Abstract
The aquatic fern Salvinia molesta D.S. Mitch. is an invasive species that can have devastating effects on the freshwater habitats it colonizes. Currently, a lack of clarity surrounding the genomic composition and genetic diversity of S. molesta impedes eradication efforts. Salvinia molesta is a polyploid hybrid with unknown and controversial parentage, first noted in Africa but morphologically similar to South American species. Giant salvinia is also thought to reproduce primarily, perhaps exclusively, through vegetative reproduction, raising the possibility that the global invasion comprises one or a few clonal genotypes. This research focuses on identifying the maternal genome donor of S. molesta, determining if this species consists of a single or multiple independently derived lineages, and evaluating invasive-range genotypic diversity. Whole chloroplast genome (plastome) sequencing from field-collected and herbarium specimens was used to quantify genetic diversity in S. molesta and the phylogenetic relationships among Salvinia species. Phylogenetic analysis revealed that S. molesta and S. herzogii share the same plastome, although S. herzogii is unlikely to be S. molesta’s maternal progenitor due to its own hybrid status and odd ploidy. Rather, we conclude that S. molesta’s maternal progenitor is either an undescribed or extinct species. The observed plastome diversity within S. molesta indicates the presence of multiple divergent genotypes which strongly suggest multiple origins of this hybrid. Additionally, this diversity clearly indicates that a single clone does not dominate the invasive range. This genomic diversity could have direct implications for the successful management of this invasive species, particularly for biological control.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
All sequencing reads generated during this project are available on the NCBI Sequencing Read Archive (SRA) (BioProject ID #PRJNA925219).
References
Ahmad R, Liow PS, Spencer DF, Jasieniuk M (2008) Molecular evidence for a single genetic clone of invasive Arundo donax in the United States. Aquat Bot 88:113–120. https://doi.org/10.1016/j.aquabot.2007.08.015
Bakker FT, Lei D, Yu J, Mohammadin S, van de Wei Z, Gravendeel B, Nieuwenhuis M, Staats M, Alquezar-Planas DE, Holmer R (2016) Herbarium genomics: plastome sequence assembly from a range of herbarium specimens using an iterative organelle Genome Assembly pipeline. Biol J Linn Soc 117:33–43. https://doi.org/10.1111/bij.12642
Beck JB, Windham MD, Yatskievych G, Pryer KM (2010) A diploids-first approach to species delimitation and interpreting polyploid evolution in the fern genus Astrolepis (Pteridaceae). Syst Bot 35:223–234. https://doi.org/10.1600/036364410791638388
Beck JB, Alexander PJ, Allphin L, Al-Shehbaz IA, Rushworth C, Bailey CD, Windham MD (2012) Does hybridization drive the transition to asexuality in diploid Boechera? Evolution 66:985–995. https://doi.org/10.1111/j.1558-5646.2011.01507.x
Beck JB, Allison JR, Pryer KM, Windham MD (2012) Identifying multiple origins of polyploid taxa: a multilocus study of the hybrid cloak fern (Astrolepis integerrima; Pteridaceae). Am J Bot 99:1857–1865. https://doi.org/10.3732/ajb.1200199
Bolger AM, Lohse M, Usadel B (2014) Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30:2114–2120. https://doi.org/10.1093/bioinformatics/btu170
Boughton AJ, Pemberton RW (2011) Limited field establishment of a weed biocontrol agent, Floracarus perrepae (Acariformes: Eriophyidae), against Old World climbing fern in Florida-a possible role of mite resistant plant genotypes. Environ Entomol 40:1448–1457. https://doi.org/10.1603/EN11030
