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Deconstructing an infamous extinction crisis: Survival of Partula species on Moorea and Tahiti

dc.contributor.authorHaponski, Amanda E.
dc.contributor.authorLee, Taehwan
dc.contributor.authorÓ Foighil, Diarmaid
dc.date.accessioned2019-05-31T18:26:44Z
dc.date.availableWITHHELD_14_MONTHS
dc.date.available2019-05-31T18:26:44Z
dc.date.issued2019-06
dc.identifier.citationHaponski, Amanda E.; Lee, Taehwan; Ó Foighil, Diarmaid (2019). "Deconstructing an infamous extinction crisis: Survival of Partula species on Moorea and Tahiti." Evolutionary Applications 12(5): 1017-1033.
dc.identifier.issn1752-4571
dc.identifier.issn1752-4571
dc.identifier.urihttps://hdl.handle.net/2027.42/149284
dc.description.abstractEleven of eighteen Society Island Partula species endemic to the Windward Island subgroup (Moorea and Tahiti) have been extirpated by an ill‐advised biological control program. The conservation status of this critically endangered tree snail radiation is of considerable import, but is clouded by taxonomic uncertainty due to the extensive lack of congruence among species designations, diagnostic morphologies, and molecular markers. Using a combination of museum, captive, and remnant wild snails, we obtained the first high‐resolution nuclear genomic perspective of the evolutionary relationships and survival of fourteen Windward Island Partula species, totaling 93 specimens. We analyzed ~1,607–28,194 nuclear genomic loci collected with the double digest restriction‐site associated sequencing method. Results from phylogenomic trees, species estimation, and population assignment tests yielded monophyly of the Windward Island subgroup. Within this group, two well‐supported clades encompassing five species complexes were recovered. Clade 1 was restricted to Tahiti and contained two species complexes: “P. affinis” (three species) and “P. otaheitana” (five species). Clade 2 occurred on Moorea and on Tahiti and consisted of three species complexes: one Tahitian, “P. clara/P. hyalina”; the other two, “P. taeniata” (three species) and “P. suturalis” (six species), Moorean. Our genomic results largely corroborated previous mitochondrial DNA survival estimates for Moorea and Tahiti, with all five species complexes having members surviving in captivity and/or as remnant wild populations, although the details vary in each case. Continued, proactive conservation and management may yet ensure a phylogenetically representative survival of the fabled Partula species of Moorea and Tahiti.
dc.publisherR Foundation for Statistical Computing
dc.publisherWiley Periodicals, Inc.
dc.subject.otherMoorea
dc.subject.otherPartula
dc.subject.otherphylogenomics
dc.subject.othersurvival
dc.subject.otherTahiti
dc.subject.otherextinction
dc.subject.otherddRADseq
dc.subject.otherconservation
dc.titleDeconstructing an infamous extinction crisis: Survival of Partula species on Moorea and Tahiti
dc.typeArticle
dc.rights.robotsIndexNoFollow
dc.subject.hlbsecondlevelEcology and Evolutionary Biology
dc.subject.hlbtoplevelScience
dc.description.peerreviewedPeer Reviewed
dc.description.bitstreamurlhttps://deepblue.lib.umich.edu/bitstream/2027.42/149284/1/eva12778.pdf
dc.description.bitstreamurlhttps://deepblue.lib.umich.edu/bitstream/2027.42/149284/2/eva12778_am.pdf
dc.description.bitstreamurlhttps://deepblue.lib.umich.edu/bitstream/2027.42/149284/3/eva12778-sup-0001-SupInfo.pdf
dc.identifier.doi10.1111/eva.12778
dc.identifier.sourceEvolutionary Applications
dc.identifier.citedreferenceMurray, J., & Clarke, B. ( 1968 ). Partial reproductive isolation in the genus Partula (Gastropoda) on Moorea. Evolution, 22, 684 – 698.
