Genetic diversity within and across gametophytic ploidy levels in a Sphagnum cryptic species complex
Eric F. Karlin
A D , Sean C. Robinson B and Peter E. Smouse C
+ Author Affiliations
- Author Affiliations
A Environmental Science Program, School of Theoretical and Applied Science, Ramapo College, Mahwah, NJ, 07430-1680, USA.
B Biology Department, SUNY College at Oneonta, Oneonta, NY, 13820-4015, USA.
C Ecology, Evolution and Natural Resources, School of Environmental and Biological Sciences, Rutgers University, New Brunswick, NJ, 08901-8551, USA.
D Corresponding author. Email: ekarlin@ramapo.edu
Australian Journal of Botany 68(1) 49-62 https://doi.org/10.1071/BT19143
Submitted: 6 September 2019 Accepted: 29 March 2020 Published: 4 May 2020
Abstract
We deploy Shannon analysis of five ancestrally (ANCE) diagnostic microsatellite loci to explore the patterns of ‘deep’ allelic genetic diversity within the peat moss Sphagnum ×australe Mitt. s.l. cryptic species complex across its Australasian distribution. There is both notable divergence among and considerable allelic overlap within the three allopolyploid lineages of this complex, two gametophytically allodiploid (R1S1 and R2S2) and one gametophytically allotriploid (FR1*S1*). Detailed biogeographic patterns reflect historical differences in genetic isolation and interbreeding. Lineage I (R1S1) occurs in both Australia and New Zealand, while Lineage II (R2S2) and Lineage III (FR1*S1*) are endemic to New Zealand, where Lineage III predominates. Available data suggest that Lineage I arose in Australia, whereas both Lineage II and Lineage III originated in New Zealand. ‘Deep’ allelic diversity provides a pronounced signal of evolutionary radiation within and among the three lineages. We develop a methodology to explore allelic diversity across ploidy levels and elaborate another for scaling additive allele-metric diversity values [0,1], relative to attainable minimal and maximal values, given the sampling frame. We suggest the following taxonomic disposition: gametophytically allodiploid Lineages I and II → S. ×australe; gametophytically allotriploid Lineage III → S. ×antarcticum. Epitypes are designated for both species.
Additional keywords: biodiversity, gametophyte, genetic diversity, mosses, speciation.
References
Alix K, Gérard PR, Schwarzacher T, Heslop-Harrison J (2017) Polyploidy and interspecific hybridization: partners for adaptation, speciation and evolution in plants. Annals of Botany 120, 183–194.| Polyploidy and interspecific hybridization: partners for adaptation, speciation and evolution in plants.Crossref | GoogleScholarGoogle Scholar | 28854567PubMed |
Allario T, Brumos J, Colmenero-Flores JM, Iglesias DJ, Pina JA, Navarro L, Talon M, Ollitrault P, Morillon R (2013) Tetraploid Rangpur lime rootstock increases drought tolerance via enhanced constitutive root abscisic acid production. Plant Cell and Environment 36, 856–868.
| Tetraploid Rangpur lime rootstock increases drought tolerance via enhanced constitutive root abscisic acid production.Crossref | GoogleScholarGoogle Scholar |
Andrews AL (1941) Notes on the Warnstorf Sphagnum herbarium II. The section Malacosphagnum. Bryolgist 44, 97–102.
| Notes on the Warnstorf Sphagnum herbarium II. The section Malacosphagnum.Crossref | GoogleScholarGoogle Scholar |
Angulo A, Icochea J (2010) Cryptic species complexes, widespread species and conservation: lessons from Amazonian frogs of the Leptodactylus marmoratus group (Anura: Leptodactylidae). Systematics and Biodiversity 8, 357–370.
| Cryptic species complexes, widespread species and conservation: lessons from Amazonian frogs of the Leptodactylus marmoratus group (Anura: Leptodactylidae).Crossref | GoogleScholarGoogle Scholar |
Bickford D, Lohman DJ, Sodhi NS, Ng PKL, Meier R, Winker K, Ingram KK, Das I (2007) Cryptic species as a window on diversity and conservation. Trends in Ecology & Evolution 22, 148–155.
| Cryptic species as a window on diversity and conservation.Crossref | GoogleScholarGoogle Scholar |
Blaine Marchant DB, Soltis DE, Soltis PS (2016) Patterns of abiotic niche shifts in allopolyploids relative to their progenitors. New Phytologist 212, 708–718.
| Patterns of abiotic niche shifts in allopolyploids relative to their progenitors.Crossref | GoogleScholarGoogle Scholar |
Crosby MR, Schultze-Motel U, Schultze-Motel W (1983) Katalog der Laubmoose von Madagaskar und den umliegenden Inseln. Willdenowia 13, 187–255.
