Cite this paper:
Kang CHEN, Weifeng WANG, Weilin ZHU, Xiuli CHEN, Huanling WANG. Morphological characteristics and genetic differentiation of Lutraria maxima in coast waters off southeast China[J]. Journal of Oceanology and Limnology, 2021, 39(4): 1387-1402

Morphological characteristics and genetic differentiation of Lutraria maxima in coast waters off southeast China

Kang CHEN1, Weifeng WANG1, Weilin ZHU2, Xiuli CHEN2, Huanling WANG1
1 Key Lab of Freshwater Animal Breeding, Key Laboratory of Agricultural Animal Genetics, Breeding and Reproduction, Ministry of Education, College of Fishery, Huazhong Agricultural University, Wuhan 430070, China;
2 Guangxi Key Laboratory of Aquatic Genetic Breeding and Healthy Aquaculture, Guangxi Academy of Fishery Sciences, Nanning 530021, China
Abstract:
To explore genetic diversity and estimate the genetic differences among populations of Lutraria maxima in the coastal waters off south to southeast China, the morphology of the species of five different geographical populations (Beihai, Weizhou Island, Zhanjiang, Xiamen, and Fuzhou) in Guangxi, Guangdong, and Fujian provinces was studied statistically in combination with the microsatellite markers. As revealed by morphological principal component analysis (PCA), the cumulative contribution rate of the first three principal components was 72.596%. The discrimination accuracy ranged from 47.5% to 80.0%, and the scatter plots of principal component and discriminant analysis were consistent in overall, showing that the Xiamen and Fuzhou populations were overlapped obviously. For microsatellite markers, 10 pairs of polymorphic primers were obtained by high-throughput transcriptome sequencing, and used for genetic diversity analysis. It was showed that the average number of alleles and effective alleles observed in each population ranged from 8.100 to 10.900, and from 3.497 to 4.228, respectively. The average observed heterozygosity (Ho) and expected heterozygosity (He) in the five populations ranged from 0.541 to 0.615, and from 0.642 to 0.733, respectively. The genetic distance (DA) ranged from 0.078 to 0.523, and the population genetic differentiation index (FST) ranged from 0.027 to 0.139. The unweighted pair-population method with arithmetic means (UPGMA) and structure analysis showed that the five populations could be divided into two main clusters, the Beibu Gulf group (Beihai and Weizhou Island) and the Southeast China Sea group (Zhanjiang, Xiamen, and Fuzhou), suggesting that L. maxima has been separated geographically by the barrier of the Leizhou Peninsula into two groups in evolution, which provided us with a scientific clue to better protect the bioresource and establish an appropriate fishery management stocks for L. maxima populations in south China.
Key words:    Lutraria maxima|morphological difference|microsatellite markers|genetic diversity|genetic differentiation|transcriptome   
Received: 2020-05-08   Revised: 2020-06-24
Tools
PDF (1641 KB) Free
Print this page
Add to favorites
Email this article to others
Authors
Articles by Kang CHEN
Articles by Weifeng WANG
Articles by Weilin ZHU
Articles by Xiuli CHEN
Articles by Huanling WANG
References:
An H Y, Park J Y. 2005. Ten new highly polymorphic microsatellite loci in the blood clam Scapharca broughtonii. Molecular Ecology Notes, 5(4):896-898, https://doi.org/10.1111/j.1471-8286.2005.01104.x.
Arnaud S, Monteforte M, Galtier N, Bonhomme F, Blanc F. 2000. Population structure and genetic variability of pearl oyster Pinctada mazatlanica along Pacific coasts from Mexico to Panama. Conservation Genetics, 1(4):299-308, https://doi.org/10.1023/a:1011575722481.
Borsa P, Zainuri M, Delay B. 1991. Heterozygote deficiency and population structure in the bivalve Ruditapes decussatus. Heredity, 66(1):1-8, https://doi.org/10.1038/hdy.1991.1.
