Genome analysis of the monoclonal marbled crayfish reveals genetic separation over a short evolutionary timescale
Jazyk angličtina Země Anglie, Velká Británie Médium electronic
Typ dokumentu časopisecké články, práce podpořená grantem
PubMed
33462402
PubMed Central
PMC7814009
DOI
10.1038/s42003-020-01588-8
PII: 10.1038/s42003-020-01588-8
Knihovny.cz E-zdroje
- MeSH
- biologická evoluce * MeSH
- fylogeografie MeSH
- genom * MeSH
- partenogeneze * MeSH
- populační růst MeSH
- severní raci genetika MeSH
- zvířata MeSH
- Check Tag
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Geografické názvy
- Evropa MeSH
The marbled crayfish (Procambarus virginalis) represents a very recently evolved parthenogenetic freshwater crayfish species that has invaded diverse habitats in Europe and in Madagascar. However, population genetic analyses have been hindered by the homogeneous genetic structure of the population and the lack of suitable tools for data analysis. We have used whole-genome sequencing to characterize reference specimens from various known wild populations. In parallel, we established a whole-genome sequencing data analysis pipeline for the population genetic analysis of nearly monoclonal genomes. Our results provide evidence for systematic genetic differences between geographically separated populations and illustrate the emerging differentiation of the marbled crayfish genome. We also used mark-recapture population size estimation in combination with genetic data to model the growth pattern of marbled crayfish populations. Our findings uncover evolutionary dynamics in the marbled crayfish genome over a very short evolutionary timescale and identify the rapid growth of marbled crayfish populations as an important factor for ecological monitoring.
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Suomalainen, E., Saura, A. & Lokki, J. Cytology and Evolution in Parthenogenesis (CRC Press, 1987).
Astaurov BL. Experimental alterations of the developmental cytogenetic mechanisms in mulberry silkworms: artificial parthenogenesis, polyploidy, gynogenesis, and androgenesis. Adv. Morphog. 1967;6:199–257. doi: 10.1016/B978-1-4831-9953-5.50010-X. PubMed DOI
Innes DJ, Hebert PDN. The origin and genetic basis of obligate parthenogenesis in daphnia pulex. Evolution. 1988;42:1024–1035. doi: 10.1111/j.1558-5646.1988.tb02521.x. PubMed DOI
Saura A, Lokki J, Suomalainen E. Origin of polyploidy in parthenogenetic weevils. J. Theor. Biol. 1993;163:449–456. doi: 10.1006/jtbi.1993.1130. DOI
Schwander T, Henry L, Crespi BJ. Molecular evidence for ancient asexuality in timema stick insects. Curr. Biol. 2011;21:1129–1134. doi: 10.1016/j.cub.2011.05.026. PubMed DOI
Birky CW., Jr. Heterozygosity, heteromorphy, and phylogenetic trees in asexual eukaryotes. Genetics. 1996;144:427–437. PubMed PMC
Mark Welch D, Meselson M. Evidence for the evolution of bdelloid rotifers without sexual reproduction or genetic exchange. Science. 2000;288:1211–1215. doi: 10.1126/science.288.5469.1211. PubMed DOI
Jaron, K. S. et al. Genomic features of parthenogenetic animals. J. Hered. 10.1093/jhered/esaa031 (2020). PubMed PMC
Scholtz G, et al. Ecology: parthenogenesis in an outsider crayfish. Nature. 2003;421:806. doi: 10.1038/421806a. PubMed DOI
Lyko F. The marbled crayfish (Decapoda: Cambaridae) represents an independent new species. Zootaxa. 2017;4363:544–552. doi: 10.11646/zootaxa.4363.4.6. PubMed DOI
Martin P, Dorn NJ, Kawai T, van der Heiden C, Scholtz G. The enigmatic Marmorkrebs (marbled crayfish) is the parthenogenetic form of Procambarus fallax (Hagen, 1870) Contrib. Zool. 2010;79:107–118. doi: 10.1163/18759866-07903003. DOI
Vogt G, et al. The marbled crayfish as a paradigm for saltational speciation by autopolyploidy and parthenogenesis in animals. Biol. Open. 2015;4:1583–1594. doi: 10.1242/bio.014241. PubMed DOI PMC
Schön, I., Martens, K. & van, Dijk P. Lost Sex. The Evolutionary Biology of Parthenogenesis (Springer, 2009).
