Microsatellite marker development and population genetic analysis revealed high connectivity between populations of a periwinkle <italic style="font-style: italic">Littoraria sinensis</italic> (Philippi, 1847)

Mengyu LI; Yuqiang LI; Tengfei XING; Yulong LI; Jinxian LIU

doi:10.1007/s00343-021-1079-9

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Microsatellite marker development and population genetic analysis revealed high connectivity between populations of a periwinkle Littoraria sinensis (Philippi, 1847)

Continued from the back cover | Updated：2023-05-20

- Microsatellite marker development and population genetic analysis revealed high connectivity between populations of a periwinkle Littoraria sinensis (Philippi, 1847)
- Journal of Oceanology and Limnology Vol. 40, Issue 3, Pages: 1097-1109(2022)
- Affiliations：
  
  1.CAS Key Laboratory of Marine Ecology and Environmental Sciences, Institute of Oceanology, Chinese Academy of Sciences, Qingdao 266071, China
  2.Laboratory for Marine Ecology and Environmental Science, Pilot National Laboratory for Marine Science and Technology (Qingdao), Qingdao 266237, China
  3.Center for Ocean Mega-Science, Chinese Academy of Sciences, Qingdao 266071, China
  4.University of Chinese Academy of Sciences, Beijing 100049, China
- Author bio：
  
  Jinxian LIU, jinxianliu@gmail.com
- Funds：
- DOI：10.1007/s00343-021-1079-9
  CLC：
- Published：2022-03
- Accepted：
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Mengyu LI, Yuqiang LI, Tengfei XING, et al. Microsatellite marker development and population genetic analysis revealed high connectivity between populations of a periwinkle Littoraria sinensis (Philippi, 1847)[J]. Journal of Oceanology and Limnology, 2022, 40(3): 1097-1109.
DOI：

Mengyu LI, Yuqiang LI, Tengfei XING, et al. Microsatellite marker development and population genetic analysis revealed high connectivity between populations of a periwinkle Littoraria sinensis (Philippi, 1847)[J]. Journal of Oceanology and Limnology, 2022, 40(3): 1097-1109. DOI： 10.1007/s00343-021-1079-9.

摘要

Abstract

Periwinkle

Littoraria sinensis

is a widely distributed gastropod in rocky intertidal zone of the northwestern Pacific. To examine genetic diversity and genetic connectivity among coastal populations of

L. sinensis

in China

1 636 pairs of primers were successfully designed using whole-genome shotgun sequencing

de novo assembly

and a bioinformatics pipeline QDD. Twelve highly variable polymorphic markers were selected to genotype 351 individuals from 15 populations. Data of nine microsatellite loci were retained for population genetic analysis

and weak genetic differentiation among populations were detected

suggesting high gene flow among populations. The long planktonic larval duration of

L. sinensis

might have played an important role in the high gene flow among populations. A tendency of genetic differentiation between north and south populations of

L. sinensis

was detected

which might be resulted from isolation due to lowered sea level in the last glacial maximum. Furthermore

the newly founded populations along the coast of Jiangsu Province were closely related to populations to the south of the Changjiang (Yangtze) River estuary

suggesting that the main source of the newly founded populations is from natural rocky populations south of the estuary.

关键词

Keywords

references

Adams T P, Miller R G, Aleynik D, Burrows M T. 2014. Offshore marine renewable energy devices as stepping stones across biogeographical boundaries. Journal of Applied Ecology , 51 (2): 330-338..

Andrade S C S, Medeiros H F, Solferini V N. 2005. Homogeneity test of hardy-Weinberg deviations in Brazilian littorinids: evidence for selection? Journal of Molluscan Studies , 71 (2): 167-174..

Antao T, Pérez-Figueroa A, Luikart G. 2011. Early detection of population declines: high power of genetic monitoring using effective population size estimators. Evolutionary Applications , 4 (1): 144-154..

Apolinário M, Coutinho R, Baeta-Neves M H. 1999. Periwinkle (Gastropoda: Littorinidae) habitat selection and its impact upon microalgal populations. Revista Brasileira de Biologia , 59 (2): 211-218..

Becker B J, Levin L A, Fodrie F J, McMillan P A. 2007. Complex larval connectivity patterns among marine invertebrate populations. Proceedings of the National Academy of Sciences of the United States of America , 104 (9): 3267-3272..

