Variation in Major Histocompatibility Complex diversity in invasive cane toad populations
Mette Lillie A B E * , Sylvain Dubey C , Richard Shine D and Katherine Belov BA Department of Medical Biochemistry and Microbiology (IMBIM), Genomics, Uppsala University, Box 582, 75236 Uppsala, Sweden.
B School of Life and Environmental Sciences, Gunn Building B19, The University of Sydney, NSW 2006 Australia.
C Department of Ecology and Evolution, Biophore Building, University of Lausanne, 1015 Lausanne, Switzerland.
D School of Life and Environmental Sciences, Heydon-Laurence Building A08, The University of Sydney, NSW 2006 Australia.
E Corresponding author. Email: mette.lillie@bioenv.gu.se
Wildlife Research 44(7) 565-572 https://doi.org/10.1071/WR17055
Submitted: 2 December 2016 Accepted: 12 September 2017 Published: 12 December 2017
Abstract
Context: The cane toad (Rhinella marina), a native species of central and southern America, was introduced to Australia in 1935 as a biocontrol agent after a complex history of prior introductions. The population rapidly expanded and has since spread through much of the Australian landmass, with severe impacts on the endemic wildlife, primarily via toxicity to predators. The invasion process has taken its toll on the cane toad, with changes in the immunological capacity across the Australian invasive population.
Aims: To investigate the immunogenetic underpinnings of these changes, we studied the diversity of the Major Histocompatiblity Complex (MHC) genes in introduced cane toad populations.
Methods: We studied the diversity of two MHC genes (the classical class I UA locus and a class II DAB locus) and compared these with neutral microsatellite markers in toads from the Australian site of introduction and the Australian invasion front. We also included toads from Hawai’i, the original source of the Australian toads, to infer founder effect.
Key results: Diversity across all markers was low across Australian and Hawai’ian samples, consistent with a reduction in genetic diversity through multiple founder effects during the course of the successive translocations. In Australia, allelic diversity at the microsatellite markers and the UA locus was reduced at the invasion front, whereas all three alleles at the DAB locus were maintained in the invasion-front toads.
Conclusions: Loss of allelic diversity observed at the microsatellite markers and the UA locus could be the result of drift and bottlenecking along the invasion process, however, the persistence of DAB diversity warrants further investigation to disentangle the evolutionary forces influencing this locus.
Implications: Through the use of different molecular markers, we provide a preliminary description of the adaptive genetic processes occurring in this invasive population. The extremely limited MHC diversity may represent low immunogenetic competence across the Australian population, which could be exploited for invasive species management.
Additional keywords: Bufo marinus, genetic drift, MHC, microsatellite markers, range expansion.
References
Aguilar, A., Roemer, G., Debenham, S., Binns, M., Garcelon, D., and Wayne, R. K. (2004). High MHC diversity maintained by balancing selection in an otherwise genetically monomorphic mammal. Proceedings of the National Academy of Sciences of the United States of America 101, 3490–3494.| High MHC diversity maintained by balancing selection in an otherwise genetically monomorphic mammal.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXisFWmsbo%3D&md5=ea605049c64149d771cb737c5b971ae0CAS |
Alford, R. A., Brown, G. P., Schwarzkopf, L., Phillips, B. L., and Shine, R. (2009). Comparisons through time and space suggest rapid evolution of dispersal behaviour in an invasive species. Wildlife Research 36, 23–28.
| Comparisons through time and space suggest rapid evolution of dispersal behaviour in an invasive species.Crossref | GoogleScholarGoogle Scholar |
Austerlitz, F., JungMuller, B., Godelle, B., and Gouyon, P. H. (1997). Evolution of coalescence times, genetic diversity and structure during colonization. Theoretical Population Biology 51, 148–164.
| Evolution of coalescence times, genetic diversity and structure during colonization.Crossref | GoogleScholarGoogle Scholar |
Barton, D. P. (1997). Introduced animals and their parasites: the cane toad, Bufo marinus, in Australia. Australian Journal of Ecology 22, 316–324.