Dawson DA, Ball AD, Spurgin LG, Martín-Gálvez D, Stewart IRK, Horsburgh GJ, Potter J, Molina-Morales M, Bicknell AWJ, Preston SAJ, Ekblom R, Slate J, Burke T (2013) High-utility conserved avian microsatellite markers enable parentage and population studies across a wide range of species. BMC Genomics 14, 176
| High-utility conserved avian microsatellite markers enable parentage and population studies across a wide range of species.Crossref | GoogleScholarGoogle Scholar | 23497230PubMed |
Eddy A (1977) Sphagnales of tropical Asia. Bulletin of the British Museum (Natural History). Historical Series 5, 359–445.
Eddy A (1985) A revision of African Sphagnales. Bulletin 659 of the British Museum Natural History (Botany) 12, 77–172.
Eddy A (1988) ‘A handbook of Malesian mosses. Vol. I: Sphagnales to Dicranales.’ (British Museum (Natural History): London)
Felsenstein J (1989) PHYLIP – Phylogeny Inference Package (ver. 3.2). Cladistics 5, 164–166.
Fife AJ (1996) A synopsis of New Zealand Sphagna, with a description of S. simplex sp. nov. New Zealand Journal of Botany 34, 309–328.
| A synopsis of New Zealand Sphagna, with a description of S. simplex sp. nov.Crossref | GoogleScholarGoogle Scholar |
Gibb ES, Wilton AD, Schönberger I, Fife AJ, Glenny DS, Beever JE, Boardman KF, Breitwieser I, Cochrane M, de Pauw B, Ford KA, Heenan PB, Korver MA, Novis PM, Prebble JM, Redmond DN, Smissen RD, Tawiri K (2017) ‘Checklist of the New Zealand flora – hornworts, liverworts and mosses.’ (Manaaki Whenua-Landcare Research, Lincoln, NZ) Available at
Glime JM, Bisang I (2017) Sexual strategies. In ‘Bryophyte ecology. Vol. 1: Physiological ecology. 2’. Available at https://digitalcommons.mtu.edu/bryophyte-ecology1/2) [Verified 3 April 2020]
Greilhuber J, Doležel J, Lysák MA, Bennett MD (2005) The origin, evolution and proposed stabilization of the terms ‘genome size’ and ‘C-value’ to describe nuclear DNA contents. Annals of Botany 95, 255–260.
| The origin, evolution and proposed stabilization of the terms ‘genome size’ and ‘C-value’ to describe nuclear DNA contents.Crossref | GoogleScholarGoogle Scholar | 15596473PubMed |
Haig D (2016) Living together and living apart: the sexual lives of bryophytes. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 371, 20150535
| Living together and living apart: the sexual lives of bryophytes.Crossref | GoogleScholarGoogle Scholar | 27619699PubMed |
He S (1998) A checklist of the mosses of Chile. Journal of the Hattori Botanical Laboratory 85, 103–189.
Hebert PDN, Penton EH, Burns JM, Janzen DH, Hallwachs W (2004) Ten species in one: DNA barcoding reveals cryptic species in the neotropical skipper butterfly Astraptes fulgerator. Proceedings of the National Academy of Sciences of the United States of America 101, 14812–14817.
| Ten species in one: DNA barcoding reveals cryptic species in the neotropical skipper butterfly Astraptes fulgerator.Crossref | GoogleScholarGoogle Scholar |
Huelsenbeck JP, Ronquist F (2001) MRBAYES: Bayesian inference of phylogeny. Bioinformatics 17, 754–755.
| MRBAYES: Bayesian inference of phylogeny.Crossref | GoogleScholarGoogle Scholar | 11524383PubMed |
Johnson MG, Shaw AJ (2015) Genetic diversity, sexual condition, and microhabitat preference determine mating patterns in Sphagnum (Sphagnaceae) peat-mosses. Biological Journal of the Linnean Society. Linnean Society of London 115, 96–113.
| Genetic diversity, sexual condition, and microhabitat preference determine mating patterns in Sphagnum (Sphagnaceae) peat-mosses.Crossref | GoogleScholarGoogle Scholar |
Jost L (2006) Entropy and diversity. Oikos 113, 363–375.
