Recent worldwide expansion of Nosema ceranae (Microsporidia) in Apis mellifera populations inferred from multilocus patterns of genetic variation

Infection, Genetics and Evolution

Volumn 31, Issue , 2015, Pages 87-94

  Gomez Moracho T ^a,b,c   Bartolome C ^b,c,d   Bello, X ^b,c,d   Martin Hernandez R ^a,e   Higes, M ^a   Maside, X ^b,c,d  

^a Junta de Comunidades de Castilla La Mancha   (Spain)

^b Universidade de Santiago de Compostela and Instituto de Investigación Sanitaria de Santiago de Compostela   (Spain)

^c Santiago University Clinical Hospital   (Spain)

^d UNIVERSITY OF SANTIAGO DE COMPOSTELA   (Spain)

^e Instituto de Recursos Humanos para la Ciencia y la Tecnología INCRECYT Fundación Parque Científico y Tecnológico de Albacete   (Spain)

Author keywords

Demographic history; Diversity; Nosema ceranae; Polar tube proteins; Population structure; Recombination

Indexed keywords

APIS MELLIFERA; ARTICLE; CONTROLLED STUDY; GENE FREQUENCY; GENE LOCUS; GENETIC POLYMORPHISM; GENETIC RECOMBINATION; GENETIC VARIABILITY; GENOME ANALYSIS; GEOGRAPHICAL VARIATION (SPECIES); HAPLOTYPE; HOST PARASITE INTERACTION; LONG TERM SURVIVAL; NONHUMAN; NOSEMA CERANAE; NUCLEOTIDE SEQUENCE; POPULATION DISTRIBUTION; POPULATION GENETICS; SEQUENCE ANALYSIS; SPECIES DIFFERENCE; SPECIES DIVERSITY; UNINDEXED SEQUENCE; ANIMAL; BEE; CLASSIFICATION; GENE; GENETICS; MULTILOCUS SEQUENCE TYPING; NOSEMA; PARASITOLOGY; PHYLOGENY;

APIS CERANA; APIS FLOREA; APIS MELLIFERA; APOIDEA; MICROSPORIDIA; NOSEMA CERANAE;

ANIMALS; BEES; GENES, PROTOZOAN; GENETIC VARIATION; GENETICS, POPULATION; HAPLOTYPES; MULTILOCUS SEQUENCE TYPING; NOSEMA; PHYLOGENY; RECOMBINATION, GENETIC;

EID: 84922371091     PISSN: 15671348     EISSN: 15677257     Source Type: Journal    
DOI: 10.1016/j.meegid.2015.01.002     Document Type: Article

References (64)

