Lost but not forgotten: MHC genotypes predict overwinter survival despite depauperate MHC diversity in a declining frog
- 200 Downloads
The amphibian disease chytridiomycosis, caused by the fungus Batrachochytrium dendrobatidis (Bd), has contributed to the decline of Chiricahua leopard frogs (Rana chiricahuensis), a federally threatened species native to the Southwestern United States. We characterized immunogenetic variability in R. chiricahuensis by sequencing an expressed Major Histocompatibility Complex (MHC) class IIβ gene across 13 natural populations in Arizona, USA, as well as 283 individuals that were captive reared from two egg masses. We recovered a total of five class IIβ MHC alleles compared to 84 alleles previously characterized in eight natural populations of the Arizona congener R. yavapaiensis, demonstrating reduced MHC diversity in R. chiricahuensis. One allele was fixed in five populations but none of the R. chiricahuensis alleles were closely related to R. yavapaiensis allele Q, which is significantly associated with chytridiomycosis resistance in laboratory trials. Nine of 13 R. chiricahuensis population localities were Bd positive, and bearing allele RachDRB*04 was the best genetic predictor of an individual being infected with Bd. A total of three class IIβ alleles were recovered from captive reared individuals, which were released to two natural population localities followed by recapture surveys to assess MHC-based survival over winter, the time when chytridiomycosis outbreaks are most severe. At one site, all released animals were fixed for a single allele and MHC-based survival could not be assessed. At the second site, fewer than half of the released but all of the recaptured individuals were homozygous for RachDRB*05, indicating that MHC genotype is important in determining Bd survival under natural field conditions. We conclude that the limited MHC variation in R. chiricahuensis is likely the consequence rather than the cause of natural selection favoring alleles that promote survival in the face of Bd. Our study highlights that preserving even low levels of functional genetic variation may be essential for population persistence, and that local disease adaptation may present as a reduction in genetic diversity. These finding also suggest that for populations that have declined due to a specific infectious pathogen, MHC-based genetically-informed reintroduction approaches may enhance species recovery efforts.
KeywordsPeptide binding region Rana Chytridiomycosis Bd
We thank Ruth Allard, Shaula Hedwall, David Hall, Bradley Poynter, Christina Akins and Michael Sredl for their assistance in planning and implementing this project in Arizona. We also thank Nancy McInerney and Rob Fleischer for supporting data generation at the Smithsonian’s Center for Conservation Genomics. This study was funded by an Association of Zoos and Aquariums Conservation Grant Fund award (12-1111) to AES and SW and an Arizona Game and Fish Department award (Central Arizona Project) to AES and SW. KPM was supported by a doctoral student grant (PD/BD/52604/2014) from the Portuguese ‘‘Fundaçao para a Ciencia e a Tecnologia”.
- Berger L, Speare R, Daszak P, Green DE, Cunningham AA, Goggin CL, Slocombe R, Ragan MA, Hyatt AD, McDonald KR, Hines HB (1998) Chytridiomycosis causes amphibian mortality associated with population declines in the rain forests of Australia and Central America. Proc Natl Acad Sci 95:9031–9036CrossRefPubMedPubMedCentralGoogle Scholar
- Coltman DW, Pilkington JG, Smith JA, Pemberton JM (1999) Parasite-mediated selection against inbred Soay sheep in a free-living, island population. Evol Int J Org Evol 53:1259–1267Google Scholar
- ESRI 2011. ArcGIS Desktop: Release 10. Environmental Systems Research Institute, RedlandsGoogle Scholar
- Hale SF, Rosen PC, Jarchow JL, Bradley GA (2005) Effects of the chytrid fungus on the Tarahumara frog (Rana tarahumarae) in Arizona and Sonora, Mexico. USDA Forest Service Proceedings, RMRS-P-36, 407–411Google Scholar
- Hedrick PW, Kim TJ (1999) Genetics of complex polymorphisms: parasites and maintenance of MHC variation. In: Singh RH, Krimbas CK (eds) Evolutionary genetics from molecules to morphology. Cambridge University Press, New YorkGoogle Scholar
- Jensen JL, Bohonak AJ, Kelley ST (2005) Isolation by distance, web service. BMC Genet, 6(13):v.3.23. http://ibdws.sdsu.edu/
- Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M, Sturrock S, Buxton S, Cooper A, Markowitz S, Duran C, Thierer T (2012) Geneious basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28:1647–1649CrossRefPubMedPubMedCentralGoogle Scholar
- Klein J, Bontrop RE, Dawkins RL, Erlich HA, Gyllensten UB, Heise ER, Jones PP, Parham P, Wakeland EK, Watkins DI (1990) Nomenclature for the major histocompatibility complexes of different species: a proposal. Immunogenetics 3:217–219Google Scholar
- Krebs CJ (1989) Ecological methodology. Harper Collins, New York, pp 16–29Google Scholar
- Mulder KP, Harris J, Cortazar M, Grant EHC, Fleisher RC, Savage AE (2017) Evolutionary dynamics of an expressed MHC class IIβ locus in the Ranidae (Anura) uncovered by genome walking and development of amplicon multiplexing primers for 17 species. Developmental and Comparative Immunology, under reviewGoogle Scholar
- Perry W, Lugo R, Hathaway SA, Vandergast AG (2011a) Genetic Landscapes GIS Toolbox: Tools to create genetic divergence and diversity landscapes in ArcGIS. U.S. Geological Survey.Google Scholar
- R Development Core Team (2008) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0, http://www.R-project.org.
- Scott NJ (1993) Postmetamorphic death syndrome. Froglog 7:1–2Google Scholar
- Sredl MJ, Jennings RD (2005) Rana chiricahuensis: Platz and Mecham, 1979, Chiricahua leopard frogs. Pages 546–549 In: Lanoo M.J. (ed), Amphibian declines: the conservation status of United States Amphibians. University of California Press, Berkeley, pp 1094Google Scholar
- U.S. Fish and Wildlife Service (USFWS) (2007) Chiricahua leopard frog (Rana chiricahuensis) recovery plan. Region 2, U.S. Fish and Wildlife Service, Albuquerque, p 429Google Scholar
- U.S. Fish and Wildlife Service (USFWS) (2009) Spotlight Species Action Plan for the Chiricahua leopard frog (Rana chiricahuensis). Region 2, U.S. Fish and Wildlife Service, AlbuquerqueGoogle Scholar
- Waldman B, Tocher M (1998) Behavioral ecology, genetic diversity, and declining amphibian populations. In: Caro T (ed) Behavioral ecology and conservation biology, pp 394–436. Oxford University Press, New YorkGoogle Scholar
- Wells S, Poynter B, Sprankle T, King AD (2001) The Phoenix Zoo Conservation and Science Department Head-starting and Husbandry Manual for the Chiricahua leopard frog (Rana chiricahuensis). The Phoenix Zoo Conservation and Science Department, PhoenixGoogle Scholar