Abstract
Phyllanthus emblica is a well-known medicinal and non-timber forest product species, widely distributed in the Indian subcontinent. Multiple disturbances like intensive fruit harvest, the spread of invasive species such as Lantana camara and Taxillus tomentosus, and other anthropogenic disturbances threaten population viability by altering ecological and genetic processes. Studying the genetic diversity and population structure of species harvested intensively and subjected to anthropogenic disturbances is crucial for evaluating their ability to survive under future environmental changes and for establishing conservation strategies. The genetic diversity and population structure of twelve populations of P. emblica that are harvested across three protected areas of the Western Ghats, the world’s most densely populated biodiversity hotspot was evaluated. Three hundred sixty samples were genotyped with nine simple sequence repeat markers. The changes in genetic diversity and genetic structure were assessed between generations by analyzing adults, seedlings, and juvenile samples. Despite intensive harvesting, the results found high genetic diversity in all the populations (mean/pop: Ho = 0.626; Hs = 0.722). However, genetic differentiation was significant between the study regions as well as between adult and seedling populations. The study also indicated a clear clustering of the twelve populations into three distinct genetic clusters. Neighbor-joining tree and hierarchical clustering analysis also showed the same pattern. The genetic data from the study provide information on how local disturbances including harvesting affect the population's genetic diversity and structure, which can provide a basis for implementing programs for conserving and sustainable utilization of P. emblica genetic resources in the future.
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Ammal EKJ, Sundara RR (1958) Polyploid and Vitamin C in Emblica officinalis Gaertn. Proc Indian Acad Sci B 47:312–314. https://doi.org/10.1007/BF03051560
Banks SC, Cary GJ, Smith AL, Davies ID, Driscoll DA, Gill AM, Lindenmayer DB, Peakall R (2013) How does ecological disturbance influence genetic diversity? Trends Ecol Evol 28:670–679. https://doi.org/10.1016/j.tree.2013.08.005
Beckman NG, Rogers HS (2013) Consequences of seed dispersal for plant recruitment in tropical forests: interactions within the seedscape. Biotropica 45:666–681. https://doi.org/10.1111/btp.12071
Bedi YS (1991) Chromosomal Conspectus and Evolutionary Status of lndian Commercial Timbers (Hardwoods). Cytologia 56:665–672. https://doi.org/10.1508/cytologia.56.665
Benestan LM, Ferchaud A, Hohenlohe PA, Garner BA, Naylor GJP, Baums IB, Schwartz MK, Kelley JL, Luikart G (2016) Conservation genomics of natural and managed populations: building a conceptual and practical framework. Molec Ecol 25:2967–2977. https://doi.org/10.1111/mec.13647
Bhat JA, Negi AK, Todaria NP (2015) Regeneration status of woody species in a protected area of Western Himalaya. Acta Ecol Sin 35:51–58. https://doi.org/10.1016/j.chnaes.2015.04.006
Brummitt NA. and Bachman SP (2010). Plants under pressure- a global assessment: the first report of the IUCN sampled red list index for plants. Royal Botanic Gardens, Kew. Available at: https://www.europarl.europa.eu/news/en/headlines/society/20200109STO69929/biodiversity-loss-what-is-causing-it-and-why-is-it-a-concern. Accessed 6 Apr 2022
Dufresne F, Stift M, Vergilino R, Mable BK (2014) Recent progress and challenges in population genetics of polyploid organisms: an overview of current state-of-the-art molecular and statistical tools. Molec Ecol 23:40–69. https://doi.org/10.1111/mec.12581
Earl DA, vonHoldt BM (2012) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genet Res 4:359–361. https://doi.org/10.1007/s12686-011-9548-7
Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software structure: A simulation study. Molec Ecol 14:2611–2620. https://doi.org/10.1111/j.1365-294X.2005.02553.x
Falush D, Stephens M, Pritchard JK (2007) Inference of population structure using multi locus genotype data: Dominant markers and null alleles. Molec Ecol Notes 7:574–578. https://doi.org/10.1111/j.1471-8286.2007.01758.x
Frantz AC, Cellina S, Krier A, Schley L, Burke T (2009) Using spatial Bayesian methods to determine the genetic structure of a continuously distributed population: clusters or isolation by distance? J Appl Ecol 46:493–505. https://doi.org/10.1111/j.1365-2664.2008.01606.x
FSI (2011) Chapter 2: Forest cover. In: State of Forest Report. Forest Survey of India, Ministry of Environment and Forests, Government of India, 11–33.
