Conservation Genetics

, Volume 17, Issue 6, pp 1459–1468 | Cite as

Population genetic diversity and geographical differentiation of MHC class II DAB genes in the vulnerable Chinese egret (Egretta eulophotes)

Research Article


Major histocompatibility complex (MHC) genes are excellent markers for the study of adaptive genetic variation occurring over different geographical scales. The Chinese egret (Egretta eulophotes) is a vulnerable ardeid species with an estimated global population of 2600–3400 individuals. In this study, we sampled 172 individuals of this egret (approximately 6 % of the global population) from five natural populations that span the entire distribution range of this species in China. We examined their population genetic diversity and geographical differentiation at three MHC class II DAB genes by identifying eight exon 2 alleles at Egeu-DAB1, eight at Egeu-DAB2 and four at Egeu-DAB3. Allelic distributions at each of these three Egeu-DAB loci varied substantially within the five populations, while levels of genetic diversity varied slightly among the populations. Analysis of molecular variance showed low but significant genetic differentiation among five populations at all three Egeu-DAB loci (haplotype-based ϕST: 0.029, 0.020 and 0.042; and distance-based ϕST: 0.036, 0.027 and 0.043, respectively; all P < 0.01). The Mantel test suggested that this significant population genetic differentiation was likely due to an isolation-by-distance pattern of MHC evolution. However, the phylogenetic analyses and the Bayesian clustering analysis based on the three Egeu-DAB loci indicated that there was little geographical structuring of the genetic differentiation among five populations. These results provide fundamental population information for the conservation genetics of the vulnerable Chinese egret.


Genetic diversity Population differentiation Geographical variation MHC Threatened species 



We thank Yufei Dai who helped collect some samples for this study. This work was funded by the National Natural Science Foundation of China (Grant Nos. 41476113 and 31272333) and by the Fujian Natural Science Foundation of China (2010Y2007).

Compliance with ethical standards

Conflict of interest

We declare that we have no conflict of interests.

Ethical approval

All procedures involving collection of animal tissue in the wild were approved by the Administration Center for Wildlife Conservation in Fujian Province (FJWCA-1208) and were in accordance with its ethical standards.

Supplementary material

10592_2016_876_MOESM1_ESM.doc (1.2 mb)
Fig. S1 Mean of log probability of L (K) and Delta K over 10 runs for each K value. Supplementary material 1 (DOC 1230 kb)
10592_2016_876_MOESM2_ESM.doc (202 kb)
Table S1 Genotyping data collected from Egeu-DAB1–3 loci in the Chinese egret. Supplementary material 2 (DOC 202 kb)