Botstein D, White R L, Skolnick M, Davis R W. 1980.Construction of a genetic linkage map in man using restriction fragment length polymorphisms. American Journal of Human Genetics, 32(3):314-331.
Brookfield J F Y.1996. A simple new method for estimating null allele frequency from heterozygote deficiency.Molecular Ecology, 5(3):453-455, https://doi.org/10.1111/j.1365-294X.1996.tb00336.x.
Cannas R, Sacco F, Follesa M C, Sabatini A, Arculeo M, Lo Brutto S, Maggio T, Deiana A M, Cau A. 2012. Genetic variability of the blue and red shrimp Aristeus antennatus in the Western Mediterranean Sea inferred by DNA microsatellite loci. Marine Ecology, 33(3):350-363, https://doi.org/10.1111/j.1439-0485.2011.00504.x.
Chareontawee K, Poompuang S, Na-Nakorn, U, Kamonrat W. 2007. Genetic diversity of hatchery stocks of giant freshwater prawn (Macrobrachium rosenbergii) in Thailand. Aquaculture, 271(1-4):121-129, https://doi.org/10.1016/j.aquaculture.2007.07.001.
Chistiakov D A, Hellemans B, Volckaert F A M. 2006.Microsatellites and their genomic distribution, evolution, function and applications:a review with special reference to fish genetics. Aquaculture, 255(1-4):1-29, https://doi.org/10.1016/j.aquaculture.2005.11.031.
Coope G R. 1979. Late Cenozoic Fossil Coleoptera:evolution, biogeography, and ecology. Annual Review of Ecology and Systematics, 10(1):247-267, https://doi.org/10.1146/annurev.es.10.110179.001335.
Eisenhour D J. 1999. Systematics of Macrhybopsis tetranema(Cypriniformes:Cyprinidae). Copeia, 1999(4):969-980, https://doi.org/10.2307/1447972.
Ellis J R, Burke J M. 2007. EST-SSRs as a resource for population genetic analyses. Heredity, 99(2):125-132, https://doi.org/10.1038/sj.hdy.6801001.
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):2 611-2 620, https://doi.org/10.1111/j.1365-294X.2005.02553.x.
Evans B, Bartlett J, Sweijd N, Cook P, Elliott N G. 2004. Loss of genetic variation at microsatellite loci in hatchery produced abalone in Australia (Haliotis rubra) and South Africa (Haliotis midae). Aquaculture, 233(1-4):109-127, https://doi.org/10.1016/j.aquaculture.2003.09.037.
Excoffier L, Laval G, Schneider S. 2005. Arlequin (version 3.0):an integrated software package for population genetics data analysis. Evolutionary Bioinformatics Online, 1:47-50.
Falush D, Stephens M, Pritchard J K. 2003. Inference of population structure using multilocus genotype data:Linked loci and correlated allele frequencies. Genetics, 164(4):1 567-1 587.
Fr�d�rich B, Liu S Y V, Dai C F. 2012. Morphological and genetic divergences in a coral reef Damselfish, Pomacentrus coelestis. Evolutionary Biology, 39(3):359-370, https://doi.org/10.1007/s11692-011-9158-z.
Gallardo M H, Pe�aloza L, Clasing E. 1998. Gene flow and allozymic population structure in the clam Venus antiqua(King of Broderip), (Bivalvia, Veneriidae) from Southern Chile. Journal of Experimental Marine Biology and Ecology, 230(2):193-205, https://doi.org/10.1016/s0022-0981(98)00069-0.
Gardner J P A, Thompson R J. 1999. High levels of shared allozyme polymorphism among strongly differentiated congeneric clams of the genus Astarte (Bivalvia:Mollusca). Heredity, 82(1):89-99, https://doi.org/10.1038/sj.hdy.6884590.
Geist J, Kuehn R. 2005. Genetic diversity and differentiation of central European freshwater pearl mussel (Margaritifera margaritifera L.) populations:implications for conservation and management. Molecular Ecology, 14(2):425-439, https://doi.org/10.1111/j.1365-294x.2004.02420.x.