1. Anderson D.L., Trueman J.W. Varroa jacobsoni (Acari: Varroidae) is more than one species. Exp. Appl. Acarol. 2000, 24:165-189.
2. Berger L., Speare R., Daszak P., Green D.E., Cunningham A.A., Goggin C.L., Slocombe R., Ragan M.A., Hyatt A.D., McDonald K.R., Hines H.B., Lips K.R., Marantelli G., Parkes H. Chytridiomycosis causes amphibian mortality associated with population declines in the rain forests of Australia and Central America. Proc. Natl. Acad. Sci. U.S.A. 1998, 95:9031-9036.
3. Blehert D.S., Hicks A.C., Behr M., Meteyer C.U., Berlowski-Zier B.M., Buckles E.L., Coleman J.T., Darling S.R., Gargas A., Niver R., Okoniewski J.C., Rudd R.J., Stone W.B. Bat white-nose syndrome: an emerging fungal pathogen?. Science 2009, 323:227.
4. Botías C., Anderson D.L., Meana A., Garrido-Bailón E., Martín-Hernández R., Higes M. Further evidence of an oriental origin for Nosema ceranae (Microsporidia: Nosematidae). J. Invertebr. Pathol. 2012, 110:108-113.
5. Botías C., Martín-Hernández R., Barrios L., Meana A., Higes M. Nosema spp. infection and its negative effects on honey bees (Apis mellifera iberiensis) at the colony level. Vet. Res. 2013, 44:25.
6. Botías C., Martín-Hernández R., Dias J., García-Palencia P., Matabuena M., Juarranz A., Barrios L., Meana A., Nanetti A., Higes M. The effect of induced queen replacement on Nosema spp. infection in honey bee (Apis mellifera iberiensis) colonies. Environ. Microbiol. 2012, 14:845-859.
7. Cepero A., Ravoet J., Gómez-Moracho T., Bernal J.L., Del Nozal M.J., Bartolomé C., Maside X., Meana A., González-Porto A.V., de Graaf D.C., Martín-Hernández R., Higes M. Holistic screening of collapsing honey bee colonies in Spain: a case study. BMC Res. Notes 2014, 7:649.
8. Chaimanee V., Chen Y., Pettis J.S., Scott Cornman R., Chantawannakul P. Phylogenetic analysis of Nosema ceranae isolated from European and Asian honeybees in Northern Thailand. J. Invertebr. Pathol. 2011, 107:229-233.
9. Chaimanee V., Warrit N., Chantawannakul P. Infections of Nosema ceranae in four different honeybee species. J. Invertebr. Pathol. 2010, 105:207-210.
10. Charlesworth B., Charlesworth D. Elements of Evolutionary Genetics 2009, Roberts and Company Publishers.
11. Chen Y., Evans J.D., Smith I.B., Pettis J.S. Nosema ceranae is a long-present and wide-spread microsporidian infection of the European honey bee (Apis mellifera) in the United States. J. Invertebr. Pathol. 2008, 97:186-188.
12. Cornman R.S., Chen Y.P., Schatz M.C., Street C., Zhao Y., Desany B., Egholm M., Hutchison S., Pettis J.S., Lipkin W.I., Evans J.D. Genomic analyses of the microsporidian Nosema ceranae, an emergent pathogen of honey bees. PLoS Pathog. 2009, 5:e1000466.
13. Dainat B., Evans J.D., Chen Y.P., Gauthier L., Neumann P. Predictive markers of honey bee colony collapse. PLoS ONE 2012, 7:e32151.
14. Daszak P., Cunningham A.A., Hyatt A.D. Emerging infectious diseases of wildlife-threats to biodiversity and human health. Science 2000, 287:443-449.
15. Delbac F., Peuvel I., Metenier G., Peyretaillade E., Vivares C.P. Microsporidian invasion apparatus: identification of a novel polar tube protein and evidence for clustering of PTP1 and PTP2 genes in three Encephalitozoon species. Infect. Immun. 2001, 69:1016-1024.
16. Dussaubat C., Sagastume S., Gómez-Moracho T., Botías C., García-Palencia P., Martín-Hernández R., Le Conte Y., Higes M. Comparative study of Nosema ceranae (Microsporidia) isolates from two different geographic origins. Vet. Microbiol. 2013, 162:670-678.
17. Edgar R.C. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 2004, 32:1792-1797.
18. Excoffier L., Lischer H.E. Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol. Ecol. Resour. 2010, 10:564-567.
19. Fries I., Feng F., da Silva A., Slemenda S.B., Pieniazek N.J. Nosema ceranae sp. (Microspora, Nosematidae), morphological and molecular characterization of a microsporidian parasite of the Asian honey bee Apis cerana (Hymenoptera, Apidae). Eur. J. Protistol. 1996, 32:356-365.
20. Fu Y.X. Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 1997, 147:915-925.
21. Genersch E. Honey bee pathology: current threats to honey bees and beekeeping. Appl. Microbiol. Biotechnol. 2010, 87:87-97.
