Genetics in conservation management: Revised recommendations for the 50/500 rules, Red List criteria and population viability analyses

Biological Conservation

Volumn 170, Issue , 2014, Pages 56-63

  Frankham, Richard ^a,b   Bradshaw, Corey J A ^c   Brook, Barry W ^c  

^a MACQUARIE UNIVERSITY   (Australia)

^b AUSTRALIAN MUSEUM   (Australia)

^c UNIVERSITY OF ADELAIDE   (Australia)

Author keywords

Effective population size; Evolutionary potential; Fragmentation; Gene flow; Inbreeding depression; Minimum viable population size

Indexed keywords

BIODIVERSITY; CONSERVATION GENETICS; CONSERVATION MANAGEMENT; DECISION MAKING; EFFECTIVE POPULATION SIZE; GENE FLOW; HABITAT FRAGMENTATION; INBREEDING DEPRESSION; POPULATION VIABILITY ANALYSIS; RED LIST; RISK ASSESSMENT;

EID: 84893170385     PISSN: 00063207     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.biocon.2013.12.036     Document Type: Review

References (85)

1. Allendorf F.W., Ryman N. The role of genetics in population viability analysis. Population viability analysis 2002, 50-85. University of Chicago Press, Chicago. S.R. Beissinger, D.R. McCullough (Eds.).
2. Allendorf F.W., Luikart G., Aitken S.N. Conservation and the Genetics of Populations 2013, Wiley-Blackwell, Oxford. second ed.
3. Bataillon T., Kirkpatrick M. Inbreeding depression due to mildly deleterious mutations in finite populations: size does matter. Genet. Res. 2000, 75:75-81.
4. Brook B.W., Tonkyn D.W., O'Grady J.J., Frankham R. Contribution of inbreeding to extinction risk in threatened species. Conserv. Ecol. 2002, 6(1):16.
5. Brook B.W., Sodhi N.S., Bradshaw C.J.A. Synergies among extinction drivers under global change. Trends Ecol. Evol. 2008, 23:453-460.
6. Brook B.W., Bradshaw C.J.A., Traill L.W., Frankham R. Minimum viable population size: not magic, but necessary. Trends Ecol. Evol. 2011, 26:619-620.
7. Brosi B.J., Briggs H.M. Single pollinator species losses reduce floral fidelity and plant reproductive function. Proc. Natl. Acad. Sci. U.S.A. 2013, 110:13044-13048.
8. Bryant E.H., Backus V.L., Clark M.E., Reed D.H. Experimental tests of captive breeding for endangered species. Conserv. Biol. 1999, 13:1487-1496.
9. Bubb K.L., Bovee D., Buckley D., Haugen E., Kibukawa M., Paddock M., Palmerieri A., Subramanian S., Zhou Y., Kaul R., Green P., Olson M.V. Scan of human genome reveals no new loci under ancient balancing selection. Genetics 2006, 173:2165-2177.
10. Charlesworth B., Hughes K.A. The maintenance of genetic variation in life-history traits. Evolutionary Genetics: From Molecules to Morphology 2000, 369-392. Cambridge University Press, Cambridge. R.S. Singh, C.B. Krimbas (Eds.).
11. Charlesworth B., Miyo T., Borthwick H. Selection response of means and inbreeding depression for female fecundity in Drosophila melanogaster suggest contributions from intermediate-frequency alleles to quantitative trait variation. Genet. Res. 2007, 89:85-91.
12. Cowen R.K., Sponaugle S. Larval dispersal and marine population connectivity. Annu. Rev. Mar. Sci. 2009, 1:443-466.
13. Crnokrak P., Roff D.A. Inbreeding depression in the wild. Heredity 1999, 83:260-270.
14. Connectivity Conservation 2006, Cambridge University Press, New York. K.R. Crooks, M. Sanjayan (Eds.).
15. Dick C.W., Hardy O.J., Jones F.A., Petit R.J. Spatial scales of pollen and seed-mediated gene flow in tropical rain forest trees. Tropical Plant Biol. 2008, 1:20-33.
