Abstract
High genetic diversity is thought to characterize successful invasive species, as the potential to adapt to new environments is enhanced and inbreeding is reduced. The red swamp crayfish, Procambarus clarkii, native to northeastern Mexico and south-central USA was introduced to Nanjing, China from Japan in 1929. Little is known about the genetic diversity and population structure of this species in China. We examined the genetic diversity and population structure of six P. clarkii populations using nine polymorphic microsatellites. Among the six populations, Nanjing population showed the highest allele number, allele richness and gene diversity, which is consistent with records indicating Nanjing may be the first site of introduction. In all six populations, significant heterozygote deficit was observed, suggesting founder effects and non-random mating. Analysis of bottleneck under infinite allele model, stepwise mutation model and two-phased model of mutation revealed evidence of a recent bottleneck in all these populations. Pairwise genetic distance analysis, AMOVA and assignment tests demonstrated high genetic differentiation between populations. Pairwise genetic distance did not fit the pairwise geographic distance, suggesting that human mediated dispersal have played a role in the population expansion and genetic differentiation.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Astanei I, Gosling E, Wilson J, Powell E (2005) Genetic variability and phylogeography of the invasive zebra mussel, Dreissena polymorpha (Pallas). Mol Ecol 14:1655–1666
Barbaresi S, Gherardi F (2006) Experimental evidence for homing in the red swamp crayfish, Procambarus clarkii. Bull Fr Pech Piscic 380:1145–1153
Barbaresi S, Fani F, Gherardi F, Mengoni A, Souty-Grosset C (2003) Genetic variability of European populations of an invasive American crayfish: preliminary results. Biol Inva 5:269–274
Barbaresi S, Gherardi F, Mengoni A, Souty-Grosset C (2007) Genetics and invasion biology in fresh waters: a pilot study of Procambarus clarkii in Europe. In: Gherardi F (ed) Biological invaders in inland water: profiles, distribution and threats. Springer, Dordrecht, pp 381–400
Belfiore NM, May B (2000) Variable microsatellite loci in red swamp crayfish, Procambarus clarkii, and their characterization in other crayfish taxa. Mol Ecol 9:2231–2234
Bryan MB, Zalinski D, Filcek KB, Libants S, Li W, Scribner KT (2005) Patterns of invasion and colonization of the sea lamprey (Petromyzon marinus) in North America as revealed by microsatellite genotypes. Mol Ecol 14:3757–3773
Conner JK (2002) Genetic mechanisms of floral trait correlations in a natural population. Nature 420:407–410
Cornuet JM, Luikart G (1996) Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics 144:2001–2014
Cruz MJ, Rebelo R (2007) Colonization of freshwater habitats by an introduced crayfish, Procambarus clarkii, in Southwest Iberian Peninsula. Hydrobiologia 575:191–201
Dupont L, Richard J, Paulet YM, Thouzeau G, Viard F (2006) Gregariousness and protandry promote reproductive insurance in the invasive gastropod Crepidula fornicata: evidence from assignment of larval paternity. Mol Ecol 15:3009–3021
Excoffier L, Laval G, Schneider S (2005) Arlequin ver. 3.0: an integrated software package for population genetics data analysis. Evol Bioinform 1:47–50
Garza JC, Williamson EG (2001) Detection of reduction in population size using data from microsatellite loci. Mol Ecol 10:305–318
Gherardi F (2006) Crayfish invading Europe: the case study of Procambarus clarkii. Mar Freshwater Behav Physiol 39:175–191
Gutierrez-Yurrita PJ, Montes C (1999) Bioenergetics and phenology of reproduction of the introduced red swamp crayfish, Procambarus clarkii, in Donana National Park, Spain, and implications for species management. Freshw Biol 42:561–574
Haag WR, Garton DW (1995) Variation in genotype frequencies during the life history of the bivalve, Dreissena Polymorpha. Evolution 49:1284–1288
Hawley DM, Hanley D, Dhondt AA, Lovette IJ (2006) Molecular evidence for a founder effect in invasive house finch (Carpodacus mexicanus) populations experiencing an emergent disease epidemic. Mol Ecol 15:263–275
Hedgecock D, Stelmach DJ, Nelson K, Lindenfelser ME, Malecha SR (1979) Genetic divergence and biogeography of natural populations of Macrobrachium rosenbergii. Proc World Maricul Soc 10:873–879
Herborg LM, Weetman D, Van Oosterhout C, Hanfling B (2007) Genetic population structure and contemporary dispersal patterns of a recent European invader, the Chinese mitten crab, Eriocheir sinensis. Mol Ecol 16:231–242
Huner JV (1988) Procambarus in North America and elsewhere. In: Holdich DM, Lowery RS (eds) Freshwater crayfish: biology, management and exploitation. Timber Press, Portland, pp 239–261
