohlsen DJ (2014) Molecular systematics, biogeography, and taxonomy of the fern family Aspleniaceae in Australasia and the south-west Pacific. PhD Thesis. The University of Melbourne, Melbourne.
Ohlsen DJ, Field AR (2013) A new species of fern for Queensland: Diplazium squamuligum. Austrobaileya 9, 114–125.
Ohlsen DJ, Perrie LR, Shepherd LD, Brownsey PJ, Bayly MJ (2014) [2015] Phylogeny of the fern family Aspleniaceae in Australasia and the south-western Pacific. Australian Systematic Botany 27, 355–371.
| [2015] Phylogeny of the fern family Aspleniaceae in Australasia and the south-western Pacific.Crossref | GoogleScholarGoogle Scholar |
Perrie LR, Brownsey PJ (2005) Genetic variation is not concordant with morphological variation in the fern Asplenium hookerianum sensu lato (Aspleniaceae). American Journal of Botany 92, 1559–1564.
| Genetic variation is not concordant with morphological variation in the fern Asplenium hookerianum sensu lato (Aspleniaceae).Crossref | GoogleScholarGoogle Scholar | 21646173PubMed |
Perrie LR, Brownsey PJ, Lockhart PJ, Brown EA, Large MF (2003a) 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, Brownsey PJ, Lockhart PJ, Large MF (2003b) Evidence for an allopolyploid complex in New Zealand Polystichum. New Zealand Journal of Botany 41, 189–215.
| Evidence for an allopolyploid complex in New Zealand Polystichum.Crossref | GoogleScholarGoogle Scholar |
Perrie LR, Shepherd LD, de Lange PJ, Brownsey PJ (2010) 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 | 1:CAS:528:DC%2BC3cXhtVyktb3J&md5=51f8746765bc0eb70f72175d49c53a3dCAS | 20579287PubMed |
Puttock CF, Quinn CJ (1980) Perispore morphology and the taxonomy of the Australian Aspleniaceae. Australian Journal of Botany 28, 305–322.
| Perispore morphology and the taxonomy of the Australian Aspleniaceae.Crossref | GoogleScholarGoogle Scholar |
Reichstein T (1981) Hybrids in European Aspleniaceae (Pteridophyta). Botanica Helvetica 91, 89–139.
Rohlf FJ (1998) NTSYS-pc: numerical taxonomy system 2. 02i. (Exeter Software: New York)
Rothfels CJ, Larsson A, Li F-W, Sigel EM, Huiet L, Burge DO, Ruhsam M, Graham SW, Stevenson DN, Wong GK-S, Korall P, Pryer KM (2013) Transcriptome-mining for single-copy nuclear markers in ferns. PLoS One 8, e76957
| Transcriptome-mining for single-copy nuclear markers in ferns.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhs1aks7vN&md5=4c67a353dc6139f52e099ed2e99c8662CAS | 24116189PubMed |
Rowe HC, Renaut S, Guggisberg A (2011) RAD in the realm of next-generation sequencing technologies. Molecular Ecology 20, 3499–3502.
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, Navarro-Gomez A, Russell SJ, Ansell S, Grundmann M, Vogel J (2013) Exploring the utility of three nuclear regions to reconstruct reticulate evolution in the fern genus Asplenium. Journal of Systematics and Evolution 51, 142–153.
| Exploring the utility of three nuclear regions to reconstruct reticulate evolution in the fern genus Asplenium.Crossref | GoogleScholarGoogle Scholar |
Schuettpelz E, Grusz AL, Windham MD, Pryer KM (2008) The utility of nuclear gapCp in resolving polyploid fern origins. Systematic Botany 33, 621–629.
| The utility of nuclear gapCp in resolving polyploid fern origins.Crossref | GoogleScholarGoogle Scholar |
Sessa EB, Zimmer EA, Givnish TJ (2012) Unraveling reticulate evolution in North American Dryopteris (Dryopteridaceae). BMC Evolutionary Biology 12,
| Unraveling reticulate evolution in North American Dryopteris (Dryopteridaceae).Crossref | GoogleScholarGoogle Scholar | 22971160PubMed |
Shepherd LD, Perrie LR, Brownsey PJ (2008) Low-copy nuclear DNA sequences reveal a predominance of allopolyploids in a New Zealand Asplenium fern complex. Molecular Phylogenetics and Evolution 49, 240–248.
| Low-copy nuclear DNA sequences reveal a predominance of allopolyploids in a New Zealand Asplenium fern complex.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtFOltr3M&md5=2d3225a4ddb5d0f215fd3087340ccf4dCAS | 18640280PubMed |
Simpson GG (1961) ‘Principles of Animal Taxonomy.’ (Columbia University Press: New York)
Sokal RR, Michener CD (1958) A statistical method for evaluating systematic relationships. The University of Kansas Science Bulletin 38, 1409–1438.