dc.identifier.citedreferenceMaddison, W. ( 1997 ). Gene trees in species trees. Systematic Biology, 46, 523 – 536. https://doi.org/10.1093/sysbio/46.3.523
dc.identifier.citedreferenceMaddison, W. P., & Knowles, L. L. ( 2006 ). Inferring phylogeny despite incomplete lineage sorting. Systematic Biology, 55, 21 – 30. https://doi.org/10.1080/10635150500354928
dc.identifier.citedreferenceMassatti, R., & Knowles, L. L. ( 2014 ). Microhabitat differences impact phylogeographic concordance of codistributed species: Genomic evidence in montane sedges ( Carex L.) from the Rocky Mountains. Evolution, 68, 2833 – 2846.
dc.identifier.citedreferenceMirarab, S., & Warnow, T. ( 2015 ). ASTRAL‐II: Coalescent‐based species tree estimation with many hundreds of taxa and thousands of genes. Bioinformatics, 31, i44 – i52. https://doi.org/10.1093/bioinformatics/btv234
dc.identifier.citedreferenceMurray, J., & Clarke, B. ( 1980 ). The genus Partula on Moorea: Speciation in progress. Proceedings of the Royal Society of London B, 211, 83 – 117.
dc.identifier.citedreferenceMurray, J., Clarke, B., & Johnson, M. S. ( 1993 ). Adaptive radiation and community structure of Partula on Moorea. Proceedings of the Royal Society of London B, 254, 205 – 211.
dc.identifier.citedreferenceMurray, J., Johnson, M. S., & Clarke, B. ( 1982 ). Microhabitat differences among genetically similar species of Partula. Evolution, 36, 316 – 325.
dc.identifier.citedreferenceMurray, J., Stine, O. C., & Johnson, M. S. ( 1991 ). The evolution of mitochondrial DNA in Partula. Heredity, 66, 93 – 104. https://doi.org/10.1038/hdy.1991.12
dc.identifier.citedreferencePasturel, J. ( 1993 ). La climatologie Des Îles. In ORSTROM (Ed.), Atlas de la Polynésie Francaise. Paris, France: ORSTROM.
dc.identifier.citedreferencePearce‐Kelly, P., Clarke, D., Walker, C., & Atkin, P. ( 1997 ). A conservation programme for the partulid tree snails of the Pacific region. Memoirs of the Museum of Victoria, 56, 431 – 433. https://doi.org/10.24199/j.mmv.1997.56.34
dc.identifier.citedreferencePeterson, B. K., Weber, J. N., Kay, E. H., Fisher, H. S., & Hoekstra, H. E. ( 2012 ). Double digest RADseq: An inexpensive method for de novo SNP discovery and genotyping in model and non‐model species. PLoS ONE, 7, e37135. https://doi.org/10.1371/journal.pone.0037135
dc.identifier.citedreferencePickrell, J. K., & Pritchard, J. K. ( 2012 ). Inference of population splits and mixtures from genome‐wide allele frequency data. PLOS Genetics, 8, e1002967. https://doi.org/10.1371/journal.pgen.1002967
dc.identifier.citedreferencePritchard, J. K., Stephens, M., & Donnelly, P. ( 2000 ). Inference of population structure using multilocus genotype data. Genetics, 155, 945 – 959.
dc.identifier.citedreferenceReich, D., Thangaraj, K., Patterson, N., Price, A. L., & Singh, L. ( 2009 ). Reconstructing Indian population history. Nature, 461, 489 – 495. https://doi.org/10.1038/nature08365
dc.identifier.citedreferenceRonquist, F., Huelsenbeck, J., & Teslenko, M. ( 2011 ). MrBayes version 3.2 Manual: Tutorials and model summaries. Retrieved from http://mrbayes.sourceforge.net/mb3.2_manual.pdf
dc.identifier.citedreferenceRonquist, F., Teslenko, M., van der Mark, P., Ayres, D. L., Darling, A., Höhna, S., Huelsenbeck, J. P., ( 2012 ). MrBayes 3.2: Efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology, 61, 539 – 542.
