Genomic Porosity between Invasive Chondrostoma nasus and Endangered Endemic Parachondrostoma toxostoma (Cyprinidae): The Evolution of MHC IIB Genes

. 2013 ; 8 (6) : e65883. [epub] 20130618

Jazyk angličtina Země Spojené státy americké Médium electronic-print

Typ dokumentu časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid23824831

Two cyprinid species, Parachondrostoma toxostoma, an endemic threatened species, and Chondrostoma nasus, an invasive species, live in sympatry in southern France and form two sympatric zones where the presence of intergeneric hybrids is reported. To estimate the potential threat to endemic species linked to the introduction of invasive species, we focused on the DAB genes (functional MHC IIB genes) because of their adaptive significance and role in parasite resistance. More specifically, we investigated (1) the variability of MHC IIB genes, (2) the selection pattern shaping MHC polymorphism, and (3) the extent to which trans-species evolution and intergeneric hybridization affect MHC polymorphism. In sympatric areas, the native species has more diversified MHC IIB genes when compared to the invasive species, probably resulting from the different origins and dispersal of both species. A similar level of MHC polymorphism was found at population level in both species, suggesting similar mechanisms generating MHC diversity. In contrast, a higher number of DAB-like alleles per specimen were found in invasive species. Invasive species tended to express the alleles of two DAB lineages, whilst native species tended to express the alleles of only the DAB3 lineage. Hybrids have a pattern of MHC expression intermediate between both species. Whilst positive selection acting on peptide binding sites (PBS) was demonstrated in both species, a slightly higher number of positively selected sites were identified in C. nasus, which could result from parasite-mediated selection. Bayesian clustering analysis revealed a similar pattern of structuring for the genetic variation when using microsatellites or the MHC approach. We confirmed the importance of trans-species evolution for MHC polymorphism. In addition, we demonstrated bidirectional gene flow for MHC IIB genes in sympatric areas. The positive significant correlation between MHC and microsatellites suggests that demographic factors may contribute to MHC variation on a short time scale.

Zobrazit více v PubMed

Hedrick PW, Parker KM, Lee RN (2001) Using microsatellite and MHC variation to identify species, ESUs, and MUs in the endangered Sonoran topminnow. Mol Ecol 10: 1399–1412. PubMed

Marsden CD, Mable BK, Woodroffe R, Rasmussen GSA, Cleaveland S, et al. (2009) Highly endangered African Wild dogs (Lycaon pictus) lack variation at the major histocompatibility complex. J Herid 100 Supplement I: S54–S65.

Smith S, Belov K, Hughes J (2010) MHC screening for marsupial conservation: extremely low levles of class II diversity indicate population vulnerability for an endangered Australian marsupial. Conserv Genet 11: 269–278.

Moutou KA, Mamuris Z, Firme T, Kontou M, Sarafidou T, et al. (2011) Patterns of variability at the major histocompatibility class I and class II loci in populations of the endangered cyprinid Ladigesocypris ghigii . Conserv Genet 12: 1159–1171.

Hansson B, Richardson DS (2005) Genetic variation in two endangered Acrocephalus species compared to a widespread congener: estimates based on functional and random loci. Anim Conserv 8: 83–90.

Miller HC, Allendorf F, Daugherty CH (2010) Genetic diversity and differentiation at MHC genes in island populations of tuatara (Sphenodon spp.). Mol Ecol 19: 3894–3908. PubMed

Říčanová Š, Bryja J, Cosson JF, Csongor G, Choleva L, et al. (2011) Depleted genetic variation of the European ground squirrel in Central Europe in both microsatellites and the major histocompatibility complex gene: implications for conservation. Conserv Genet 12: 1115–1129.

