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Type: Article
Published: 2024-06-25
Page range: 173-186
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Genomic and morphological data reveal a critically endangered new species from the Atlantic Forest, Paepalanthus salimenae (Eriocaulaceae)

Programa de Pós-Graduação em Botânica, Escola Nacional de Botânica Tropical, Instituto de Pesquisas Jardim Botânico do Rio de Janeiro, R. Pacheco Leão 2040, 22460-036, Rio de Janeiro - RJ, Brazil
Diretoria de Pesquisa, Instituto de Pesquisas Jardim Botânico do Rio de Janeiro, R. Pacheco Leão 915, 22460-040, Rio de Janeiro - RJ, Brazil
Tohoku University, Kawatabi Field Science Center, Graduate School of Agricultural Science, 232-3 Yomogida, Naruko-onsen, Osaki, Miyagi 989-6711, Japan
Tohoku University, Kawatabi Field Science Center, Graduate School of Agricultural Science, 232-3 Yomogida, Naruko-onsen, Osaki, Miyagi 989-6711, Japan
Tohoku University, Kawatabi Field Science Center, Graduate School of Agricultural Science, 232-3 Yomogida, Naruko-onsen, Osaki, Miyagi 989-6711, Japan
Programa de Pós-Graduação em Botânica, Escola Nacional de Botânica Tropical, Instituto de Pesquisas Jardim Botânico do Rio de Janeiro, R. Pacheco Leão 2040, 22460-036, Rio de Janeiro - RJ, Brazil
Programa de Pós-Graduação em Botânica, Escola Nacional de Botânica Tropical, Instituto de Pesquisas Jardim Botânico do Rio de Janeiro, R. Pacheco Leão 2040, 22460-036, Rio de Janeiro - RJ, Brazil. Departamento de Botânica, Instituto de Biologia, Universidade Federal do Rio de Janeiro, CCS, Bloco A1, Cidade Universitária, 21941-590, Rio de Janeiro, Rio de Janeiro, Brazil.
Conservation genetic diversity MIG-seq Paepalanthoideae taxonomy Monocots

Abstract

During our investigation of the genetic and morphological variation within the distribution range of Paepalanthus calvus, we observed that specimens from Juiz de Fora municipality, Minas Gerais (Brazil) were morphologically divergent. Through genome-wide analyses using MIG-seq and detailed morphological comparisons, we were able to establish consistent differences between P. calvus and the Juiz de Fora specimens, which supported the recognition of a new species, Paepalanthus salimenae sp. nov. This new species is primarily distinguished by the narrow leaves; trichomes on the leaves, spathes, and scapes; densely pilose involucral bracts; and the tufted apex of some floral organs. Paepalanthus salimenae exhibits low genetic diversity and strong population structure. A preliminary conservation risk assessment suggests this species as Critically Endangered, highlighting the urgent need for conservation efforts to protect its habitat and intraspecific diversity. We provide photographs, line drawings and additional commentaries on the distribution, habitat, and morphological affinities of P. salimenae to congeneric taxa.

References

  1. Alves, R., Silva, N.G., Oliveira, J.A. & Medeiros, D. (2014) Circumscribing campo rupestre–megadiverse Brazilian rocky montane savanas. Brazilian Journal of Biology 74: 355–362. http://dx.doi.org/10.1590/1519-6984.23212
  2. Antonelli, A. (2015) Multiple origins of mountain life. Nature 524: 300–301. https://doi.org/10.1038/nature14645
  3. Azevedo, L., Zappi, D.C., Oliveira, D.M.G., Meyer, L., Lughadha, E.N., Clegg, R., Meireles, L.D., Melo, P.H.A., Pennington, R.T. & Neves, D.M. (2024) On the rocks: Biogeography and floristic identity of rocky ecosystems in eastern South America. Journal of Systematics and Evolution 62: 1–16. https://doi.org/10.1111/jse.13052
  4. Bachman, S., Moat, J., Hill, A.W., de la Torre, J. & Scott, B. (2011) Supporting Red List threat assessments with GeoCAT: geospatial conservation assessment tool. In: Smith, V. & Penev, L. (Eds.) e-Infrastructures for data publishing in biodiversity science. ZooKeys 150: 117–126.