dc.identifier.citedreferenceRosenberg, N. A. ( 2004 ). Distruct: A program for the graphical display of population structure. Molecular Ecology Notes, 4, 137 – 138. https://doi.org/10.1046/j.1471-8286.2003.00566.x
dc.identifier.citedreferenceRousset, F. ( 2008 ). GENEPOP’007: A complete re‐implementation of the GENEPOP software for Windows and Linux. Molecular Ecology Resources, 8, 103 – 106. https://doi.org/10.1111/j.1471-8286.2007.01931.x
dc.identifier.citedreferenceSalzburger, W. ( 2018 ). Understanding explosive diversification through cichlid fish genomics. Nature Reviews Genetics, 19, 705 – 717. https://doi.org/10.1038/s41576-018-0043-9
dc.identifier.citedreferenceSilva, O. D. ( 2018 ). RAD Tools: vcf2treemix.py. Retrieved from https://github.com/CoBiG2/RAD_Tools/blob/master/vcf2treemix.py
dc.identifier.citedreferenceStamatakis, 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
dc.identifier.citedreferenceSwofford, D. L. ( 2002 ). PAUP*. Phylogenetic analysis using parsimony (*and other methods). Version 4. Sunderland, MA: Sinauer Associates.
dc.identifier.citedreferenceThomaz, A. T., Malabarba, L. R., & Knowles, L. L. ( 2017 ). Genomic signatures of paleodrainages in a freshwater fish along the southeastern coast of Brazil: Genetic structure reflects past riverine properties. Heredity, 119, 287 – 294. https://doi.org/10.1038/hdy.2017.46
dc.identifier.citedreferenceUto, K., Yamamoto, Y., Sudo, M., Uchiumi, S., Ishizuka, O., Kogiso, T., & Tsunakawa, H. ( 2007 ). New K‐Ar ages of the Society Islands, French Polynesia, and implications for the Society hotspot feature. Earth Planets Space, 59, 879 – 885. https://doi.org/10.1186/BF03352750
dc.identifier.citedreferenceWallis, G. P., Cameron‐Christie, S. R., Kennedy, H. L., Palmer, G., Sanders, T. R., & Winter, D. J. ( 2017 ). Interspecific hybridization causes long‐term phylogenetic discordance between nuclear and mitochondrial genomes in freshwater fishes. Molecular Ecology, 26, 3116 – 3127. https://doi.org/10.1111/mec.14096
dc.identifier.citedreferenceAndrews, S. ( 2018 ). Fastqc: A quality control tool for high throughput sequence data. Retrieved from https://www.bioinformatics.babraham.ac.uk/projects/fastqc/
dc.identifier.citedreferenceBick, C. S., Ó Foighil, D., & Coote, T. ( 2016 ). Differential survival among Tahitian tree snails during a mass extinction event: Persistence of the rare and fecund. Oryx, 50, 169 – 175. https://doi.org/10.1017/S0030605314000325
dc.identifier.citedreferenceBongaerts, P. ( 2018 ). RAD‐seq script library. Retrieved from https://github.com/pimbongaerts/radseq
dc.identifier.citedreferenceChiba, S., & Cowie, R. H. ( 2016 ). Evolution and extinction of land snails on oceanic islands. Annual Review of Ecology, Evolution, and Systematics, 47, 123 – 141. https://doi.org/10.1146/annurev-ecolsys-112414-054331
dc.identifier.citedreferenceChifman, J., & Kubatko, L. ( 2014 ). Quartet inference from SNP data under the coalescent model. Bioinformatics, 30, 3317 – 3324. https://doi.org/10.1093/bioinformatics/btu530
dc.identifier.citedreferenceChou, J., Gupta, A., Yaduvanshi, S., Davidson, R., Nute, M., Mirarab, S., & Warnow, T. ( 2015 ). A comparative study of SVDquartets and other coalescent‐based species tree estimation methods. BMC Genomics, 16, S2.