Brandes U, Furevik BB, Nielsen LR, Kjær ED, Rosef L, Fjellheim S (2019) Introduction history and population genetics of intracontinental scotch broom (Cytisus scoparius) invasion. Divers Distrib 25:1773–1786. https://doi.org/10.1603/EN11030
Burdon JJ, Groves RH, Cullen JM (1981) The impact of biological control on the distribution and abundance of Chondrilla juncea in south-eastern Australia. J Appl Ecol 18:957–966. https://doi.org/10.2307/2402385
Campanella DM, McEvoy PB, Mundt CC (2009) Interaction effects of two biological control organisms on resistant and susceptible weed biotypes of Chondrilla juncea in western North America. Biol Control 50:50–59. https://doi.org/10.1016/j.biocontrol.2009.01.005
Clement M, Snell Q, Walker P, Posada D, Crandall K (2002) TCS: estimating gene genealogies. In: Proceedings of the 16th International parallel distributed processing symposium 2:184
Coetzee JA, Hill MP (2020) Salvinia molesta D. Mitch. (Salviniaceae): impact and control. CAB Rev 15:1–11. https://doi.org/10.1079/PAVSNNR202015033
Darling JA (2015) Genetic studies of aquatic biological invasions: closing the gap between research and management. Biol Invasions 17:951–971. https://doi.org/10.1007/s10530-014-0726-x
Dillenberger MS, Wei N, Tennessen JA, Ashman TL, Liston A (2018) Plastid genomes reveal recurrent formation of allopolyploid Fragaria. Am J Bot 105:862–874. https://doi.org/10.1002/ajb2.1085
Dormontt EE, Gardner MG, Breed MF, Rodger JG, Prentis PJ, Lowe AJ (2014) Genetic bottlenecks in time and space: reconstructing invasions from contemporary and historical collections. PLoS ONE 9:e106874. https://doi.org/10.1371/journal.pone.0106874
Ellstrand NC, Schierenbeck KA (2000) Hybridization as a stimulus for the evolution of invasiveness in plants? PNAS 97:7043–7050. https://doi.org/10.1073/pnas.97.13.7043
Galam D, Silva J, Sanders D, Oard JH (2015) Morphological and genetic survey of Giant Salvinia populations in Louisiana and Texas. Aquat Bot 127:20–25. https://doi.org/10.1016/j.aquabot.2015.07.005
Garcia-Rossi D, Rank N, Strong DR (2003) Potential for self-defeating biological control? Variation in herbivore vulnerability among invasive Spartina genotypes. Ecol Appl 13:1640–1649. https://doi.org/10.1890/01-5301
Gaskin JF, Bon MC, Cock MJ, Cristofaro M, De Biase A, De Clerck-Floate R, Ellison CA, Hinz HL, Hufbauer RA, Julien MH, Sforza R (2011) Applying molecular-based approaches to classical biological control of weeds. Biol Control 58:1–21. https://doi.org/10.1890/01-5301
Geng Y, van Klinken RD, Sosa A, Li B, Chen J, Xu CY (2016) The relative importance of genetic diversity and phenotypic plasticity in determining invasion success of a clonal weed in the USA and China. Front Plant Sci 7:213. https://doi.org/10.3389/fpls.2016.00213
Goolsby J, Cortés Mendoza E, Moran P, Adamczyk J, García M, Kirk A (2013) Evaluation of spanish Arundo scale Rhizaspidiotus donacis (Hemiptera; Diaspididae) survival and fecundity on three new world genotypes of Arundo donax (Poaceae; Arundinoideae). Biocontrol Sci Technol 23:499–506. https://doi.org/10.1080/09583157.2013.772562
Harms N, Shearer J, Cronin JT, Gaskin JF (2020) Geographic and genetic variation in susceptibility of Butomus umbellatus to foliar fungal pathogens. Biol Invasions 22:535–548. https://doi.org/10.1007/s10530-019-02109-3