Bulleri F, Airoldi L. 2005. Artificial marine structures facilitate the spread of a non-indigenous green alga, Codium fragile ssp. tomentosoides , in the north Adriatic Sea. Journal of Applied Ecology , 42 (6): 1063-1072..

Carvalho J, Pereira C, Sotelo G, Costa D, Galindo J, Faria R. 2015. De novo isolation of 17 microsatellite loci for flat periwinkles ( Littorina fabalis and L. obtusata ) and their application for species discrimination and hybridization studies. Journal of Molluscan Studies , 81 (3): 421-425..

Chapuis M P, Estoup A. 2007. Microsatellite null alleles and estimation of population differentiation. Molecular Biology and Evolution , 24 (3): 621-631..

Cornwell B H. 2020. Gene flow in the anemone Anthopleura elegantissima limits signatures of local adaptation across an extensive geographic range. Molecular Ecology , 29 (14): 2550-2566..

Cowen R K, Gawarkiewicz G, Pineda J, Thorrold S R, Werner F E. 2007. Population connectivity in marine systems: an overview. Oceanography , 20 (3): 14-21..

Cowen R K, Sponaugle S. 2009. Larval dispersal and marine population connectivity. Annual Review of Marine Science , 1 : 443-466..

Cubit J D. 1984. Herbivory and the seasonal abundance of algae on a high intertidal rocky shore. Ecology , 65 (6): 1904-1917..

Dakin E E, Avise J C. 2004. Microsatellite null alleles in parentage analysis. Heredity , 93 (5): 504-509..

Denisov G, Walenz B, Halpern A L, Miller J, Miller N, Levy S, Sutton G. 2008. Consensus generation and variant detection by Celera Assembler. Bioinformatics , 24 (8): 1035-1040..

Do C, Waples R S, Peel D, Macbeth G M, Tillett B J, Ovenden J R. 2014. NeEstimator v2: re-implementation of software for the estimation of contemporary effective population size ( N e ) from genetic data. Molecular Ecology Resources , 14 (1): 209-214..

Dong Y W, Huang X W, Wang W, Li Y, Wang J. 2016. The marine 'Great Wall' of China: local- and broad-scale ecological impacts of coastal infrastructure on intertidal macrobenthic communities. Diversity and Distributions , 22 (7): 731-744..

Doropoulos C, Roff G, Bozec Y M, Zupan M, Werminghausen J, Mumby P J. 2016. Characterizing the ecological tradeoffs throughout the early ontogeny of coral recruitment. Ecological Monographs , 86 (1): 20-44..

Dupanloup I, Schneider S, Excoffier L. 2002. A simulated annealing approach to define the genetic structure of populations. Molecular Ecology , 11 (12): 2571-2581..

Estoup A, Presa P, Krieg F, Vaiman D, Guyomard R. 1993. (CT) n and (GT) n microsatellites: a new class of genetic markers for Salmo trutta L. (brown trout). Heredity , 71 (5): 488-496..

Evanno G, Regnaut S, Goudet J. 2005. Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Molecular Ecology , 14 (8): 2611-2620..

Excoffier L, Lischer H E L. 2010. Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Molecular Ecology Resources , 10 (3): 564-567..

Fauvelot C, Bertozzi F, Costantini F, Airoldi L, Abbiati M. 2009. Lower genetic diversity in the limpet Patella caerulea on urban coastal structures compared to natural rocky habitats. Marine Biology , 156 (11): 2313-2323..

Fauvelot C, Costantini F, Virgilio M, Abbiati M. 2012. Do artificial structures alter marine invertebrate genetic makeup? Marine Biology , 159 (12): 2797-2807..

Flanagan S P, Jones A G. 2019. The future of parentage analysis: from microsatellites to SNPs and beyond. Molecular Ecology , 28 (3): 544-567..

Glasby T M, Connell S D, Holloway M G, Hewitt C L. 2007. Nonindigenous biota on artificial structures: could habitat creation facilitate biological invasions? Marine Biology , 151 (3): 887-895..

Göl S, Göktay M, Allmer J, Doğanlar J, Frary A. 2017. Newly developed SSR markers reveal genetic diversity and geographical clustering in spinach ( Spinacia oleracea ). Molecular Genetics and Genomics , 292 (4): 847-855..