Gaire BP, Subedi L (2015) Phytochemistry pharmacology and medicinal properties of Phyllanthus emblica Linn. Chin J Integr Med 2014:1–8. https://doi.org/10.1007/s11655-014-1984-2
Ganesan R (2004) Identification, distribution, and conservation of Phyllanthus indofischeri, another source of Indian gooseberry. Curr Sci 84:1515–1518
Ganesan R, Setty S (2004) Regeneration of amla, an important non-timber forest product from Southern India. Conserv Soc 2:365–375
Geethika E, Triveni HN, Srirama R, Siva R, Setty S, Ravikanth G (2018) Development and characterization of microsatellite markers for Phyllanthus emblica Linn., important non-timber forest product species. J Genet 97:1001–1006. https://doi.org/10.1007/s12041-018-0979-8
Geethika E, Siva R, Ravikanth G (2023) Phyllanthus emblica and Phyllanthus indofischeri: Wild fruits with multifarious uses. In: Rajasekharn PE, Rao VR (eds) Fruits and nuts, A Series- Handbooks of Crop Diversity: Conservation and Use of Plant Genetic Resources. Springer, Singapore, pp 1–18. https://doi.org/10.1007/978-981-99-1586-6_19-1
Geldmann J, Barnes M, Coad L, Craigie ID, Hockings M, Burgess ND (2013) Effectiveness of terrestrial protected areas in reducing habitat loss and population declines. Biol Conserv 161:230–238. https://doi.org/10.1016/j.biocon.2013.02.018
Giustina LD, Luz LN, Vieira FS, Rossi FS, Soares-Lopes CRA, Pereira TNS, Rossi AAB (2014) Population structure and genetic diversity in natural populations of Theobroma speciosum Willd. Ex Spreng (Malvaceae). Genet Molec Res 13:3510–3519. https://doi.org/10.4238/2014
Goldstein DB, Bares AR, Cavalli-Sforza LL, Feldman MW (1995) An evaluation of genetic distances for use with microsatellite loci. Genetics 139:463–471. https://doi.org/10.1093/genetics/139.1.463
Hamrick JL, Godt MJW, Sherman-Broyles SL (1992) Factors influencing levels of genetic diversity in woody plant species. New Forests 6:95–124. https://doi.org/10.1007/bf00120641
Hasan R, Islam N, Islam RN (2016) Phytochemistry, pharmacological activities and traditional uses of Emblica officinalis: A review. Int Curr Pharm J 5:14–21. https://doi.org/10.3329/icpj.v5i2.26441
IUCN (2010) Plants Under Pressure, a Global Assessment. The First Report of the IUCN Sampled Red List. Royal Botanic Gardens, Kew, UK, Natural History Museum, London, and International Union for Conservation of Nature. Surrey, Kew
Jain PK, Das D, Pandey N, Jain P (2016) Traditional Indian herb Emblica officinalis and its medicinal importance. Int J Pharm Sci 4:1–15
Jighly A, Abbott RJ, Daetwyler HD (2019) Editorial: Polyploid population genetics and evolution—from theory to practice. Frontiers Ecol Evol 7:460. https://doi.org/10.3389/fevo.2019.00460
Kalinowski ST (2010) The computer program STRUCTURE does not reliably identify the main genetic clusters within species: simulations and implications for human population structure. Heredity 106:625–632. https://doi.org/10.1038/hdy.2010.95
Kannan R, Shackleton CM, Uma Shaanker R (2013) Invasive alien species as drivers in socio-ecological systems: local adaptations towards use of Lantana in Southern India. Environm Dev Sustain 16:649–669. https://doi.org/10.1007/s10668-013-9500-y
Khan ML, Rai JPN, Tripathi RS (1987) Population structure of some tree species in disturbed and protected sub-tropical forests of North East India. Acta Oecol (Oecol Appl) 8:247–255
Kopelman NM, Mayzel J, Jakobsson M, Rosenberg NA, Mayrose I (2015) CLUMPAK: a program for identifying clustering modes and packaging population structure inferences across K. Molec Ecol Resources 15:1179–1191. https://doi.org/10.1111/1755-0998.12387
Langella O (2011) Populations 1.2.32: Population genetic software (individuals or population distances, phylogenetic trees). Available at: http://www.bioinformatics.org/project/?group_id=84