Gibson A R, Baker A J, Moeed A. 1984. Morphometric variation in introduced populations of the common myna(Acridotheres tristis):an application of the jackknife to principal component analysis. Systematic Biology, 33(4):408-421, https://doi.org/10.1093/sysbio/33.4.408.
Grabherr M G, Haas B J, Yassour M, Levin J Z, Thompson D A, Amit I, Adiconis X, Fan L, Raychowdhury R, Zeng Q D, Chen Z H, Mauceli E, Hacohen N, Gnirke A, Rhind N, Di Palma F, Birren B W, Nusbaum C, Lindblad-Toh K, Friedman N, Regev A. 2011. Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nature Biotechnology, 29(7):644-652, https://doi.org/10.1038/nbt.1883.
Guillemaud T, Mieuzet L, Simon J C. 2003. Spatial and temporal genetic variability in French populations of the peach-potato aphid, Myzus persicae. Heredity, 91(2):143-152, https://doi.org/10.1038/sj.hdy.6800292.
Huang D W, Licuanan W Y, Hoeksema B W, Chen C A, Ang P O, Huang H, Lane D J W, Vo S T, Waheed Z, Affendi Y A, Yeemin T, Chou L M. 2015. Extraordinary diversity of reef corals in the South China Sea. Marine Biodiversity, 45(2):157-168, https://doi.org/10.1007/s12526-014-0236-1.
Ignacio B L, Absher T M, Lazoski C, Sol�-Cava A M. 2000.Genetic evidence of the presence of two species of Crassostrea (Bivalvia:Ostreidae) on the coast of Brazil.Marine Biology, 136(6):987-991, https://doi.org/10.1007/s002270000252.
Jakobsson M, Rosenberg N A. 2007. CLUMPP:a cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinformatics, 23(14):1 801-1 806, https://doi.org/10.1093/bioinformatics/btm233.
Kalinowski S T, Taper M L, Marshall T C. 2007. Revising how the computer program CERVUS accommodates genotyping error increases success in paternity assignment. Molecular Ecology, 16(5):1 099-1 106, https://doi.org/10.1111/j.1365-294x.2007.03089.x.
Kelly M W, Rhymer J M. 2005. Population genetic structure of a rare unionid (Lampsilis cariosa) in a recently glaciated landscape. Conservation Genetics, 6(5):789-802, https://doi.org/10.1007/s10592-005-9037-1.
Kong L F, Li Q, Qiu Z X. 2007. Genetic and morphological differentiation in the clam Coelomactra antiquata(Bivalvia:Veneroida) along the coast of China. Journal of Experimental Marine Biology and Ecology, 343(1):110-117, https://doi.org/10.1016/j.jembe.2006.12.003.
Kumar S, Stecher G, Tamura K. 2016. MEGA7:molecular evolutionary genetics analysis version 7.0 for bigger datasets. Molecular Biology and Evolution, 33(7):1 870-1 874, https://doi.org/10.1093/molbev/msw054.
Lambeck K, Esat T M, Potter E K. 2002. Links between climate and sea levels for the past three million years.Nature, 419(6903):199-206, https://doi.org/10.1038/nature01089.
Laudien J, Flint N S, van der Bank F H, Brey T. 2003. Genetic and morphological variation in four populations of the surf clam Donax serra (R�ding) from southern African sandy beaches. Biochemical Systematics and Ecology, 31(7):751-772, https://doi.org/10.1016/s0305-1978(02)00252-1.
Lee H J, Boulding E G. 2009. Spatial and temporal population genetic structure of four northeastern Pacific littorinid gastropods:the effect of mode of larval development on variation at one mitochondrial and two nuclear DNA markers. Molecular Ecology, 18(10):2 165-2 184, https://doi.org/10.1111/j.1365-294X.2009.04169.x.