Göstring L, Chew M T, Orlova A, Höidén-Guthenberg I, Wennborg A, Carlsson J, Frejd F Y. 2010. Quantification of internalization of EGFR-binding Affibody molecules: methodological aspects. International Journal of Oncology , 36 (4): 757-763..

Hayden M J, Nguyen T M, Waterman A, Chalmers K J. 2008. Multiplex-ready PCR: a new method for multiplexed SSR and SNP genotyping. BMC Genomics , 9 : 80..

Hedgecock D, Li G, Hubert S, Bucklin K, Ribes V. 2004. Widespread null alleles and poor cross-species amplification of microsatellite DNA loci cloned from the Pacific oyster, Crassostrea gigas . Journal of Shellfish Research , 23 (2): 379-385..

Holborn M K, Krick M V, Pedersen S, Hunt D A G A, Boulding E G. 2015. Polymorphic microsatellite loci for Littorina plena show no population structure between the eastern and western coasts of Vancouver Island, Canada. Journal of Molluscan Studies , 81 (3): 407-411..

Hui M, Nuryanto A, Kochzius M. 2017. Concordance of microsatellite and mitochondrial DNA markers in detecting genetic population structure in the boring giant clam Tridacna crocea across the Indo-Malay Archipelago. Marine Ecology , 38 (1): e12389..

Jensen J L, Bohonak A J, Kelley S T. 2005. Isolation by distance, web service. BMC Genetics , 6 : 13..

Kennington W J, Lukehurst S S, Johnson M S. 2008. Characterization of microsatellite loci for the littorine snail Bembicium vittatum . Molecular Ecology Resources , 8 (6): 1463-1465..

Li Y L, Liu J X. 2018. StructureSelector: a web-based software to select and visualize the optimal number of clusters using multiple methods. Molecular Ecology Resources , 18 (1): 176-177..

Liu S X, Hou W, Sun T L, Xu Y T, Li P, Yue B S, Fan Z X, Li J. 2017. Genome-wide mining and comparative analysis of microsatellites in three macaque species. Molecular Genetics and Genomics , 292 (3): 537-550..

Lopez-Marquez V, Garcia-Jimenez R, Calvo M, Templado J, Machordom A. 2018. Isolation of microsatellite loci for the endangered vermetid gastropod Dendropoma lebeche using Illumina MiSeq next generation sequencing technology. Molecular Biology Reports , 45 (6): 2775-2781..

Lopez-Marquez V, Garcia-Jimenez R, Templado J, Machordom A. 2016. Development and characterization of 26 novel microsatellite loci for the trochid gastropod Gibbula divaricata (Linnaeus, 1758), using Illumina MiSeq next generation sequencing technology. PeerJ , 4 : e1789..

McInerney C E, Allcock A L, Johnson M P, Bailie D A, Prodöhl P A. 2011. Comparative genomic analysis reveals speciesdependent complexities that explain difficulties with microsatellite marker development in molluscs. Heredity , 106 (1): 78-87..

Meglécz E, Costedoat C, Dubut V, Gilles A, Malausa T, Pech N, Martin J F. 2010. QDD: a user-friendly program to select microsatellite markers and design primers from large sequencing projects. Bioinformatics , 26 (3): 403-404..

Menge B A. 2000. Top-down and bottom-up community regulation in marine rocky intertidal habitats. Journal of Experimental Marine Biology and Ecology , 250 (1-2): 257-289..

Ng T P T, Williams G A. 2012. Contrasting reproductive traits in two species of mangrove-dwelling littorinid snails in a seasonal tropical habitat. Invertebrate Biology , 131 (3): 177-186..

Ni G, Li Q, Kong L F, Yu H. 2014. Comparative phylogeography in marginal seas of the northwestern Pacific. Molecular Ecology , 23 (3): 534-548..

Nikula R, Spencer H G, Waters J M. 2011. Comparison of population-genetic structuring in congeneric kelp-versus rock-associated snails: a test of a dispersal-by-rafting hypothesis. Ecology and Evolution , 1 (2): 169-180..

Panova M, Makinen T, Fokin M, André C, Johannesson K. 2008. Microsatellite cross-species amplification in the genus Littorina and detection of null alleles in Littorina saxatilis . Journal of Molluscan Studies , 74 (2): 111-117..