  5. Bolger, A.M., Lohse, M. & Usadel, B. (2014) Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30: 2114–2120. https://doi.org/10.1093/BIOINFORMATICS/BTU170
  6. Chang, C.C., Chow, C.C., Tellier, L.C.A.M., Vattikuti, S., Purcell, S.M. & Lee, J.J. (2015) Second-generation PLINK: Rising to the challenge of larger and richer datasets. GigaScience 4: 7. https://doi.org/10.1186/S13742-015-0047-8/2707533
  7. Costa, F.N., Trovó, M. & Sano, P.T. (2008) Eriocaulaceae na Cadeia do Espinhaço: riqueza, endemismo e ameaças. Megadiversidade 4: 117–125.
  8. Earl, D.A. & von Holdt, B.M. (2012) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conservation Genetics Resources 4: 359–361. https://doi.org/10.1007/s12686-011-9548-7
  9. Evanno, G., Regnaut, S. & Goudet, J. (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Molecular Ecology 14: 2611–2620. https://doi.org/10.1111/j.1365-294X.2005.02553.x
  10. Excoffier, L., Laval, G. & Schneider, S. (2005) Arlequin (version 3.0): an integrated software package for population genetics data analysis. Evolutionary Bioinformatics Online 1: 47–50. https://doi.org/10.1177/117693430500100003
  11. Exposito-Alonso, M., Booker, T.R., Czech, L., Gillespie, L., Hateley, S., Kyriazis, C.C., Lang, P.L.M., Leventhal, L., Nogues-Bravo, D. Pagowski, V., Ruffley, M., Spence, J.P., Arana, S.E.T., Weib, C., Zess, E. & Zess, E. (2022) Genetic diversity loss in the Anthropocene. Science 377: 1431–1435. https://doi.org/10.1126/science.abn5642
  12. Gamba, D. & Muchhala, N. (2020) Global patterns of population genetic differentiation in seed plants. Molecular Ecology 29: 3413–3428. https://doi.org/10.1111/mec.15575
  13. Giulietti, A.M., De Queiroz, L.P., Wanderley, M.D.G.L. & van den Berg, C. (2005) Biodiversidade e conservação das plantas no Brasil. Megadiversidade 1: 52–61.
  14. Giulietti, A.M., Andrade, M.J.G., Scatena, V.L., Trovó, M., Coan, A.I., Sano, P.T., Santos, F.A.R. & van den Berg, C. (2012) Molecular phylogeny, morphology and their implications for the taxonomy of Eriocaulaceae. Rodriguésia 63: 1–19. https://doi.org/10.1590/S2175-78602012000100001
  15. Goudet, J., Jombart, T. & Goudet, M.J. (2015) Package ‘hierfstat’. Estimation and Tests of Hierarchical F-Statistics. Available from: https://cran.r-project.org/ (accessed 13 December 2023).
  16. Guedes, T.B., Azevedo, J.A., Bacon, C.D., Provete, D.B. & Antonelli, A. (2020) Diversity, endemism, and evolutionary history of montane biotas outside the Andean Region. In: Rull, V. & Carnaval, A. (Eds.) Neotropical Diversification: Patterns and Processes. Springer, New York, pp. 299–328. https://doi.org/10.1007/978-3-030-31167-4_13
  17. Hamrick, J.L. & Godt, M.J.W. (1990) Plant population genetics, breeding, and genetic resources. In: Brown, A.H.D., Clegg, M.T., Kahler, A.L. & Weir, B.S. (Eds.) Allozyme diversity in plant species. Sinauer Associates, Sunderland, pp. 43–63.
  18. Harms, H. (1928) Bromeliaceae Novae I. Notizblatt des Botanischen Gartens und Museums zu Berlin-Dahlem 10: 211–218.
  19. Hartl, D.L. & Clark, A.G. (2010) Princípios de Genética de Populações 4 ed. Artmed Editora, 659 pp.
  20. Heinken, T. & Weber, E. (2013) Consequences of habitat fragmentation for plant species: do we know enough? Perspectives in Plant Ecology, Evolution and Systematics 15: 205–216. https://doi.org/10.1016/j.ppees.2013.05.003
  21. Husson, F., Josse, J., Le, S., Mazet, J. & Husson, M.F. (2016) Package ‘factominer’. An R package. Available from: https://cran.r-project.org/ (accessed 13 December 2023).
