Wildlife Research Wildlife Research Society
Ecology, management and conservation in natural and modified habitats
RESEARCH ARTICLE

Genetics in conservation and wildlife management: a revolution since Caughley

Stephen D. Sarre A B and Arthur Georges A

A Institute for Applied Ecology, University of Canberra, ACT 2601, Australia.

B Corresponding author. Email: sarre@aerg.canberra.edu.au

Wildlife Research 36(1) 70-80 http://dx.doi.org/10.1071/WR08066
Submitted: 6 May 2008  Accepted: 24 October 2008   Published: 21 January 2009

Abstract

In his 1994 review of conservation biology, Graeme Caughley questioned the central role for genetics in that discipline. His central theme was that there was no known case of genetic malfunction leading to the extinction of a population or species, and that driving forces such as overkill, habitat fragmentation and introduced predators as well as environmental and demographic stochasticity of small populations should be considered ahead of genetics in the debate about extinction prevention. At the time, only indirect and theoretical evidence existed for genetic contributions to the declines of wildlife and most of the debate revolved around the impact of genetic variation on fitness and long-term persistence. In addition, the application of DNA technologies to the study of wildlife was in its infancy. Though this was not Caughley’s intention, many within wildlife management took his criticisms of genetic aspects of species decline as the cue to dismiss this branch of science as of minor relevance to conservation biology. Since Caughley’s critique, there has been a revolution in genetic technologies for non-model organisms with the arrival of highly informative hypervariable DNA markers. Perhaps even more importantly, developments in DNA and gene technologies have provided the opportunity to study fundamental life-history traits such as disease resistance in more direct ways than previously possible. In concert with these tools, conservation geneticists have risen to Caughley’s challenge and demonstrated unambiguously a clear role for genetic analysis in conservation biology. Despite these impressive advances, there remains an important gap between the genetic approaches available and their uptake by managers. Bridging this gap will greatly increase the capacity of wildlife managers to generate the data necessary for sound management.


References

Alacs E. A. Hillyer M. J. Georges A. FitzSimmons N. N. Hughes J. M. 2008 Development of microsatellite markers in the Australasian snake-necked turtle Chelodina rugosa, and cross-species amplification. Molecular Ecology Resources In press.

Allendorf F. W. , and Luikart G. (2006). ‘Conservation and the Genetics of Populations.’ (Blackwell: Malden, MA.)

ANZECC (1998). Interim Marine and Coastal Regionalisation for Australia: an ecosystem-based classification for marine and coastal environments. IMCRA Technical Group, Australian and New Zealand Environment and Conservation Council, Australia.

Ardern S. L. Lambert D. M. 1997 Is the black robin in genetic peril? Molecular Ecology 6 21 28
doi:10.1046/j.1365-294X.1997.00147.x

Asquith N. M. 2001 Misdirections in conservation biology. Conservation Biology 15 345 352 doi:10.1046/j.1523-1739.2001.015002345.x

Banks S. C. , and Taylor A. C. (2004). Genetic analyses in fauna conservation: issues and applications to Australian forests. In ‘Conservation of Australia’s Forest Fauna’. (Ed. D. Lunney.) pp. 576–590. (Royal Zoological Society of New South Wales: Sydney.)

Banks S. C. Hoyle S. D. Horsup A. Sunnucks P. Taylor A. C. 2003 Demographic monitoring of an entire species (the northern hairy-nosed wombat, Lasiorhinus krefftii) by genetic analysis of non-invasively collected material. Animal Conservation 6 101 107 doi:10.1017/S1367943003003135

Bennett P. 2000 Microsatellites. Journal of Clinical Pathology – Molecular Pathology 53 177 183 doi:10.1136/mp.53.4.177

Bensch S. Akesson M. 2005 Ten years of AFLP in ecology and evolution: why so few animals? Molecular Ecology 14 2899 2914 doi:10.1111/j.1365-294X.2005.02655.x

Berger L. Speare R. Daszak P. Green D. E. Cunningham A. A., et al 1998 Chytridiomycosis causes amphibian mortality associated with population declines in the rain forests of Australia and Central America. Proceedings of the National Academy of Sciences of the United States of America 95 9031 9036 doi:10.1073/pnas.95.15.9031