dc.identifier.citedreferenceClarke, B., Johnson, M. S., Murray, J., Hewitt, G., & Wragg, G. M. ( 1996 ). Clines in the genetic distance between two species of island land snails: How ‘molecular leakage’ can mislead us about speciation [and discussion]. Philosophical Transactions of the Royal Society of London B, 351, 773 – 784.
dc.identifier.citedreferenceClarke, B., & Murray, J. ( 1969 ). Ecological genetics and speciation in land snails of the genus Partula. Biological Journal of the Linnean Society, 1, 31 – 42. https://doi.org/10.1111/j.1095-8312.1969.tb01810.x
dc.identifier.citedreferenceClarke, B., Murray, J., & Johnson, M. S. ( 1984 ). The extinction of endemic species by a program of biological control. Pacific Sciences, 38, 97 – 104.
dc.identifier.citedreferenceCoote, T. ( 2007 ). Partulids on Tahiti: Differential persistence of a minority of endemic taxa among relict populations. American Malacological Bulletin, 22, 83 – 87. https://doi.org/10.4003/0740-2783-22.1.83
dc.identifier.citedreferenceCoote, T., & Loève, E. ( 2003 ). From 61 species to five: Endemic tree snails of the Society Islands fall prey to an ill‐judged biological control programme. Oryx, 37, 91 – 96. https://doi.org/10.1017/S0030605303000176
dc.identifier.citedreferenceCowie, R. H. ( 1992 ). Evolution and extinction of Partulidae, endemic Pacific Island land snails. Philosophical Transactions of the Royal Society London B, 335, 167 – 191.
dc.identifier.citedreferenceCrampton, H. E. ( 1916 ). Studies on the variation, distribution, and evolution of the genus Partula. The species inhabiting Tahiti. Carnegie Institution of Washington Publication, 228, 1 – 311.
dc.identifier.citedreferenceCrampton, H. E. ( 1932 ). Studies on the variation, distribution and evolution of the genus Partula. The species inhabiting Moorea. Carnegie Institution of Washington Publication, 410, 1 – 335.
dc.identifier.citedreferenceR Development Core Team ( 2017 ). R: A language and environment for statistical computing. Vienna, Italy: R Foundation for Statistical Computing.
dc.identifier.citedreferenceDuncan, R. A., Fisk, M. R., White, W. M., & Nielsen, R. L. ( 1994 ). Tahiti: Geochemical evolution of a French Polynesia volcano. Journal of Geophysical Research, 99, 24341 – 24357.
dc.identifier.citedreferenceEarl, D. A., & vonHoldt, 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
dc.identifier.citedreferenceEaton, D. A. ( 2014 ). PyRAD: Assembly of de novo RADseq loci for phylogenetic analyses. Bioinformatics, 30, 1844 – 1849. https://doi.org/10.1093/bioinformatics/btu121
dc.identifier.citedreferenceEaton, D. A., & Overcast, I. ( 2018 ). ipyrad: Interactive assembly and analysis of RAD‐seq datasets. Retrieved from https://github.com/dereneaton/ipyrad
dc.identifier.citedreferenceEvanno, 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
dc.identifier.citedreferenceFunk, V. A., & Wagner, W. L. ( 1995 ). Biogeographic patterns in the Hawaiian Islands. In W. L. Wagner, & V. A. Funk (Eds.), Hawaiian biogeography: Evolution on a hotspot archipelago (pp. 379 – 419 ). Washington, DC: Smithsonian Institution Press.
dc.identifier.citedreferenceGargominy, O. ( 2008 ). Beyond the alien invasion: A recently discovered radiation of Nesopupinae (Gastropoda: Pulmonata: Vertiginidae) from the summits of Tahiti (Society Islands, French Polynesia). Journal of Conchology, 39, 517 – 536.