  1. Acevedo-Whitehouse K, Cunningham AA (2006) Is MHC enough for understanding wildlife immunogenetics? Trends Ecol Evol 21:433–438. doi: 10.1016/j.tree.2006.05.010 CrossRefPubMedGoogle Scholar
  2. Addis BR, Lowe WH, Hossack BR, Allendorf FW (2015) Population genetic structure and disease in montane boreal toads: more heterozygous individuals are more likely to be infected with amphibian chytrid. Conserv Genet 16:833–844. doi: 10.1007/s10592-015-0704-6 CrossRefGoogle Scholar
  3. Aguilar A, Smith TB, Wayne RK (2005) A comparison of variation between a MHC pseudogene and microsatellite loci of the little greenbul (Andropadus virens). BMC Evol Biol 5:47. doi: 10.1186/1471-2148-5-47 CrossRefPubMedPubMedCentralGoogle Scholar
  4. Alcaide M, Edwards SV, Negro JJ, Serrano D, Tella JL (2008) Extensive polymorphism and geographical variation at a positively selected MHC class II B gene of the lesser kestrel (Falco naumanni). Mol Ecol 17:2652–2665. doi: 10.1111/j.1365-294X.2008.03791.x CrossRefPubMedGoogle Scholar
  5. Balakrishnan CN, Ekblom R, Völker M, Westerdahl H, Godinez R, Kotkiewicz H, Burt DW, Graves T, Griffin DK, Warren WC, Edwards SV (2010) Gene duplication and fragmentation in the zebra finch major histocompatibility complex. BMC Biol 8:29. doi: 10.1186/1741-7007-8-29 CrossRefPubMedPubMedCentralGoogle Scholar
  6. Bevan MJ (1987) Class discrimination in the world of immunology. Nature 325:192–194. doi: 10.1038/325192b0 CrossRefPubMedGoogle Scholar
  7. Bichet C, Moodley Y, Penn DJ, Sorci G, Garnier S (2015) Genetic structure in insular and mainland populations of house sparrows (Passer domesticus) and their hemosporidian parasites. Ecol Evol 5:1639–1652. doi: 10.1002/ece3.1452 CrossRefPubMedPubMedCentralGoogle Scholar
  8. BirdLife International (2015) Species factsheet: Egretta eulophotes. Available via DIALOG. Accessed 27 Jan 2015
  9. Corrêa TC, Del Lama SN, De Souza JR, Miño CI (2015) Genetic structuring among populations of the great egret, Ardea alba egretta, in major Brazilian wetlands. Aquat Conserv Mar Freshw Ecosyst 26:333–349. doi: 10.1002/aqc.2588 CrossRefGoogle Scholar
  10. Doherty PC, Zinkernagel RM (1975) Enhanced immunological surveillance in mice heterozygous at H-2 gene complex. Nature 256:50–52. doi: 10.1038/256050a0 CrossRefPubMedGoogle Scholar
  11. Ekblom R, Saether SA, Jacobsson P, Fiske P, Sahlman T, Grahn M, Kålås JA, Höglund J (2007) Spatial pattern of MHC class II variation in the great snipe (Gallinago media). Mol Ecol 16:1439–1451. doi: 10.1111/j.1365-294X.2007.03281.x CrossRefPubMedGoogle Scholar
  12. Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14:2611–2620. doi: 10.1111/j.1365-294X.2005.02553.x CrossRefPubMedGoogle Scholar
  13. Excoffier L, Lischer HE (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. doi: 10.1111/j.1755-0998.2010.02847.x CrossRefPubMedGoogle Scholar
  14. Fabiani A, Hoelzel AR, Galimberti F, Muelbert MMC (2003) Long-range paternal gene flow in the southern elephant seal. Science 299:676. doi: 10.1126/science.299.5607.676 CrossRefPubMedGoogle Scholar
  15. Falush D, Stephens M, Pritchard JK (2003) Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics 164:1567–1587. doi: 10.3410/f.1015548.197423 PubMedPubMedCentralGoogle Scholar
  16. Funk WC, McKay JK, Hohenlohe PA, Allendorf FW (2012) Harnessing genomics for delineating conservation units. Trends Ecol Evol 27:489–496. doi: 10.1016/j.tree.2012.05.012 CrossRefPubMedPubMedCentralGoogle Scholar
  17. Germain RN, Castellino F, Han R, Sousa CRE, Romagnoli P, Sadegh-Nasseri S, Zhong G (1996) Processing and presentation of endocytically acquired protein antigens by MHC class II and class I molecules. Immunol Rev 151:5–30. doi: 10.1111/j.1600-065X.1996.tb00701.x CrossRefGoogle Scholar