Berry O. Sarre S. D. 2007 Gel-free species identification using melt-curve analysis. Molecular Ecology Notes 7 1 4 doi:10.1111/j.1471-8286.2006.01541.x

Berry O. Tocher M. D. Sarre S. D. 2004 Can assignment tests measure dispersal? Molecular Ecology 13 551 561 doi:10.1046/j.1365-294X.2004.2081.x

Berry O. Sarre S. D. Farrington L. Aitken N. 2007 Faecal DNA detection of invasive species: the case of feral foxes in Tasmania. Wildlife Research 34 1 7 doi:10.1071/WR06082

Boore J. L. 1999 Animal mitochondrial genomes. Nucleic Acids Research 27 1767 1780 doi:10.1093/nar/27.8.1767

Boyle D. G. Boyle D. B. Olsen V. Morgan J. A. T. Hyatt A. D. 2004 Rapid quantitative detection of chytridiomycosis (Batrachochytrium dendrobatidis) in amphibian samples using real-time Taqman PCR assay. Diseases of Aquatic Organisms 60 141 148 doi:10.3354/dao060141

Caro T. M. Laurenson M. K. 1994 Ecological and genetic factors in conservation: a cautionary tale. Science 263 485 486 doi:10.1126/science.8290956

Caughley G. 1994 Directions in conservation biology. Journal of Animal Ecology 63 215 244 doi:10.2307/5542

Clinchy M. Krebs C. J. 1997 Viva Caughley! Conservation Biology 11 832 833

Clout M. N. Elliott G. P. Robertson B. C. 2002 Effects of supplementary feeding on the offspring sex ratio of kakapo: a dilemma for the conservation of a polygynous parrot. Biological Conservation 107 13 18
doi:10.1016/S0006-3207(01)00267-1

Cook B. D. Bunn S. E. Hughes J. M. 2007 A comparative analysis of population structuring and genetic diversity in sympatric lineages of freshwater shrimp (Atyidae: Paratya): concerted or independent responses to hydrographic factors? Freshwater Biology 52 2156 2171 doi:10.1111/j.1365-2427.2007.01842.x

Cooper S. J. B. Bull C. M. Gardner M. G. 1997 Characterization of microsatellite loci from the socially monogamous lizard Tiliqua rugosa using a PCR-based isolation technique. Molecular Ecology 6 793 795 doi:10.1046/j.1365-294X.1997.00242.x

Dethmers K. E. M. Broderick D. Moritz C. Fitzsimmons N. N. Limpus C. J. Lavery S. Whiting S. Guinea M. Prince R. I. T. Kennett R. 2006 The genetic structure of Australasian green turtles (Chelonia mydas): exploring the geographical scale of genetic exchange. Molecular Ecology 15 3931 3946 doi:10.1111/j.1365-294X.2006.03070.x

Diamond J. M. (1984). “Normal” extinctions of isolated populations. In ‘Extinctions’. (Ed. M. H. Nitecki.) pp. 191–246. (University of Chicago Press: Chicago, IL.)

Dove C. J. , Heacker M. , and Rotzel N. (2000). ‘The Birdstrike Identification Program at the Smithsonian Institution and New Recommendations for DNA Sampling.’ (Smithsonian Institution: Washington, DC.)

Ellegren H. 2000 Heterogeneous mutation processes in human microsatellite DNA sequences. Nature Genetics 24 400 402 doi:10.1038/74249

Ernest H. B. , and Boyce W. M. (2000). DNA identification of mountain lions involved in livestock predation and public safety incidents and investigations. In ‘Proceedings of the 19th Vertebrate Pest Conference’. (Eds T. P. Slamon and A. C. Crabb.) pp. 290–294. (University of California: Davis, CA.)

Frankel O. H. , and Soule M. E. (1981). ‘Conservation and Evolution.’ (Cambridge University Press: Cambridge.)

