Conservation of pūpū whakarongotaua - the snail that listens for the war party
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Prehistoric translocations, Placostylus ambagiosus, shell shape, conservation geneticsAbstract
Snail ecotypes are an indicator of local forms that can have cultural value and also represent evolutionary potential. Conservation of both regional diversity and evolutionary potential can be improved by recognition and documentation of genetically determined phenotypic variation. The large threatened terrestrial snail pūpū whakarongotau (Placostylus ambagiosus) is a range restricted species that is valued by the indigenous people of the northern most region of New Zealand, valued as both a security alarm and food source. Some populations of this rare species are restricted to sites of human occupation and oral history suggests these distinct populations represent prehistoric translocations. We used 2-D geometric morphometrics and nuclear markers to document the distribution of variation. We aimed to determine whether shell shape variation was entirely an ecophenotypic plastic response, and whether or not prehistoric human movement of snails and establishment of food populations on pā sites (fortified settlements) had resulted in the loss of spatial genetic structure within this species. We could discriminate specimens due to shape variation among population samples. Using samples from prehistoric sites we infer shell shape in this species is not purely a plastic response to the local environment but reveals evolutionary potential. Genotypes with 1738 nuclear loci for 19 individuals from ten locations revealed some evidence of population mixing, but genetic variation was mostly partitioned among locations, with strong spatial structure revealed. Thus, we advocate conservation measures that will preserve will local forms that represent evolutionary potential of this species.
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Andrews KR, Luikart G (2014) Recent novel approaches for population genomics data analysis. Molecular Ecology 23:1661–1667. https://doi.org/10.1111/mec.12686
Bandelt HJ, 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
Barker GM, Brodie G, Bogitini L, Pippard H (2016) Diversity and current conservation status of Melanesian–New Zealand placostyline land snails (Gastropoda : Bothriembryontidae), with discussion of conservation imperatives, priorities and methodology issues. Pacific Conservation Biology 22: 203. https://doi.org/10.1071/PC14929
Beaglehole JC (1962) The Endeavour journal of Joseph Banks: 1768-1771. Vol. 1. The Trustees of the Public Library of New South Wales in association with Angus and Robertson, Sydney, Australia.
Brook FJ (1999) Stratigraphy, landsnail faunas, and paleoenvironmental history of coastal dunefields at Te Werahi, northernmost New Zealand. Journal of the Royal Society of New Zealand, 29:361-393. DOI: 10.1080/03014223.1999.9517603
Buckley T, Stringer I, Gleeson D, Howitt R, Attanayake D, Parrish R, … Rohan M (2011) A revision of the New Zealand Placostylus land snails using mitochondrial DNA and shell morphometric analyses, with implications for conservation. New Zealand Journal of Zoology 38:55–81. https://doi.org/10.1080/03014223.2010.527997
Cameron RAD, Cook LM (2012) Habitat and the shell polymorphism of Cepaea nemoralis (L.): interrogating the Evolution Megalab database. Journal of Molluscan Studies 78:179–184. https://doi.org/10.1093/mollus/eyr052
Catchen JM, Amores, A, Hohenlohe P, Cresko W, Postlethwait, JH (2011) Stacks: building and genotyping loci de novo from short-read sequences. G3: Genes, Genomes, Genetics 1:171–182. https://doi.org/10.1534/g3.111.000240
Catchen J, Hohenlohe PA, Bassham S, Amores A, Cresko WA (2013) Stacks: an analysis tool set for population genomics. Molecular Ecology, 22:3124–3140. https://doi.org/10.1111/mec.12354
Chiba S (2004) Ecological and morphological patterns in communities of land snails of the genus Mandarina from the Bonin Islands. Journal of Evolutionary Biology 17:131–143. https://doi.org/10.1046/j.1420-9101.2004.00639.x
Collins KS, Gazley MF (2017) Does my posterior look big in this? The effect of photographic distortion on morphometric analyses. Paleobiology 43:508-520. DOI: 10.1017/pab.2016.48
Costall JA, Carter RJ, Shimada Y, Anthony D, Rapson GL (2006) The endemic tree Corynocarpus laevigatus (karaka) as a weedy invader in forest remnants of southern North Island, New Zealand. New Zealand Journal of Botany 44: 5–22.
Cowie RH, Régnier C, Fontaine B, Bouchet P (2017) Measuring the Sixth Extinction: what do mollusks tell us? The Nautilus 113:3-41.
Darwin C (1859) On the origin of the species by natural selection. John Murray,
London, UK
Dowle EJ, Morgan-Richards M, Brescia F, Trewick SA (2015) Correlation between shell phenotype and local environment suggests a role for natural selection in the evolution of Placostylus snails. Molecular Ecology 24:4205–4221. https://doi.org/10.1111/mec.13302
Earl DA, vonHoldt BM (2011) 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
Eilaguirre C, Baltazar-Soares M (2014) Evolutionary conservation-evaluating the adaptive potential of species. Evolutionary Application 7:963-967. https://doi.org/10.1111/eva.12227
Fraley C, Raftery AE (2002) Model-based clustering, discriminant analysis and density estimation. Journal of the American Statistical Association 97:611-631.