Park S D E. 2002. Trypanotolerace in West African Cattle and the Population Genetic Effects Of Selection. University of Dublin, Dublin.

Peakall R, Smouse P E. 2012. GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research-an update. Bioinformatics , 28 (19): 2537-2539..

Pérez M, Guinez R, Llavona A, Toro J E, Astorga M, Presa P. 2008. PERMANENT GENETIC RESOURCES: Development of microsatellite markers for the ecosystem bioengineer mussel Perumytilus purpuratus and cross-priming testing in six Mytilinae genera. Molecular Ecology Resources , 8 (2): 449-451..

Pierson J C, Graves T A, Banks S C, Kendall K C, Lindenmayer D B. 2018. Relationship between effective and demographic population size in continuously distributed populations. Evolutionary Applications , 11 (7): 1162-1175..

Piry S, Luikart G, Cornuet J M. 1999. Computer note. BOTTLENECK: a computer program for detecting recent reductions in the effective size using allele frequency data. Journal of Heredity , 90 (4): 502-503..

Plutchak L L, Simmons R E, Woodruff D S. 2006. Multilocus allozyme heterozygote deficiencies in Crepidula onyx : geographic and temporal patterns among adult snails in Mission Bay, California. Journal of Molluscan Studies , 72 (4): 337-348..

Pritchard J K, Stephens M, Donnelly P. 2000. Inference of population structure using multilocus genotype data. Genetics , 155 (2): 945-959..

Raffaelli D, Paine R T. 1995. Marine rocky shores and community ecology: an experimentalist′s perspective. Journal of Animal Ecology , 64 (3): 425-427..

Reid D G, Dyal P, Williams S T. 2010. Global diversification of mangrove fauna: a molecular phylogeny of Littoraria (Gastropoda: Littorinidae). Molecular Phylogenetics and Evolution , 55 (1): 185-201..

Reid D G. 1989. The comparative morphology, phylogeny and evolution of the gastropod family Littorinidae. Philosophical Transactions of the Royal Society of London. Series B , Biological Sciences , 324 (1220): 1-110..

Reid D G. 2001. New data on the taxonomy and distribution of the genus Littoraria Griffith and Pidgeon, 1834 (Gastropoda: Littorinidae) in Indo-West Pacific mangrove forests. Nautilus , 115 (4): 115-139..

Rico C, Cuesta J A, Drake P, Macpherson E, Bernatchez L, Marie A D. 2017. Null alleles are ubiquitous at microsatellite loci in the Wedge Clam ( Donax trunculus ). PeerJ , 5 : e3188..

Robinson J D, Moyer G R. 2013. Linkage disequilibrium and effective population size when generations overlap. Evolutionary Applications , 6 (2): 290-302..

Rosa A L, Lima-Rezende C A, Rodrigues F P, Caparroz R. 2019. Development and characterization of 19 polymorphic microsatellite loci from the red-cowled cardinal ( Paroaria dominicana , Passeriformes, Aves) using next-generation sequencing. Molecular Biology Reports , 46 (5): 5531-5536..

Rousset F. 2008. GENEPOP'007: a complete reimplementation of the GENEPOP software for Windows and Linux. Molecular Ecology Resources , 8 (1): 103-106..

Rozen S, Skaletsky H. 2000. Primer3 on the WWW for general users and for biologist programmers. Methods in Molecular Biology , 132 : 365-386..

Sandoval-Castillo J, Robinson N A, Hart A M, Strain L W S, Beheregaray L B. 2018. Seascape genomics reveals adaptive divergence in a connected and commercially important mollusc, the greenlip abalone ( Haliotis laevigata ), along a longitudinal environmental gradient. Molecular Ecology , 27 (7): 1603-1620..

Schoebel C N, Brodbeck S, Buehler D, Cornejo C, Gajurel J, Hartikainen H, Keller D, Leys M, Říčanová Š, Segelbacher G, Werth S, Csencsics D. 2013. Lessons learned from microsatellite development for nonmodel organisms using 454 pyrosequencing. Journal of Evolutionary Biology , 26 (3): 600-611..

Schuelke M. 2000. An economic method for the fluorescent labeling of PCR fragments. Nature Biotechnology , 18 (2): 233-234..