| Introduced animals and their parasites: the cane toad, Bufo marinus, in Australia.Crossref | GoogleScholarGoogle Scholar |
Bernatchez, L., and Landry, C. (2003). MHC studies in nonmodel vertebrates: what have we learned about natural selection in 15 years? Journal of Evolutionary Biology 16, 363–377.
| MHC studies in nonmodel vertebrates: what have we learned about natural selection in 15 years?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXkt1Gqtbo%3D&md5=5c1bf963a8da624d715cd185c4ef413fCAS |
Bessa-Silva, A. R., Vallinoto, M., Sodre, D., da Cunha, D. B., Hadad, D., Asp, N. E., Sampaio, I., Schneider, H., and Sequeira, F. (2016). Patterns of genetic variability in island populations of the cane toad (Rhinella marina) from the mouth of the Amazon. PLoS One 11, e0152492.
| Patterns of genetic variability in island populations of the cane toad (Rhinella marina) from the mouth of the Amazon.Crossref | GoogleScholarGoogle Scholar |
Brown, G. P., and Shine, R. (2014). Immune response varies with rate of dispersal in invasive cane toads (Rhinella marina). PLoS One 9, e99734.
| Immune response varies with rate of dispersal in invasive cane toads (Rhinella marina).Crossref | GoogleScholarGoogle Scholar |
Brown, G. P., Phillips, B. L., and Shine, R. (2014). The straight and narrow path: the evolution of straight-line dispersal at a cane toad invasion front. Proceedings of the Royal Society B-Biological Sciences 281, 20141385.
| The straight and narrow path: the evolution of straight-line dispersal at a cane toad invasion front.Crossref | GoogleScholarGoogle Scholar |
Brown, G. P., Phillips, B. L., Dubey, S., and Shine, R. (2015). Invader immunology: invasion history alters immune system function in cane toads (Rhinella marina) in tropical Australia. Ecology Letters 18, 57–65.
| Invader immunology: invasion history alters immune system function in cane toads (Rhinella marina) in tropical Australia.Crossref | GoogleScholarGoogle Scholar |
Clegg, S. M., Degnan, S. M., Kikkawa, J., Moritz, C., Estoup, A., and Owens, I. P. F. (2002). Genetic consequences of sequential founder events by an island-colonizing bird. Proceedings of the National Academy of Sciences of the United States of America 99, 8127–8132.
| 1:CAS:528:DC%2BD38XkvVGju74%3D&md5=0041a5f5a48bb7feab32146b5334a4d7CAS |
Crawford, N. G. (2010). smogd: software for the measurement of genetic diversity. Molecular Ecology Resources 10, 556–557.
| smogd: software for the measurement of genetic diversity.Crossref | GoogleScholarGoogle Scholar |
Delvinquier, B. L. J., and Freeland, W. J. (1988). Protozoan parasites of the cane toad, Bufo-marinus, in Australia. Australian Journal of Zoology 36, 301–316.
| Protozoan parasites of the cane toad, Bufo-marinus, in Australia.Crossref | GoogleScholarGoogle Scholar |
Dionne, M., Miller, K. M., Dodson, J. J., Caron, F., and Bernatchez, L. (2007). Clinal variation in mhc diversity with temperature: evidence for the role of host-pathogen interaction on local adaptation in Atlantic salmon. Evolution 61, 2154–2164.
| Clinal variation in mhc diversity with temperature: evidence for the role of host-pathogen interaction on local adaptation in Atlantic salmon.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXltFOqt74%3D&md5=0fdf53aa4659459f10b0af1b0f75829eCAS |
Dubey, S., and Shine, R. (2008). Origin of the parasites of an invading species, the Australian cane toad (Bufo marinus): are the lungworms Australian or American? Molecular Ecology 17, 4418–4424.
| Origin of the parasites of an invading species, the Australian cane toad (Bufo marinus): are the lungworms Australian or American?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhsVGgtL7E&md5=677746e6d932b172af170c8700f6ee06CAS |
Easteal, S. (1981). The history of introductions of Bufo-marinus (Amphibia, Anura) – a natural experiment in evolution. Biological Journal of the Linnean Society. Linnean Society of London 16, 93.