  22. Işik, K. (2011) Rare and endemic species: why are they prone to extinction? Turkish Journal of Botany 35: 411–417. https://doi.org/10.3906/bot-1012-90
  23. IUCN Standards Petitions Sub-committee (2022) Guidelines for using the IUCn Red List Categories and Criteria. Version 15.1. Available from: http:// www.iucn.org (accessed 18 December 2023).
  24. Jesus, F.F., Solferini, V.N., Semir, J. & Prado, P.I. (2001) Local genetic differentiation in Proteopsis argentea (Asteraceae), a perennial herb endemic in Brazil. Plant Systematics and Evolution 226: 59–68. https://doi.org/10.1007/s006060170073
  25. Jesus, F.F., Abreu, A.G., Semir, J. & Solferini, V.N. (2009) Low genetic diversity but local genetic differentiation in endemic Minasia (Asteraceae) species from Brazil. Plant Systematics and Evolution 277: 187–196. https://doi.org/10.1007/s00606-008-0128-6
  26. Jombart, T., Kamvar, Z.N., Collins, C., Lustrik, R., Beugin, M.P., Knaus, B.J. & Jombart, M.T. (2018) Package ‘adegenet’. Available from: https://cran.r-project.org/ (accessed 13 December 2023).
  27. Kassambara, A. & Mundt, F. (2017) Package ‘factoextra’. Extract and visualize the results of multivariate data analyses. Available from: https://cran.r-project.org/ (accessed on 13 December 2023).
  28. Körnicke, F.A. (1863) Eriocaulaceae In: Martius, K.F.P. & Eichler, A.G. (Eds.) Flora Brasiliensis. Vol. 3. Fleisher, Munich, pp. 271–508. https://doi.org/10.5962/bhl.title.454
  29. Lacy, R.C. (1997) Importance of genetic variation to the viability of mammalian populations. Journal of Mammalogy 78: 320–335. https://doi.org/10.2307/1382885
  30. Lande, R. (1998) Anthropogenic, ecological and genetic factors in extinction and conservation. Population Ecology 40: 259–269. https://doi.org/10.1007/BF02763457
  31. Le Stradic, S., Buisson, E., Negreiros, D., Campagne, P. & Fernandes, W.G. (2014) The role of native woody species in the restoration of Campos Rupestres in quarries. Applied Vegetation Science 17: 109–120. https://doi.org/10.1111/avsc.12058
  32. Le Stradic, S., Fernandes, G.W. & Buisson, E. (2018) No recovery of campo rupestre grasslands after gravel extraction: implications for conservation and restoration. Restoration Ecology 26: 151–159. https://doi.org/10.1111/rec.12713
  33. Ledig, F.T. (1992) Human impacts on genetic diversity in forest ecosystems. Oikos 63: 87–108. https://doi.org/10.2307/3545518
  34. Lienert, J. (2004) Habitat fragmentation effects on fitness of plant populations–a review. Journal for Nature Conservation 12: 53–72. https://doi.org/10.1016/j.jnc.2003.07.002
  35. Lischer, H.E. & Excoffier, L. (2012) PGDSpider: an automated data conversion tool for connecting population genetics and genomics programs. Bioinformatics 28: 298–299. https://doi.org/10.1093/bioinformatics/btr642
  36. Luo, Q., Li, F., Yu, L., Wang, L., Xu, G. & Zhou, Z. (2021) Genetic diversity of natural populations of Taxus mairei. Conservation Genetics 22: 63–74. https://doi.org/10.1007/s10592-021-01403-9
  37. Markert, J.A., Champlin, D.M., Gutjahr-Gobell, R., Grear, J.S., Kuhn, A., McGreevy, T.J., Roth, A., Bagley, M.J. & Nacci, D.E. (2010) Population genetic diversity and fitness in multiple environments. BMC Evolutionary Biology 10: 1–13. https://doi.org/10.1186/1471-2148-10-205
  38. Martins, E.R.J., Costa, A.C.G., Pinheiro, P.M., Navarro, D., Thomas, W.W., Giulietti, A.M. & Machado, I.C. (2022) Mixed pollination system and floral signals of Paepalanthus (Eriocaulaceae): insects and geitonogamy ensure high reproductive success. Annals of Botany 129: 473–484. https://doi.org/10.1093/aob/mcac008