| Entropy and diversity.Crossref | GoogleScholarGoogle Scholar |
Jost L (2007) Partitioning diversity into independent alpha and beta components. Ecology 88, 2427–2439.
| Partitioning diversity into independent alpha and beta components.Crossref | GoogleScholarGoogle Scholar | 18027744PubMed |
Karlin EF (2014) Subgenome analysis of two southern hemisphere allotriploid species in Sphagnum (Sphagnaceae). Journal of Bryology 36, 165–179.
| Subgenome analysis of two southern hemisphere allotriploid species in Sphagnum (Sphagnaceae).Crossref | GoogleScholarGoogle Scholar |
Karlin EF, Robinson SC (2017) Update on the Holantarctic Sphagnum ×falcatulum s.l. (Sphagnaceae) complex: S. irritans is associated with the allo-diploid plants. Journal of Bryology 39, 8–15.
| Update on the Holantarctic Sphagnum ×falcatulum s.l. (Sphagnaceae) complex: S. irritans is associated with the allo-diploid plants.Crossref | GoogleScholarGoogle Scholar |
Karlin EF, Smouse PE (2017) Allo-allo-triploid Sphagnum ×falcatulum: single individuals contain most of the Holantarctic diversity for ancestrally indicative markers. Annals of Botany 120, 221–231.
| Allo-allo-triploid Sphagnum ×falcatulum: single individuals contain most of the Holantarctic diversity for ancestrally indicative markers.Crossref | GoogleScholarGoogle Scholar | 28088765PubMed |
Karlin EF, Smouse PE (2019) Holantarctic diversity varies widely among genetic loci within the gametophytically allotriploid peat moss Sphagnum ×falcatulum. American Journal of Botany 106, 137–144.
| Holantarctic diversity varies widely among genetic loci within the gametophytically allotriploid peat moss Sphagnum ×falcatulum.Crossref | GoogleScholarGoogle Scholar | 30644542PubMed |
Karlin E, Boles SB, Ricca M, Temsch E, Greilhuber J, Shaw AJ (2009) Three-genome mosses: complex double allopolyploid origins for triploid gametophytes in Sphagnum. Molecular Ecology 18, 1439–1454.
| Three-genome mosses: complex double allopolyploid origins for triploid gametophytes in Sphagnum.Crossref | GoogleScholarGoogle Scholar | 19368647PubMed |
Karlin EF, Andrus RE, Boles SB, Shaw AJ (2011a) One haploid parent contributes 100% of the gene pool for a wide spread species in northwest North America. Molecular Ecology 20, 753–767.
| One haploid parent contributes 100% of the gene pool for a wide spread species in northwest North America.Crossref | GoogleScholarGoogle Scholar | 21199037PubMed |
Karlin EF, Boles SB, Seppelt RD, Terracciano S, Shaw AJ (2011b) The peat moss Sphagnum cuspidatum in Australia: microsatellites provide a global perspective. Systematic Botany 36, 22–32.
| The peat moss Sphagnum cuspidatum in Australia: microsatellites provide a global perspective.Crossref | GoogleScholarGoogle Scholar |
Karlin EF, Hotchkiss SC, Boles SB, Stenøien HK, Hassel K, Flatberg KI, Shaw AJ (2012) High genetic diversity in a remote island population system: sans sex. New Phytologist 193, 1088–1097.
| High genetic diversity in a remote island population system: sans sex.Crossref | GoogleScholarGoogle Scholar | 22188609PubMed |
Karlin EF, Buck WR, Seppelt RD, Boles SB, Shaw AJ (2013) The double allopolyploid Sphagnum ×falcatulum (Sphagnaceae) in Tierra del Fuego, a Holantarctic perspective. Journal of Bryology 35, 157–172.
| The double allopolyploid Sphagnum ×falcatulum (Sphagnaceae) in Tierra del Fuego, a Holantarctic perspective.Crossref | GoogleScholarGoogle Scholar |
Karlin EF, Temsch EM, Bizuru E, Marino J, Boles SB, Devos N, Shaw AJ (2014) Invisible in plain sight: recurrent double allopolyploidy in the African Sphagnum × planifolium (Sphagnaceae). The Bryologist 117, 187–201.
| Invisible in plain sight: recurrent double allopolyploidy in the African Sphagnum × planifolium (Sphagnaceae).Crossref | GoogleScholarGoogle Scholar |
Kyrkjeeide MO, Hassel K, Flatberg KJ, Shaw AJ, Brochmann C, Stenoien H (2016) Long-distance dispersal and barriers shape genetic structure of peatmosses (Sphagnum) across the Northern Hemisphere. Journal of Biogeography 43, 1215–1226.