Li B, He J F, Ou X L, Su X J, Pan Y, Luo F G, Zheng H F, Qin Z B. 2011a. Morphological and genetic diversity analysis among three populations of clam Lutraria siebaldii in coastal Guangxi and Guangdong provinces. Journal of Dalian Ocean University, 26(5):414-421. (in Chinese with English abstract)
Li G, Hubert S, Bucklin K, Ribes V, Hedgecock D. 2003a.Characterization of 79 microsatellite DNA markers in the Pacific oyster Crassostrea gigas. Molecular Ecology Notes, 3(2):228-232, https://doi.org/10.1046/j.1471-8286.2003.00406.x.
Li Q Z, Chen R F, Tong W P, Jiang Y. 2004. Influence of salinity upon the embryogenesis of Lutraria maxima Janas. Journal of Guangxi Academy of Sciences, 20(1):33-34. (in Chinese with English abstract)
Li Q Z, Tong W P, Su Q, Liu W N. 2003b. The morphogenesis of the Lutraria maxima's embryo, larvae and spat.Guangxi Sciences, 10(4):296-299. (in Chinese with English abstract)
Li Q, Yu H, Yu R. 2006. Genetic variability assessed by microsatellites in cultured populations of the Pacific oyster (Crassostrea gigas) in China. Aquaculture, 254(1-4):95-102. http://doi.org/10.1016/j.aquaculture.2006.05.030.
Li S F, Zhao Y, Fan W J, Cai W Q, Xu Y F. 2011b. Possible genetic reproductive isolation between two tilapiine genera and species:Oreochromis niloticus and Sarotherodon melanotheron. Zoological Research, 32(5):521-527, https://doi.org/10.3724/SP.J.1141.2011.05521.
Li Z M, Xie L, Ye F L, Chen G L. 2010. SSR analysis of three species from primary parent and their first generation of Litopenaeus vannamei. Agricultural Science and Technology, 11(3):57-61.
Liu J, Li Q, Kong L F, Zheng X D. 2011. Cryptic diversity in the pen shell Atrina pectinata (Bivalvia:Pinnidae):high divergence and hybridization revealed by molecular and morphological data. Molecular Ecology, 20(20):4 332-4 345, https://doi.org/10.1111/j.1365-294x.2011.05275.x.
Ma H Y, Jiang W, Liu P, Feng N N, Ma Q Q, Ma C Y, Li S J, Liu Y X, Qiao Z G, Ma L B. 2014. Identification of transcriptome-derived microsatellite markers and their association with the growth performance of the mud crab(Scylla paramamosain). PLoS One, 9(2):e89134, https://doi.org/10.1371/journal.pone.0089134.
Mariani S, Ketmaier V, de Matthaeis E. 2002. Genetic structuring and gene flow in Cerastoderma glaucum(Bivalvia:Cardiidae):evidence from allozyme variation at different geographic scales. Marine Biology, 140(4):687-697, https://doi.org/10.1007/s00227-001-0753-x.
Murat T, Aykut K. 2015. Genetic and morphologic diversity of Pseudophoxinus (Cyprinidae):implication for conservation in Anatolia. Environmental Biology of Fishes, 98(2):571-583, https://doi.org/10.1007/s10641-014-0291-2.
Nei M, Maruyama T, Chakraborty R. 1975. The bottleneck effect and genetic variability in populations. Evolution, 29(1):1-10, https://doi.org/10.1111/j.1558-5646.1975.tb00807.x.
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, https://doi.org/10.1111/mec.12620.
Pan Y, Qin X M, Pan H P. 2007. Analysis and evaluation of nutritive composition in edible part of Lutraria maxima. Journal of Guangdong Ocean University, 27(3):78-81.(in Chinese with English abstract)
Pan Y, Su Y P. 2007. The karyotype of Lutraria maxima Jonas. Marine Sciences, 31(9):87-90. (in Chinese with English abstract)
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):2 537-2 539, https://doi.org/10.1093/bioinformatics/bts460.
Pemberton J M, Slate J, Bancroft D R, Barrett J A. 1995.Nonamplifying alleles at microsatellite loci:a caution for parentage and population studies. Molecular Ecology, 4(2):249-252, https://doi.org/10.1111/j.1365-294x.1995.tb00214.x.