Laurance WF, Useche DC, Rendeiro J, Kalka M, Bradshaw CJA, Sloan SP, Zamzani F (2012) Averting biodiversity collapse in tropical forest protected areas. Nature 489:290–294. https://doi.org/10.1038/nature11318
Lucas PHC (1982) The role of protected areas in sustaining society. In: McNeely JA, Miller KR (eds) National parks, conservation, and development. Proceedings of the World Congress on National Parks, Bali, pp 72–77
Meirmans PG (2020) GENODIVE version 3.0: Easy-to-use software for the analysis of genetic data of diploids and polyploids. Molec Ecol Resources 20:1126–1131. https://doi.org/10.1111/1755-0998.13145
Meirmans PG, van Tienderen PH (2004) Genotype and Genodive: two programs for the analysis of genetic diversity of asexual organisms. Molec Ecol Not 4:792–794. https://doi.org/10.1111/j.1471-8286.2004.00770.x
Meirmans P, Van Tienderen P (2013) The effects of inheritance in tetraploidson genetic diversity and population divergence. Heredity 110:131–137. https://doi.org/10.1038/hdy.2012.80
Meirmans PG, Liu S, van Tienderen PH (2018) The analysis of polyploid genetic data. J Heredity 109:283–296. https://doi.org/10.1093/jhered/esy006
Miller KI, Webster GL (1966) Chromosome Numbers in the Euphorbiaceae. Brittonia 18:372–379
Murali KS, Siddappa Setty R (2001) Effect of Lantana camara and Chromelina odorata growth on the species diversity, regeneration and stem density of tree and shrub layer in BRT sanctuary. Curr Sci 80:675–678
Murali KS, Shankar U, Uma Shaanker R, Ganeshaiah KN, Bawa KS (1996) Extraction of Non-timber forest products in the forests of Biligiri Rangan Hills, India. Impact of NTFP Extraction on Regeneration, Population Structure, and Species Composition. Econ Bot 50:252–269. https://doi.org/10.1007/BF02907329
Niphadkar M, Ficetola GF, Bonardi A, Nagendra H, Padoa-Schioppa E (2016) Effects of landscape context on the invasive species Lantana camara in Biligiri Rangaswamy Temple Tiger Reserve, India. Trop Ecol 57:9–21
OriginPro (2020) OriginPro 2020b (9.7.5.184). The ultimate software for graphing and analysis. Origin Lab Corporation, Northampton
Pacheco LF, Simonetti JA (2000) Genetic structure of a Mimosoid tree deprived of its seed disperser, the spider monkey. Conserv Biol 14:1766–1775. https://doi.org/10.1111/j.1523-1739.2000.99182.x
Padmini S, Rao MN, Ganeshaiah KN, Uma Shaanker R (2001) Genetic diversity of Phyllanthus emblica in tropical forests of south India: impact of anthropogenic pressures. J Trop Forest Sci 13:297–310
Palop-Esteban M, Segarra-Moragues JG, González-Candelas F (2011) Polyploid origin, genetic diversity and population structure in the tetraploid sea lavender Limonium narbonense Miller (Plumbaginaceae) from eastern Spain. Genetica 139:1309–1322. https://doi.org/10.1007/s10709-012-9632-2
Pandey M, Changtragoon S (2012) Isolation and characterization of microsatellites in a medicinal plant, Phyllanthus emblica (Euphorbiaceae). Amer J Bot 99:468–469. https://doi.org/10.3732/ajb.1200157
Pandey AK, Tripathi YC, Kumar A (2016) Non-timber forest products (NTFPs) for sustained livelihood: challenges and strategies. Res J Forest 10:1–7. https://doi.org/10.3923/rjf.2016.1.7
Prasad S, Chellam R, Krishnaswamy J, Goyal SP (2004) Frugivory of Phyllanthus emblica at Rajaji National Park, Northwest India. Curr Sci 87:1188–1190
Prasad S, Krishnaswamy J, Chellam R, Goyal SP (2006) Ruminant-mediated seed dispersal of an economically valuable tree in Indian dry forests. Biotropica 38:679–682. https://doi.org/10.1111/j.1744-7429.2006.00182.x
Prasad S, Pittet A, Sukumar R (2010) Who really ate the fruit? A novel approach to camera trapping for quantifying frugivory by ruminants. Ecol Res 25:225–231. https://doi.org/10.1007/s11284-009-0650-1
Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multi locus genotype data. Genetics 155:945–959. https://doi.org/10.1093/genetics/155.2.945