  18. Goudet J (1995) FSTAT, a program to estimate and test gene diversities and fixation indices (version 1.2). J Hered 86:485–486Google Scholar
  19. Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98Google Scholar
  20. Hughes AL (1991) MHC polymorphism and the design of captive breeding programs. Conserv Biol 5:249–251. doi: 10.1111/j.1523-1739.1991.tb00130.x CrossRefGoogle Scholar
  21. Hughes AL, Nei M (1992) Maintenance of MHC polymorphism. Nature 355:402–403. doi: 10.1038/355402b0 CrossRefPubMedGoogle Scholar
  22. Hull JM, Anderson R, Bradbury M, Estep JA, Ernest HB (2008) Population structure and genetic diversity in Swainson’s Hawks (Buteo swainsoni): implications for conservation. Conserv Genet 9:305–316. doi: 10.1007/s10592-007-9342-y CrossRefGoogle Scholar
  23. IUCN (2015) IUCN Red list of threatened species. Available via DIALOG. Accessed 27 Jan 2015
  24. Janeway CA, Murphy K, Travers P, Ehrenstein M (2008) Janeway’s immunobiology. Garland, New YorkGoogle Scholar
  25. Jensen JL, Bohonak AJ, Kelley ST (2005) Isolation by distance, web service. BMC Genet 6:13. doi: 10.1186/1471-2156-6-13 CrossRefPubMedPubMedCentralGoogle Scholar
  26. Jones MR, Cheviron ZA, Carling MD (2014) Variation in positively selected major histocompatibility complex class I loci in rufous-collared sparrows (Zonotrichia capensis). Immunogenetics 66:693–704. doi: 10.1007/s00251-014-0800-7 CrossRefPubMedGoogle Scholar
  27. Klareskog L, Sandgerg-Tragardh L, Rask L, Lindblom JB, Curman B, Peterson PA (1977) Chemical properties of human Ia antigens. Nature 265:248–251. doi: 10.1038/265248a0 CrossRefPubMedGoogle Scholar
  28. Klein J (1986) Natural history of the major histocompatibility complex. Wiley, New YorkGoogle Scholar
  29. Klein J, Bontrop RE, Dawkins RL, Erlich HA, Gyllensten UB, Heise ER, Jones PP, Wakeland EK, Watkins DI (1990) Nomenclature for major histocompatibility complexes of different species: a proposal. Immunogenetics 31:217–219. doi: 10.1007/978-3-642-77506-2_32 PubMedGoogle Scholar
  30. Klein J, Satta Y, O’hUigin C, Takahata N (1993) The molecular descent of the major histocompatibility complex. Annu Rev Immunol 11:269–295. doi: 10.1146/annurev.iy.11.040193.001413 CrossRefPubMedGoogle Scholar
  31. Kohyama TI, Omote K, Nishida C, Takenaka T, Saito K, Fujimoto S, Masuda R (2015) Spatial and temporal variation at major histocompatibility complex class IIB genes in the endangered Blakiston’s fish owl. Zool Lett 1:13. doi: 10.1186/s40851-015-0013-4 CrossRefGoogle Scholar
  32. Koutsogiannouli EA, Moutou KA, Stamatis C, Walter L, Mamuris Z (2014) Genetic variation in the major histocompatibility complex of the European brown hare (Lepus europaeus) across distinct phylogeographic areas. Immunogenetics 66:379–392. doi: 10.1007/s00251-014-0772-7 CrossRefPubMedGoogle Scholar
  33. Kushlan JA, Hancock JA (2005) The Herons. Oxford University Press, OxfordGoogle Scholar
  34. Lanfear R, Calcott B, Ho SY, Guindon S (2012) Partitionfinder: combined selection of partitioning schemes and substitution models for phylogenetic analyses. Mol Biol Evol 29:1695–1701. doi: 10.1093/molbev/mss020 CrossRefPubMedGoogle Scholar
  35. Lei W, Fang W, Lin Q, Zhou X, Chen X (2015) Characterization of a non-classical MHC class II gene in the vulnerable Chinese egret (Egretta eulophotes). Immunogenetics 67:463–472. doi: 10.1007/s00251-015-0846-1 CrossRefPubMedGoogle Scholar
  36. Lei W, Zhou X, Fang W, Lin Q, Chen X (2016) Major histocompatibility complex class II DAB alleles associated with intestinal parasite load in the vulnerable Chinese egret (Egretta eulophotes). Ecol Evol 6:4421–4434. doi: 10.1002/ece3.2226 CrossRefPubMedPubMedCentralGoogle Scholar