Frankham R. 1998 Inbreeding and extinction: island populations. Conservation Biology 12 665 675 doi:10.1046/j.1523-1739.1998.96456.x

Frankham R. 2005 Genetics and extinction. Biological Conservation 126 131 140 doi:10.1016/j.biocon.2005.05.002

Frankham R. Ralls K. 1998 Conservation biology – inbreeding leads to extinction. Nature 392 441 442 doi:10.1038/33022

Frankham R. Smith G. J. Briscoe D. A. 1993 Effects on heterozygosity and reproductive fitness of inbreeding with and without selection on fitness in Drosophila melanogaster. Theoretical and Applied Genetics 86 155 162 doi:10.1007/BF00211056

Franklin J. R. (1980). Evolutionary change in small populations. In ‘Conservation Biology: An Evolutionary–Ecological Perspective’. (Eds M. E. Soulé and B. A. Wilcox.) pp. 135–150. (Sinauer Associates: Sunderland, MA.)

Georges A. Adams M. McCord W. P. 2002 Electrophoretic delineation of species boundaries within the genus Chelodina (Testudines: Chelidae) of Australia, New Guinea and Indonesia. Zoological Journal of the Linnean Society 134 401 421 doi:10.1046/j.1096-3642.2002.00007.x

Georges A. , Walsh R. , Spencer R. J. , Welsh M. , and Shaffer H. (2007). The Bellinger Emydura. Challenges for Management. Report to NSW National Parks and Wildlife Service, Sydney, by the Institute for Applied Ecology, University of Canberra, July 2007 .

Hawkins C. E. Baars C. Hesterman H. Hocking G. J. Jones M. E., et al 2006 Emerging disease and population decline of an island endemic, the Tasmanian devil Sarcophilus harrisii. Biological Conservation 131 307 324 doi:10.1016/j.biocon.2006.04.010

Hedrick P. W. Lacy R. C. Allendorf F. W. Soulé M. E. 1996 Directions in conservation biology: comments on Caughley. Conservation Biology 10 1312 1320 doi:10.1046/j.1523-1739.1996.10051312.x

Hoehn M. Sarre S. D. Henle K. 2007 The tales of two geckos: does dispersal prevent extinction in recently fragmented populations? Molecular Ecology 16 3299 3312 doi:10.1111/j.1365-294X.2007.03352.x

Hsieh H. M. Huang L. H. Tsai L. C. Liu C. L. Kuo Y. C. Hsiao C. Linacre A. Linacre L. James C. I. 2006 Species identification of Kachuga tecta using the cytochrome b gene. Journal of Forensic Sciences 51 52 56 doi:10.1111/j.1556-4029.2005.00004.x

Jamieson I. G. 2007 Role of genetic factors in extinction of island endemics: complementary or competing explanations? Animal Conservation 10 151 153 doi:10.1111/j.1469-1795.2007.00111.x

Jones M. E. Paetkau D. Geffen E. Moritz C. 2004 Genetic diversity and population structure of Tasmanian devils, the largest marsupial carnivore. Molecular Ecology 13 2197 2209 doi:10.1111/j.1365-294X.2004.02239.x

Kinnear J. E. Sumner N. R. Onus M. L. 2002 The red fox in Australia – an exotic predator turned biocontrol agent. Biological Conservation 108 335 359 doi:10.1016/S0006-3207(02)00116-7

Kurtz J. Scharsack J. P. 2007 Resistance is skin-deep: innate immunity may help amphibians to survive a deadly fungus. Animal Conservation 10 422 424 doi:10.1111/j.1469-1795.2007.00149.x

Leberg P. L. Firmin B. D. 2008 Role of inbreeding depression and purging in captive breeding and restoration programmes. Molecular Ecology 17 334 343 doi:10.1111/j.1365-294X.2007.03433.x

Lee J. H. Hassan H. Hill G. Cupp E. W. Higazi T. B. Mitchell C. J. Godsey M. S. J. Unnasch T. R. 2002 Identification of mosquito avian-derived blood meals by polymerase chain reaction-heteroduplex analysis. The American Journal of Tropical Medicine and Hygiene 66 599 604

Lee P. L. M. Prys-Jones R. P. 2008 Extracting DNA from museum bird eggs, and whole genome amplification of archive DNA. Molecular Ecology Resources 8 551 560
doi:10.1111/j.1471-8286.2007.02042.x

Levine J. M. D’Antonio C. M. 2003 Forecasting biological invasions with increasing international trade. Conservation Biology 17 322 326 doi:10.1046/j.1523-1739.2003.02038.x

Lewontin R. C. 1991 Twenty-five years ago in genetics: electrophoresis in the development of evolutionary genetics: milestone or millstone. Genetics 128 657 662