Pyšek P, Hulme PE, Simberloff D, Bacher S, Blackburn TM, Carlton JT, Dawson W, Essl F, Foxcroft LC, Genovesi P, Jeschke JM, Kühn I, Liebhold AM, Mandrak NE, Meyerson LA, Pauchard A, Pergl J, Roy HE, Seebens H, van Kleunen M, Vilà M, Wingfield MJ, Richardson DM (2020) Scientists’ warning on invasive alien species. Biol Rev 95:1511–1534. https://doi.org/10.1111/brv.12627
Ramesha BT, Ravikanth G, Rao NM, Ganeshaiah KN, Uma Shaanker R (2007) Genetic structure of the rattan Calamus thwaitesii in core, buffer and peripheral regions of three protected areas in central Western Ghats, India: do protected areas serve as refugia for genetic resources of economically important plants? J Genet 86:9–18. https://doi.org/10.1007/s12041-007-0002-2
Rao NM, Ravikanth G, Ganeshaiah KN, Uma Shaanker R (2010) Role of protected area in conserving the population and genetic structure of economically important bamboo species. In: Rao NM, Soneji JR (eds) Tree and forest biodiversity. Bioremediation Biodivers Bioavailability 4:69–76
Ravikanth G, Rao NM, Ganeshaiah KN, Uma Shaanker R (2009) Impacts of harvesting on genetic diversity of NTFP species: Implications for conservation. In: Uma Shaanker R, Joseph GC, Hiremath AJ (eds) Management, utilization, and conservation of non-timber forest products in the South Asia region. Universities Press, Bangalore, pp 53–63
Ravikanth G, and Setty S (2017) Shrinking harvest: Genetic consequences and challenges for sustainable harvesting of non-timber forest products. In: Hiremath AJ, Rai ND, and Siddhartha A (eds) Transcending boundaries: Reflecting on twenty years of action and research at ATREE. Ashoka Trust for Research in Ecology and the Environment, Bangalore, pp 20–27
Rist L, Uma Shaankar U, Milner-Gulland EJ, Ghazoul J (2008) Managing mistletoes: The value of total practices for a non-timber forest resource. Forest Ecol Managem 255:1684–1691. https://doi.org/10.1016/j.foreco.2007.11.030
Rist L, Uma Shaanker R, Milner-Gulland EJ, Ghazoul J (2010) The use of traditional ecological knowledge in forest management: an example from India. Ecol Soc 15:3
Rist L, Uma Shaanker R, Ghazoul J (2011) The spatial distribution of mistletoe in a Southern Indian tropical forest at multiple scales. Biotropica 43:50–57. https://doi.org/10.1111/j.1744-7429.2010.00643.x
Roland C (2020) Phyllanthus emblica. The IUCN Red List of Threatened Species. https://doi.org/10.2305/IUCN.UK.2020-3.RLTS.T149444430A149548926.en
Ronfort J, Jenczewski E, Bataillon T, Rousset F (1998) Analysis of population structure in autotetraploid species. Genetics 150:921–930
Schulze K, Knights K, Coad L, Geldmann J, Leverington F, Eassom A, Marr M, Butchart SHM, Hockings M, Burgess ND (2018) An assessment of threats to terrestrial protected areas. Conserv Lett 11:e12435. https://doi.org/10.1111/conl.12435
Sinha P, Bal P, Panda PC (2018) Assessment of genetic diversity among six species of Calamus (Arecaceae) in Eastern Ghats of India using molecular markers. Assessment 3:656–668
Sundaram B, Krishnan S, Hiremath AJ, Joseph G (2012) Ecology and impacts of the invasive species, Lantana camara, in a social-ecological system in South India: perspectives from local knowledge. Human Ecol 40:931–942. https://doi.org/10.1007/s10745-012-9532-1
Thriveni HN, Sumangala RC, Shivaprakash KN, Ravikanth G, Vasudeva R, Babu RHN (2014) Genetic structure and diversity of Coscinium fenestratum: a critically endangered liana of Western Ghats, India. Pl Syst Evol 300:403–413. https://doi.org/10.1007/s00606-013-0890-y
Ticktin T, Ganesan R, Paramesha M, Setty S (2012) Disentangling the effects of multiple anthropogenic drivers on the decline of two tropical dry forest trees. J Appl Ecol 49:774–784. https://doi.org/10.1111/j.1365-2664.2012.02156.x
Ticktin T, Ganesan R, Paramesha M, Setty S (2014) Disentangling again the drivers of population decline for two harvested species: a response to Prasad et al. (2014). J Appl Ecol 51:648–654. https://doi.org/10.1111/1365-2664.12249