dc.identifier.citedreferenceGerlach, J. ( 1994 ). The ecology and behavior of Euglandina rosea. Thesis, Oxford University, Oxford, UK.
dc.identifier.citedreferenceGerlach, J. ( 2016 ). Icons of evolution: Pacific Island tree‐snails of the family Partulidae. Cambridge, UK: Phelsuma Press.
dc.identifier.citedreferenceGillespie, R. ( 2004 ). Community assembly through adaptive radiation in Hawaiian spiders. Science, 303, 356 – 359. https://doi.org/10.1126/science.1091875
dc.identifier.citedreferenceGoodacre, S. L. ( 2001 ). Genetic variation in a Pacific island land snail: Population history versus current drift and selection. Proceedings of the Royal Society of London B, 268, 121 – 126.
dc.identifier.citedreferenceGoodacre, S. L. ( 2002 ). Population structure, history, and gene flow in a group of closely related land snails: Genetic variation in Partula from the Society Islands of the Pacific. Molecular Ecology, 11, 55 – 68. https://doi.org/10.1046/j.0962-1083.2001.01422.x
dc.identifier.citedreferenceGould, S. J. ( 1994 ). Eight little piggies: Reflections in natural history. London, UK: Penguin Science.
dc.identifier.citedreferenceGuillou, H., Maury, R. C., Blais, S., Cotten, J., Legendre, C., Guille, G., & Caroff, M. ( 2005 ). Age progression along the Society hotspot chain (French Polynesia) based on new unspiked K‐Ar ages. Bulletin De La Société Géologique De France, 2, 135 – 150. https://doi.org/10.2113/176.2.135
dc.identifier.citedreferenceHaponski, A. E., Lee, T. & Ó Foighil, D. ( 2017 ). Moorean and Tahitian Partula tree snail survival after a mass extinction: New genomic insights using museum specimens. Molecular Phylogenetics and Evolution, 106, 151 – 157. https://doi.org/10.1016/j.ympev.2016.09.021
dc.identifier.citedreferenceHildenbrand, A., Gillot, P.‐Y., & Le Roy, I. ( 2004 ). Volcano‐tectonic and geochemical evolution of an oceanic intra‐plate volcano: Tahiti‐Nui (French Polynesia). Earth and Planetary Science Letters, 217, 349 – 365. https://doi.org/10.1016/S0012-821X(03)00599-5
dc.identifier.citedreferenceHildenbrand, A., Gillot, P.‐Y., & Marlin, C. ( 2008 ). Geomorphological study of long‐term erosion on a tropical volcanic island: Tahiti‐Nui (French Polynesia). Geomorphology, 93, 460 – 481.
dc.identifier.citedreferenceHolder, M., & Lewis, P. O. ( 2003 ). Phylogeny estimation: Traditional and Bayesian approaches. Nature Reviews Genetics, 4, 275 – 284. https://doi.org/10.1038/nrg1044
dc.identifier.citedreferenceHubisz, M. J., Falush, D., Stephens, M., & Pritchard, J. K. ( 2009 ). Inferring weak population structure with the assistance of sample group information. Molecular Ecology Resources, 9, 1322 – 1332. https://doi.org/10.1111/j.1755-0998.2009.02591.x
dc.identifier.citedreferenceJohnson, M. S., Murray, J., & Clarke, B. C. ( 1986a ) An electrophoretic analysis of the phylogeny and evolutionary rates in the genus Partula from the Society Islands. Proceedings of the Royal Society of London B, 227, 161 – 177.
dc.identifier.citedreferenceJohnson, M. S., Clarke, B., & Murray, J. ( 1977 ). Genetic variation and reproductive isolation in Partula. Evolution, 31, 116 – 126.
dc.identifier.citedreferenceJohnson, M. S., Murray, J., & Clarke, B. ( 1986b ). Allozymic similarities among species of Partula on Moorea. Heredity, 56, 319 – 337.