| Long-distance dispersal and barriers shape genetic structure of peatmosses (Sphagnum) across the Northern Hemisphere.Crossref | GoogleScholarGoogle Scholar |
Levin DA (2019) Plant speciation in the age of climate change. Annals of Botany 124, 769–775.
| Plant speciation in the age of climate change.Crossref | GoogleScholarGoogle Scholar | 31250895PubMed |
Lewis LR, Behling E, Gousse H, Qian E, Elphick CS, Lamarre J-F, Bêty J, Liebezeit J, Rozzi R, Goffinet B (2014) First evidence of bryophyte diaspores in the plumage of transequatorial migrant birds. PeerJ 2, e424
| First evidence of bryophyte diaspores in the plumage of transequatorial migrant birds.Crossref | GoogleScholarGoogle Scholar | 24949241PubMed |
Magill RE (1981) Bryophyta. Part 1. Mosses. Fasc. I. Sphagnaceae – Grimmiaceae. In ‘Flora of Southern Africa’. (Ed. O.A. Leistner) p. 291 (Botanical Research Institute, Department of Agriculture and Fisheries Pretoria, Republic of South Africa).
Magill RE, Schelpe EA (1979) The bryophytes of Southern Africa, an annotated checklist. In ‘Memoirs of the Botanical Survey of South Africa’. (Ed. D.J.B. Killick) p. 19 (Botanical Research Institute, Dept. of Agricultural Technical Services: Pretoria, Republic of South Africa).
McGlone MS (2009) Postglacial history of New Zealand wetlands and implications for their conservation. New Zealand Journal of Ecology 33, 1–23.
McIntyre PJ (2012) Polyploidy associated with altered and broader ecological niches in the Claytonia perfoliata (Portulacaceae) species complex. American Journal of Botany 99, 655–662.
| Polyploidy associated with altered and broader ecological niches in the Claytonia perfoliata (Portulacaceae) species complex.Crossref | GoogleScholarGoogle Scholar | 22434773PubMed |
McLeod DS (2010) Of least concern? Systematics of a cryptic species complex: Limnonectes kuhlii (Amphibia: Anura: Dicroglossidae). Molecular Phylogenetics and Evolution 56, 991–1000.
| Of least concern? Systematics of a cryptic species complex: Limnonectes kuhlii (Amphibia: Anura: Dicroglossidae).Crossref | GoogleScholarGoogle Scholar | 20385247PubMed |
Meirmans PG, Liu S (2018) Analysis of molecular variance (AMOVA) for autopolyploids. Frontiers in Ecology and Evolution 6, 66.
| Analysis of molecular variance (AMOVA) for autopolyploids.Crossref | GoogleScholarGoogle Scholar |
Meleshko O, Stenøien HK, Speed JDM, Flatberg KI, Kyrkjeeide MO, Hassel K (2018) Is interspecific gene flow and speciation in peatmosses (Sphagnum) constrained by phylogenetic relationship and life-history traits? Lindbergia 41,
| Is interspecific gene flow and speciation in peatmosses (Sphagnum) constrained by phylogenetic relationship and life-history traits?Crossref | GoogleScholarGoogle Scholar |
Michaelis D (2011) ‘Die Sphagnum-arten der welt.’ (Schweizerbart Science Publishers: Stuttgart, Germany)
Nygren A, Parapar J, Pons J, Meißner K, Bakken T, Kongsrud JA, Oug E, Gaeva D, Sikorski A, Johansen RA, Hutchings PA, Lavesque N, Capa M (2018) A mega-cryptic species complex hidden among one of the most common annelids in the North East Atlantic. PLoS One 13, e0198356
| A mega-cryptic species complex hidden among one of the most common annelids in the North East Atlantic.Crossref | GoogleScholarGoogle Scholar | 29924805PubMed |
O’Shea BJ (2006) Checklist of the mosses of sub-Saharan Africa, version 5. Tropical Bryology Research Reports 6, 1–252.
