Conserving the endangered Mexican fishing bat (Myotis vivesi): Genetic variation indicates extensive gene flow among islands in the Gulf of California

Conservation Genetics

Volumn 11, Issue 3, 2010, Pages 813-822

  Floyd, Chris H ^a,d   Flores Martínez, José Juan ^b   Herrera M , L Gerardo ^c   Mejía, Omar ^b   May, Bernie ^d  

^a UNIVERSITY OF WISCONSIN EAU CLAIRE   (United States)

^b INSTITUTO POLITÉCNICO NACIONAL   (Mexico)

^c UNIVERSIDAD NACIONAL AUTÓNOMA DE MÉXICO   (Mexico)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Dispersal; Gene flow; Gulf of California; Vespertilionidae

Indexed keywords

BAT; CONSERVATION GENETICS; DISPERSAL; ENDANGERED SPECIES; EXTINCTION; GENE FLOW; GENETIC MARKER; GENETIC STRUCTURE; GENETIC VARIATION; GENOTYPE; INTRODUCED SPECIES; ISOLATED POPULATION; MITOCHONDRIAL DNA; PHILOPATRY; POPULATION DECLINE; PREDATION; RECOLONIZATION; SPATIAL DISTRIBUTION; SPECIES CONSERVATION; VULNERABILITY;

GULF OF CALIFORNIA; PACIFIC OCEAN;

MYOTIS VIVESI; RATTUS; VERTEBRATA; VESPERTILIONIDAE;

EID: 77952889029     PISSN: 15660621     EISSN: 15729737     Source Type: Journal    
DOI: 10.1007/s10592-009-9902-4     Document Type: Article

References (69)

