Standing on the shoulders of giants: molecular data confirm Kükenthal’s systematic placement of the Australian endemic Carex archeri (Cyperaceae)
Ana Morales-Alonso A B * , Karen Wilson C , Kerry A. Ford D , Mónica Míguez B , Pedro Jiménez-Mejías B and Santiago Martín-Bravo BA
B
C
D
Abstract
Archer’s sedge (Carex archeri Boott) is a small, rare (or possibly overlooked by collectors due to the diminutive size) species restricted to alpine and subalpine habitats in south-eastern mainland Australia and Tasmania. The systematic placement has been obscure with the species having been historically associated with sections in four of the six recognised Carex subgenera. We investigated the placement of C. archeri by addition to the available Carex molecular phylogenetic framework. Our results support C. archeri belonging to sect. Junciformes (in subg. Psyllophorae), making this the only representative of the subgenus in Australia. This placement was first proposed by Kükenthal (1909) who regarded C. archeri as a synonym of the New Zealand endemic C. acicularis Boott but our phylogenetic analyses support C. archeri as a separate taxon. Our approach highlights the utility of molecular barcoding for elucidating systematic relationships of poorly known taxa. Biogeographic reconstruction suggests Late Miocene dispersal from South America to the south-western Pacific but does not clarify whether New Zealand or Australia was colonised first. We evaluate the conservation status of Carex archeri using IUCN criteria as Endangered at the global level. At the state level, we propose Critically Endangered status in New South Wales, Endangered in Victoria and Data Deficient in Tasmania.
Keywords: Australia, biogeography, conservation, endangered plants, molecular systematics, plant DNA barcoding, Southern Hemisphere.
References
Auld J, Everingham SE, Hemmings FA, Moles AT (2022) Alpine plants are on the move: quantifying distribution shifts of Australian alpine plants through time. Diversity and Distributions 28, 943-955.
| Crossref | Google Scholar |
Bachman S, Moat J, Hill AW, de Torre J, Scott B (2011) Supporting Red List threat assessments with GeoCAT: geospatial conservation assessment tool. ZooKeys 150, 117-126.
| Crossref | Google Scholar | PubMed |
Benítez-Benítez C, Otero A, Ford KA, García-Moro P, Donadío S, Luceño M, Martín-Bravo S, Jiménez-Mejías P (2021) An evolutionary study of Carex subg. Psyllophorae (Cyperaceae) sheds light on a strikingly disjunct distribution in the Southern Hemisphere, with emphasis on its Patagonian diversification. Frontiers in Plant Science 12, 735302.
| Crossref | Google Scholar | PubMed |
Bridle KL, Kirkpatrick JB, Cullen P, Shepherd RR (2001) Recovery in alpine heath and grassland following burning and grazing, Eastern Central Plateau, Tasmania, Australia. Arctic, Antarctic, and Alpine Research 33, 348-356.
| Crossref | Google Scholar |
Doyle JJ, Doyle JL (1987) A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochemical Bulletin 19, 11-15.
| Crossref | Google Scholar |
Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research 32, 1792-1797.
| Crossref | Google Scholar | PubMed |
Edmonds T, Lunt ID, Roshier DA, Louis J (2006) Annual variation in the distribution of summer snowdrifts in the Kosciuszko alpine area, Australia, and its effect on the composition and structure of alpine vegetation. Austral Ecology 31, 837-848.
| Crossref | Google Scholar |
García-Moro P, Otero A, Benítez-Benítez C, Costa L, Martín-Bravo S, Naczi RFC, Reznicek AA, Roalson EH, Starr JR, Jiménez-Mejías P (2022) Biogeography and systematics of Carex subgenus Uncinia (Cyperaceae): A unique radiation for the genus Carex in the Southern Hemisphere. Taxon 71, 587-607.
| Crossref | Google Scholar |
Global Carex Group (2015) Making Carex monophyletic (Cyperaceae, tribe Cariceae): a new broader circumscription. Botanical Journal of the Linnean Society 179, 1-42.
| Crossref | Google Scholar |
Hamlin BG (1962) Studies in New Zealand Carices—VI. Subgenus Primocarex Kükenthal. Transactions of the Royal Society of New Zealand, Botany 1, 269-277.
| Google Scholar |
Hoang DT, Chernomor O, von Haeseler A, Minh BQ, Vinh LS (2018) UFBoot2: Improving the ultrafast bootstrap approximation. Molecular Biology and Evolution 35, 518-522.