Herben T, Suda J, Klimešová J (2017) Polyploid species rely on vegetative reproduction more than diploids: a re-examination of the old hypothesis. Ann Bot 120:341–349. https://doi.org/10.1093/aob/mcx009
Hoot SB, Napier NS, Taylor WC (2004) Revealing unknown or extinct lineages within Isoetes (Isoetaceae) using DNA sequences from hybrids. Am J Bot 91:899–904. https://doi.org/10.3732/ajb.91.6.899
iNaturalist (2020) Available at https://www.inaturalist.org
Jacono CC (1999) Salvinia molesta (Salvineaceae) new to Texas and Louisiana. SIDA 18:927–928
Jacono CC, Davern TR, Center TD (2001) The adventive status of Salvinia minima and S. molesta in the southern United States and the related distribution of the weevil Cyrtobagous salviniae. Castanea 66:214–226
Kates HR, Doby JR, Siniscalchi CM, LaFrance R, Soltis DE, Soltis PS, Guralnick RP, Folk RA (2021) The effects of herbarium specimen characteristics on short-read NGS sequencing success in nearly 8000 specimens: old, degraded samples have lower DNA yields but consistent sequencing success. Front Plant Sci. https://doi.org/10.3389/fpls.2021.669064
Katoh K, Misawa K, Kuma KI, Miyata T (2002) MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucl Acids Res 30:3059–3066. https://doi.org/10.1093/nar/gkf436
Kim S-T, Sultan SE, Donoghue MJ (2008) Allopolyploid speciation in Persicaria (Polygonaceae): insights from a low-copy nuclear region. PNAS 105:12370–12375. https://doi.org/10.1073/pnas.080514110
Kuriachan P (1979) Interspecific origin of Salvinia molesta Mitchell–evidence from karyotype. Indian J Bot 2:51–54
Lal A (2016) Salvinia molesta: an assessment of the effects and methods of eradication. M.S. Thesis, University of San Francisco
Leigh JW, Bryant D (2015) PopART: full-feature software for haplotype network construction. Methods Ecol Evol 6:1110–1116. https://doi.org/10.1111/2041-210X.12410
Li FW, Brouwer P, Carretero-Paulet L, Cheng S, De Vries J, Delaux PM et al (2018) Fern genomes elucidate land plant evolution and cyanobacterial symbioses. Nat Plants 4:460–472. https://doi.org/10.1038/s41477-018-0188-8
Liu J, Dong M, Miao SL, Li ZY, Song MH, Wang RQ (2006) Invasive alien plants in China: role of clonality and geographical origin. Biol Invasions 8:1461–1470. https://doi.org/10.1007/s10530-005-5838-x
Loomis ES, Fishman L (2009) A continent-wide clone: population genetic variation of the invasive plant Hieracium aurantiacum (Orange Hawkweed; Asteraceae) in North America. Int J Plant Sci 170:759–765. https://doi.org/10.1086/599241
Loyal DS, Grewal RK (1966) Cytological study on sterility in Salvinia auriculata Aublet with a bearing on its reproductive mechanism. Cytologia 31:330–338. https://doi.org/10.1508/cytologia.31.330
Luque GM, Bellard C, Bertelsmeier C, Bonnaud E, Genovesi P, Simberloff D, Courchamp F (2014) The 100th of the world’s worst invasive alien species. Biol Invasions 16:981–985. https://doi.org/10.1007/s10530-013-0561-5
Lym RG, Nissen SJ, Rowe ML, Lee DJ, Masters RA (1996) Leafy spurge (Euphorbia esula) genotype affects gall midge (Spurgia esulae) establishment. Weed Sci 44:629–633. https://doi.org/10.1017/S0043174500094455
Machado SA, Oliveira AV, Fabrin TM, Prioli SM, Prioli AJ (2016) Molecular characterization of the species Salvinia (Salviniaceae) from the upper Paraná River floodplain. Genet Mol Res 15:1–11. https://doi.org/10.4238/gmr.15038575
Manrique V, Cuda JP, Overholt WA, Williams DA, Wheeler GS (2008) Effect of host-plant genotypes on the performance of three candidate biological control agents of Schinus terebinthifolius in Florida. Biol Control 47:167–171. https://doi.org/10.1016/j.biocontrol.2008.07.005