  37. Li L, Zhou X, Chen X (2011) Characterization and evolution of MHC class II B genes in ardeid birds. J Mol Evol 72:474–483. doi: 10.1007/s00239-011-9446-3 CrossRefPubMedGoogle Scholar
  38. Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452. doi: 10.1093/bioinformatics/btp187 CrossRefPubMedGoogle Scholar
  39. Lillie M, Grueber CE, Sutton JT, Howitt R, Bishop PJ, Gleeson D, Belov K (2015) Selection on MHC class II supertypes in the New Zealand endemic Hochstetter’s frog. BMC Evol Biol 15:63. doi: 10.1186/s12862-015-0342-0 CrossRefPubMedPubMedCentralGoogle Scholar
  40. Luo M, Pan H, Liu Z, Li M (2012) Balancing selection and genetic drift at major histocompatibility complex class II genes in isolated populations of golden snub-nosed monkey (Rhinopithecus roxellana). BMC Evol Biol 12:207. doi: 10.1186/1471-2148-12-207 CrossRefPubMedPubMedCentralGoogle Scholar
  41. Martínez-Cruz B, Godoy JA, Negro JJ (2004) Population genetics after fragmentation: the case of the endangered Spanish imperial eagle (Aquila adalberti). Mol Ecol 13:2243–2255. doi: 10.1111/j.1365-294X.2004.02220.x CrossRefPubMedGoogle Scholar
  42. Meyers LA, Bull JJ (2002) Fighting change with change: adaptive variation in an uncertain world. Trends Ecol Evol 17:551–557. doi: 10.1016/S0169-5347(02)02633-2 CrossRefGoogle Scholar
  43. Miller HC, Lambert DM (2004) Genetic drift outweighs balancing selection in shaping post-bottleneck major histocompatibility complex variation in New Zealand robins (Petroicidae). Mol Ecol 13:3709–3721. doi: 10.1111/j.1365-294X.2004.02368.x CrossRefPubMedGoogle Scholar
  44. Morin PA, Luikart G, Wayne RK, The SNP workshop group (2004) SNPs in ecology, evolution and conservation. Trends Ecol Evol 19:208–216. doi: 10.1016/j.tree.2004.01.009 CrossRefGoogle Scholar
  45. Nei M, Rooney AP (2005) Concerted and birth-and-death evolution of multigene families. Annu Rev Genet 39:121–152. doi: 10.1146/annurev.genet.39.073003.112240 CrossRefPubMedPubMedCentralGoogle Scholar
  46. Nguyen-Phuc H, Fulton JE, Berres ME (2016) Genetic variation of major histocompatibility complex (MHC) in wild Red Junglefowl (Gallus gallus). Poult Sci 95:400–411. doi: 10.3382/ps/pev364 CrossRefPubMedGoogle Scholar
  47. Penn DJ, Potts WK (1999) The evolution of mating preferences and major histocompatibility genes. Am Nat 153:145–164. doi: 10.1086/303166 CrossRefGoogle Scholar
  48. Piertney SB (2003) Major histocompatibility complex B-LB gene variation in red grouse Lagopus lagopus scoticus. Wildl Biol 9:251–259Google Scholar
  49. Piertney SB, Oliver MK (2006) The evolutionary ecology of the major histocompatibility complex. Heredity 96:7–21. doi: 10.1038/sj.hdy.6800724 PubMedGoogle Scholar
  50. Poelstra JW, Vijay N, Bossu CM, Lantz H, Ryll B, Muller I, Baglione V, Unneberg P, Wikelski M, Grabherr MG, Wolf JBW (2014) The genomic landscape underlying phenotypic integrity in the face of gene flow in crows. Science 344:1410–1414. doi: 10.1126/science.1253226 CrossRefPubMedGoogle Scholar
  51. Promerová M, Králová T, Bryjová A, Albrecht T, Bryja J (2013) MHC class IIB exon 2 polymorphism in the Grey partridge (Perdix perdix) is shaped by selection, recombination and gene conversion. PLoS One 8:e69135. doi: 10.1371/journal.pone.0069135 CrossRefPubMedPubMedCentralGoogle Scholar
  52. Rousset F (2008) GENEPOP’007: a complete re-implementation of the GENEPOP software for Windows and Linux. Mol Ecol Resour 8:103–106. doi: 10.1111/j.1471-8286.2007.01931.x CrossRefPubMedGoogle Scholar
  53. Schut E, Rivero-de Aguilar J, Merino S, Magrath MJ, Komdeur J, Westerdahl H (2011) Characterization of MHC-I in the blue tit (Cyanistes caeruleus) reveals low levels of genetic diversity and trans-population evolution across European populations. Immunogenetics 63:531–542. doi: 10.1007/s00251-011-0532-x CrossRefPubMedPubMedCentralGoogle Scholar