Marsden CD, Woodroffe R, Mills MGL, McNutt JW, Creel S, et al. (2012) Spatial and temporal patterns of neutral and adaptive genetic variation in the endangered African wild dog (Lycaon pictus). Mol Ecol 21: 1379–1393. PubMed

Klein J, Figueroa F (1986) Evolution of MHC. CRC Cr Rev Imunol 6: 295–386. PubMed

Clarke B, Kirby DRS (1966) Maintenance of histocompatibility polymorphisms. Nature 211: 999–1000. PubMed

Hughes AL, Nei M (1992) Maintenance of MHC polymorphism. Nature 355: 402–403. PubMed

Penn DJ, Potts WK (1999) The evolution of mating preferences and major histocompatibility complex genes. Am Nat 153: 145–164. PubMed

Reusch TBH, Haberli MA, Aeschlimann PB, Milinski M (2001) Female sticklebacks count alleles in a strategy of sexual selection explaining MHC polymorphism. Nature 414: 300–302. PubMed

Milinski M (2006) The major histocompatibility complex, sexual selection, and mate choice. Annu Rev Ecol Evol S 37: 159–186.

Seifertová M, Šimková A (2011) Structure, diversity and evolutionary patterns of expressed MHC class IIB genes in chub (Squalius cephalus), a cyprinid fish species from Europe. Immunogenetics 63: 167–181. PubMed

Reusch TBH, Langefors A (2005) Inter- and intralocus recombination drive MHC class IIB gene diversification in a teleost, the three-spined stickleback Gasterosteus aculeatus . J Mol Evol 61: 531–541. PubMed

Alcaide M, Edwards SV, Negro JJ, Serrano D, Tella JL (2008) Extensive polymorphism and geographical variation at a positively selected MHC class IIB gene of the lesser kestrel (Falco naumanni). Mol Ecol 17: 2652–2665. PubMed

Landry C, Bernatchez L (2001) Comparative analysis of population structure across environments and geographical scales at major histocompatibility complex and microsatellite loci in Atlantic salmon (Salmo salar). Mol Ecol 10: 2525–2539. PubMed

Loiseau C, Richard M, Garnier S, Chastel O, Julliard R, et al. (2009) Diversifying selection on MHC class I in the house sparrow (Passer domesticus). Mol Ecol 18: 1331–1340. PubMed

Radwan J, Biedrzycka A, Babik W (2010) Does reduced MHC diversity decrease viability of vertebrate populations? Biol Conserv 143: 537–544. PubMed PMC

Doherty PC, Zinkernagel RM (1975) Enhanced immunological surveillance in mice heterozygous at H-2 gene complex. Nature 256: 50–52. PubMed

Klein J (1987) Origin of major histocompatibility complex polymorphism: the trans-species hypothesis. Hum Immunol 19: 155–162. PubMed

Wegner KM, Eizaguirre C (2012) New(t)s and views from hybridizing MHC genes: introgression rather than trans-species polymorphism may shape allelic repertoires. Mol Ecol 21: 779–781. PubMed

Nadachowska-Brzyska K, Zielinski P, Radwan J, Babiks W (2012) Interspecific hybridization increases MHC class II diversity in two sister species of newts. Mol Ecol 21: 887–906. PubMed

Dowling TE, Demarais BD (1993) Evolutionary significance of introgressive hybridization in cyprinid fishes. Nature 362: 444–446.

Costedoat C, Pech N, Chappaz R, Salducci MD, Lim P, et al. (2004) Étude de l'hybridation introgressive entre Chondrostoma t. toxostoma et Chondrostoma n. nasus (Téléostéen, Cyprinidae) en utilisant une approach multiple. Cybium 28: 51–61.

Costedoat C, Pech N, Salducci MD, Chappaz R, Gilles A (2005) Evolution of mosaic hybrid zone between invasive and endemic species of Cyprinidae through space and time. Biol J Linn Soc 85: 135–155.

Costedoat C, Pech N, Chappaz R, Gilles A (2007) Novelties in hybrid zones: crossroads between population genomic and ecological approaches. PLoS ONE 2 4: e357. PubMed PMC

Corse E, Costedoat C, Pech N, Chappaz R, Grey J, et al. (2009) Trade-off between morphological convergence and opportunistic diet behaviour in fish hybrid zone. Front Zool 6: 26. PubMed PMC

Corse E, Costedoat C, Chappaz R, Pech N, Martin JF, et al. (2010) A PCR-based method for diet analysis in freshwater organisms using 18SrDNA barcoding on faeces. Mol Ecol Res 10: 96–108. PubMed

Corse E (2010) Le barcoding alimentaire: développement d'un 645 nouvel outil d'écologie moléculaire pour les milieux d'eau douce. Exemple au travers de l'étude de la zone hybride Durance entre les deux Chondrostomes français. PhD thesis. Université de Provence, Marseille (in French).