  39. Masuda, K., Setoguchi, H., Nagasawa, K., Ishihara, M.I., Sawa, K., Horie, K., Tsuboi, H., Fukumoto, D., Tango, T. & Sakaguchi, S. (2022) Rear-edge daylily populations show legacies of habitat fragmentation due to the Holocene climate warming. Journal of Biogeography 50: 551–563. https://doi.org/10.1111/jbi.14552
  40. Moldenke, H.N. (1975) Notes on new and noteworthy plants LXX. Phytologia 31: 273–274. [https://www.biodiversitylibrary.org/page/13038975]
  41. Moldenke, H.N. (1978) Notes on new and noteworthy plants CXI. Phytologia 39: 236–239. [https://www.biodiversitylibrary.org/page/13163577]
  42. Mucina, L. (2019) Biome: evolution of a crucial ecological and biogeographical concept. New Phytologist 222: 97–114. https://doi.org/10.1111/nph.15609
  43. Negreiros, D., Fernandes, G.W., Berbara, R.L.L., Rodarte, L.H. & Barbosa, N.P.U. (2011) Caracterização fisico-quimica de solos quartziticos degradados e areas adjacentes de campo rupestre na Serra do Cipó, MG, Brasil. Neotropical Biology and Conservation 6: 156–161.
  44. Okabe, N., Yahara, T., Tagane, S., Mitsuyuki, C., Matsuo, A., Sasaki, T., Moritsuka, E., Fuse, K., Shimizu-Kaya, U., Sang, J.A., Sylvester, R. & Suyama, Y. (2021) A new species of Actinodaphne (Lauraceae), A. lambirensis from Sarawak, Malaysia, and an analysis of its phylogenetic position using MIG-seq and ITS sequences. Acta Phytotaxonomica et Geobotanica 72: 43–59. https://doi.org/10.18942/apg.202005
  45. Oliveira, R.P., Borba, E.L., Longhi-Wagner, H.M., Pereira, A.C.S. & Lambert, S.M. (2008) Genetic and morphological variability in the Raddia brasiliensis complex (Poaceae: Bambusoideae). Plant Systematics and Evolution 274: 25–35. https://doi.org/10.1007/s00606-008-0034-y
  46. Oostermeijer, J.G.B., Luijten, S.H. & Den Nijs, J.C.M. (2003) Integrating demographic and genetic approaches in plant conservation. Biological Conservation 113: 389–398. https://doi.org/10.1016/S0006-3207(03)00127-7
  47. Oriani, A., Sano, P.T. & Scatena, V.L. (2009) Pollination biology of Syngonanthus elegans (Eriocaulaceae–Poales). Australian Journal of Botany 57: 94–105. https://doi.org/10.1071/BT08119
  48. Ouborg, N.J., Vergeer, P. & Mix, C. (2006) The rough edges of the conservation genetics paradigm for plants. Journal of Ecology 94: 1233–1248. https://doi.org/10.1111/j.1365-2745.2006.01167.x
  49. Parra, L.R., Giulietti, A.M., Andrade, M.J.G. & van den Berg, C. (2010) Reestablishment and new circumscription of Comanthera (Eriocaulaceae). Taxon 59: 1135–1146. https://doi.org/10.1002/tax.594013
  50. Pereira, A.C.S., Ribeiro, P.L. & Giulietti, A.M. (2016) Comanthera borbae (Eriocaulaceae): A new species endemic to the Northern portion of the Chapada Diamantina, Bahia, Brazil. Phytotaxa 270: 25–32. https://doi.org/10.11646/phytotaxa.270.1.2
  51. Phair, N.L., Toonen, R.J., Knapp, I.S.S. & von der Heyden, S. (2020) Anthropogenic pressures negatively impact genomic diversity of the vulnerable seagrass Zostera capensis. Journal of Environmental Management 255: 1–10. https://doi.org/10.1016/j.jenvman.2019.109831
  52. Pritchard, J.K., Stephens, M. & Donnelly, P. (2000) Inference of population structure using multilocus genotype data. Genetics 155: 945–959. https://doi.org/10.1093/genetics/155.2.945
  53. R Core Team. (2024) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna. Available from: https://www.r-project.org/ (accessed 24 January 2024)
  54. Radford, A.E., Dickson, W.C., Massey, J.R. & Bell, C.R. (1974) Vascular Plant systematics. Harper & Row Pub, New York, 891 pp.