Li Y. Hill J. A. Yue G. Chen F. Orban L. 2002 a Extensive search does not identify genomic sex marker in Tetraodon nigroviridis. Journal of Fish Biology 61 1314 1317
doi:10.1111/j.1095-8649.2002.tb02475.x

Li Y. C. Korol A. B. Fahima T. Beiles A. Nevo E. 2002 b Microsatellites: genomic distribution, putative functions and mutational mechanisms: a review. Molecular Ecology 11 2453 2465 doi:10.1046/j.1365-294X.2002.01643.x

Lisitsyn N. Lisitsyn N. Wigler M. 1993 Cloning the differences between two complex genomes. Science 259 946 951 doi:10.1126/science.8438152

Madsen T. Shine R. Olsson M. Wittzell H. 1999 Conservation biology – restoration of an inbred adder population. Nature 402 34 35 doi:10.1038/46941

Madsen T. Ujvari B. Olsson M. 2004 Novel genes continue to enhance population growth in adders (Vipera berus). Biological Conservation 120 145 147 doi:10.1016/j.biocon.2004.01.022

McGlashan D. J. Hughes J. M. 2000 Reconciling patterns of genetic variation with stream structure, earth history and biology in the Australian freshwater fish Craterocephalus stercusmuscarum (Atherinidae). Molecular Ecology 9 1737 1751 doi:10.1046/j.1365-294x.2000.01054.x

McKelvey K. S. von Kienast J. Aubry K. B. Koehler G. M. Maletzke B. T. Squires J. R. Lindquist E. L. Loch S. Schwartz M. K. 2006 DNA analysis of hair and scat collected along snow tracks to document the presence of Canada lynx. Wildlife Society Bulletin 34 451 455 doi:10.2193/0091-7648(2006)34[451:DAOHAS]2.0.CO;2

Meffe G. K. Vrijenhoek R. C. 1988 Conservation genetics in the management of desert fishes. Conservation Biology 2 157 169 doi:10.1111/j.1523-1739.1988.tb00167.x

Melton T. Holland C. 2007 Routine forensic use of the mitochondrial 12S ribosomal RNA gene for species identification. Journal of Forensic Sciences 52 1305 1307

Morgan J. A. T. Vredenburg V. T. Rachowicz L. J. Knapp R. A. Stice M. J., et al 2007 Population genetics of the frog-killing fungus Batrachochytrium dendrobatidis. Proceedings of the National Academy of Sciences of the United States of America 104 13845 13850
doi:10.1073/pnas.0701838104

Moritz C. 1994 Defining ‘evolutionary significant units’ for conservation. Trends in Ecology & Evolution 9 373 375 doi:10.1016/0169-5347(94)90057-4

O’Brien S. J. 1994 The cheetah’s conservation controversy. Conservation Biology 8 1153 1155 doi:10.1046/j.1523-1739.1994.08041153.x

O’Brien S. J. Wildt D. E. Goldman D. Merril C. R. Mitchell B. 1983 The cheetah is depauperate in genetic variation. Science 221 459 462 doi:10.1126/science.221.4609.459

O’Grady J. J. Brook B. W. Reed D. H. Ballou J. D. Tonkyn D. W. Frankham R. 2006 Realistic levels of inbreeding depression strongly affect extinction risk in wild populations. Biological Conservation 133 42 51 doi:10.1016/j.biocon.2006.05.016

Olden J. D. Kennard M. J. Pusey B. J. 2008 Species invasions and the changing biogeography of Australian freshwater fishes. Global Ecology and Biogeography 17 25 37

Palomares F. Godoy J. A. Piriz A. O’Brien S. J. Johnson W. E. 2002 Faecal genetic analysis to determine the presence and distribution of elusive carnivores: design and feasibility for the Iberian lynx. Molecular Ecology 11 2171 2182
doi:10.1046/j.1365-294X.2002.01608.x

Palsboll P. J. Bérube M. Allendorf F. W. 2007 Identification of management units using population genetic data. Trends in Ecology & Evolution 22 11 16 doi:10.1016/j.tree.2006.09.003

Palumbi S. R. Cipriano F. J. 1998 Species identification using genetic tools: the value of nuclear and mitochondrial gene sequences in whale conservation. Heredity 89 459 464 doi:10.1093/jhered/89.5.459