22. Gisder S., Hedtke K., Mockel N., Frielitz M.C., Linde A., Genersch E. Five-year cohort study of Nosema spp. in Germany: does climate shape virulence and assertiveness of Nosema ceranae?. Appl. Environ. Microbiol. 2010, 76:3032-3038.
23. Goblirsch M., Huang Z.Y., Spivak M. Physiological and behavioral changes in honey bees (Apis mellifera) induced by Nosema ceranae Infection. PLoS ONE 2013, 8:e58165.
24. Gómez-Moracho T., Bartolomé C., Martín-Hernández R., Higes M., Maside X. Evidence for weak genetic recombination at the PTP2 locus of Nosema ceranae. Environ. Microbiol 2014, [Epub ahead of print]. 10.1111/1462-2920.12574.
25. Gómez-Moracho T., Maside X., Martín-Hernández R., Higes M., Bartolomé C. High levels of genetic diversity in Nosema ceranae within Apis mellifera colonies. Parasitology 2014, 141:475-481.
26. Graystock P., Yates K., Darvill B., Goulson D., Hughes W.O. Emerging dangers: deadly effects of an emergent parasite in a new pollinator host. J. Invertebr. Pathol. 2013, 114:114-119.
27. Hall T.A. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp. Ser. 1999, 41:95-98.
28. Hatjina F., Tsoktouridis G., Bouga M., Charistos L., Evangelou V., Avtzis D., Meeus I., Brunain M., Smagghe G., de Graaf D.C. Polar tube protein gene diversity among Nosema ceranae strains derived from a Greek honey bee health study. J. Invertebr. Pathol. 2011, 108:131-134.
29. Higes M., García-Palencia P., Botías C., Meana A., Martín-Hernández R. The differential development of microsporidia infecting worker honey bee (Apis mellifera) at increasing incubation temperature. Environ. Microbiol. Rep. 2010, 2:745-748.
30. Higes M., Martín-Hernández R., Meana A. Nosema ceranae, a new microsporidian parasite in honeybees in Europe. J. Invertebr. Pathol. 2006, 92:93-95.
31. Higes M., Meana A., Bartolomé C., Botías C., Martín-Hernández R. Nosema ceranae (Microsporidia), a controversial 21st century honey bee pathogen. Environ. Microbiol. Rep. 2013, 5:17-29.
32. Huang W.F., Bocquet M., Lee K.C., Sung I.H., Jiang J.H., Chen Y.W., Wang C.H. The comparison of rDNA spacer regions of Nosema ceranae isolates from different hosts and locations. J. Invertebr. Pathol. 2008, 97:9-13.
33. Huang W.F., Jiang J.H., Chen Y.W., Wang C.H. A Nosema ceranae isolate from the honeybee Apis mellifera. Apidologie 2007, 38:30-37.
34. Huang W.F., Solter L.F. Comparative development and tissue tropism of Nosema apis and Nosema ceranae. J. Invertebr. Pathol. 2013, 113:35-41.
35. Hudson R.R. A new statistic for detecting genetic differentiation. Genetics 2000, 155:2011-2014.
36. Hudson R.R. Two-locus sampling distributions and their application. Genetics 2001, 159:1805-1817.
37. Invernizzi C., Abud C., Tomasco I.H., Harriet J., Ramallo G., Campa J., Katz H., Gardiol G., Mendoza Y. Presence of Nosema ceranae in honeybees (Apis mellifera) in Uruguay. J. Invertebr. Pathol. 2009, 101:150-153.
38. Ironside J.E. Multiple losses of sex within a single genus of Microsporidia. BMC Evol. Biol. 2007, 7:48.
39. Jukes T.H., Cantor C.R. Evolution of protein molecules. Mammalian Protein Metabolism 1969, 21-132. Academic Press, New York. H.N. Munro (Ed.).
40. Klee J., Besana A.M., Genersch E., Gisder S., Nanetti A., Tam D.Q., Chinh T.X., Puerta F., Ruz J.M., Kryger P., Message D., Hatjina F., Korpela S., Fries I., Paxton R.J. Widespread dispersal of the microsporidian Nosema ceranae, an emergent pathogen of the western honey bee, Apis mellifera. J. Invertebr. Pathol. 2007, 96:1-10.
41. Lee S.C., Corradi N., Byrnes E.J., Torres-Martinez S., Dietrich F.S., Keeling P.J., Heitman J. Microsporidia evolved from ancestral sexual fungi. Curr. Biol. 2008, 18:1675-1679.
42. Li J., Chen W., Wu J., Peng W., An J., Schmid-Hempel P., Schmid-Hempel R. Diversity of Nosema associated with bumblebees (Bombus spp.) from China. Int. J. Parasitol. 2012, 42:49-61.
43. Librado P., Rozas J. DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 2009, 25:1451-1452.
44. Martín-Hernandez R., Botías C., Bailón E.G., Martínez-Salvador A., Prieto L., Meana A., Higes M. Microsporidia infecting Apis mellifera: coexistence or competition. Is Nosema ceranae replacing Nosema apis?. Environ. Microbiol. 2012, 14:2127-2138.