| Crossref | Google Scholar | PubMed |
Hutchinson MF, Stein JL, Stein JA, Anderson H, Tickle PK (2008) GEODATA 9 second DEM and D8: Digital Elevation Model Version 3 and Flow Direction Grid 2008. Record DEM-9S.v3. (Geoscience Australia: Canberra, ACT, Australia) Available at https://pid.geoscience.gov.au/dataset/ga/66006 [Dataset, verified November 2023]
International Union for Conservation of Nature and Natural Resources (2022) Guidelines for using the IUCN Red List categories and criteria. Version 15.1. Prepared by the Standards and Petitions Committee. (IUCN) Available at https://www.iucnredlist.org/documents/RedListGuidelines.pdf
Jiménez-Mejías P, Hahn M, Lueders K, Starr JR, Brown BH, Chouinard BN, Chung K-S, Escudero M, Ford BA, Ford KA, Gebauer S, Gehrke B, Hoffmann MH, Jin X-F, Jung J, Kim S, Luceño M, Maguilla E, Martín-Bravo S, Míguez M, Molina A, Naczi RFC, Pender JE, Reznicek AA, Villaverde T, Waterway MJ, Wilson KL, Yang J-C, Zhang S, Hipp A, Roalson EH (2016a) Megaphylogenetic specimen-level approaches to the Carex (Cyperaceae) phylogeny using ITS, ETS, and matK: implications for classification. Systematic Botany 41, 500-518.
| Crossref | Google Scholar |
Jiménez-Mejías P, Martinetto P, Momohara E, Popova S, Smith SY, Roalson EH (2016b) A commented synopsis of the Pre-Pleistocene fossil record of Carex (Cyperaceae). The Botanical Review 82, 258-345.
| Crossref | Google Scholar |
Jiménez-Mejías P, Benítez-Benítez C, Beltrán H, Cano A, Donadío S, Escudero M, Gebauer S, Hipp AL, Míguez M, Naczi R, Reznicek A, Roalson EH, Márquez-Corro JI, Villaverde T, Dorr L, Martín-Bravo S, Luceño M (2018) Carex (Cyperaceae) in South America: diversity, phylogenetics and biogeography of a Boreotemperate Element in the Neotropics. In ‘Monocots VI International Conference’, 7–12 October 2018, Natal, Brazil. Poster contribution. 10.13140/RG.2.2.15139.30248
Jiménez-Mejías P, Saldivia P, Gebauer S, Martín-Bravo S (2021) A new remarkable dwarf sedge (Carex phylloscirpoides, Cyperaceae) from northern Chile, with insights on the evolution of austral Carex section Racemosae. Systematic Botany 46, 34-47.
| Crossref | Google Scholar |
Kalyaanamoorthy S, Minh BQ, Wong TKF, von Haeseler A, Jermiin LS (2017) ModelFinder: fast model selection for accurate phylogenetic estimates. Nature Methods 14, 587-589.
| Crossref | Google Scholar | PubMed |
Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M, Sturrock S, Buxton S, Cooper A, Markowitz S, Duran C, Thierer T, Ashton B, Meintjes P, Drummond A (2012) Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28(12), 1647-1649.
| Crossref | Google Scholar |
Luceño M, Villaverde T, Márquez-Corro JI, Sánchez-Villegas R, Maguilla E, Escudero M, Jiménez-Mejías P, Sánchez-Villegas M, Míguez M, Benítez-Benítez C, Muasya AM, Martín-Bravo S (2021) An integrative monograph of Carex section Schoenoxiphium (Cyperaceae). PeerJ 9, e11336.
| Crossref | Google Scholar | PubMed |
McGlone MS (2005) Goodbye Gondwana. Journal of Biogeography 32, 739-740.
| Crossref | Google Scholar |
McGlone M, Duncan RP, Heenan PB (2001) Endemism, species selection and the origin and distribution of the vascular plant flora of New Zealand. Journal of Biogeography 28, 199-216.
| Crossref | Google Scholar |
McLoughlin S (2001) The breakup history of Gondwana and its impact on pre-Cenozoic floristic provincialism. Australian Journal of Botany 49, 271-300.
| Crossref | Google Scholar |
Martín-Bravo S, Jiménez-Mejías P, Villaverde T, Escudero M, Hahn M, Spalink D, Roalson EH, Hipp AL, , The Global Carex Group (2019) A tale of worldwide success: behind the scenes of Carex (Cyperaceae) biogeography and diversification. Journal of Systematics and Evolution 57, 695-718.