Miranda CV, Schwartsburd PB (2016) Aquatic ferns from Viçosa (MG, Brazil): Salviniales (Filicopsida; Tracheophyta). Braz J of Bot 39:935–942. https://doi.org/10.1007/s40415-016-0284-9
Miranda CV, Schwartsburd PB (2019) Salvinia (Salviniaceae) in southern and southeastern Brazil—including new taxa, new distribution records, and new morphological characters. Braz J Bot 42:171–188. https://doi.org/10.1007/s40415-019-00522-5
Mitchell D (1972) The kariba weed: Salvinia molesta. Br Fern Gaz 10:251–252
Mitchell DS, Thomas PA (1972) Ecology of water weeds in the neotropics. UNESCO, Paris
Mitchell DS, Tur NM (1975) The rate of growth of Salvinia molesta (S. auriculata Auct.) In laboratory and natural conditions. J Appl Ecol 12:213–225. https://doi.org/10.2307/2401730
Mora-Olivo A, Yatskievych G (2009) Salvinia molesta in Mexico. Am Fern J 99:56–58
Nagalingum NS, Nowak MD, Pryer KM (2008) Assessing phylogenetic relationships in extant heterosporous ferns (Salviniales), with a focus on Pilularia and Salvinia. Bot J Linn Soc 157:673–685. https://doi.org/10.1111/j.1095-8339.2008.00806.x
Paolacci S, Bog M, Lautenschlager U, Bonfield R, Appenroth KJ, Oberprieler C, Jansen MA (2021) Clonal diversity amongst island populations of alien, invasive Lemna minuta Kunth. Biol Invasions 23:2649–2660. https://doi.org/10.1007/s10530-021-02530-7
Pappert RA, Hamrick JL, Donovan LA (2000) Genetic variation in Pueraria lobata (Fabaceae), an introduced, clonal, invasive plant of the southeastern United States. Am J Bot 87:1240–1245. https://doi.org/10.2307/2656716
Poulin J, Weller SG, Sakai AK (2005) Genetic diversity does not affect the invasiveness of fountain grass (Pennisetum setaceum) in Arizona, California and Hawaii. Divers Distrib 11:241–247. https://doi.org/10.1111/j.1366-9516.2005.00136.x
Rani VU, Bhambie S (1983) A study on the growth of Salvinia molesta Mitchell in relation to light and temperature. Aquat Bot 17:119–124. https://doi.org/10.1016/0304-3770(83)90108-0
Room PM (1983) `Falling apart’ as a lifestyle: the rhizome architecture and population growth of Salvinia molesta. J Ecol 71:349–365. https://doi.org/10.2307/2259719
Rottenberg A, Parker JS (2004) Asexual populations of the invasive weed Oxalis pes–caprae are genetically variable. Proc R Soc Lond Ser B 7:S206–S208. https://doi.org/10.1098/rsbl.2003.0135
Saeidi S, McKain MR, Kellogg EA (2018) Robust DNA isolation and high-throughput sequencing library construction for herbarium specimens. J Vis Exp JoVE. https://doi.org/10.3791/56837
Saltonstall K (2002) Cryptic invasion by a non-native genotype of the common reed, Phragmites australis, into North America. PNAS 99:2445–2449. https://doi.org/10.1073/pnas.03247799
Schaffner U (2001) Host range testing of insects for biological weed control: How can it be better interpreted? Bioscience 51:951–959
Schneller J (1980) Cytotaxonomic investigations of Salvinia herzogii de la Sota. Aquat Bot 9:279–283. https://doi.org/10.1016/0304-3770(80)90027-3
Sigel EM, Windham MD, Pryer KM (2014) Evidence for reciprocal origins in Polypodium hesperium (Polypodiaceae): a fern model system for investigating how multiple origins shape allopolyploid genomes. Am J Bot 101:1476–1485. https://doi.org/10.3732/ajb.1400190
Stamatakis A (2014) RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30:1312–1313. https://doi.org/10.1093/bioinformatics/btu033
Straub SC, Parks M, Weitemier K, Fishbein M, Cronn RC, Liston A (2012) Navigating the tip of the genomic iceberg: next-generation sequencing for plant systematics. Am J Bot 99:349–364. https://doi.org/10.3732/ajb.1100335