45. Martín-Hernández R., Botías C., Barrios L., Martínez-Salvador A., Meana A., Mayack C., Higes M. Comparison of the energetic stress associated with experimental Nosema ceranae and Nosema apis infection of honeybees (Apis mellifera). Parasitol. Res. 2011, 109:605-612.
46. Mayr E. Systematics and the Origin of Species 1942, Columbia University Press, New York.
47. McVean G., Awadalla P., Fearnhead P. A coalescent-based method for detecting and estimating recombination from gene sequences. Genetics 2002, 160:1231-1241.
48. Myers S.R., Griffiths R.C. Bounds on the minimum number of recombination events in a sample history. Genetics 2003, 163:375-394.
49. Nei M. Molecular Evolutionary Genetics 1987, Columbia University Press, New York.
50. Paxton R.J., Klee J., Korpela S., Fries I. Nosema ceranae has infected Apis mellifera in Europe since at least 1998 and may be more virulent than Nosema apis. Apidologie 2007, 38:558-565.
51. Peuvel I., Peyret P., Metenier G., Vivares C.P., Delbac F. The microsporidian polar tube: evidence for a third polar tube protein (PTP3) in Encephalitozoon cuniculi. Mol. Biochem. Parasitol. 2002, 122:69-80.
52. Plischuk S., Martín-Hernández R., Prieto L., Lucía M., Botías C., Meana A., Abrahamovich A.H., Lange C., Higes M. South American native bumblebees (Hymenoptera: Apidae) infected by Nosema ceranae (Microsporidia), an emerging pathogen of honeybees (Apis mellifera). Environ. Microbiol. Rep. 2009, 1:131-135.
53. Ramírez-Soriano A., Ramos-Onsins S.E., Rozas J., Calafell F., Navarro A. Statistical power analysis of neutrality tests under demographic expansions, contractions and bottlenecks with recombination. Genetics 2008, 179:555-567.
54. Ramos-Onsins S.E., Rozas J. Statistical properties of new neutrality tests against population growth. Mol. Biol. Evol. 2002, 19:2092-2100.
55. Ravoet J., Maharramov J., Meeus I., De Smet L., Wenseleers T., Smagghe G., de Graaf D.C. Comprehensive bee pathogen screening in Belgium reveals Crithidia mellificae as a new contributory factor to winter mortality. PLoS ONE 2013, 8:e72443.
56. Robinson R.A., Lawson B., Toms M.P., Peck K.M., Kirkwood J.K., Chantrey J., Clatworthy I.R., Evans A.D., Hughes L.A., Hutchinson O.C., John S.K., Pennycott T.W., Perkins M.W., Rowley P.S., Simpson V.R., Tyler K.M., Cunningham A.A. Emerging infectious disease leads to rapid population declines of common British birds. PLoS ONE 2010, 5:e12215.
57. Roudel M., Aufauvre J., Corbara B., Delbac F., Blot N. New insights on the genetic diversity of the honeybee parasite Nosema ceranae based on multilocus sequence analysis. Parasitology 2013, 140:1346-1356.
58. Sagastume S., del Aguila C., Martín-Hernández R., Higes M., Henriques-Gil N. Polymorphism and recombination for rDNA in the putatively asexual microsporidian Nosema ceranae, a pathogen of honeybees. Environ. Microbiol. 2011, 13:84-95.
59. Tajima F. Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 1989, 123:585-595.
60. Van der Zee R., Gómez-Moracho T., Pisa L., Sagastume S., García-Palencia P., Maside X., Bartolomé C., Martín-Hernández R., Higes M. Virulence and polar tube protein genetic diversity of Nosema ceranae (Microsporidia) field isolates from Northern and Southern Europe in honeybees (Apis mellifera iberiensis). Environ. Microbiol. Rep. 2014, 6:401-413.
61. Villa J.D., Bourgeois A.L., Danka R.G. Negative evidence for effects of genetic origin of bees on Nosema ceranae, positive evidence for effects of Nosema ceranae on bees. Apidologie 2013, 44:511-518.
62. Walsh P.D., Abernethy K.A., Bermejo M., Beyers R., De Wachter P., Akou M.E., Huijbregts B., Mambounga D.I., Toham A.K., Kilbourn A.M., Lahm S.A., Latour S., Maisels F., Mbina C., Mihindou Y., Obiang S.N., Effa E.N., Starkey M.P., Telfer P., Thibault M., Tutin C.E., White L.J., Wilkie D.S. Catastrophic ape decline in western equatorial Africa. Nature 2003, 422:611-614.
63. Watterson G.A. On the number of segregating sites in genetical models without recombination. Theor. Popul. Biol. 1975, 7:256-276.
64. Yang B., Peng G., Li T., Kadowaki T. Molecular and phylogenetic characterization of honey bee viruses, Nosema microsporidia, protozoan parasites, and parasitic mites in China. Ecol. Evol. 2013, 3:298-311.