1. 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. doi: 10. 1046/j. 1365-294X. 2000. 105339. x.
2. Bohonak AJ (1999) Dispersal, gene flow, and population structure. Q Rev Biol 74: 21-45. doi: 10. 1086/392950.
3. Burland TM, Barratt EM, Racey PA (1998) Isolation and characterization of microsatellite loci in the brown long-eared bat, Plecotus auritus, and cross-species amplification within the family Vespertilionidae. Mol Ecol 7: 133-140. doi: 10. 1046/j. 1365-294X. 1998. 00298. x.
4. Burland TM, Barratt EM, Beaumont MA, Racey PA (1999) Population genetic structure and gene flow in a gleaning bat, Pleocotus auritus. Proc R Soc Lond B Biol Sci 266: 975-980. doi: 10. 1098/rspb. 1999. 0732.
5. Castella V, Ruedi M (2000) Characterization of highly variable microsatellite loci in the bat Myotis myotis (Chiroptera: Vespertilionidae). Mol Ecol 9: 993-1011. doi: 10. 1046/j. 1365-294x. 2000. 00939. x.
6. Castella V, Ruedi M, Excoffier L, Ibañez C, Arlettaz R, Hausser J (2000) Is the Gibraltar Strait a barrier to gene flow for the bat Myotis myotis (Chiroptera: Vespertilionidae)? Mol Ecol 9: 1761-1772. doi: 10. 1046/j. 1365-294x. 2000. 01069. x.
7. Castella V, Ruedi M, Excoffier L (2001) Contrasted patterns of mitochondrial and nuclear structure among nursery colonies of the bat Myotis myotis. J Evol Biol 14: 708-720. doi: 10. 1046/j. 1420-9101. 2001. 00331. x.
8. Ceballos G, Navarro D (1991) Diversity and conservation of Mexican mammals. In: Mares MA, Schmidly DJ (eds) Latin American mammalogy: history, biodiversity and conservation. University of Oklahoma Press, Norman, pp 167-198.
9. Chen S-F, Jones G, Rossiter SJ (2008) Sex-biased gene flow and colonization in the Formosan lesser horseshoe bat: inference from nuclear and mitochondrial markers. J Zool (Lond) 274: 207-215. doi: 10. 1111/j. 1469-7998. 2007. 00391. x.
10. Donlan JC, Howald GR, Tershy BR, Croll DA (2003) Evaluating alternative rodenticides for island conservation: roof rat eradication from the San Jorge Islands, Mexico. Biol Conserv 114: 29-34. doi: 10. 1016/S0006-3207(02)00401-9.
11. Etterson MA (2003) Conspecific attraction in loggerhead shrikes: implications for habitat conservation and reintroduction. Biol Conserv 114: 199-205. doi: 10. 1016/S0006-3207(03)00024-7.
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.
13. Excoffier L, Laval G, Schneider S (2005) Arlequin (version 3. 0): an integrated software package for population genetics data analysis. Evol Bioinform Online 1: 47-50.
14. 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.
15. Flores-Martínez JJ (2005) Estado de conservación del murciélago pescador Myotis vivesi (Vespertilionidae) en el Golfo de California México, a través de métodos genéticos y ecológicos. M. Sc thesis, Instituto Politécnico Nacional, Escuela Nacional de Ciencias Biológicas, Mexico.
16. Flores-Martínez JJ, Floyd CH, Herrera LG, May B (2005) Genetic variation and population size of the endangered fishing bat, Myotis vivesi in Isla Partida. In: Sánchez-Cordero V, Medellín RA (eds) Contribuciones mastozoológicas en homenaje a Bernardo Villa. Instituto de Biología, UNAM, Instituto de Ecología, UNAM, CONABIO, Mexico, pp 187-192.
17. Frankham R, Ballou JD, Briscoe DA (2002) Introduction to conservation genetics. Cambridge University Press, Cambridge.
18. Fumagalli L, Taberlet P, Favre L, Hausser J (1996) Origin and evolution of homologous repeating sequences in the mitochondrial DNA control region of shrews. Mol Biol Evol 13: 31-46.
19. Garner A, Rachlow JL, Waits LP (2005) Genetic diversity and population divergence in fragmented habitats: conservation of Idaho ground squirrels. Conserv Genet 6: 759-774. doi: 10. 1007/s10592-005-9035-3.
20. Gotelli NJ, Ellison AM (2004) A primer of ecological statistics. Sinauer Associates, Sunderland.
21. Goudet J (1995) fstat (version 1. 2): a computer program to calculate F-statistics. J Hered 86: 485-486.
22. Hahn BA, Silverman ED (2007) Managing breeding forest songbirds with conspecific song playbacks. Anim Conserv 10: 436-441. doi: 10. 1111/j. 1469-1795. 2007. 00128. x.
23. Hanski I (1999) Metapopulation ecology. Oxford University Press, Oxford.
24. Hartl DL (2000) A primer of population genetic, 3rd edn. Harvard University, MA.
25. Herrera LG, Flores-Martínez JJ (2002) Conserving fishing bats in the Sea of Cortez. Bat Conserv Int 19: 7-11.