16. Dunlop E., Shuter B.J., Dieckmann U. Demographic and evolutionary consequences of selective mortality: predictions from an eco-genetic model for smallmouth bass. Trans. Am. Fish. Soc. 2007, 136:749-765.
17. Falconer D.S., Mackay T.F.C. Introduction to Quantitative Genetics 1996, Longman, Harlow, England. fourth ed.
18. Flather C.H., Hayward G.D., Beissinger S.R., Stephens P.A. Minimum viable populations: is there a 'magic number' for conservation practitioners?. Trends Ecol. Evol. 2011, 26:307-316.
19. Fox C.W., Reed D.H. Inbreeding depression increases with environmental stress: an experimental study and meta-analysis. Evolution 2010, 65:246-258.
20. Frankham R. Effective population size/adult population size ratios in wildlife: a review. Genet. Res. 1995, 66:95-107.
21. Frankham R. Relationship of genetic variation to population size in wildlife. Conserv. Biol. 1996, 10:1500-1508.
22. Frankham R. Genetics and extinction. Biol. Conserv. 2005, 126:131-140.
23. Frankham R. Genetic adaptation to captivity in species conservation programs. Mol. Ecol. 2008, 17:325-333.
24. Frankham R. Genetic architecture of reproductive fitness and its consequences. Adaptation and Fitness in Animal Populations: Evolutionary and Breeding Perspectives on Genetic Resource Management 2009, 15-39. Springer, Dordrecht. J. van der Werf, H.-U. Graser, R. Frankham, C. Gondro (Eds.).
25. Frankham R. How closely does genetic diversity in finite populations conform to predictions of neutral theory? Large deficits in regions of low recombination. Heredity 2012, 108:167-178.
26. Frankham R., Ballou J.D., Briscoe D.A. Introduction to Conservation Genetics 2010, Cambridge University Press, Cambridge, U.K. second ed.
27. Frankham R., Ballou J.D., Eldridge M.D.B., Lacy R.C., Ralls K., Dudash M.R., Fenster C.B. Predicting the probability of outbreeding depression. Conserv. Biol. 2011, 25:465-475.
28. Frankham R., Brook B.W., Bradshaw C.J.A., Traill L.W., Spielman D. 50/500 rule and minimum viable populations: response to Jamieson and Allendorf. Trends Ecol. Evol. 2013, 28:187-188.
29. Franklin I.R. Evolutionary change in small populations. Conservation Biology: An Evolutionary-Ecological Perspective 1980, 135-149. Sinauer, Sunderland, MA. M.E. Soulé, B.A. Wilcox (Eds.).
30. Gilbert B., Levine J.M. Plant invasions and extinction debts. Proc. Nat. Acad. Sci. U.S.A. 2013, 110:1744-1749.
31. Gilpin M.E., Soulé M.E. Minimum viable populations: processes of species extinction. Conservation Biology: An Evolutionary-Ecological Perspective 1986, 19-34. Sinauer, Sunderland, MA. M.E. Soulé, B.A. Wilcox (Eds.).
32. Grueber C.E., Laws R.J., Nakagawa S., Jamieson I.G. Inbreeding depression accumulation across life-history stages of the endangered takahe. Conserv. Biol. 2010, 24:1617-1625.
33. Hamrick J.L. Pollen and seed movement in disturbed tropical landscapes. Molecular Approaches in natural Resource Conservation and Management 2010, 190-211. Cambridge University Press, New York. J.A. DeWoody, J.W. Bickham, C. Michler, K. Nichols, D. Rhodes, K. Woeste (Eds.).
34. Hanski I., Alho J., Moilanen A. Estimating the parameters of survival and migration of individuals in metapopulations. Ecology 2000, 81:239-251.
35. Hedrick P.W. Lethals in finite populations. Evolution 2002, 56:654-657.
36. e/N ratio. Evolution 2005, 59:1596-1599.
37. Hedrick P.W. Genetic polymorphism in heterogeneous environments: the age of genomics. Annu. Rev. Ecol. Evol. Syst. 2006, 37:67-93.
38. Hedrick P.W. What is the evidence for heterozygote advantage selection?. Trends Ecol. Evol. 2012, 27:698-704.