Šimková A, Navrátilová P, Dávidová M, Ondračková M, Sinama M, et al. (2012) Does invasive Chondrostoma nasus shift the parasite community structure of endemic Parachondrostoma toxostoma in sympatric zones? Parasite Vector 5 1: 200. PubMed PMC

Dubut V, Sinama M, Martin JF, Meglecz E, Fernandez J, et al. (2010) Cross-species amplification of 41 microsatellites in European cyprinids: A tool for evolutionary, population genetics and hybridization studies. BMC Res Notes 3: 135. PubMed PMC

Anderson EC, Thompson EA (2002) A model-based method for identifying species hybrids using multilocus genetic data. Genetics 160: 1217–1229. PubMed PMC

Chatterji S, Pachter L (2006) Reference based annotation with GeneMapper. Genome Biol 7: R29. PubMed PMC

Ottová E, Šimková A, Martin JF, de Bellocq JG, Gelnar M, et al. (2005) Evolution and trans-species polymorphism of MHC class IIB genes in cyprinid fish. Fish Shellfish Immun 18: 199–222. PubMed

Meglécz E, Piry S, Desmarais E, Galan M, Gilles A, et al. (2011) SESAME (SEquence Sorter & AMplicon Explorer): genotyping based on high throughput multiplex amplicon sequencing. Bioinformatics 27: 277–278. PubMed PMC

Zagalska-Neubauer M, Babik W, Stuglik M, Gustafsson L, Cichon M, et al. (2010) 454 sequencing reveals extreme complexity of the class II Major Histocompatibility Complex in the collared flycatcher. BMC Evol Biol 10: 395. PubMed PMC

Longeri M, Zanotti M, Damiani G (2002) Recombinant DRB sequences produced by mismatch repair of heteroduplexes during cloning in Escherichia coli . Eur J Immunogenet 29: 517–523. PubMed

Klein J, Bontrop RE, Dawkins RL, Erlich HA, Gyllensten UB, et al. (1990) Nomenclature for the major histocompatibility complexes of different species: a proposal. Immunogenetics 31: 217–219. PubMed

Dixon B, Nagelkerke LAJ, Sibbing FA, Egberts E, Stet RJM (1996) Evolution of MHC class II beta chain-encoding genes in the Lake Tana barbel species flock (Barbus intermedius complex). Immunogenetics 44: 419–431. PubMed

Rakus KL, Wiegertjes GF, Jurecka P, Walker PD, Pilarczyk A, et al. (2009) Major histocompatibility (MH) class IIB gene polymorphism influences disease resistance of common carp (Cyprinus carpio L.). Aquaculture 288: 44–50.

Swofford DL (2003) PAUP*. Phylogenetic Analysis Using Parsimony (*and Other Methods). Version 4. Sunderland, Massachusetts: Sinauer Associates.

Posada D, Crandall KA (1998) Modeltest: Testing the model of DNA substitution. Bioinformatics 14: 817–818. PubMed

Yang ZH (2007) PAML4: Phylogenetic analysis by maximum likelihood. Mol Biol Evol 24: 1586–1591. PubMed

Sawyer SA (1999) GENECONV: a computer package for the statistical detection of gene conversion Distributed by the author, Department of Mathematics, Washington University in St. Louis, available at http://www.math.wustl.edu/~sawyer

Nei M, Gojobori T (1986) Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. Mol Biol Evol 3: 418–426. PubMed

Jukes TH, Cantor CR (1969) Evolution of protein molecules. In: Munro HN, editor. Mammalian Protein Metabolism. New York: Academic Press. pp. 21–132.