Ibrahim KM, Nichols RA, Hewitt GM (1996) Spatial patterns of genetic variation generated by different forms of dispersal during range expansion. Heredity 77:282–291
Jensen JL, Bohonak AJ, Kelley ST (2005) Isolation by distance. BMC Genet 6:13
Keller LF, Waller DM (2002) Inbreeding effects in wild populations. Trends Ecol Evol 17:230–241
Kolbe KJ, Glor RE, Schettino LR, Lara AC, Larson A, Losos JB (2004) Genetic variation increases during biological invasion by a Cuban lizard. Nature 431:177–181
Lewis PO and Zaykin D (2000) Genetic data analysis: available at http://hydrodictyon.eeb.uconn.edu/people/plewis/software.php
Li ZY, Xie Y (2002) Invasive alien species in China. Forestry Press, Beijing
Li SC, Xu YX, Du LQ, Yi XL, Men XD, Xie JY (2005) Investigation on and analysis of alien invasions in Chinese farming industry. Chin Agri Sci Bull 21:156–159
Li JL, Dong ZG, Li YS, Wang CH (2007) Invasive aquatic species in China. Shanghai Science and Technology Publisher, Shanghai
Lundy CJ, Rico C, Hewitt GM (2000) Temporal and spatial genetic variation in spawning grounds of European hake (Merluccius merluccius) in the Bay of Biscay. Mol Ecol 9:2067–2079
Minch E (1996) Microsat, http://hpgl.stanford.edu/projects/microsat/
Mkoji GM, Boyce TG, Mungai BN, Copeland RS, Hofkin BV, Loker ES (1999) Predation of aquatic stages of Anopheles gambiae by the Louisiana red swamp crawfish (Procambarus clarkii). J Am Mosq Contr Asso 15:69–71
Nichols KM, Young WP, Danzmann RG, Robison BD, Rexroad C, Noakes M, Phillips RB, Bentzen P, Spies I, Knudsen K, Allendorf FW, Cunningham BM, Brunelli J, Zhang H, Ristow S, Drew R, Brown KH, Wheeler PA, Thorgaard GH (2003) A consolidated linkage map for rainbow trout (Oncorhynchus mykiss). Anim Genet 34:102–115
Paetkau D, Waits LP, Clarkson PL, Craighead L, Strobeck C (1997) An empirical evaluation of genetic distance statistics using microsatellite data from bear (Ursidae) populations. Genetics 147:1943–1957
Perez JE, Alfonsi C, Nirchio M, Barrios J (2006) The inbreeding paradox in invasive species. Interciencia 31:544–546
Rousset F (1997) Genetic differentiation and estimation of gene flow from F-statistics under isolation by distance. Genetics 145:1219–1228
Saccheri I, Kuussaari M, Kankare M, Vikman P, Fortelius W, Hanski I (1998) Inbreeding and extinction in a butterfly metapopulation. Nature 392:491–494
Sakai AK, Allendorf FW, Holt JS, Lodge DM, Molofsky J, With KA, Baughman S, Cabin RJ, Cohen JC, Ellstrand NC, McCauley DE, O’Neil P, Parker IM, Thompson JN, Weller SG (2001) The population biology of invasive species. Ann Rev Ecol System 35:305–332
Singh SM, Green RH (1984) Excess of allozyme homozygosity in marine mollusks and its possible biological significance. Malacologia 25:569–581
Spielman D, Brook BW, Frankham R (2004) Most species are not driven to extinction before genetic factors impact them. Proc Natl Acad Sci USA 101:15261–15264
Villanelli F, Gherardi F (1998) Breeding in the crayfish, Austropotamobius pallipes: mating patterns, mate choice and intermale competition. Freshw Biol 40:305–315
Wang CM, Lo LC, Zhu ZY, Yue GH (2006) Genome-scan QTL for growth-related traits in an F1 family from a breeding population of Asian seabass. BMC Genomics 7:274
Weinig C, Stinchcombe JR, Schmitt J (2003) QTL architecture of resistance and tolerance traits in Arabidopsis thaliana in natural environments. Mol Ecol 12:1153–1163
Williamsom MH (1998) Biological invasion. Chapman & Hall, London
Wilson AB, Naish KA, Boulding EG (1999) Multiple dispersal strategies of the invasive quagga mussel (Dreissena bugensis) as revealed by microsatellite analyses. Can J Fish Aquat Sci 56:2248–2261
Xia AJ, Tang JQ, Li JJ (2009) Current status of culture of red swamp crayfish in Jiangsu province. http://www.jsof.gov.cn/art/2009/5/5/art_64_36486.html
Yue GH, Orban L (2005) A simple and affordable method for high throughput DNA extraction from animal tissues for PCR. Electrophoresis 26:3081–3083
Yue GH, Zhu ZY, Lo LC, Wang CM, Lin G, Feng F, Pang HY, Li J, Liu HM, Gong P, Tan J, Lim HS, Chou R, Orban L (2009) Genetic variation and population structure of Asian seabass (Lates calcarifer) in the Asia-Pacific region. Aquaculture 293:22–28
Zhu ZY, Yue GH (2008) Polymorphic microsatellites from the genome of red swamp crayfish (Procambarus clarkii). Mol Ecol Res 8:796–798
Acknowledgments
This study is supported by the internal research fund from the Temasek Life Sciences Laboratory, the Republic of Singapore. The author would like to thank Professors Wang Genlin and Zhu Bingquan, and Dr. Zeyuan Zhu for helping collect samples in China, and Dr. Mamta Chauhan for English editing.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Yue, G.H., Li, J., Bai, Z. et al. Genetic diversity and population structure of the invasive alien red swamp crayfish. Biol Invasions 12, 2697–2706 (2010). https://doi.org/10.1007/s10530-009-9675-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10530-009-9675-1