Peakall R, Smouse PE (2006) GenAlEx 6: genetic analysis in Excel. Population genetic software for teaching and research. Molecular Ecology Notes 6, 288–295.
| GenAlEx 6: genetic analysis in Excel. Population genetic software for teaching and research.Crossref | GoogleScholarGoogle Scholar |
Peakall R, Smouse PE (2012) GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research-an update. Bioinformatics 28, 2537–2539.
| GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research-an update.Crossref | GoogleScholarGoogle Scholar | 22820204PubMed |
Ramsay HP (1984) Census of New South Wales mosses. Telopea 2, 455–533.
| Census of New South Wales mosses.Crossref | GoogleScholarGoogle Scholar |
Ricca M, Shaw AJ (2010) Allopolyploidy and homoploid hybridization in the Sphagnum subsecundum complex (Sphagnaceae: Bryophyta). Biological Journal of the Linnean Society. Linnean Society of London 99, 135–151.
| Allopolyploidy and homoploid hybridization in the Sphagnum subsecundum complex (Sphagnaceae: Bryophyta).Crossref | GoogleScholarGoogle Scholar |
Robinson SC, Miller NG (2013) Bryophyte diversity on Adirondack alpine summits is maintained by dissemination and establishment of vegetative fragments and spores. The Bryologist 116, 382–391.
| Bryophyte diversity on Adirondack alpine summits is maintained by dissemination and establishment of vegetative fragments and spores.Crossref | GoogleScholarGoogle Scholar |
Ronquist F, Huelsenbeck JP (2003) MRBAYES 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19, 1572–1574.
| MRBAYES 3: Bayesian phylogenetic inference under mixed models.Crossref | GoogleScholarGoogle Scholar | 12912839PubMed |
Rother H, Fink D, Shulmeister J, Mifsud C, Evans M, Pughe J (2014) The early rise and late demise of New Zealand’s last glacial maximum. Proceedings of the National Academy of Sciences of the United States of America 111, 11630–11635.
| The early rise and late demise of New Zealand’s last glacial maximum.Crossref | GoogleScholarGoogle Scholar | 25071171PubMed |
Scott GAM, Stone IG, Rosser C (1976) ‘The Mosses of southern Australia.’ (Academic Press: London)
Seppelt RD (2006) Sphagnaceae. In ‘Flora of Australia. Vol. 51. Mosses 1’. pp. 89–104. (CSIRO Publishing: Melbourne, Vic., Australia)
Shaw AJ, Tong C, Wang L-S, Flatberg KJ, Flatberg B, Shaw B, Zhou P, Boles S, Terracciano S (2008) Genetic variation in three Chinese peat mosses based on microsatellite markers, with primer information and analysis of ascertainment bias. The Bryologist 111, 271–281.
| Genetic variation in three Chinese peat mosses based on microsatellite markers, with primer information and analysis of ascertainment bias.Crossref | GoogleScholarGoogle Scholar |
Shaw AJ, Devos N, Liu Y, Cox CJ, Goffinet B, Flatberg KJ, Shaw B (2016) Organellar phylogenomics of an emerging model system: Sphagnum (peatmoss). Annals of Botany 118, 185–196.
| Organellar phylogenomics of an emerging model system: Sphagnum (peatmoss).Crossref | GoogleScholarGoogle Scholar |
Sherwin WB (2010) Entropy and information approaches to genetic diversity and its expression: genomic geography. Entropy 12, 1765–1798.
| Entropy and information approaches to genetic diversity and its expression: genomic geography.Crossref | GoogleScholarGoogle Scholar |
Sherwin WB, Jabot F, Rush R, Rossetto M (2006) Measurement of biological information with applications from genes to landscapes. Molecular Ecology 15, 2857–2869.
| Measurement of biological information with applications from genes to landscapes.Crossref | GoogleScholarGoogle Scholar | 16911206PubMed |
Sherwin WB, Chao A, Jost L, Smouse PE (2017) Information theory widens the spectrum of molecular evolution and ecology. Trends in Ecology & Evolution 32, 948–963.
| Information theory widens the spectrum of molecular evolution and ecology.Crossref | GoogleScholarGoogle Scholar |
Smouse PE, Whitehead MR, Peakall R (2015) An informational diversity analysis framework, illustrated with sexually deceptive orchids in early stages of speciation. Molecular Ecology Resources 15, 1375–1384.
| An informational diversity analysis framework, illustrated with sexually deceptive orchids in early stages of speciation.Crossref | GoogleScholarGoogle Scholar | 25916981PubMed |
Warnstorf C (1911) Sphagnales – Sphagnaceae (Sphagnologia universalis). Pflanzenr 51, 1–546.
Willis JH (1953) Systematic notes on Victorian mosses – 2. Victorian Naturalist 70, 55–57.