  55. Rapini, A., Ribeiro, P.L., Lambert, S. & Pirani, J.R. (2008) A flora dos campos rupestres da Cadeia dos Espinhaço. Megadiversidade 4: 16–24.
  56. Rapini, A., Bitencourt, C., Luebert, F. & Cardoso, D. (2021) An escape-to-radiate model for explaining the high plant diversity and endemism in campos rupestres. Biological Journal of the Linnean Society 133: 481–498. https://doi.org/10.1093/biolinnean/blaa179
  57. Ribeiro, P.L., Borba, E.L., de Camargo, S.E., Lambert, S.M., Schnadelbach, A.S. & van den Berg, C. (2008) Genetic and morphological variation in the Bulbophyllum exaltatum (Orchidaceae) complex occurring in the Brazilian “campos rupestres”: implications for taxonomy and biogeography. Plant Systematics and Evolution 270: 109–137. https://doi.org/10.1007/s00606-007-0603-5
  58. Ribeiro, P.L., Pereira, A.C.S., Borba, E.L. & Giulietti, A.M. (2018) Genetic and morphological diversity and evidence of hybridization in the “sempre-vivas” (Comanthera, Eriocaulaceae) endemic to the Chapada Diamantina, Bahia, Brazil. Flora 238: 60–71. https://doi.org/10.1016/j.flora.2017.09.013
  59. Rochette, N.C., Rivera-Colon, A.G. & Catchen, J.M. (2019) Stacks 2: Analytical methods for paired-end sequencing improve RADseq-based population genomics. Molecular Ecology 28: 4737–4754. https://doi.org/10.1111/mec.15253
  60. Safford, H.D. (1999) Brazilian páramos I. An introduction to the physical environment and vegetation of the campos de altitude. Journal of Biogeography 26: 693–712. https://doi.org/10.1046/j.1365-2699.1999.00313.x
  61. Safford, H.D. (2007) Brazilian páramos IV. Phytogeography of the campos de altitude. Journal of Biogeography 34: 1701–1722. https://doi.org/10.1111/j.1365-2699.2007.01732.x
  62. Sano, P.T., Echternacht, L.A., Trovó, M. & Giulietti, A.M. (2009) Eriocaulaceae In: Stehmann, J.R., Forzza, R.C., Salino, M., Sobral, M., Costa, D.P. & Kamino, L.H.Y. (Eds.) Plantas da Floresta Atlântica. Jardim Botânico do Rio de Janeiro, Rio de Janeiro, pp. 242–246.
  63. Schlick-Steiner, B.C., Steiner, F.M., Seifert, B., Stauffer, C., Christian, E. & Crozier, R.H. (2010) Integrative taxonomy: a multisource approach to exploring biodiversity. Annual Review of Entomology 55: 421–438. https://doi.org/10.1146/annurev-ento-112408-085432
  64. Silveira, F.A., Negreiros, D., Barbosa, N.P., Buisson, E., Carmo, F.F., Carstensen, D.W., Abel, A.C., Cornelissen, T.G., Echternacht, L., Fernandes, G.W., Garcia, Q.S., Guerra, T.J., Jacobi, C.M., Lemos-Filho, J.P., Le Stradic, S., Morellato, L.P.C., Neves, F.S., Oliveira, R.S., Schaefer, C.E., Viana, P.L. & Lambers, H. (2016) Ecology and evolution of plant diversity in the endangered campo rupestre: a neglected conservation priority. Plant and Soil 403: 129–152. https://doi.org/10.1007/s11104-015-2637-8
  65. Slatkin, M. (1987) Gene flow and the geographic structure of natural populations. Science 236: 787–792. https://doi.org/10.1126/science.3576198
  66. Stuessy, T.F. (1990) Plant taxonomy, the systematic evaluation of comparative data. Columbia University, Press New York, 562 pp.