Tamura K, Peterson D, Peterson N, Stecher G, Nei M, et al. (2011) MEGA 5: Molecular Evolutionary Genetics Analysis using Maximum Likelihood, Evolutionary Distance, and Maximum Parsimony Methods. Mol Biol Evol 28: 2731–2739. PubMed PMC

Brown JH, Jardetzky TS, Gorga JC, Stern LJ, Urban RG, et al. (1993) Three-dimensional structure of the human class II histocompatibility antigen HLA-DR1 . Nature 364: 33–39. PubMed

Yang ZH, Nielsen R, Goldman N, Pedersen AMK (2000) Codon-substitution models for heterogeneous selection pressure at amino acid sites. Genetics 155: 431–449. PubMed PMC

Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155: 945–959. PubMed PMC

Falush D, Stephens M, Pritchard JK (2007) Inference of population structure using multilocus genotype data: dominant markers and null alleles. Mol Ecol 7: 574–578. PubMed PMC

Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol Notes 14: 2611–2620. PubMed

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. PubMed

Excoffier L, Lischer HEL (2010) Arlequin suite ver 3.5: A new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Resour 10: 564–567. PubMed

Van Oosterhout C, Hutchinson WF, Derek P, Wills M, Shipley P (2004) MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 4: 535–539.

Goudet J (1995) FSTAT (Version 1.2): A computer program to calculate F-statistics. J Hered 86: 485–486.

Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J Roy Stat Soc B 57: 289–300.

Storey JD (2002) A direct approach to false discovery rates. J Roy Stat Soc B 64: 479–498.

Peakall R, Smouse PE (2005) GenAlEx 6: Genetic analysis in Excel. Population genetic software for teaching and research. Mol Ecol Notes 6: 288–295. PubMed PMC

Mason RAB, Browning TL, Eldridge MDB (2011) Reduces MHC class II diversity in island compared to mainland populations of the black-footed rock-wallaby (Petrogale lateralis lateralis). Conserv Genet 12: 91–103.

Klein J, O'Huigin C (1994) MHC polymorphism and parasites. Phil Trans R Soc Lond B 346: 351–358. PubMed

Šimková A, Ottová E, Morand S (2006) MHC variability, life-traits and parasite diversity of European cyprinid fish. Evol Ecol 20: 465–477.

van Erp SHM, Egberts E, Stet RJM (1996) Characterization of class II A and B genes in a gynogenetic carp clone. Immunogenetics 44: 192–202. PubMed

Rakus KL, Wiegertjes GF, Stet RJM, Savelkoul HFJ, Pilarczyk A, et al. (2003) Polymorphism of major histocompatibility class IIB genes in different lines of the common carp (Cyprinus carpio). Aquat Living Resour 16: 432–437.

Ottová E, Šimková A, Morand S (2007) The role of major histocompatibility complex diversity in vigour of fish males (Abramis brama L.) and parasite selection. Biol J Linn Soc 90: 525–538.

Eizaguirre C, Lenz TL, Traulsen A, Milinski M (2009) Speciation accelerated and stabilized by pleiotropic major histocompatibility complex immunogenes. Ecol Lett 12: 5–12. PubMed

Whitney KD, Randell RA, Rieseberg LH (2006) Adaptive introgression of herbivore resistance traits in the weedy sunflower Helianthus annuus . Am Nat 167: 794–807. PubMed

Graser R, O'hUigin C, Vincek V, Meyer A, Klein J (1996) Trans-species polymorphism of class II Mhc loci in danio fishes. Immunogenetics 44: 36–48. PubMed

Figueroa F, Mayer WE, Sültmann H, O'hUigin C, Tichy H, et al. (2000) MHC class IIB gene evolution in East African cichlid fishes. Immunigenetics 51: 556–575. PubMed

Cohen S (2002) Strong positive selection and habitat-specific amino acid substitution patterns in Mhc from an Estuarine Fish under intense pollution stress. Mol Biol Evol 19: 1870–1888. PubMed

Biedrzycka A, Radwan J (2008) Population fragmentation and major histocompatibility complex variation in the spotted suslik, Spermophilus suslicus . Molec Ecol 17: 4801–4811. PubMed

Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl Acid S 41: 95–98.

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...