| Crossref | Google Scholar |
Martín-Bravo S, McCarthy J, Márquez-Corro JI, Sanz-Arnal M, Ford KA (2022) The genus Carex (Cyperaceae) in New Zealand: a southern hemisphere diversity hotspot in a boreotemperate genus. In ‘Botany 2022: Plants at the Extreme!’, 24–27 June 2022, Anchorage, AK, USA. Abstract. (Botanical Society of America) Available at https://biosystematics2023.org/wp-content/uploads/2023/11/The-genus-Carex-Cyperaceae-in-New-Zealand-a-southern-hemisphere-diversity-hotspot-in-a-boreotemperate-genus.pdf
Meudt HM, Simpson BB (2006) The biogeography of the austral, subalpine genus Ourisia (Plantaginaceae) based on molecular phylogenetic evidence: South American origin and dispersal to New Zealand and Tasmania. Biological Journal of the Linnean Society 87, 479-513.
| Crossref | Google Scholar |
Míguez M, Bertolucci F, Jiménez-Mejías P, Martín-Bravo S (2022) Re-evaluating the presence of Carex microcarpa (Cyperaceae) in Italy based on herbarium material and DNA barcoding. Plant Biosystems 156, 628-634.
| Crossref | Google Scholar |
Moon KL, Chown SL, Fraser CI (2017) Reconsidering connectivity in the sub-Antarctic. Biological Reviews 92, 2164-2181.
| Crossref | Google Scholar | PubMed |
Morales-Alonso A, Muñoz-Schüler P, Pereira-Silva L, Donadío S, Martín-Bravo S, Jiménez-Mejías P (2024a) A synopsis of Carex subgenus Psyllophorae, sect. Junciformes (Cyperaceae) in South America. Botanical Journal of the Linnean Society 20, 1-41.
| Crossref | Google Scholar |
Morales-Alonso A, Gebauer S, Cano A, Oleas NH, Pinto-Zárate J, Martín-Bravo S, Jiménez-Mejías P (2024b) Fieldwork, herbarium revisions and DNA barcode: basic ingredients to shed light on the dark realms of plant biodiversity. An example with two enigmatic Andean Carex (Cyperaceae) species. Systematic Botany 49, 209-226.
| Crossref | Google Scholar |
Muñoz J, Felicísimo AM, Cabezas F, Burgaz AR, Martínez I (2004) Wind as a long-distance dispersal vehicle in the Southern Hemisphere. Science 304, 1144-1147.
| Crossref | Google Scholar | PubMed |
Muñoz-Schüler P, Morales-Alonso A, Márquez-Corro JI, Arroyo MTK, Martín-Bravo S, Jiménez-Mejías P (2024) Carex recondita Muñoz-Schüler, Martín-Bravo & Jim.Mejías (Carex section Junciformes Kük., Cyperaceae), a new sedge species from the Andes of central Chile. PhytoKeys 243, 15-30.
| Crossref | Google Scholar | PubMed |
Nguyen LT, Schmidt HA, von Haeseler A, Minh BQ (2015) IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Molecular Biology and Evolution 32, 268-274.
| Crossref | Google Scholar | PubMed |
NSW National Parks and Wildlife Service (2023) Archer’s Carex (Carex archeri) Conservation Action Plan. (NSW Environment and Heritage) Available at https://www.environment.nsw.gov.au/research-and-publications/publications-search/conservation-action-plan-archers-carex-carex-archeri [Verified December 2023]
NSW Threatened Species Scientific Committee (2004) Endangered species listing, final determination. Carex archeri (a herb). (NSW Environment and Heritage) Available at https://www.environment.nsw.gov.au/Topics/Animals-and-plants/Threatened-species/NSW-Threatened-Species-Scientific-Committee/Determinations/Final-determinations/2004-2007/Carex-archeri-a-herb-endangered-species-listing [Verified November 2023]
Otero A, Jiménez-Mejías P, Valcárcel V, Vargas P (2019) Worldwide long-distance dispersal favored by epizoochorous traits in the biogeographic history of Omphalodeae (Boraginaceae). Journal of Systematics and Evolution 57, 579-593.
| Crossref | Google Scholar |
Ree RH, Sanmartín I (2018) Conceptual and statistical problems with the DEC+J model of founder-event speciation and its comparison with DEC via model selection. Journal of Biogeography 45, 741-749.
| Crossref | Google Scholar |
Ree RH, Smith SA (2008) Maximum likelihood inference of geographic range evolution by dispersal, local extinction, and cladogenesis. Systematic Biology 57, 4-14.
| Crossref | Google Scholar | PubMed |
Roalson E, Jiménez-Mejías P, Hipp AL, Benítez-Benítez C, Bruederle LP, Chung K-S, Escudero M, Ford BA, Ford K, Gebauer S, Gehrke B, Hahn M, Qasim Hayat M, Hoffmann MH, Jin X-F, Kim S, Larridon I, Léveillé-Bourret É, Lu Y-F, Luceño M, Maguilla E, Márquez-Corro JI, Martín-Bravo S, Masaki T, Míguez M, Naczi RFC, Reznicek AA, Spalink D, Starr JR, Uzma , Villaverde T, Waterway MJ, Wilson KL, Zhang S (2021) A framework infrageneric classification of Carex (Cyperaceae) and its organizing principles. Journal of Systematics and Evolution 59, 726-762.