  54. Slatkin M (1993) Isolation by distance in equilibrium and non-equilibrium populations. Evolution 47:264–279. doi: 10.2307/2410134 CrossRefGoogle Scholar
  55. Smith S, Goüy de Bellocq J, Suchentrunk F, Schaschl H (2011) Evolutionary genetics of MHC class II beta genes in the brown hare, Lepus europaeus. Immunogenetics 63:743–751. doi: 10.1007/s00251-011-0539-3 CrossRefPubMedPubMedCentralGoogle Scholar
  56. Sommer S (2005) The importance of immune gene variability (MHC) in evolutionary ecology and conservation. Front Zool 2:16. doi: 10.1186/1742-9994-2-16 CrossRefPubMedPubMedCentralGoogle Scholar
  57. Spurgin LG, Richardson DS (2010) How pathogens drive genetic diversity: MHC, mechanisms and misunderstandings. Proc R Soc B 277:979–988. doi: 10.1098/rspb.2009.2084 CrossRefPubMedPubMedCentralGoogle Scholar
  58. Spurgin LG, van Oosterhout C, Illera JC, Bridgett S, Gharbi K, Emerson BC, Richardson DS (2011) Gene conversion rapidly generates major histocompatibility complex diversity in recently founded bird populations. Mol Ecol 20:5213–5225. doi: 10.1111/j.1365-294X.2011.05367.x CrossRefPubMedGoogle Scholar
  59. Takahata N, Nei M (1990) Allelic genealogy under overdominant and frequency-dependent selection and polymorphism of major histocompatibility complex loci. Genetics 124:967–978PubMedPubMedCentralGoogle Scholar
  60. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA 6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729. doi: 10.1093/molbev/mst197 CrossRefPubMedPubMedCentralGoogle Scholar
  61. Vásquez-Carrillo C, Friesen F, Hall L, Peery MZ (2013) Variation in MHC class II B genes in marbled murrelets: implications for delineating conservation units. Anim Conserv 17:244–255. doi: 10.1111/acv.12089 CrossRefGoogle Scholar
  62. Wang Z, Zhou X, Lin Q, Fang W, Chen X (2013) Characterization, polymorphism and selection of major histocompatibility complex (MHC) DAB genes in vulnerable Chinese egret (Egretta eulophotes). PLoS One 8:e74185. doi: 10.1371/journal.pone.0074185 CrossRefPubMedPubMedCentralGoogle Scholar
  63. Weber DS, Stewart BS, Schienman J, Lehman N (2004) Major histocompatibility complex variation at three class II loci in the northern elephant seal. Mol Ecol 13:711–718. doi: 10.1111/j.1365-294X.2004.02095.x CrossRefPubMedGoogle Scholar
  64. Witzenberger KA, Hochkirch A (2011) Ex situ conservation genetics: a review of molecular studies on the genetic consequences of captive breeding programmes for endangered animal species. Biodivers Conserv 20:1843–1861. doi: 10.1007/s10531-011-0074-4 CrossRefGoogle Scholar
  65. Zeng Q, He K, Sun D, Ma M, Ge Y, Fang S, Wan Q (2016) Balancing selection and recombination as evolutionary forces caused population genetic variations in golden pheasant MHC class I genes. BMC Evol Biol 16:42. doi: 10.10.1186/s12862-016-0609-0 CrossRefPubMedPubMedCentralGoogle Scholar
  66. Zhou X, Fang W, Chen X (2010) Mitochondrial DNA diversity of the vulnerable Chinese Egret (Egretta eulophotes) from China. J Ornithol 151:409–414. doi: 10.1007/s10336-009-0470-7 CrossRefGoogle Scholar
  67. Zhu Y, Wan Q, Yu B, Ge Y, Fang S (2013) Patterns of genetic differentiation at MHC class I genes and microsatellites identify conservation units in the giant panda. BMC Evol Biol 13:227. doi: 10.1186/1471-2148-13-227 CrossRefPubMedPubMedCentralGoogle Scholar

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© Springer Science+Business Media Dordrecht 2016

Authors and Affiliations

  1. 1.Key Laboratory of Ministry of Education for Coast and Wetland Ecosystems, College of the Environment and EcologyXiamen UniversityXiamenPeople’s Republic of China

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