P�rez-Losada M, Guerra A, Carvalho G R, Sanjuan A, Shaw P W. 2002. Extensive population subdivision of the cuttlefish Sepia officinalis (Mollusca:Cephalopoda) around the Iberian Peninsula indicated by microsatellite DNA variation. Heredity, 89(6):417-424, https://doi.org/10.1038/sj.hdy.6800160.
Qin Y, Shi G, Sun Y. 2013. Evaluation of genetic diversity in Pampus argenteus using SSR markers. Genetics and Molecular Research, 12(4):5 833-5 841, https://doi.org/10.4238/2013.November.22.10.
R�os C, Sanz S, Saavedra C, Pe�a J B. 2002. Allozyme variation in populations of scallops, Pecten jacobaeus(L.) and P. maximus (L.) (Bivalvia:Pectinidae), across the Almeria-Oran front. Journal of Experimental Marine Biology and Ecology, 267(2):223-244, https://doi.org/10.1016/s0022-0981(01)00371-9.
Rosenberg N A. 2004. DISTRUCT:a program for the graphical display of population structure. Molecular Ecology Notes, 4(1):137-138, https://doi.org/10.1046/j.1471-8286.2003.00566.x.
Ruiz-Campos G, Camarena-Rosales F, Varela-Romero A, S�nchez-Gonz�lez S, De La Rosa-V�lez J. 2003.Morphometric variation of wild trout populations from northwestern Mexico (Pisces:Salmonidae). Reviews in Fish Biology and Fisheries, 13(1):91-110, https://doi.org/10.1023/a:1026367113735.
Sato M, Kawamata K, Zaslavskaya N, Nakamura A, Ohta T, Nishikiori T, Brykov V, Nagashima K. 2005. Development of microsatellite markers for Japanese scallop(Mizuhopecten yessoensis) and their application to a population genetic study. Marine Biotechnology, 7(6):713-728, https://doi.org/10.1007/s10126-004-0127-8.
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, https://doi.org/10.1111/j.1461-0248.2006.00889.x.
Serapion J, Kucuktas H, Feng J N, Liu Z J. 2004. Bioinformatic mining of type i microsatellites from expressed sequence tags of channel catfish (Ictalurus punctatus). Marine Biotechnology, 6(4):364-377, https://doi.org/10.1007/s10126-003-0039-z.
Silva A. 2003. Morphometric variation among sardine (Sardina pilchardus) populations from the northeastern Atlantic and the western Mediterranean. ICES Journal of Marine Science, 60(6):1 352-1 360, https://doi.org/10.1016/s1054-3139(03)00141-3.
Smith C, Benzie J A H, Wilson K J. 2003. Isolation and characterization of eight microsatellite loci from silverlipped pearl oyster Pinctada maxima. Molecular Ecology Notes, 3(1):125-127, https://doi.org/10.1046/j.1471-8286.2003.00377.x.
So N, Maes G E, Volckaert F A M. 2006. High genetic diversity in cryptic populations of the migratory sutchi catfish Pangasianodon hypophthalmus in the Mekong River.Heredity, 96(2):166-174, https://doi.org/10.1038/sj.hdy.6800781.
Su Q, Tong W P, Li Q Z, Yang J L, Chen R F, Jiang Y, Cai D J. 2009. The technologe for factory breeding of Lutraria(Psammophila) maxima Jonas. Guangxi Sciences, 16(3):342-345. (in Chinese with English abstract)
Tautz D, Renz M. 1984. Simple sequences are ubiquitous repetitive components of eukaryotic genomes. Nucleic Acids Research, 12(10):4 127-4 138, https://doi.org/10.1093/nar/12.10.4127.
Ueno S, Wen Y F, Tsumura Y. 2015. Development of EST-SSR markers for Taxus cuspidata from publicly available transcriptome sequences. Biochemical Systematics and Ecology, 63:20-26, https://doi.org/10.1016/j.bse.2015.09.016.