Pearse A. M. Swift K. 2006 Transmission of devil facial-tumour disease – an uncanny similarity in the karyotype of these malignant tumours means that they could be infective. Nature 439 549 doi:10.1038/439549a

Quinn A. E. Georges A. Sarre S. D. Guarino F. Ezaz T. Graves J. A. M. 2007 Temperature sex reversal implies sex gene dosage in a reptile. Science 316 411 doi:10.1126/science.1135925

Reed D. H. Nicholas A. C. Stratton G. E. 2007 Genetic quality of individuals impacts population dynamics. Animal Conservation 10 275 283 doi:10.1111/j.1469-1795.2007.00120.x

Rollins L. A. Woolnough A. P. Sherwin W. B. 2006 Population genetic tools for pest management: a review. Wildlife Research 33 251 261 doi:10.1071/WR05106

Roman J. Bowen B. W. 2000 The mock turtle syndrome: genetic identification of turtle meat purchased in the southeast United States. Animal Conservation 3 61 65 doi:10.1111/j.1469-1795.2000.tb00087.x

Rudnick J. A. Katzner T. E. Bragin E. A. de Woody J. A. 2007 Species identification of birds through genetic analysis of naturally shed feathers. Molecular Ecology Notes 7 757 762 doi:10.1111/j.1471-8286.2007.01796.x

Saccheri I. Kuussaari M. Kankare M. Vikman P. Fortelius W. Hanski I. 1998 Inbreeding and extinction in a butterfly metapopulation. Nature 392 491 494 doi:10.1038/33136

Saunders G. , Lane C. , Harris S. , and Dickman C. (2006). Foxes in Tasmania: a report on the incursion of an invasive species. Unpublished report to Invasive Animals Cooperative Research Centre, Canberra.

Schoenwald-Cox C. , Chambers S. M. , MacBryde B. , and Thomas L. (Eds) (1983). ‘Genetics and Conservation: A Reference for Managing Wild Animal and Plant.’ (Benjamin/Cummings Publ. Co.: Menlo Park, CA.)

Seddon J. M. Parker H. G. Ostrander E. A. Ellegren H. 2005 SNPs in ecological and conservation studies: a test in the Scandinavian wolf population. Molecular Ecology 14 503 511 doi:10.1111/j.1365-294X.2005.02435.x

Selkoe K. A. Toonen R. J. 2006 Microsatellites for ecologists: a practical guide to using and evaluating microsatellite markers. Ecology Letters 9 615 629 doi:10.1111/j.1461-0248.2006.00889.x

Short J. Smith A. 1994 Mammal decline and recovery in Australia. Journal of Mammalogy 75 288 297 doi:10.2307/1382547

Siddle H. V. Kreiss A. Eldridge M. D. B. Noonan E. Clarke C. J. Pyecroft S. Woods G. M. Belov K. 2007 Transmission of a fatal clonal tumor by biting occurs due to depleted MHC diversity in a threatened carnivorous marsupial. Proceedings of the National Academy of Sciences of the United States of America 104 16221 16226 doi:10.1073/pnas.0704580104

Skerratt L. F. Berger L. Speare R. Cashins S. McDonald K. R. Phillott A. D. Hines H. B. Kenyon N. 2007 Spread of chytridiomycosis has caused the rapid global decline and extinction of frogs. EcoHealth 4 125 134 doi:10.1007/s10393-007-0093-5

Smith C. T. Templin W. D. Seeb J. E. Seeb U. W. 2005 Single nucleotide polymorphisms provide rapid and accurate estimates of the proportions of US and Canadian Chinook salmon caught in Yukon River fisheries. North American Journal of Fisheries Management 25 944 953 doi:10.1577/M04-143.1

Soulé M. E. (Ed.) (1987). ‘Viable Populations for Conservation.’ (Cambridge University Press: Cambridge.)