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 |
Vogel JC, Russell SJ, Rumsey FJ, Barrett JA, Gibby M (1998) Evidence for maternal transmission of chloroplast DNA in the genus Asplenium (Aspleniaceae, Pteridophyta). Botanica Acta 111, 247–249.
| Evidence for maternal transmission of chloroplast DNA in the genus Asplenium (Aspleniaceae, Pteridophyta).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXktVaquro%3D&md5=c01d14168f4ebd3261344454478ee236CAS |
Vos P, Hogers R, Bleeker M, Reijans M, van de Lee T, Hornes M, Frijters A, Pot J, Peleman J, Kuiper M (1995) AFLP: a technique for DNA fingerprinting. Nucleic Acids Research 23, 4407–4414.
| AFLP: a technique for DNA fingerprinting.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXpslensbo%3D&md5=3a4ea6d787a74561268798e9807fff7fCAS | 7501463PubMed |
Wagner WH (1954) Reticulate evolution in the Appalachian aspleniums. Evolution 8, 103–118.
| Reticulate evolution in the Appalachian aspleniums.Crossref | GoogleScholarGoogle Scholar |
Wagner WH (1962) Irregular morphological development in hybrid ferns. Phytomorphology 12, 87–100.
Wagner WH (1983) Reticulistics: the recognition of hybrids and their role in cladistics and classification In ‘Advances in Cladistics’. (Eds NI Platnick, VA Funk) pp. 63–79. (New York Botanical Garden: New York)
Wagner WH, Chen KL (1965) Abortion of spores and sporangia as a tool in the detection of Dryopteris hybrids. American Fern Journal 55, 9–29.
| Abortion of spores and sporangia as a tool in the detection of Dryopteris hybrids.Crossref | GoogleScholarGoogle Scholar |
Wagner WH, Wagner FS (1969) A new natural hybrid in the Appalachian Asplenium complex and its taxonomic significance. Brittonia 21, 178–186.
| A new natural hybrid in the Appalachian Asplenium complex and its taxonomic significance.Crossref | GoogleScholarGoogle Scholar |
Wagner WH, Wagner FS, Taylor WC (1986) Detecting abortive spores in herbarium specimens of sterile hybrids. American Fern Journal 76, 129–140.
| Detecting abortive spores in herbarium specimens of sterile hybrids.Crossref | GoogleScholarGoogle Scholar |
Walker TG (1966) Apomixis and vegetative reproduction in ferns. In ‘Reproductive Biology and Taxonomy of Vascular Plants’. (Ed. JG Hawkes) pp. 152–161. (Botanical Society of the British Isles Conference Reproduction 9: London)
Walker TG (1979) The cytogenetics of ferns. In ‘The Experimental Biology of Ferns’. (Ed. AF Dyer) pp. 87–123. (Academic Press: London)
Wherry ET (1925) The Appalachian aspleniums. American Fern Journal 15, 47–54.
| The Appalachian aspleniums.Crossref | GoogleScholarGoogle Scholar |
Willing E-M, Dreyer C, van Oosterhout C (2012) Estimates of genetic differentiation measured by F ST do not necessarily require large sample sizes when using many SNP markers. PLoS One 7, e42649
| Estimates of genetic differentiation measured by F ST do not necessarily require large sample sizes when using many SNP markers.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xht1ejt7nF&md5=2674407c1cd5db21f1c788c83c0e45bbCAS | 22905157PubMed |
Winter S, Chizzola R, Kriechbaum M, Kropf M (2013) Hybridisation in Jacobaea: characterisation of hybrids between Jacobaea aquatic and J. vulgaris in Austria. Plant Ecology & Diversity 6, 217–229.
| Hybridisation in Jacobaea: characterisation of hybrids between Jacobaea aquatic and J. vulgaris in Austria.Crossref | GoogleScholarGoogle Scholar |
Woodhead M, Russell J, Squirrel J, Hollingsworth PM, MacKenzie K, Gibby M, Powell W (2005) Comparative analysis of population genetic structure in Athyrium distentifolium (Pteridophyta) using AFLPs and SSRs from anonymous and transcribed gene regions. Molecular Ecology 14, 1681–1695.
| Comparative analysis of population genetic structure in Athyrium distentifolium (Pteridophyta) using AFLPs and SSRs from anonymous and transcribed gene regions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXkvVeqtr8%3D&md5=d30fe9821da59a4217314b50d7d1a7f0CAS | 15836642PubMed |
