Individual haplotyping of whale sharks from seawater environmental DNA.
eDNA
elasmobranchs
environmental DNA
haplotype
intraspecific diversity
mtDNA
population genetics
Journal
Molecular ecology resources
ISSN: 1755-0998
Titre abrégé: Mol Ecol Resour
Pays: England
ID NLM: 101465604
Informations de publication
Date de publication:
Jan 2022
Jan 2022
Historique:
revised:
07
05
2021
received:
04
12
2020
accepted:
03
06
2021
pubmed:
20
6
2021
medline:
22
12
2021
entrez:
19
6
2021
Statut:
ppublish
Résumé
Population genetic data can provide valuable information on the demography of a species. For rare and elusive marine megafauna, samples for generating the data are traditionally obtained from tissue biopsies, which can be logistically difficult and expensive to collect and require invasive sampling techniques. Analysis of environmental DNA (eDNA) offers an alternative, minimally invasive approach to provide important genetic information. Although eDNA approaches have been studied extensively for species detection and biodiversity monitoring in metabarcoding studies, the potential for the technique to address population-level questions remains largely unexplored. Here, we applied "eDNA haplotyping" to obtain estimates of the intraspecific genetic diversity of a whale shark (Rhincodon typus) aggregation at Ningaloo reef, Australia. Over 2 weeks, we collected seawater samples directly behind individual sharks prior to taking a tissue biopsy sample from the same animal. Our data showed a 100% match between mtDNA sequences recovered in the eDNA and tissue sample for all 28 individuals sampled. In the seawater samples, >97% of all reads were assigned to six dominant haplotypes, and a clear dominant signal (~99% of sample reads) was recovered in each sample. Our study demonstrates accurate individual-level haplotyping from seawater eDNA. When DNA from one individual clearly dominates each eDNA sample, it provides many of the same opportunities for population genetic analyses as a tissue sample, potentially removing the need for tissue sampling. Our results show that eDNA approaches for population-level analyses have the potential to supply critical demographic data for the conservation and management of marine megafauna.
Identifiants
pubmed: 34146448
doi: 10.1111/1755-0998.13451
doi:
Substances chimiques
DNA, Environmental
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
56-65Informations de copyright
© 2021 John Wiley & Sons Ltd.
Références
Adams, C. I. M., Knapp, M., Gemmell, N. J., Jeunen, G., Bunce, M., Lamare, M. D., & Taylor, H. R. (2019). Beyond biodiversity: Can environmental DNA (eDNA) cut it as a population genetics tool? Genes, 10, 1-24. https://doi.org/10.3390/genes10030192
Alam, M. T., Petit, R. A., III, Read, T. D., & Dove, A. D. (2014). The complete mitochondrial genome sequence of the world’s largest fish, the whale shark (Rhincodon typus), and its comparison with those of related shark species. Genes, 539, 44-49. https://doi.org/10.1016/j.gene.2014.01.064
Baker, C. S., Steel, D., Nieukirk, S., & Klinck, H. (2018). Environmental DNA (eDNA) from the wake of the whales: droplet digital PCR for detection and species identification. Frontiers in Marine Science, 5, 1-11. https://doi.org/10.3389/fmars.2018.00133
Bandelt, H., Forster, P., & Rohl, A. (1999). Median-joining networks for inferring intraspecific phylogenies. Molecular Biology and Evolution, 16, 37-48. https://doi.org/10.1093/oxfordjournals.molbev.a026036
Bravington, M. V., Grewe, P. M., & Davies, C. R. (2016). Absolute abundance of southern bluefin tuna estimated by close-kin mark-recapture. Nature Communications, 7. https://doi.org/10.1038/ncomms13162
Callahan, B. J., McMurdie, P. J., Rosen, M. J., Han, A. W., Johnson, A. J., & Holmes, S. P. (2016). DADA2: High-resolution sample inference from Illumina amplicon data. Nature Methods, 13, 581-583. https://doi.org/10.1038/nmeth.3869
Castro, A. L. F., Stewart, B. S., Wilson, G., Hueter, R. E., Meekan, M. G., Motta, P. J., Bowen, B. W., & Karl, S. A. (2007). Population genetic structure of Earth’s largest fish, the whale shark (Rhincodon typus). Molecular Ecology, 16, 5183-5192. https://doi.org/10.1111/j.1365-294X.2007.03597.x