Selkoe K A, D'aloia C C, Crandall E D, Iacchei M, Liggins L, Puritz J B, von der Heyden S, Toonen R J. 2016. A decade of seascape genetics: contributions to basic and applied marine connectivity. Marine Ecology Progress Series , 554 : 1-19..

Selkoe K A, Toonen R J. 2006. Microsatellites for ecologists: a practical guide to using and evaluating microsatellite markers. Ecology Letters , 9 (5): 615-629..

Sharma P C, Grover A, Kahl G. 2007. Mining microsatellites in eukaryotic genomes. Trends in Biotechnology , 25 (11): 490-498..

Shriver M D, Jin L, Boerwinkle E, Deka R, Ferrell R E, Chakraborty R. 1995. A novel measure of genetic distance for highly polymorphic tandem repeat loci. Molecular Biology and Evolution , 12 (5): 914-920..

Takezaki N, Nei M, Tamura K. 2010. POPTREE2: software for constructing population trees from allele frequency data and computing other population statistics with Windows interface. Molecular Biology and Evolution , 27 (4): 747-752..

Tie A D, Boulding E G, Naish K A. 2000. Polymorphic microsatellite DNA markers for the marine gastropod Littorina subrotundata . Molecular Ecology , 9 (1): 108-110..

Vucetich J A, Waite T A. 2003. Spatial patterns of demography and genetic processes across the species' range: Null hypotheses for landscape conservation genetics. Conservation Genetics , 4 (5): 639-645..

Wang J L, Whitlock M C. 2003. Estimating effective population size and migration rates from genetic samples over space and time. Genetics , 163 (1): 429-446..

Wang J, Tsang L M, Dong Y W. 2015. Causations of phylogeographic barrier of some rocky shore species along the Chinese coastline. BMC Evolutionary Biology , 15 : 114..

Wang P X. 1999. Response of Western Pacific marginal seas to glacial cycles: paleoceanographic and sedimentological features. Marine Geology , 156 (1-4): 5-39..

Wright P G R, Schofield H, Mathews F. 2021. Can effective population size estimates be used to monitor population trends of woodland bats? A case study of Myotis bechsteinii. Ecology and Evolution , 11 (5): 2015-2023..

Xue D X, Li Y L, Liu J X. 2017. A rapid and cost-effective approach for the development of polymorphic microsatellites in non-model species using paired-end RAD sequencing. Molecular Genetics and Genomics , 292 (5): 1165-1174..

Zhang G F, Fang X D, Guo X M, Li L, Luo R B, Xu F, Yang P C, Zhang L L, Wang X T, Qi H G, Xiong Z Q, Que H Y, Xie Y L, Holland P W H, Paps J, Zhu Y B, Wu F C, Chen Y X, Wang J F, Peng C F, Meng J, Yang L, Liu J, Wen B, Zhang N, Huang Z Y, Zhu Q H, Feng Y, Mount A, Hedgecock D, Xu Z, Liu Y J, Domazet-Lošo T, Du Y S, Sun X Q, Zhang S D, Liu B H, Cheng P Z, Jiang X T, Li J, Fan D D, Wang W, Fu W J, Wang T, Wang B, Zhang J B, Peng Z Y, Li Y X, Li N, Wang J P, Chen M S, He Y, Tan F J, Song X R, Zheng Q M, Huang R L, Yang H L, Du X D, Chen L, Yang M, Gaffney P M, Wang S, Luo L H, She Z C, Ming Y, Huang W, Zhang S, Huang B Y, Zhang Y, Qu T, Ni P X, Miao G Y, Wang J Y, Wang Q, Steinberg C E W, Wang H Y, Li N, Qian L M, Zhang G J, Li Y R, Yang H M, Liu X, Wang J, Yin Y, Wang J. 2012. The oyster genome reveals stress adaptation and complexity of shell formation. Nature , 490 (7418): 49-54..

Zhang X M, Zhou Y, Li Y L, Liu J X. 2019. Development of microsatellite markers for the seagrass Zostera japonica using next-generation sequencing. Molecular Biology Reports , 46 (1): 1335-1341..

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Microsatellite marker development and population genetic analysis revealed high connectivity between populations of a periwinkle Littoraria sinensis (Philippi, 1847)

DOI：10.1007/s00343-021-1079-9

摘要

Abstract

关键词

Keywords

references