| The history of introductions of Bufo-marinus (Amphibia, Anura) – a natural experiment in evolution.Crossref | GoogleScholarGoogle Scholar |
Eimes, J. A., Bollmer, J. L., Whittingham, L. A., Johnson, J. A., Van Oosterhout, C., and Dunn, P. O. (2011). Rapid loss of MHC class II variation in a bottlenecked population is explained by drift and loss of copy number variation. Journal of Evolutionary Biology 24, 1847–1856.
| Rapid loss of MHC class II variation in a bottlenecked population is explained by drift and loss of copy number variation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhsVGgtbfI&md5=b58e131ab39b32aa3c5ff6eb7dac95adCAS |
Ejsmond, M. J., and Radwan, J. (2011). MHC diversity in bottlenecked populations: a simulation model. Conservation Genetics 12, 129–137.
| MHC diversity in bottlenecked populations: a simulation model.Crossref | GoogleScholarGoogle Scholar |
Ekblom, R., Saether, S. A., Jacobsson, P., Fiske, P., Sahlman, T., Grahn, M., Kalas, J. A., and Hoglund, J. (2007). Spatial pattern of MHC class II variation in the great snipe (Gallinago media). Molecular Ecology 16, 1439–1451.
| Spatial pattern of MHC class II variation in the great snipe (Gallinago media).Crossref | GoogleScholarGoogle Scholar |
Estoup, A., Wilson, I. J., Sullivan, C., Cornuet, J. M., and Moritz, C. (2001). Inferring population history from microsatellite and enzyme data in serially introduced cane toads, Bufo marinus. Genetics 159, 1671–1687.
| 1:CAS:528:DC%2BD38XntFKqsA%3D%3D&md5=b081f92b84be07dd796552fc846e2e63CAS |
Estoup, A., Beaumont, M., Sennedot, F., Moritz, C., and Cornuet, J. M. (2004). Genetic analysis of complex demographic scenarios: spatially expanding populations of the cane toad, Bufo marinus. Evolution 58, 2021–2036.
| Genetic analysis of complex demographic scenarios: spatially expanding populations of the cane toad, Bufo marinus.Crossref | GoogleScholarGoogle Scholar |
Excoffier, L., and Lischer, H. E. L. (2010). Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Molecular Ecology Resources 10, 564–567.
| Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows.Crossref | GoogleScholarGoogle Scholar |
Excoffier, L., and Ray, N. (2008). Surfing during population expansions promotes genetic revolutions and structuration. Trends in Ecology & Evolution 23, 347–351.
| Surfing during population expansions promotes genetic revolutions and structuration.Crossref | GoogleScholarGoogle Scholar |
Goudet, J. (1995). FSTAT (Version 1.2): A computer program to calculate F-statistics. The Journal of Heredity 86, 485–486.
| FSTAT (Version 1.2): A computer program to calculate F-statistics.Crossref | GoogleScholarGoogle Scholar |
Hall, T. (1999). BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series 41, 95–98.
| 1:CAS:528:DC%2BD3cXhtVyjs7Y%3D&md5=a72811b8a59dd088e5d671040d9d2a05CAS |
Hallatschek, O., and Nelson, D. R. (2008). Gene surfing in expanding populations. Theoretical Population Biology 73, 158–170.
| Gene surfing in expanding populations.Crossref | GoogleScholarGoogle Scholar |
Hallatschek, O., Hersen, P., Ramanathan, S., and Nelson, D. R. (2007). Genetic drift at expanding frontiers promotes gene segregation. Proceedings of the National Academy of Sciences of the United States of America 104, 19926–19930.
| Genetic drift at expanding frontiers promotes gene segregation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXitFSquw%3D%3D&md5=1d769952e1d51640d4972b76adf39525CAS |
Hartigan, A., Fiala, I., Dykova, I., Jirku, M., Okimoto, B., Rose, K., Phalen, D. N., and Slapeta, J. (2011). A suspected parasite spill-back of two novel Myxidium spp. (Myxosporea) causing disease in Australian endemic frogs found in the invasive cane toad. PLoS One 6, e18871.
| A suspected parasite spill-back of two novel Myxidium spp. (Myxosporea) causing disease in Australian endemic frogs found in the invasive cane toad.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXlsFemurY%3D&md5=0986c39b1bd72d23b155d144c4b7898eCAS |
Hedrick, P. W. (2002). Pathogen resistance and genetic variation at MHC loci. Evolution 56, 1902–1908.