Fraley C, Raftery AE (2003) Enhanced model-based clustering, density estimation, and discriminant analysis software: MCLUST. Journal of Classification 20:263–286.
Fraley C, Raftery AE (2012) Mclust version 4 for R: normal mixture modelling for model-based clustering, classification, and density estimation. Technical Report 597, University of Washington, USA
Galindo J, Grahame JW (2014) Ecological Speciation and the Intertidal Snail Littorina saxatilis. Advances in Ecology e239251. https://doi.org/10.1155/2014/239251
Goodfriend GA (1986) Variation in land-snail shell form and size and its causes: a review. Systematic Zoology 35:204-223.
Harvey MG, Judy CD, Seeholzer GF, Maley JM, Graves GR, Brumfield RT (2015) Similarity thresholds used in DNA sequence assembly from short reads can reduce the comparability of population histories across species. PeerJ, 3: e895. https://doi.org/10.7717/peerj.895
Hastie T, Tibshirani R, Friedman J (2009) The Elements of Statistical Learning: Data Mining, Inference, and Prediction. Springer Series in Statistics. Springer-Verlag, New York, USA
Hendry AP, Nosil P, Rieseberg LH (2007) The speed of ecological speciation. Functional Ecology 21:455–464. https://doi.org/10.1111/j.1365-2435.2007.01240.x
Huang H, Knowles LL (2016) Unforeseen Consequences of Excluding Missing Data from Next-Generation Sequences: Simulation Study of RAD Sequences. Systematic Biology 65:357-365 https://doi.org/10.1093/sysbio/syu046
Jakobsson M, Rosenberg NA (2007) CLUMPP: a cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinformatics 23:1801–1806. https://doi.org/10.1093/bioinformatics/btm233
Jombart T (2008) Adegenet: a R package for the multivariate analysis of genetic markers. Bioinformatics 24:1403–1405.
Jones JS, Leith BH, Rawlings P (1977) Polymorphism in Cepaea – a problem with too many solutions? Annual Review of Ecology and Systematics 8:109–143.
Jensen JL, Bohonak AJ, Kelley ST (2005) Isolation by distance, web service. BMC Genetics 6:13. https://doi.org/10.1186/1471-2156-6-13
Klingenberg CP (2011) MorphoJ: an integrated software package for geometric morphometrics. Molecular Ecology Resources 11:353–357. https://doi.org/10.1111/j.1755-0998.2010.02924.x
Landguth EL, Fedy BC, Oyler-McCance SJ, Garey AL, Emel SL, Mumma M, … Cushman SA (2012) Effects of sample size, number of markers, and allelic richness on the detection of spatial genetic pattern. Molecular Ecology Resources 12:276–284. https://doi.org/10.1111/j.1755-0998.2011.03077.x
Leach H, Stowe C (2005) Oceanic arboriculture at the margins – the case of the karaka (Corynocarpus laevigatus) in Aotearoa. The Journal of the Polynesian Society 114:7-27.
Leigh JW, 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
Lux J, Holland W, Rate S, Beadel S (2009) Natural areas of Te Paki Ecological District. Department of Conservation, Whangarei NZ.
Lydeard C, Cowie RH, Ponder WF, Bogan AE, Bouchet P, Clark SA, Cummings KS, Frest TJ ….. Tompson FG (2004) The global decline of nonmarine mollusks. BioScience 54:321-330.
Mallet J (2008) Hybridization, ecological races and the nature of species: empirical evidence for the ease of speciation. Philosophical Transactions of the Royal Society B: Biological Sciences 363:2971–2986. https://doi.org/10.1098/rstb.2008.0081
Mitteroecker P, Gunz P (2009) Advances in Geometric morphometrics. Evolutionary Biology 36:235–247.
Nichols KM, Kozfkay CC, Narum SR (2016) Genomic signatures among Oncorhynchus nerka ecotypes to inform conservation and management of endangered Sockeye Salmon. Evolutionary Applications 9:1285-1300.
Outomuro D, Johansson F (2017) A potential pitfall in studies of biological shape: does size matter? Journal of Animal Ecology 86:1447–1457.
Parent CE, Crespi BJ (2009) Ecological opportunity in adaptive radiation of Galápagos endemic land snails. The American Naturalist 174:898-905
Parkyn J, Newell DA (2013) Australian land snails: a review of ecological research and conservation approaches. Molluscan Research 33:116-129 doi.org/10.1080/13235818.2013.782793.
Parrish GR, Stringer IAN, Sherley GH (2014) The biology of Placostylus ambagiosus (Pulmonata: Bulimulidae) in New Zealand: Part 1. Behaviour, habitat use, abundance, site fidelity, homing and the dimensions of eggs and snails. Molluscan Research 34:139-154.
Penniket ASW (1981) Population studies of land snails of the genus Placostylus in the north of New Zealand. Unpublished MSc thesis. Auckland University, Auckland, NZ.
Peterson BK, Weber JN, Kay EH, Fisher HS, Hoekstra HE (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
Powell AWB (1947) Distribution of Placostylus Land Snails in Northern most New Zealand. Records of the Auckland Institute and Museum 3:173–188.