| Crossref | Google Scholar |
Ronquist F (1997) Dispersal–vicariance analysis: a new approach to the quantification of historical biogeography. Systematic Biology 46, 195-203.
| Crossref | Google Scholar |
Sanmartín I, Ronquist F (2004) Southern Hemisphere biogeography inferred by event‐based models: plant versus animal patterns. Systematic Biology 53, 216-243.
| Crossref | Google Scholar | PubMed |
Sanmartín I, Wanntorp L, Winkworth RC (2007) West Wind Drift revisited: testing for directional dispersal in the Southern Hemisphere using event-based tree fitting. Journal of Biogeography 34, 398-416.
| Crossref | Google Scholar |
Sanz-Arnal M, García-Moro P, Benítez-Benítez C, et al. (in press) The importance of expert curation in taxonomically problematic groups: an improved occurrences database for the genus Carex (Cyperaceae). Scientific Data
| Google Scholar |
Schönberger I, Wilton AD, Boardman KF, Breitwieser I, de Lange PJ, de Pauw B, Ford KA, Gibb ES, Glenny DS, Greer PA, Heenan PB, Maule HG, Novis PM, Prebble JM, Smissen RD, Tawiri K (2022) ‘Checklist of the New Zealand Flora – Seed Plants.’ (Manaaki Whenua-Landcare Research: Lincoln, New Zealand) 10.26065/sw4r-0w62
Shaw J, Shafer HL, Leonard OR, Kovach MJ, Schorr M, Morris AB (2005) The tortoise and the hare II: relative utility of 21 noncoding chloroplast DNA sequences for phylogenetic analysis. American Journal of Botany 92, 142-166.
| Crossref | Google Scholar | PubMed |
Smith SA, O’Meara BC (2012) treePL: divergence time estimation using penalized likelihood for large phylogenies. Bioinformatics 28, 2689-2690.
| Crossref | Google Scholar | PubMed |
Tamura K, Stecher G, Kumar S (2021) MEGA11: Molecular Evolutionary Genetics Analysis version 11. Molecular Biology and Evolution 38, 3022-3027.
| Crossref | Google Scholar | PubMed |
Threatened Species Scientific Committee (2023) EPBC Act List of Threatened Flora. (Department of Climate Change, Energy, the Environment and Water: Canberra, ACT, Australia) Available at http://www.environment.gov.au/cgi-bin/sprat/public/publicthreatenedlist.pl?wanted=flora [Verified December 2023]
Van de Wouw M, van Dijk P, Huiskes AHL (2008) Regional genetic diversity patterns in Antarctic hairgrass (Deschampsia antarctica Desv.). Journal of Biogeography 35, 365-376.
| Crossref | Google Scholar |
Victoria State Government (2023) Flora and Fauna Guarantee Act Threatened list. (Victoria Department of Energy, Environment and Climate Action: Melbourne, Vic., Australia) Available at https://www.environment.vic.gov.au/conserving-threatened-species/threatened-list [Verified December 2023]
Villaverde T, Jiménez-Mejías P, Luceño M, Waterway MJ, Kim S, Lee B, Rincón-Barrado M, Hahn M, Maguilla E, Roalson EH, Hipp AL, Global Carex Group (2020) A new classification of Carex (Cyperaceae) subgenera supported by a Hyb-Seq backbone phylogenetic tree. Botanical Journal of the Linnean Society 194, 141-163.
| Crossref | Google Scholar |
Waters JM (2008) Driven by the West Wind Drift? A synthesis of southern temperate marine biogeography, with new directions for dispersalism. Journal of Biogeography 35, 417-427.
| Crossref | Google Scholar |
Wheeler GA (1989) The taxonomy of Carex sect. Aciculares (Cyperaceae) in South America. Systematic Botany 14, 168-188.
| Crossref | Google Scholar |
Williams R, Papst W, McDougall K, Mansergh I, Heinze D, Camac J, Nash M, Morgan J, Hoffmann A (2014) Alpine ecosystems. Chapter 6. In ‘Biodiversity and Environmental change ‒ Monitoring, challenges and direction’. (Eds D Lindenmayer, E Burns, N Thurgate, A Lowe) (CSIRO Publishing: Melbourne, Vic., Australia) [e-book]
Winkworth RC (2010) Darwin and dispersal. Biology International 47, 139-144.
| Google Scholar |