Hedrick, P. W., Thomson, G., and Klitz, W. (1987). Evolutionary genetics and HLA – another classic example. Biological Journal of the Linnean Society. Linnean Society of London 31, 311–331.
| Evolutionary genetics and HLA – another classic example.Crossref | GoogleScholarGoogle Scholar |
Hughes, A. L., and Yeager, M. (1998). Natural selection at major histocompatibility complex loci of vertebrates. Annual Review of Genetics 32, 415–435.
| Natural selection at major histocompatibility complex loci of vertebrates.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXjvFWltQ%3D%3D&md5=fea6899aa069fb696eb0f694789996eeCAS |
Kelehear, C., Webb, J. K., and Shine, R. (2009). Rhabdias pseudosphaerocephala infection in Bufo marinus: lung nematodes reduce viability of metamorph cane toads. Parasitology 136, 919–927.
| Rhabdias pseudosphaerocephala infection in Bufo marinus: lung nematodes reduce viability of metamorph cane toads.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD1MvlvVentw%3D%3D&md5=40ec32ddc7942e263027bb82d090a40fCAS |
Kelehear, C., Webb, J. K., Hagman, M., and Shine, R. (2011). Interactions between infective helminth larvae and their anuran hosts. Herpetologica 67, 378–385.
| Interactions between infective helminth larvae and their anuran hosts.Crossref | GoogleScholarGoogle Scholar |
Kelehear, C., Brown, G. P., and Shine, R. (2013). Invasive parasites in multiple invasive hosts: the arrival of a new host revives a stalled prior parasite invasion. Oikos 122, 1317–1324.
| Invasive parasites in multiple invasive hosts: the arrival of a new host revives a stalled prior parasite invasion.Crossref | GoogleScholarGoogle Scholar |
Klein, J. (1986). ‘Natural History of the Major Histocompatibility Complex.’ (Wiley & Sons: New York.)
Leblois, R., Rousset, F., Tikel, D., Moritz, C., and Estoup, A. (2000). Absence of evidence for isolation by distance in an expanding cane toad (Bufo marinus) population: an individual-based analysis of microsatellite genotypes. Molecular Ecology 9, 1905–1909.
| Absence of evidence for isolation by distance in an expanding cane toad (Bufo marinus) population: an individual-based analysis of microsatellite genotypes.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3M%2FosVersw%3D%3D&md5=2aa0c41028f84c9a61240de488a0762dCAS |
Lee, K. A., and Klasing, K. C. (2004). A role for immunology in invasion biology. Trends in Ecology & Evolution 19, 523–529.
| A role for immunology in invasion biology.Crossref | GoogleScholarGoogle Scholar |
Lever C. (2001). ‘The Cane Toad: the History and Ecology of a Successful Colonist.’ (Westbury Academic & Scientific Publishing: Otley.)
Lillie, M., Shine, R., and Belov, K. (2014). Characterisation of major histocompatibility complex class i in the Australian cane toad, Rhinella marina. PLoS One 9, e102824.
| Characterisation of major histocompatibility complex class i in the Australian cane toad, Rhinella marina.Crossref | GoogleScholarGoogle Scholar |
Lillie, M., Cui, J., Shine, R., and Belov, K. (2016). Molecular characterization of MHC class II in the Australian invasive cane toad reveals multiple splice variants. Immunogenetics 68, 449–460.