Martin P, Kohlmann K, Scholtz G. The parthenogenetic Marmorkrebs (marbled crayfish) produces genetically uniform offspring. Naturwissenschaften. 2007;94:843–846. doi: 10.1007/s00114-007-0260-0. PubMed DOI
Vogt G, et al. Production of different phenotypes from the same genotype in the same environment by developmental variation. J. Exp. Biol. 2008;211:510–523. doi: 10.1242/jeb.008755. PubMed DOI
Vogt G, Tolley L, Scholtz G. Life stages and reproductive components of the Marmorkrebs (marbled crayfish), the first parthenogenetic decapod crustacean. J. Morphol. 2004;261:286–311. doi: 10.1002/jmor.10250. PubMed DOI
Kato M, Hiruta C, Tochinai S. The behavior of chromosomes during parthenogenetic oogenesis in Marmorkrebs Procambarus fallax f. virginalis. Zool. Sci. 2016;33:426–430. doi: 10.2108/zs160018. PubMed DOI
Gutekunst J, et al. Clonal genome evolution and rapid invasive spread of the marbled crayfish. Nat. Ecol. Evol. 2018;2:567–573. doi: 10.1038/s41559-018-0467-9. PubMed DOI
Chucholl, C. Marbled crayfish gaining ground in Europe: the role of the pet trade as invasion pathway. in Freshwater Crayfish: Global Overview (eds Kawai, T. et al.) 83–114 (CRC Press, 2015).
Jones JPG, et al. The perfect invader: a parthenogenic crayfish poses a new threat to Madagascar’s freshwater biodiversity. Biol. Invasions. 2009;11:1475–1482. doi: 10.1007/s10530-008-9334-y. DOI
Kawai T, et al. Parthenogenetic alien crayfish (Decapoda: Cambaridae) spreading in Madagascar. J. Crust. Biol. 2009;29:562–567. doi: 10.1651/08-3125.1. DOI
Andriantsoa R, et al. Ecological plasticity and commercial impact of invasive marbled crayfish populations in Madagascar. BMC Ecol. 2019;19:8. doi: 10.1186/s12898-019-0224-1. PubMed DOI PMC
Chucholl C, Pfeiffer M. First evidence for an established Marmorkrebs (Decapoda, Astacida, Cambaridae) population in Southwestern Germany, in syntopic occurrence with Orconectes limosus (Rafinesque, 1817) Aquat. Invasions. 2010;5:405–412. doi: 10.3391/ai.2010.5.4.10. DOI
Lipták B, et al. Expansion of the marbled crayfish in Slovakia: beginning of an invasion in the Danube catchment? J. Limnol. 2016;75:305–312.
Novitsky RA, Son MO. The first records of Marmorkrebs [Procambarus fallax (Hagen, 1870) f. virginalis] (Crustacea, Decapoda, Cambaridae) in Ukraine. Ecol. Montenegrina. 2016;5:44–46. doi: 10.37828/em.2016.5.8. DOI
Patoka J, et al. Predictions of marbled crayfish establishment in conurbations fulfilled: evidences from the Czech Republic. Biologia. 2016;71:1380–1385. doi: 10.1515/biolog-2016-0164. DOI
Pârvulescu L, et al. First established population of marbled crayfish Procambarus fallax (Hagen, 1870) f. virginalis (Decapoda, Cambaridae) in Romania. Bioinvasions Rec. 2017;6:357–362. doi: 10.3391/bir.2017.6.4.09. DOI
Deidun A, et al. Invasion by non-indigenous freshwater decapods of Malta and Sicily, central Mediterranean Sea. J. Crust. Biol. 2018;38:748–753.
Ercoli F, Kaldre K, Paaver T, Gross R. First record of an established marbled crayfish Procambarus virginalis (Lyko, 2017) population in Estonia. Bioinvasions Rec. 2019;8:675–683. doi: 10.3391/bir.2019.8.3.25. DOI
Charlesworth B. Fundamental concepts in genetics: effective population size and patterns of molecular evolution and variation. Nat. Rev. Genet. 2009;10:195–205. doi: 10.1038/nrg2526. PubMed DOI
Ellegren H, Galtier N. Determinants of genetic diversity. Nat. Rev. Genet. 2016;17:422–433. doi: 10.1038/nrg.2016.58. PubMed DOI
Munoz J, Chaturvedi A, De Meester L, Weider LJ. Characterization of genome-wide SNPs for the water flea Daphnia pulicaria generated by genotyping-by-sequencing (GBS) Sci. Rep. 2016;6:28569. doi: 10.1038/srep28569. PubMed DOI PMC
Flynn JM, Chain FJ, Schoen DJ, Cristescu ME. Spontaneous mutation accumulation in Daphnia pulex in selection-free vs. competitive environments. Mol. Biol. Evol. 2017;34:160–173. doi: 10.1093/molbev/msw234. PubMed DOI
Fazalova V, Nevado B. Low spontaneous mutation rate and pleistocene radiation of pea aphids. Mol. Biol. Evol. 2020;37:2045–2051. doi: 10.1093/molbev/msaa066. PubMed DOI
Krebs, C. J. Estimating abundance in animal and plant populations. in Ecological Methodology https://www.zoology.ubc.ca/~krebs/downloads/krebs_chapter_02_2020.pdf (2014).