Collins, R. A., Wangensteen, O. S., O’Gorman, E. J., Mariani, S., Sims, D. W., & Genner, M. J. (2018). Persistence of environmental DNA in marine systems. Communications Biology, 1. https://doi.org/10.1038/s42003-018-0192-6
de la Parra Venegas, R., Hueter, R., González Cano, J. G., Tyminski, J., Gregorio Remolina, J., Maslanka, M., Ormos, A., Weigt, L., Carlson, B., & Dove, A. (2011). An unprecedented aggregation of whale sharks, Rhincodon typus, in Mexican coastal waters of the Caribbean Sea. PLoS One, 6. https://doi.org/10.1371/journal.pone.0018994
Dicken, M. L., Booth, A. J., & Smale, M. J. (2006). Preliminary observations of tag shedding, tag reporting, tag wounds, and tag biofouling for raggedtooth sharks (Carcharias Taurus) tagged off the east coast of South Africa. ICES Journal of Marine Science, 63, 1640-1648. https://doi.org/10.1016/j.icesjms.2006.06.009
Dugal, L., Thomas, L., Jensen, M. R., Sigsgaard, E. E., Simpson, T., Jarman, S., Thomsen, P. F., & Meekan, M. (2020). Raw MiSeq and Sanger sequence data, demultiplex indice file, ASV file, R script; Zenodo. https://doi.org/10.5281/zenodo.4922417; Retrieved from https://zenodo.org/record/4922417
Frøslev, T. G., Kjoller, R., Bruun, H. H., Ejrnaes, R., Brunbjerg, A. K., Pietroni, C., & Hansen, A. J. (2017). Algorithm for post-clustering curation of DNA amplicon data yields reliable biodiversity estimates. Nature Communications, 8, 1188-1199. https://doi.org/10.1038/s41467-017-01312-x.
Greenfield, P. (2017). Greenfield Hybrid Analysis Pipeline (GHAP). CSIRO. Software Collection. https://doi.org/10.4225/08/59f98560eba25
Hsieh, T. C., Ma, K. H., & Chao, A. (2016). iNEXT: An R package for rarefaction and extrapolation of species diversity (Hill numbers). Methods in Ecology and Evolution, 7, 1451-1456. https://doi.org/10.1111/2041-210X.12613
Jamy, M., Foster, R., Barbera, P., Czech, L., Kozlov, A., Stamatakis, A., Bending, G., Hilton, S., Bass, D., & Burki, F. (2020). Long-read metabarcoding of the eukaryotic rDNA operon to phylogenetically and taxonomically resolve environmental diversity. Molecular Ecology Resources, 20, 429-443. https://doi.org/10.1111/1755-0998.13117
Jensen, M. R., Sigsgaard, E. E., Liu, S., Manica, A., Bach, S. S., Hansen, M. M., Møller, P. R., & Thomsen, P. F. (2020). Genome-scale target capture of mitochondrial and nuclear environmental DNA from water samples. Molecular Ecology Resources, 21(3), 690-702. https://doi.org/10.1111/1755-0998.13293. Accepted Article
Jeunen, G., Knapp, M., Spencer, H. G., Lamare, M. D., Taylor, H. R., Stat, M., Bunce, M., & Gemmell, N. J. (2018). Environmental DNA (eDNA) metabarcoding reveals strong discrimination among diverse marine habitats connected by water movement. Molecular Ecology Resources, 19, 426-438. https://doi.org/10.1111/1755-0998.12982
Knudsen, S. W., Ebert, R. B., Hesselsøe, M., Kuntke, F., Hassingboe, J., Mortensen, P. B., Thomsen, P. F., Sigsgaard, E. E., Hansen, B. K., Nielsen, E. E., & Møller, P. R. (2019). Species-specific detection and quantification of environmental DNA from marine fishes in the Baltic Sea. Journal of Experimental Marine Biology and Ecology, 510, 31-45. https://doi.org/10.1016/j.jembe.2018.09.004
Leigh, J. W., & Bryant, D. (2015). PopART: Full-feature software for haplotype network construction. Methods in Ecology and Evolution, 6, 1110-1116. https://doi.org/10.1111/2041-210X.12410
Lester, E., Meekan, M. G., Barnes, P., Raudino, H., Rob, D., Waples, K., & Speed, C. W. (2020). Multi-year patterns in scarring, survival and residency of whale sharks in Ningaloo Marine Park, Western Australia. Marine Ecology Progress Series, 634, 115-125. https://doi.org/10.3354/meps13173
Li, W., Wang, Y., & Norman, B. (2012). A preliminary survey of whale shark Rhincodon typus catch and trade in China: An emerging crisis. Journal of Fish Biology, 80, 1608-1618. https://doi.org/10.1111/j.1095-8649.2012.03250.x
Meekan, M. G., Austin, C. M., Tan, M. H., Wei, N. V., Miller, A., Pierce, S. J., Rowat, D., Stevens, G., Davies, T. K., Ponzo, A., & Gan, M. H. (2017). iDNA at sea: Recovery of whale shark (Rhincodon typus) mitochondrial DNA sequences from the whale shark copepod (Pandarus rhincodonicus) confirms global population structure. Frontiers in Marine Science, 4. https://doi.org/10.3389/fmars.2017.00420