Untergasser A, Cutcutache I, Koressaar T, Ye J, Faircloth B C, Remm M, Rozen S G. 2012. Primer3-new capabilities and interfaces. Nucleic Acids Research, 40(15):e115, https://doi.org/10.1093/nar/gks596.
Van Oosterhout C, Hutchinson W F, Wills D P M, Shipley P. 2004. Micro-checker:software for identifying and correcting genotyping errors in microsatellite data.Molecular Ecology Notes, 4(3):535-538, https://doi.org/10.1111/j.1471-8286.2004.00684.x.
Voss R S, Marcus L F, Escalante P P. 1990. Morphological evolution in Muroid rodents I. Conservative patterns of craniometric covariance and their ontogenetic basis in the neotropical genus Zygodontomys. Evolution, 44(6):1 568-1 587, https://doi.org/10.1111/j.1558-5646.1990.tb03847.x.
Wang C Y, Yu X M, Tong J G. 2007. Microsatellite diversity and population genetic structure of redfin culter (Culter erythropterus) in fragmented lakes of the Yangtze River.Hydrobiologia, 586(1):321-329, https://doi.org/10.1007/s10750-007-0702-x.
Wanna W, Rolland J L, Bonhomme F, Phongdara A. 2004.Population genetic structure of Penaeus merguiensis in Thailand based on nuclear DNA variation. Journal of Experimental Marine Biology and Ecology, 311(1):63-78, https://doi.org/10.1016/j.jembe.2004.04.018.
Wolfus G M, Garcia D K, Alcivar-Warren A. 1997. Application of the microsatellite technique for analyzing genetic diversity in shrimp breeding programs. Aquaculture, 152(1-4):35-47, https://doi.org/10.1016/s0044-8486(96)01527-x.
Wright S. 1965. The interpretation of population structure by F-statistics with special regard to systems of mating. Evolution, 19(3):395-420, https://doi.org/10.1111/j.1558-5646.1965.tb01731.x.
Yang Q, Zhao F, Song C, Zhang T, Miao Z B, Zhuang P. 2019.Analysis of morphological variations among four different geographic populations of Coilia mystus in the Yangtze River Estuary and its adjacent waters. Marine Fisheries, 41(3):294-303. (in Chinese with English abstract)
Yue G H, Ho M Y, Orban L, Komen J. 2004. Microsatellites within genes and ESTs of common carp and their applicability in silver crucian carp. Aquaculture, 234(1-4):85-98, https://doi.org/10.1016/j.aquaculture.2003.12.021.
Zhan A B, Bao Z M, Wang X L, Hu J J. 2005. Microsatellite markers derived from bay scallop Argopecten irradians expressed sequence tags. Fisheries Science, 71(6):1 341-1 346, https://doi.org/10.1111/j.1444-2906.2005.01100.x.
Zhan A B, Hu J J, H X L, Zhou Z C, Hui M, Wang S, Peng W, Wang M L, Bao Z M. 2009. Fine-scale population genetic structure of Zhikong scallop (Chlamys farreri):do local marine currents drive geographical differentiation? Marine Biotechnology, 11(2):223-235, https://doi.org/10.1007/s10126-008-9138-1.
Zhang L W, Li A Q, Wang X F, Xu J T, Zhang G Q, Su J G, Qi J M, Guan C Y. 2013. Genetic diversity of Kenaf (Hibiscus cannabinus) evaluated by Inter-Simple Sequence Repeat(ISSR). Biochemical Genetics, 51(9-10):800-810, https://doi.org/10.1007/s10528-013-9608-7.
Zhao Y Y, Zhu X C, Li Z, Xu W B, Dong J, Wei H, Li Y D, Li X D. 2019. Genetic diversity and structure of Chinese grass shrimp, Palaemonetes sinensis, inferred from transcriptome-derived microsatellite markers. BMC Genetics, 20:75, https://doi.org/10.1186/s12863-019-0779-z.
Copyright © Haiyang Xuebao