  67. Stützel, T. & Trovó, M. (2013) Inflorescences in Eriocaulaceae: taxonomic relevance and practical implications. Annals of Botany 12: 1505–1522. https://doi.org/10.1093/aob/mct234
  68. Suyama, Y. & Matsuki, Y. (2015) MIG-seq: an effective PCR-based method for genome-wide single-nucleotide polymorphism genotyping using the next-generation sequencing platform. Scientific Reports 5: 1–12. https://doi.org/10.1038/srep16963
  69. Suyama, Y., Hirota, S.K., Matsuo, A., Tsunamoto, Y., Mitsuyuki, C., Shimura, A. & Okano, K. (2022) Complementary combination of multiplex high-throughput DNA sequencing for molecular phylogeny. Ecological Research 37: 171–181. https://doi.org/10.1111/1440-1703.12270
  70. Thiers, B. (2024 [continuously updated]) Index Herbariorum: A global directory of public herbaria and associated staff. New York Botanical Garden’s Virtual Herbarium. Available from: http://sweetgum.nybg.org/ih/ (accessed 2 March 2024)
  71. Tilman, D. & Lehman, C. (2001) Human-caused environmental change: impacts on plant diversity and evolution. Proceedings of the National Academy of Sciences 98: 5433–5440. https://doi.org/10.1073/pnas.091093198
  72. Trovó, M. & Stützel, T. (2011) Diaspores in Eriocaulaceae: morphology, mechanisms, and implications. Feddes Repertorium 122: 456–464. https://doi.org/10.1002/fedr.201200003
  73. Trovó, M., Echternacht, L., Costa, F.N., Giulietti, A.M. & Sano, P.T. (2015) Nomenclatural and taxonomic notes on Eriocaulaceae from the Atlantic Forest, Brazil. Phytotaxa 205: 249–258. http://dx.doi.org/10.11646/phytotaxa.205.4.4
  74. Trovó, M., Fraga, C.N.D. & Sano, P.T. (2016) Paepalanthus capixaba (Eriocaulaceae), a new microendemic species from Espírito Santo, Brazil. Phytotaxa 258: 83–88. http://dx.doi.org/10.11646/phytotaxa.258.1.6
  75. Turland, N.J., Wiersema, J.H., Barrie, F.R., Greuter, W., Hawksworth, D.L., Herendeen, P.S., Knapp, S., Kusber, W.H., Li, D.Z., Marhold, K., May, T.W., McNeill, J., Monro, A.M., Prado, J., Price, M.J. & Smith, G.F. (Eds.) (2018) International Code of Nomenclature for algae, fungi, and plants (Shenzhen Code) adopted by the Nineteenth International Botanical Congress Shenzhen, China, July 2017. Regnum Vegetabile 159. Koeltz Botanical Books, Glashütten, 254 pp. https://doi.org/10.12705/Code.2018
  76. Vasconcelos, M.F.D. (2011) O que são campos rupestres e campos de altitude nos topos de montanha do Leste do Brasil? Brazilian Journal of Botany 34: 241–246. https://doi.org/10.1590/S0100-84042011000200012
  77. Weir, B.S. & Cockerham, C.C. (1984) Estimating F-statistics for the analysis of population structure. Evolution 39: 1358–1370. https://doi.org/10.2307/2408641
  78. Wright, S. (1965) The interpretation of population structure by F-statistics with special regard to systems of mating. Evolution 395–420. https://doi.org/10.2307/2406450
  79. Yeates, D.K., Seago, A., Nelson, L., Cameron, S.L., Joseph, L.E.O. & Trueman, J.W. (2011) Integrative taxonomy, or iterative taxonomy? Systematic Entomology 36: 209–217. https://doi.org/10.1111/j.1365-3113.2010.00558.x