| Molecular characterization of MHC class II in the Australian invasive cane toad reveals multiple splice variants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28XovFWhsr8%3D&md5=de8e836b2eb2994462ec6e75b759765bCAS |
Lindstrom, T., Brown, G. P., Sisson, S. A., Phillips, B. L., and Shine, R. (2013). Rapid shifts in dispersal behavior on an expanding range edge. Proceedings of the National Academy of Sciences of the United States of America 110, 13452–13456.
| 1:CAS:528:DC%2BC3sXhtlCrtb3F&md5=de531e54b2faaf9f1f576ebe8b125736CAS |
Llewellyn, D., Thompson, M. B., Brown, G. P., Phillips, B. L., and Shine, R. (2012). Reduced investment in immune function in invasion-front populations of the cane toad (Rhinella marina) in Australia. Biological Invasions 14, 999–1008.
| Reduced investment in immune function in invasion-front populations of the cane toad (Rhinella marina) in Australia.Crossref | GoogleScholarGoogle Scholar |
Llewelyn, J., Phillips, B. L., Alford, R. A., Schwarzkopf, L., and Shine, R. (2010). Locomotor performance in an invasive species: cane toads from the invasion front have greater endurance, but not speed, compared to conspecifics from a long-colonised area. Oecologia 162, 343–348.
| Locomotor performance in an invasive species: cane toads from the invasion front have greater endurance, but not speed, compared to conspecifics from a long-colonised area.Crossref | GoogleScholarGoogle Scholar |
Miller, H. C., and Lambert, D. M. (2004). Genetic drift outweighs balancing selection in shaping post-bottleneck major histocompatibility complex variation in New Zealand robins (Petroicidae). Molecular Ecology 13, 3709–3721.
| Genetic drift outweighs balancing selection in shaping post-bottleneck major histocompatibility complex variation in New Zealand robins (Petroicidae).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtVGntA%3D%3D&md5=db402c570633a023a89408b22bcb483dCAS |
Monzón-Argüello, C., de Leaniz, C. G., Gajardo, G., and Consuegra, S. (2014). Eco-immunology of fish invasions: the role of MHC variation. Immunogenetics 66, 393–402.
| Eco-immunology of fish invasions: the role of MHC variation.Crossref | GoogleScholarGoogle Scholar |
Neefjes, J., Jongsma, M. L. M., Paul, P., and Bakke, O. (2011). Towards a systems understanding of MHC class I and MHC class II antigen presentation. Nature Reviews. Immunology 11, 823–836.
| 1:CAS:528:DC%2BC3MXhsVCntLnF&md5=15e35f179562051805969457172a0deeCAS |
Nei, M., Maruyama, T., and Chakraborty, R. (1975). Bottleneck effect and genetic-variability in populations. Evolution 29, 1–10.
| Bottleneck effect and genetic-variability in populations.Crossref | GoogleScholarGoogle Scholar |
Oliver, M. K., and Piertney, S. B. (2012). Selection maintains MHC diversity through a natural population bottleneck. Molecular Biology and Evolution 29, 1713–1720.
| Selection maintains MHC diversity through a natural population bottleneck.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XovVWmtrs%3D&md5=0d7c8b98a2be2c344e6d79b39a261265CAS |
Peakall, R., and Smouse, P. E. (2006). GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Molecular Ecology Notes 6, 288–295.
| GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research.Crossref | GoogleScholarGoogle Scholar |
Phillips, B. L., Brown, G. P., Webb, J. K., and Shine, R. (2006). Invasion and the evolution of speed in toads. Nature 439, 803.
| Invasion and the evolution of speed in toads.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhsVSktbs%3D&md5=54b9a5c92f4844d2b43ffa9a35bc34a1CAS |
Phillips, B. L., Brown, G. P., Greenlees, M., Webb, J. K., and Shine, R. (2007). Rapid expansion of the cane toad (Bufo marinus) invasion front in tropical Australia. Austral Ecology 32, 169–176.
| Rapid expansion of the cane toad (Bufo marinus) invasion front in tropical Australia.Crossref | GoogleScholarGoogle Scholar |
Phillips, B. L., Brown, G. P., and Shine, R. (2010a). Evolutionarily accelerated invasions: the rate of dispersal evolves upwards during the range advance of cane toads. Journal of Evolutionary Biology 23, 2595–2601.