26. Hisheh S, How RA, Suyanto A, Schmitt LH (2004) Implications of contrasting patterns of genetic variability in two vespertilionid bats from the Indonesian archipelago. Biol J Linn Soc Lond 83: 421-431. doi: 10. 1111/j. 1095-8312. 2004. 00401. x.
27. Hutchison DW, Templeton AR (1999) Correlation of pairwise genetic and geographic distance measures: inferring the relative influences of gene flow and drift on the distribution of genetic variability. Evol Int J Org Evol 53: 1898-1914. doi: 10. 2307/2640449.
28. IUCN (2006) IUCN red list of threatened species. www. iucnredlist. org. Accessed 1 Sept 2007.
29. Kerth G, Petit E (2005) Colonization and dispersal in a social species, the Bechstein's bat (Myotis bechsteinii). Mol Ecol 14: 3943-3950. doi: 10. 1111/j. 1365-294X. 2005. 02719. x.
30. Kerth G, Mayer F, Petit E (2002a) Extreme sex-biased dispersal in the communally breeding, nonmigratory Bechstein's bat (Myotis bechsteinii). Mol Ecol 11: 1491-1498. doi: 10. 1046/j. 1365-294X. 2002. 01528. x.
31. Kerth G, Safi K, König B (2002b) Mean colony relatedness is a poor predictor of colony structure and female philopatry in the communally breeding Bechstein's bat (Myotis bechsteinii). Behav Ecol Sociobiol 52: 203-210. doi: 10. 1007/s00265-002-0499-6.
32. Kerth G, Kiefer A, Trappmann C, Weishaar M (2003) High genetic diversity at swarming sites suggest hot spots for gene flow in the endangered Bechstein's bat. Conserv Genet 4: 491-499. doi: 10. 1023/A: 1024771713152.
33. Kerth G, Petrov B, Conti A, Anastasov D, Weishaar M, Gazaryan S, Jaquiéry J, König B, Perrin N, Bruyndonckx N (2008) Communally breeding Bechstein's bats have a stable social system that is independent from the post-glacial history and location of the populations. Mol Ecol 17: 2368-2381. doi: 10. 1111/j. 1365-294X. 2008. 03768. x.
34. Kocher TD, Thomas WK, Meyer A, Edwards SV, Pääbo S, Villablanca FX, Wilson AC (1989) Dynamics of mitochondrial DNA evolution in animals: amplification and sequencing with conserved primers. Proc Natl Acad Sci USA 86: 6196-6200. doi: 10. 1073/pnas. 86. 16. 6196.
35. Loewl SS, Williams DF, Ralls K, Pilgrim K, Fleischer RC (2005) Population structure and genetic variation in the endangered Giant Kangaroo Rat (Dipodomys ingens). Conserv Genet 6: 495-510.
36. Macdonald DW, Johnson DDP (2001) Dispersal in theory and practice: consequences for conservation biology. In: Clobert J, Danchin E, Dhondt AA, Nichols JD (eds) Dispersal. Oxford University Press, Oxford, pp 358-372.
37. Mantel N (1967) The detection of disease clustering and a generalized regression approach. Cancer Res 27: 209-220.
38. Maya JA (1968) The natural history of the fish-eating bat, Pizonyx vivesi. Dissertation, University of Arizona, Tucson.
39. Mellink E (2002) Invasive vertebrates on islands of the Sea of Cortés. In: Tellman B (ed) Invasive exotic species in the Sonoran region. University of Arizona Press, Tucson, pp 112-125.
40. Miller P (1997) Tools for population genetic analysis (TFPGA) 1. 3: a Windows program for the analysis of allozyme and molecular population genetic data. Computer software distributed by the author.
41. Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New York.
42. 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.
43. Petit E, Mayer F (1999) Male dispersal in the noctule bat (Nyctalus noctula): where are the limits? Proc R Soc Lond B Biol Sci 266: 1717-1722. doi: 10. 1098/rspb. 1999. 0837.
44. Petri B, Pääbo S, Von Haeseler A, Tautz D (1997) Paternity assessment and population subdivision in a natural population of the larger mouse-eared bat Myotis myotis. Mol Ecol 6: 235-242. doi: 10. 1046/j. 1365-294X. 1997. 00176. x.
45. Piry S, Alapetite A, Cornuet J-M, Paetkau D, Baudouin L, Estoup A (2004) GENECLASS2: a software for genetic assignment and first-generation migrant detection. J Hered 95: 536-539. doi: 10. 1093/jhered/esh074.
46. Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155: 945-959.
47. Racey PA, Barratt EM, Burland TM, Deaville R, Gotelli D, Jones G, Piertney SB (2007) Microsatellite DNA polymorphism confirms reproductive isolation and reveals differences in population genetic structure of cryptic pipistrelle bat species. Biol J Linn Soc Lond 90: 539-550. doi: 10. 1111/j. 1095-8312. 2007. 00746. x.
48. Raymond M, Rousset F (1995) Genepop (v. 1. 2): population genetics software for exact tests and ecumenicism. J Hered 86: 248-249.
49. Reed JM (1999) The role of behavior in recent avian extinctions and endangerments. Conserv Biol 13: 232-241. doi: 10. 1046/j. 1523-1739. 1999. 013002232. x.