dc.identifier.citedreferenceJohnson, M. S., Murray, J., & Clarke, B. ( 1993a ). The ecological genetics and adaptive radiation of Partula on Moorea. Oxford Surveys in Evolutionary Biology, 9, 167 – 238.
dc.identifier.citedreferenceJohnson, M. S., Murray, J., & Clarke, B. ( 1993b ). Evolutionary relationships and extreme genital variation in a closely related group of Partula. Malacologia, 35, 43 – 61.
dc.identifier.citedreferenceJombart, T. ( 2008 ). adegenet: A R package for the multivariate analysis of genetic markers. Bioinformatics, 24, 1403 – 1405. https://doi.org/10.1093/bioinformatics/btn129
dc.identifier.citedreferenceJombart, T., Devillard, S., & Balloux, F. ( 2010 ). Discriminant analysis of principal components: A new method for the analysis of genetically structured populations. BMC Genetics, 11, 94. https://doi.org/10.1186/1471-2156-11-94
dc.identifier.citedreferenceKopelman, N. M., Mayzel, J., Jakobsson, M., Rosenberg, N. A., & Mayrose, I. ( 2015 ). Clumpak: A program for identifying clustering modes and packaging population structure inferences across K. Molecular Ecology Resources, 15, 1179 – 1191.
dc.identifier.citedreferenceKutschera, V. E., Bidon, T., Hailer, F., Rodi, J. L., Rain, S. R., & Janke, A. ( 2014 ). Bears in a forest of gene trees: Phylogenetic inference is complicated by incomplete lineage sorting and gene flow. Molecular Biology and Evolution, 31, 2004 – 2017. https://doi.org/10.1093/molbev/msu186
dc.identifier.citedreferenceLanave, C., Preparata, G., Saccone, C., & Serio, G. ( 1984 ). A new method for calculating evolutionary substitution rates. Journal of Molecular Evolution, 20, 86 – 93. https://doi.org/10.1007/BF02101990
dc.identifier.citedreferenceLee, T., Burch, J. B., Coote, T., Fontaine, B., Gargominy, O., Pearce‐Kelly, P., & Ó Foighil, D. ( 2007 ) Prehistoric inter‐archipelago trading of Polynesian tree snails leaves a conservation legacy. Proceedings of the Royal Society of London B, 274, 2907 – 2914.
dc.identifier.citedreferenceLee, T., Burch, J. B., Coote, T., Pearce‐Kelly, P., Hickman, C., Meyer, J. Y., & Ó Foighil, D. ( 2009 ). Moorean tree snail survival revisited: A multi‐island genealogical perspective. BMC Evolutionary Biology, 9, 204. https://doi.org/10.1186/1471-2148-9-204
dc.identifier.citedreferenceLee, T., Burch, J. B., Jung, Y., Coote, T., Pearce‐Kelly, P., & Ó Foighil, D. ( 2007 ). Tahitian treesnail mitochondrial clades survived recent mass extirpation. Current Biology, 17, R502 – R503.
dc.identifier.citedreferenceLee, T., Li, J., Churchill, C. K. C., & Ó Foighil, D. ( 2014 ). Evolutionary history of a vanishing radiation: Isolation‐dependent persistence and diversification in Pacific Island partulid tree snails. BMC Evolutionary Biology, 14, 202. https://doi.org/10.1186/s12862-014-0202-3
dc.identifier.citedreferenceLee, T., Meyer, J. Y., Burch, J. B., Pearce‐Kelly, P., & Ó Foighil, D. ( 2008 ). Not completely lost: Two partulid tree snail species persist on the highest peak of Raiatea, French Polynesia. Oryx, 42, 615 – 619. https://doi.org/10.1017/S0030605308001427
dc.identifier.citedreferenceLischer, H. E. L., & 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
dc.owningcollnameInterdisciplinary and Peer-Reviewed


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