Meekan, M. G., Bradshaw, C. J. A., Press, M., McLean, C., Richards, A., Quasnichka, S., & Taylor, J. G. (2006). Population size and structure of whale sharks Rhincodon typus at Ningaloo Reef, Western Australia. Marine Ecology Progress Series, 319, 275-285. https://doi.org/10.3354/meps319275
Meekan, M. G., Taylor, B. M., Lester, E., Ferreira, L. C., Sequeira, A. M. M., Dove, A. D. M., Birt, M. J., Aspinall, A., Brooks, K., & Thums, M. (2020). Asymptotic growth of whale sharks suggests sex-specific life-history strategies. Frontiers in Marine Science, 7, 1-9. https://doi.org/10.3389/fmars.2020.575683
Meenakshisundaram, A., Thomas, L., Kennington, W. J., Thums, M., Lester, E., Meekan, M. (2021). Genetic markers validate photo-identification and uniqueness of spot patterns in whale sharks. Marine Ecology Progress Series, 668, 177-183. http://dx.doi.org/10.3354/meps13729
Nguyen, B. N., Shen, E. W., Seemann, J., Correa, A. M. S., O’Donnell, J. L., Altieri, A. H., Knowlton, N., Crandall, K. A., Egan, S. P., McMillan, W. O., & Leray, M. (2019). Environmental DNA survey captures patterns of fish and invertebrate diversity across a tropical seascape. Scientific Reports, 10. https://doi.org/10.1038/s41598-020-62565-9
Paradis, E. (2010). Pegas: An R package for population genetics with an integrated-modular approach. Bioinformatics, 26, 419-420. https://doi.org/10.1093/bioinformatics/btp696
Parsons, K. M., Everett, M., Dahlheim, M., & Park, L. (2018). Water, water everywhere: Environmental DNA can unlock population structure in elusive marine species. Royal Society of Open Science, 5, 1-12. https://doi.org/10.1098/rsos.180537
Pierce, S. J., & Norman, B. (2016). Rhincodon typus. The IUCN Red List of Endangered Species. Whale Shark. e.T19488A2365291, https://doi.org/10.2305/IUCN.UK.2016-1.RLTS.T19488A2365291.en.
Riley, M. J., Hale, M. S., Harman, A., & Rees, R. G. (2010). Analysis of whale shark Rhincodon typus aggregations near South Ari Atoll. Maldives Archipelago. Aquatic Biology., 8, 145-150. https://doi.org/10.3354/ab00215
Rowat, D., & Brooks, K. S. (2012). A review of the biology, fisheries and conservation of the whale shark Rhincodon typus. Journal of Fish Biology, 80, 1019-1056. https://doi.org/10.1111/j.1095-8649.2012.03252.x
Ruzzante, D. E., McCracken, G. R., Førland, B., MacMillan, J., Notte, D., Buhariwalla, C., Flemming, J. M., & Skaug, H. (2019). Validation of close-kin mark-recapture (CKMR) methods for estimating population abundance. Methods in Ecology and Evolution, 10, 1445-1453. https://doi.org/10.1111/2041-210X.13243
Schmidt, J. V., Chen, C. C., Sheikh, S., Meekan, M. G., Norman, B., & Joung, S. J. (2010). Paternity analysis in a litter of whale shark embryos. Endangered Species Research, 12, 117-124. https://doi.org/10.3354/esr00300
Schmidt, J. V., Schmidt, C. L., Ozer, F., Ernst, R. E., Feldheim, K. A., Ashley, M. V., & Levine, M. (2009). Low genetic differentiation across the three major ocean populations of the whale shark, Rhincodon typus. PLoS One, 4. https://doi.org/10.1371/journal.pone.0004988
Sigsgaard, E. E., Carl, H., Møller, P. R., & Thomsen, P. F. (2015). Monitoring the near-extinct European weather loach in Denmark based on environmental DNA from water samples. Biological Conservation, 183, 46-52. https://doi.org/10.1016/j.biocon.2014.11.023
Sigsgaard, E. E., Jensen, M. R., Winkelmann, I. E., Møller, P. R., Hansen, M. M., & Thomsen, P. F. (2020). Population-level inferences from environmental DNA- Current status and future perspectives. Evolutionary Applications, 13(2), 245-262. https://doi.org/10.1111/eva.12882
Sigsgaard, E. E., Nielsen, I. B., Bach, S. S., Lorenzen, E. D., Robinson, D. P., Knudsen, S. W., Pedersen, M. W., Al Jaidah, M., Orlando, L., Willerslev, E., Møller, P. R., & Thomsen, P. F. (2016). Population characteristics of a large whale shark aggregation inferred from seawater environmental DNA. Nature Ecology and Evolution, 1. https://doi.org/10.1038/s41559-016-0004.