Uma Shaanker R, Ganeshaiah KN (1997a) Mapping Genetic diversity of Phyllanthus emblica: Forest gene banks as a new approach for in situ conservation of genetic resources. Curr Sci 73:163–168
Uma Shaanker R, Ganeshaiah KN (1997b) Mapping genetic diversity of Phyllanthus emblica: forest gene banks as a new approach for in situ conservation of genetic resources. Curr Sci 73:163–168
Uma Shaanker R, Ganeshaiah KN, Rao N (2001) Genetic diversity of medicinal plant species in deciduous forest of South India: impact of harvesting and other anthropogenic pressures. J Pl Biol 28:91–97
Uma Shaanker R, Ganeshaiah KN, Krishnan S, Ramya R, Meera C, Aravind NA, Kumar A, Rao D, Vanaraj G, Ramachandra J, Gauthier R, Ghazoul J, Poole N, Reddy BVC (2004) Livelihood gains and ecological costs of non-timber forest product dependence: assessing the roles of dependence, ecological knowledge and market structure in three contrasting human and ecological settings in South India. Environm Conserv 31:242–253
Vallejo-Marin M, Dorken ME, Barrett SCH (2010) The ecological and evolutionary consequences of clonality for plant mating. Annual Rev Ecol Evol Syst 41:193–213
Varghese A, Ticktin T, Mandle L, Nath S (2015) Assessing the effects of multiple stressors on the recruitment of fruit harvested trees in a tropical dry forest, Western Ghats, India. PLOS ONE 10:e0119634. https://doi.org/10.1371/journal.pone.0119634
Variya BC, Bakrania AK, Patel SS (2016) Emblica officinalis (Amla): A review for its phytochemistry, ethnomedicinal uses and medicinal potentials with respect to molecular mechanisms. Pharmacol Res 111:180–200. https://doi.org/10.1016/j.phrs.2016.06.013
Voigt FA, Arafeh R, Farwig N, Griebeler EM, Bohning-Gaese K (2009) Linking seed dispersal and genetic structure of trees: A biogeographical approach. J Biogeogr 36:242–254. https://doi.org/10.1111/j.1365-2699.2008.02002.x
Acknowledgements
The work was supported by grants from the Department of Biotechnology, New Delhi, India (BT/PR29859/FCB/125/23/2018). The authors also thank the Forest Department for permitting the study (C2/WL/Research/CR-/2016-17 and PCCF (WL)/E2/CR-22/2013-14). The authors thank Dr. Siddappa Setty, Dr. Harisha R.P., Dr. Kailash, Mr. Venkat Naidu, Mr. Madesha and Mr. Narayanan was providing logistical support in the field.
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Department of Biotechnology,Ministry of Science and Technology,India,BT/PR29859/FCB/125/23/2018.
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RG and SR conceived the study. RG and GE collected the samples. GE did the lab work and analyzed the data. GE, RG and SR wrote the manuscript.
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Online Resource 1. Sample collection details of Phyllanthus emblica from 12 populations of BRT, MM Hills, and CWLS.
Online Resource 2. Genetic diversity of each locus in Phyllanthus emblica based on 360 samples representing 12 populations from BRT, MM Hills and CWLS.
Online Resource 3. Genetic diversity of each locus in 12 populations of BRT, MM Hills, and CWLS.
Online Resource 4. a Pairwise Fst values of 12 populations of Phyllanthus emblica. b Pairwise Fst between three study areas.
Online Resource 5. PCA (Principal Component Analysis) of Phyllanthus emblica all individuals.
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Geethika, E., Ramamoorthy, S. & Ravikanth, G. Does long-term harvesting impact genetic diversity and population genetic structure? A study of Indian gooseberry (Phyllanthus emblica) in the Central Western Ghats region in India. Plant Syst Evol 310, 22 (2024). https://doi.org/10.1007/s00606-024-01906-1
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DOI: https://doi.org/10.1007/s00606-024-01906-1