Sun Y, Beuchat C, Müller-Schärer H (2020) Is biocontrol efficacy rather driven by the plant or the antagonist genotypes? A conceptual bioassay approach. NeoBiota 7:81–101. https://doi.org/10.3897/neobiota.63.54962
Te Beest M, Le Roux JJ, Richardson DM, Brysting AK, Suda J, Kubešová M, Pyšek P (2012) The more the better? The role of polyploidy in facilitating plant invasions. Ann Bot 109:19–45. https://doi.org/10.1093/aob/mcr277
Thomas PA, Room AP (1986) Taxonomy and control of Salvinia molesta. Nature 320:581–584
Thum RA, Chorak GM, Newman RM, Eltawely JA, Latimore J, Elgin E, Parks S (2020) Genetic diversity and differentiation in populations of invasive eurasian (Myriophyllum spicatum) and hybrid (Myriophyllum spicatum× Myriophyllum sibiricum) watermilfoil. Invasive Plant Sci Manag 13:59–67. https://doi.org/10.1017/inp.2020.12
Whitton J, Sears CJ, Baack EJ, Otto SP (2008) The dynamic nature of apomixis in the angiosperms. Int J Plant Sci 169:169–182. https://doi.org/10.1086/523369
Williams DA, Harms NE, Knight IA, Grewell BJ, Futrell CJ, Pratt PD (2020) High genetic diversity in the clonal aquatic weed Alternanthera philoxeroides in the United States. Invasive Plant Sci Manag 13:217–225. https://doi.org/10.1017/inp.2020.32
Windham MD, Yatskievych G (2005) A novel hybrid Polypodium (Polypodiaceae) from Arizona. Am Fern J 95:57–67. https://doi.org/10.1640/0002-8444(2005)095[0057:ANHPPF]2.0.CO;2
Wolf PG, Roper JM, Duffy AM (2010) The evolution of chloroplast genome structure in ferns. Genome 53:731–738. https://doi.org/10.1139/G10-061
Zeng CX, Hollingsworth PM, Yang J, He ZS, Zhang ZR, Li DZ, Yang JB (2018) Genome skimming herbarium specimens for DNA barcoding and phylogenomics. Plant Methods 14:43. https://doi.org/10.1186/s13007-018-0300-0
Zhang YY, Zhang DY, Barrett SC (2010) Genetic uniformity characterizes the invasive spread of water hyacinth (Eichhornia crassipes), a clonal aquatic plant. Mol Ecol 19:1774–1786. https://doi.org/10.1111/j.1365-294X.2010.04609.x
Acknowledgements
The authors would like to thank Garrie Landry for help with fieldwork, and the curators of ARIZ, BRIT, F, FLAS, FLOR, FUEL, FURB, MBM, MBML, MO, NY, US and VIC for permission to sample from herbarium specimens.
Funding
This work was supported by National Science Foundation award OIA 1920858 to EMS and JBB, by the Wichita State University Department of Biological Sciences and by the University of Louisiana at Lafayette Department of Biology.
Author information
Authors and Affiliations
Contributions
SH, JB and ES contributed to study conception and design. Fieldwork was conducted by SH, JB, ES, Brittany Sutherland, and Pedro Bond Schwartsburd. Data collection and analysis was conducted by SH and JB. The first draft of the manuscript was written by Stacy Holt and James Beck and all authors commented on previous versions of the manuscript. All authors read and approved of the final manuscript.
Corresponding author
Ethics declarations
Conflict of interest
The authors have no relevant financial or non-financial interests to disclose.
Additional information
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Holt, S.D., Sigel, E.M., Sutherland, B.L. et al. What is Salvinia molesta (Salviniaceae)? Determining the maternal progenitor and genetic diversity of the clonal invasive fern giant salvinia. Biol Invasions 25, 2131–2141 (2023). https://doi.org/10.1007/s10530-023-03028-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10530-023-03028-0