| Evolutionarily accelerated invasions: the rate of dispersal evolves upwards during the range advance of cane toads.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3cbmsl2qug%3D%3D&md5=64c8bc66c35728ba6d1448ad38dfdf6cCAS |
Phillips, B. L., Kelehear, C., Pizzatto, L., Brown, G. P., Barton, D., and Shine, R. (2010b). Parasites and pathogens lag behind their host during periods of host range advance. Ecology 91, 872–881.
| Parasites and pathogens lag behind their host during periods of host range advance.Crossref | GoogleScholarGoogle Scholar |
Piertney, S. B., and Oliver, M. K. (2006). The evolutionary ecology of the major histocompatibility complex. Heredity 96, 7–21.
| 1:CAS:528:DC%2BD28XjsFOrsLY%3D&md5=643b79367659535684aac1e6cb5601c4CAS |
Radwan, J., Biedrzycka, A., and Babik, W. (2010). Does reduced MHC diversity decrease viability of vertebrate populations? Biological Conservation 143, 537–544.
| Does reduced MHC diversity decrease viability of vertebrate populations?Crossref | GoogleScholarGoogle Scholar |
Rozas, J., Sanchez-DelBarrio, J. C., Messeguer, X., and Rozas, R. (2003). DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19, 2496–2497.
| DnaSP, DNA polymorphism analyses by the coalescent and other methods.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXpvVSisLo%3D&md5=bc9713a983a01e4e149c05035ac505d8CAS |
Seddon, J. M., and Baverstock, P. R. (1999). Variation on islands: major histocompatibility complex (MHC) polymorphism in populations of the Australian bush rat. Molecular Ecology 8, 2071–2079.
| Variation on islands: major histocompatibility complex (MHC) polymorphism in populations of the Australian bush rat.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3c%2FpvVersg%3D%3D&md5=f7ff002886c6ea29ab977935362bd42eCAS |
Shine, R. (2010). The ecological impact of invasive cane toads (Bufo marinus) in Australia. The Quarterly Review of Biology 85, 253–291.
| The ecological impact of invasive cane toads (Bufo marinus) in Australia.Crossref | GoogleScholarGoogle Scholar |
Shine, R., Brown, G. P., and Phillips, B. L. (2011). An evolutionary process that assembles phenotypes through space rather than through time. Proceedings of the National Academy of Sciences of the United States of America 108, 5708–5711.
| An evolutionary process that assembles phenotypes through space rather than through time.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXkvVChs7w%3D&md5=983edf257303e35dccac9b8a8baf766aCAS |
Sommer, S. (2005). The importance of immune gene variability (MHC) in evolutionary ecology and conservation. Frontiers in Zoology 2, 1–18.
| The importance of immune gene variability (MHC) in evolutionary ecology and conservation.Crossref | GoogleScholarGoogle Scholar |
Speare, R. (1990). A review of the diseases of the cane toad, bufo-marinus, with comments on biological-control. Australian Wildlife Research 17, 387–410.
| A review of the diseases of the cane toad, bufo-marinus, with comments on biological-control.Crossref | GoogleScholarGoogle Scholar |
Spurgin, L. G., and Richardson, D. S. (2010). How pathogens drive genetic diversity: MHC, mechanisms and misunderstandings. Proceedings. Biological Sciences 277, 979–988.
| How pathogens drive genetic diversity: MHC, mechanisms and misunderstandings.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXkslShtro%3D&md5=a16359a44cd7b995065d19368e6d07e2CAS |
Sutton, J. T., Nakagawa, S., Robertson, B. C., and Jamieson, I. G. (2011). Disentangling the roles of natural selection and genetic drift in shaping variation at MHC immunity genes. Molecular Ecology 20, 4408–4420.
| Disentangling the roles of natural selection and genetic drift in shaping variation at MHC immunity genes.Crossref | GoogleScholarGoogle Scholar |
Sutton, J. T., Robertson, B. C., and Jamieson, I. G. (2015). MHC variation reflects the bottleneck histories of New Zealand passerines. Molecular Ecology 24, 362–373.
| MHC variation reflects the bottleneck histories of New Zealand passerines.Crossref | GoogleScholarGoogle Scholar |
Taylor, S. S., and Jamieson, I. G. (2008). No evidence for loss of genetic variation following sequential translocations in extant populations of a genetically depauperate species. Molecular Ecology 17, 545–556.