Powell AWB (1951) On Further Colonies of Placostylus Land Snails from Northernmost New Zealand. Records of the Auckland Institute and Museum 4: 134–140.
Powell AWB (1979) New Zealand Mollusca: marine, land, and freshwater shells. Collins, Hong Kong.
Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959.
Quenu M, Trewick SA, Brescia F, Morgan-Richards M (2020) Geometric morphometrics and machine learning challenge the division of Placostylus snails from the Isle of Pines, New Caledonia into just two species. Journal of Molluscan Studies. In Press.
R Core Team (2016) R: A Language and Environment for Statistical Computing. Version: 3.2.5. R Foundation for Statistical Computing, Vienna, Austria.
Räsänen K, Hendry AP (2008) Disentangling interactions between adaptive divergence and gene flow when ecology drives diversification. Ecology Letters 11:624–636. https://doi.org/10.1111/j.1461-0248.2008.01176.x
Rohlf F (2013) tpsUtil 1.58 and tpsDig 2.17. (Version 2.17). Department of Ecology and Evolution, State University of New York. Retrieved from http://life.bio.sunysb.edu/morph/
Rosenberg NA (2003) 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
Rundle HD, Nosil P (2005) Ecological speciation. Ecology Letters 8:336–352. https://doi.org/10.1111/j.1461-0248.2004.00715.x
Schilthuizen M, Haase M (2010) Disentangling true shape differences and experimenter bias: are dextral and sinistral snail shells exact mirror images? Journal of Zoology (London) 282:191–200. https://doi.org/10.1111/j.1469-7998.2010.00729.x
Segura I, Rocha-Olivares A, Flores-Ramírez S, Rojas-Bracho L (2006) Conservation implications of the genetic and ecological distinction of Tursiops truncatus ecotypes in the Gulf of California. Biological Conservation 133:336-346.
Sheets HD (2014) Integrated Morphometrics Package (IMP)8. Retrieved from http://www3.canisius.edu/~sheets/morphsoft.html
Sherley G (1996) Morphological variation in the shells of Placostylus species (Gastropoda: Bulimulidae) in New Zealand and implications for their conservation. New Zealand Journal of Zoology 23:73–82. https://doi.org/10.1080/03014223.1996.9518067
Slatkin M (1987) Gene flow and the geographic structure of natural populations. Science, 236:787-792.
Slatkin M (1993) Isolation by Distance in Equilibrium and Non-Equilibrium Populations. Evolution 47:264–279. https://doi.org/10.2307/2410134.
Stankowski S (2013) Ecological speciation in an island snail: evidence for the parallel evolution of a novel ecotype and maintenance by ecologically dependent postzygotic isolation. Molecular Ecology 22:2726–2741. https://doi.org/10.1111/mec.12287
Stringer IAN, Parrish GR, Sherley GH, Mackenzie DI (2014) The biology of Placostylus ambagiosus (Pulmonata: Bulimulidae) in New Zealand: Part 2. Population changes, growth, mortality and life expectancy. Molluscan Research 34:155-175.
Stringer IAN, Parrish GR, Sherley GH (2017) Homing, dispersal and mortality after translocation of long-lived land snails Placostylus ambagiosus and P. hongii (Gastropoda: Bothriembryontidae) in New Zealand. Molluscan Research 38. https://doi.org/10.1080/13235818.2017.1323368
Triggs SJ, Sherley GH (1993) Allozyme genetic diversity in Placostylus land snails and implications for conservation. New Zealand Journal of Zoology 20:19–33. https://doi.org/10.1080/03014223.1993.10423239
Van Bocxlaer B, Schultheiß R (2010) Comparison of morphometric techniques for shapes with few homologous landmarks based on machine-learning approaches to biological discrimination. Paleobiology 36:497–515.
Vaux F, Crampton JS, Marshall BA, Trewick SA, Morgan-Richards M (2017) Geometric morphometric analysis reveals that the shells of male and female siphon whelks Penion chathamensis are the same size and shape. Molluscan Research 37:194-201. https://doi.org/10.1080/13235818.2017.1279474
Vaux F, Trewick SA, Crampton JS, Marshall BA, Beu AG, Hills SFK, Morgan-Richards M (2018) Evolutionary lineages of marine snails identified using molecular phylogenetics and geometric morphometric analysis of shells. Molecular Phylogenetics and Evolution 127:626-637. https://doi.org/10.1016/j.ympev.2018.06.009
Webster M, Sheets HD (2010) A practical introduction to landmark-based geometric morphometrics. Quantitative Methods in Paleobiology 16:168–188.
Wehi PM (2009) Indigenous ancestral sayings contribute to modern conservation partnerships: examples using Phormium tenax. Ecological Application 19:267-275. https://doi.org/10.1890/07-1693.1
Wickham H (2016). ggplot2: Elegant Graphics for Data Analysis. Springer-Verlag New York. USA. https://ggplot2.tidyverse.org.
Zelditch ML, Swiderski DL, Sheets HD, Fink WL (2010) Geometric Morphometrics for Biologists: A Primer. Elsevier Academic Press, London, UK.
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