Spielman D. Brook B. W. Frankham R. 2004 Most species are not driven to extinction before genetic factors impact them. Proceedings of the National Academy of Sciences of the United States of America 101 15261 15264 doi:10.1073/pnas.0403809101

Stuart B. L. Parham J. F. 2006 Recent hybrid origin of three rare Chinese turtles. Conservation Genetics 8 169 175 doi:10.1007/s10592-006-9159-0

Sugimoto T. Nagata J. Aramilev V. V. Belozor A. Higashi S. McCullough D. R. 2006 Species and sex identification from faecal samples of sympatric carnivores, Amur leopard and Siberian tiger, in the Russian Far East. Conservation Genetics 7 799 802 doi:10.1007/s10592-005-9071-z

Sunnucks P. 2000 Efficient genetic markers for population biology. Trends in Ecology & Evolution 15 199 203 doi:10.1016/S0169-5347(00)01825-5

Sunnucks P. , and Taylor A. C. (2008). The application of genetic markers to landscape management. In ‘Landscape Analysis and Visualisation: Spatial Models for Natural Resource Management and Planning’. (Eds C. Pettit, W. Cartwright, I. Bishop, K. Lowell, D. Pullar and D. Duncan.) pp. 211–234. (Springer: Berlin.)

Taberlet P. Griffin S. Goossens B. Questiau S. Manceau V. Escaravage N. Waits L. P. Bouvet J. 1996 Reliable genotyping of samples with very low DNA quantities using PCR. Nucleic Acids Research 24 3189 3194 doi:10.1093/nar/24.16.3189

Taylor A. C. Sherwin W. B. Wayne R. K. 1994 Genetic variation of microsatellite loci in a bottlenecked species – the northern hairy-nosed wombat (Lasiorhinus krefftii). Molecular Ecology 3 277 290 doi:10.1111/j.1365-294X.1994.tb00068.x

Taylor S. S. Jamieson I. G. Armstrong D. P. 2005 Successful island reintroductions of New Zealand robins and saddlebacks with small numbers of founders. Animal Conservation 8 415 420 doi:10.1017/S1367943005002337

Thackway R. , and Cresswell I. D. (Ed.) (1995). ‘An Interim Biogeographic Regionalisation for Australia: A Framework for Establishing the National System of Reserves.’ (Australian National Conservation Agency: Canberra.)

Vos P. Hogers R. Bleeker M. Reijans M. Vandelee T., et al 1995 AFLP– a new technique for DNA-fingerprinting. Nucleic Acids Research 23 4407 4414 doi:10.1093/nar/23.21.4407

Waters J. M. Wallis G. P. 2000 Across the Southern Alps by river capture? Freshwater fish phylogeography in South Island, New Zealand. Molecular Ecology 9 1577 1582 doi:10.1046/j.1365-294x.2000. 01035.x

Weldon C. du Preez L. H. Hyatt A. D. Muller R. Speare R. 2004 Origin of the amphibian chytrid fungus. Emerging Infectious Diseases 10 2100 2105

Woodhams D. C. Rollins-Smith L. A. Alford R. A. Simon M. A. Harris R. N. 2007 a Innate immune defenses of amphibian skin: antimicrobial peptides and more. Animal Conservation 10 425 428
doi:10.1111/j.1469-1795.2007.00150.x

Woodhams D. C. Vredenburg V. T. Simon M. A. Billheimer D. Shakhtour B. Shyr Y. Briggs C. J. Rollins-Smith L. A. Harris R. N. 2007 b Symbiotic bacteria contribute to innate immune defenses of the threatened mountain yellow-legged frog, Rana muscosa. Biological Conservation 138 390 398 doi:10.1016/j.biocon.2007.05.004

Woods G. M. Kreiss A. Belov K. Siddle H. V. Obendorf D. L. Muller H. K. 2007 The immune response of the Tasmanian devil (Sarcophilus harrisii) and devil facial tumour disease. EcoHealth 4 338 345 doi:10.1007/s10393-007-0117-1

Yip P. Y. Chau C. F. Mak C. Y. Kwan H. S. 2007 DNA methods for identification of Chinese medicinal materials. Chinese Medicine 2 (9) Available online at http://www.cmjournal.org/content/2/1/9

Young T. Harcourt A. H. 1997 Viva Caughley! Conservation Biology 11 831 832 doi:10.1046/j.1523-1739.1997.011004831.x

Zhu D. Degnan S. Moritz C. 1998 Evolutionary distinctiveness and status of the endangered Lake Eacham rainbowfish (Melanotaenia eachamensis). Conservation Biology 12 80 93 doi:10.1046/j.1523-1739.1998.96330.x



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