Sigsgaard, E. E., Torquato, F., Frøslev, T. G., Moore, A. B. M., Sørensen, J. M., Range, P., Ben-Hamadou, R., Bach, S. S., Møller, P. R., & Thomsen, P. F. (2020). Using vertebrate environmental DNA from seawater in biomonitoring of marine habitats. Conservation Biology, 34, 697-710. https://doi.org/10.1111/cobi.13437.
Speed, C. W., Meekan, M. G., Rowat, D., Pierce, S. J., Marshall, A. D., & Bradshaw, C. J. A. (2008). Scarring patterns and relative mortality rates of Indian Ocean whale sharks. Journal of Fish Biology, 72, 1488-1503. https://doi.org/10.1111/j.1095-8649.2008.01810.x
Stat, M., Huggett, M. J., Bernasconi, R., DiBattista, J. D., Berry, T. E., Newman, S. J., Harvey, E. S., & Bunce, M. (2017). Ecosystem biomonitoring with eDNA: Metabarcoding across the tree of life in a tropical marine environment. Scientific Reports, 7, 1-11. https://doi.org/10.1038/s41598-017-12501-5
Tajima, F. (1983). Evolutionary relationship of DNA sequences in finite populations. Genetics, 105, 437-460. https://doi.org/10.1093/genetics/105.2.437
Thomsen, P. F., Kielgast, J., Iversen, L. L., Møller, P. R., Rasmussen, M., & Willerslev, E. (2012). Detection of a diverse marine fish fauna using environmental DNA from seawater samples. PLoS One, 7, 1-9. https://doi.org/10.1371/journal.pone.0041732
Thomsen, P. F., Kielgast, J., Iversen, L. L., Wiuf, C., Rasmussen, M., Gilbert, M. T. P., Orlando, L., & Willerslev, E. (2012). Monitoring endangered freshwater biodiversity using environmental DNA. Molecular Ecology, 21, 2565-2573. https://doi.org/10.1111/j.1365-294X.2011.05418.x
Thomsen, P. F., Møller, P. R., Sigsgaard, E. E., Knudsen, S. W., Jorgensen, O. A., & Willerslev, E. (2016). Environmental DNA from seawater samples correlate with trawl catches of Subarctic, deepwater fishes. PLoS One, 11, e0165252. https://doi.org/10.1371/journal.pone.0165252
Tsuji, S., Miya, M., Ushio, M., Sato, H., Minamoto, T., & Yamanaka, H. (2020). Evaluating intraspecific genetic diversity using environmental DNA and denoising approach: A case study using tank water. Environmental DNA, 2, 42-52. https://doi.org/10.1002/edn3.44
van Bleijswjik, J. D. L., Engelmann, J. C., Klunder, L., Witte, H. J., Witte, J. I., & van der Veer, H. W. (2020). Analysis of a coastal North Sea fish community: Comparison of aquatic environmental DNA concentration to fish catches. Environmental DNA, 1-17. https://doi.org/10.1002/edn3.67
Van Tienhoven, A. M., Den Hartog, J. E., Reijns, R. A., & Peddemors, V. M. (2007). A computer-aided program for pattern-matching of natural marks on the spotted raggedtooth shark Carcharias Taurus. Journal of Applied Ecology, 44, 273-280. https://doi.org/10.1111/j.1365-2664.2006.01273.x
Vignaud, T. M., Maynard, J. A., Leblois, R., Meekan, M. G., Vázquez-Juárez, R., Ramírez-Macías, D., Pierce, S. J., Rowat, D., Berumen, M. L., Beeravolu, C., Baksay, S., & Planes, S. (2014). Genetic structure of populations of whale sharks among ocean basins and evidence for their historic rise and recent decline. Molecular Ecology, 23, 2590-2601. https://doi.org/10.1111/mec.12754