50. Ricketts TH, Dinerstein E, Boucher T, Brooks TM, Butchart SHM, Hoffmann M, Lamoreux JF, Morrison J, Parr M, Pilgrim JD, Rodrigues ASL, Sechrest W, Wallace GE, Berlin K, Bielby J, Burgess ND, Church DR, Cox N, Knox D, Loucks C, Luck GW, Master LL, Moore R, Naidoo R, Ridgely R, Schatz GE, Shire G, Strand H, Wettengel W, Wikramanayake E (2005) Pinpointing and preventing imminent extinctions. Proc Natl Acad Sci USA 102: 18497-18501. doi: 10. 1073/pnas. 0509060102.
51. Rivers NM, Butlin RK, Altringham JD (2005) Genetic population structure of Natterer's bats explained by mating at swarming sites and philopatry. Mol Ecol 14: 4299-4312.
52. Ruedi M, Castella V (2003) Genetic consequences of the ice ages on nurseries of the bat Myotis myotis: a mitochondrial and nuclear survey. Mol Ecol 12: 1527-1540. doi: 10. 1046/j. 1365-294X. 2003. 01828. x.
53. Scott T, Wehtje W, Wehtje M (2001) The need for strategic planning in passive restoration of wildlife populations. Restor Ecol 9: 262-271. doi: 10. 1046/j. 1526-100x. 2001. 009003262. x.
54. SEMARNAT (2002) Norma Oficial Mexicana NOM-ECOL-059-(2001) Protección ambiental Especies nativas de México de flora y fauna silvestres-Categorías de riesgo y especificaciones para su inclusión, exclusión o cambio-Lista de especies en riesgo. Diario Oficial de la Federación, D. F., Mexico.
55. Slatkin M (1985) Gene flow in natural populations. Annu Rev Ecol Syst 16: 393-430. doi: 10. 1146/annurev. ecolsys. 16. 1. 393.
56. Stephens PA, Sutherland WJ (1999) Consequences of the Allee effect for behaviour, ecology and conservation. Trends Ecol Evol 14: 401-405. doi: 10. 1016/S0169-5347(99)01684-5.
57. Telfer S, Dallas JF, Aars J, Piertney SB, Stewart WA, Lambin X (2003) Demographic and genetic structure of fossorial water voles (Arvicola terrestris) on Scottish islands. J Zool (Lond) 259: 23-29. doi: 10. 1017/S0952836902003321.
58. Tershy BR, Donlan CJ, Keitt BS, Croll DA, Sánchez JA, Wood B, Hermosillo MA, Howald GR, Biavaschi N (2002) Island conservation in north-west Mexico: a conservation model integrating research, education and exotic mammal eradication. In: Veitch CR, Clout MN (eds) Turning the tide: the eradication of invasive species. IUCN SSCS Invasive Species Specialist Group, Gland, Switzerland and Cambridge, pp 293-300.
59. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DJ (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25: 4876-4882. doi: 10. 1093/nar/25. 24. 4876.
60. Towns DR (2002) Korapuki Island as a case study for restoration of insular ecosystems in New Zealand. J Biogeogr 29: 593-607. doi: 10. 1046/j. 1365-2699. 2002. 00709. x.
61. Vázquez-Domínguez E, Ceballos G, Cruzado J (2004) Extirpation of an insular subspecies by a single introduced cat: the case of the endemic deer mouse Peromyscus guardia on Estanque Island, México. Oryx 38: 347-350. doi: 10. 1017/S0030605304000602.
62. Veith M, Beer N, Kiefer A, Johannesen J, Seitz A (2004) The role of swarming sites for maintaining gene flow in the brown long-eared bat (Plecotus auritus). Heredity 93: 342-349. doi: 10. 1038/sj. hdy. 6800509.
63. Villa B (1979) Algunas aves y la rata noruega Rattus norvegicus "versus" el murciélago insulano Pizonyx vivesi en las islas del Mar de Cortés, México. An Inst Biol Univ Nac Auton Mex Ser Zool 50: 729-736.
64. Waples RS, Gaggiotti O (2006) What is a population? An empirical evaluation of some genetic methods for identifying the number of gene pools and their degree of connectivity. Mol Ecol 15: 1419-1439. doi: 10. 1111/j. 1365-294X. 2006. 02890. x.
65. Ward MP, Schlossberg S (2004) Conspecific attraction and the conservation of territorial songbirds. Conserv Biol 18: 519-525. doi: 10. 1111/j. 1523-1739. 2004. 00494. x.
66. Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evol Int J Org Evol 38: 1358-1370. doi: 10. 2307/2408641.
67. Wilkinson GS, Boughman JW (1998) Social calls coordinate foraging in greater spear-nosed bats. Anim Behav 55: 337-350. doi: 10. 1006/anbe. 1997. 0557.
68. Wood B, Tershy BR, Hermosillo MA, Donlan CJ, Sánchez JA, Keitt BS, Croll DA, Howald GR, Biavaschi N (2002) Removing cats from islands in north-west Mexico. In: Veitch CR, Clout MN (eds) Turning the tide: the eradication of invasive species. IUCN SSCS Invasive Species Specialist Group. IUCN, Gland, Switzerland and Cambridge, pp 374-380.
69. Worthington Wilmer J, Barratt E (1996) A non-lethal method of tissue sampling for genetic studies of Chiropterans. Bat Res News 37: 1-3.