Taylor, S. S., Jenkins, D. A., and Arcese, P. (2012). Loss of MHC and neutral variation in peary caribou: genetic drift is not mitigated by balancing selection or exacerbated by MHC allele distributions. PLoS One 7, e36748.
| Loss of MHC and neutral variation in peary caribou: genetic drift is not mitigated by balancing selection or exacerbated by MHC allele distributions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XotVyqu78%3D&md5=3ff33582e4328ec55db5eb5043611706CAS |
Tikel, D., Paetkau, D., Cortinas, M. N., Leblois, R., Moritz, C., and Estoup, A. (2000). Polymerase chain reaction primers for polymorphic microsatellite loci in the invasive toad species Bufo marinus. Molecular Ecology 9, 1927–1929.
| 1:CAS:528:DC%2BD3cXos1ymtbk%3D&md5=3e75ac3f6039c2e854fcac487338d320CAS |
Urban, M. C., Phillips, B. L., Skelly, D. K., and Shine, R. (2007). The cane toad’s (Chaunus Bufo marinus) increasing ability to invade Australia is revealed by a dynamically updated range model. Proceedings. Biological Sciences 274, 1413–1419.
| The cane toad’s (Chaunus Bufo marinus) increasing ability to invade Australia is revealed by a dynamically updated range model.Crossref | GoogleScholarGoogle Scholar |
Urban, M. C., Phillips, B. L., Skelly, D. K., and Shine, R. (2008). A toad more traveled: the heterogeneous invasion dynamics of cane toads in Australia. American Naturalist 171, E134–E148.
| A toad more traveled: the heterogeneous invasion dynamics of cane toads in Australia.Crossref | GoogleScholarGoogle Scholar |
van Oosterhout, C., Joyce, D. A., Cummings, S. M., Blais, J., Barson, N. J., Ramnarine, I. W., Mohammed, R. S., Persad, N., and Cable, J. (2006). Balancing selection, random genetic drift, and genetic variation at the major histocompatibility complex in two wild populations of guppies (Poecilia reticulata). Evolution 60, 2562–2574.
| Balancing selection, random genetic drift, and genetic variation at the major histocompatibility complex in two wild populations of guppies (Poecilia reticulata).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhsFamsrg%3D&md5=c0845863e7d5fce43628d0ed4983a78bCAS |
Wang, S. P., Zhu, W., Gao, X., Li, X. P., Yan, S. F., Liu, X., Yang, J., Gao, Z. X., and Li, Y. M. (2014). Population size and time since island isolation determine genetic diversity loss in insular frog populations. Molecular Ecology 23, 637–648.
| Population size and time since island isolation determine genetic diversity loss in insular frog populations.Crossref | GoogleScholarGoogle Scholar |
White, T. A., and Perkins, S. E. (2012). The ecoimmunology of invasive species. Functional Ecology 26, 1313–1323.
| The ecoimmunology of invasive species.Crossref | GoogleScholarGoogle Scholar |
Zeisset, I., and Beebee, T. J. C. (2014). Drift rather than selection dominates MHC class ii allelic diversity patterns at the biogeographical range scale in natterjack toads Bufo calamita. PLoS One 9, e100176.
| Drift rather than selection dominates MHC class ii allelic diversity patterns at the biogeographical range scale in natterjack toads Bufo calamita.Crossref | GoogleScholarGoogle Scholar |
Zug, G. R., and Zug, P. B. (1979). The marine toad, Bufo marinus: a natural history resume of native populations. Smithsonian Contributions to Zoology 284, 1–58.
| The marine toad, Bufo marinus: a natural history resume of native populations.Crossref | GoogleScholarGoogle Scholar |