van der Heiden CA, Dorn NJ. Benefits of adjacent habitat patches to the distribution of a crayfish population in a hydro-dynamic wetland landscape. Aquat. Ecol. 2017;51:219–233. doi: 10.1007/s10452-016-9612-1. DOI
Liu H, et al. Direct determination of the mutation rate in the bumblebee reveals evidence for weak recombination-associated mutation and an approximate rate constancy in insects. Mol. Biol. Evol. 2017;34:119–130. doi: 10.1093/molbev/msw226. PubMed DOI PMC
Vandel A. La parthénogenèse géographique. Contribution à l’étude biologique et cytologique de la parthénogenèse naturelle. Bull. Biol. Fr. Belg. 1928;62:164–281.
Baker, H. G. Characteristics and modes of origin of weeds. in The Genetics of Colonising Species (eds Baker, H. G. & Stebbins, G. L.) 147–172 (Academic Press, 1965).
Tilquin A, Kokko H. What does the geography of parthenogenesis teach us about sex? Philos. Trans. R. Soc. Lond. B Biol. Sci. 2016;371:20150538. doi: 10.1098/rstb.2015.0538. PubMed DOI PMC
Van Doninck K, Schon I, De Bruyn L, Martens K. A general purpose genotype in an ancient asexual. Oecologia. 2002;132:205–212. doi: 10.1007/s00442-002-0939-z. PubMed DOI
Van Doninck K, Schon I, Martens K, Backeljau T. Clonal diversity in the ancient asexual ostracod Darwinula stevensoni assessed by RAPD-PCR. Heredity. 2004;93:154–160. doi: 10.1038/sj.hdy.6800486. PubMed DOI
Gatzmann F, et al. The methylome of the marbled crayfish links gene body methylation to stable expression of poorly accessible genes. Epigenetics Chromatin. 2018;11:57. doi: 10.1186/s13072-018-0229-6. PubMed DOI PMC
Carneiro VC, Lyko F. Rapid epigenetic adaptation in animals and its role in invasiveness. Integr. Comp. Biol. 2020;60:267–274. doi: 10.1093/icb/icaa023. PubMed DOI PMC
Mauvisseau Q, Tönges S, Andriantsoa R, Lyko F, Sweet M. Early detection of an emerging invasive species: eDNA monitoring of a parthenogenetic crayfish in freshwater systems. Manag. Biol. Invasions. 2019;10:461–472. doi: 10.3391/mbi.2019.10.3.04. DOI
Andriantsoa R, et al. Perceived socio-economic impacts of the marbled crayfish invasion in Madagascar. PLoS ONE. 2020;15:e0231773. doi: 10.1371/journal.pone.0231773. PubMed DOI PMC
Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics. 2014;30:2114–2120. doi: 10.1093/bioinformatics/btu170. PubMed DOI PMC
Langmead B, Salzberg SL. Fast gapped-read alignment with Bowtie 2. Nat. Methods. 2012;9:357–359. doi: 10.1038/nmeth.1923. PubMed DOI PMC
Li H, Durbin R. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics. 2009;25:1754–1760. doi: 10.1093/bioinformatics/btp324. PubMed DOI PMC
McKenna A, et al. The Genome Analysis Toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res. 2010;20:1297–1303. doi: 10.1101/gr.107524.110. PubMed DOI PMC
Cingolani P, et al. A program for annotating and predicting the effects of single nucleotide polymorphisms, SnpEff: SNPs in the genome of Drosophila melanogaster strain w1118; iso-2; iso-3. Fly. 2012;6:80–92. doi: 10.4161/fly.19695. PubMed DOI PMC
Paradis E, Claude J, Strimmer K. APE: analyses of phylogenetics and evolution in R language. Bioinformatics. 2004;20:289–290. doi: 10.1093/bioinformatics/btg412. PubMed DOI
Revell L. J. phytools: an R package for phylogenetic comparative biology (and other things) Methods Ecol. Evol. 2012;3:217–223. doi: 10.1111/j.2041-210X.2011.00169.x. DOI
Guindon S, et al. New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst. Biol. 2010;59:307–321. doi: 10.1093/sysbio/syq010. PubMed DOI
Stacklies W, Redestig H, Scholz M, Walther D, Selbig J. pcaMethods–a bioconductor package providing PCA methods for incomplete data. Bioinformatics. 2007;23:1164–1167. doi: 10.1093/bioinformatics/btm069. PubMed DOI
Johnson KE, et al. Cancer cell population growth kinetics at low densities deviate from the exponential growth model and suggest an Allee effect. PLoS Biol. 2019;17:e3000399. doi: 10.1371/journal.pbio.3000399. PubMed DOI PMC
Maiakovska, O. & Legrand, C. OlenaMaiakovska/Population_Analysis_MC. Zenodo, 10.5281/zenodo.4110932 (2020).