39. Hereford J. A quantitative survey of local adaptation and fitness trade-offs. Amer. Nat. 2009, 173:579-588.
40. Houle D., Morikawa B., Lynch M. Comparing mutational variabilities. Genetics 1996, 143:1467-1483.
41. IUCN, 2013. IUCN Red List of Threatened Species. <>. http://www.redlist.org/.
42. Jamieson I.G., Allendorf F.W. How does the 50/500 rule apply to MVPs?. Trends Ecol. Evol. 2012, 27:578-584.
43. Jones G.P., Almany G.R., Russ G.R., Sale P.F., Steneck R.S., van Oppen M.J.H., Willis B.L. Larval retention and connectivity among populations of corals and reef fishes: history, advances and challenges. Coral Reefs 2009, 28:307-325.
44. Kuparinen A., Hutchings J.A. Consequences of fisheries-induced evolution for population productivity and recovery potential. Proc. Roy. Soc. Lond. B 2012, 279:2571-2579.
45. Lande R., Barrowclough G.F. Effective population size, genetic variation, and their use in population management. Viable Populations for Conservation 1987, 87-123. Cambridge University Press, Cambridge. M.E. Soulé (Ed.).
46. Latter B.D.H., Mulley J.C. Genetic adaptation to captivity and inbreeding depression in small laboratory populations of Drosophila melanogaster. Genetics 1995, 139:255-266.
47. Leroy G., Mary-Huard T., Verrier E., Danvy S., Charvolin E. Methods to estimate effective population size using pedigree data: examples in dog, sheep, cattle and horse. Genet. Sel. Evol. 2013, 45:1.
48. Lindsley D.L., Zimm G.G. The Genome of Drosophila melanogaster 1992, Academic Press, San Diego.
49. Luikart G., Ryman N., Tallmon D.A., Schwartz M.K., Allendorf F.W. Estimation of census and effective population sizes: the increasing usefulness of DNA-based approaches. Conserv. Genet. 2010, 11:355-373.
50. Mace G.M., Lande R. Assessing extinction threats: towards a reevaluation of IUCN threatened species categories. Conserv. Biol. 1991, 5:148-157.
51. Mace G.M., Collar N.J., Gaston K.J., Hilton-Taylor C., Akçakaya H.R., Leader-Williams N., Milner-Gulland E.J., Stewart S.N. Quantification of extinction risk: IUCN's system for classifying threatened species. Conserv. Biol. 2008, 22:1424-1442.
52. Mattila A.L.K., Duplouy A., Kirjokangas M., Lehtonen R., Rastas P., Hanski I. High genetic load in an old isolated butterfly population. Proc. Nat. Acad. Sci. U.S.A. 2012, 109:E2496-E2505.
53. McDonald-Madden E., Bode M., Game E.T., Grantham H., Possingham H.P. The need for speed: informed land acquisitions for conservation in a dynamic property market. Ecol. Lett. 2008, 11:1169-1177.
54. McNeely, J.A., Miller, K.R., Reid, W.V., Mittermeier, R.A., Werner, T.B., 1990. Conserving the World's Biological Diversity. IUCN, World Resources Institute, Conservation International, WWF-US and the World Bank, Washington, DC.
55. Mousseau T.A., Roff D.A. Natural selection and the heritability of fitness components. Heredity 1987, 59:181-197.
56. Nei M. The frequency distribution of lethal chromosomes in finite populations. Proc. Nat. Acad. Sci. U.S.A. 1968, 60:517-524.
57. Newman D., Pilson D. Increased probability of extinction due to decreased genetic effective population size: experimental populations of Clarkia pulchella. Evolution 1997, 51:354-362.
58. O'Grady J.J., Brook B.W., Reed D.H., Ballou J.D., Tonkyn D.W., Frankham R. Realistic levels of inbreeding depression strongly affect extinction risk in wild populations. Biol. Conserv. 2006, 133:42-51.
59. O'Grady J.J., Reed D.H., Brook B.W., Frankham R. Extinction risk scales better to generations than years. Anim. Conserv. 2008, 11:442-451.
60. Palstra F.P., Fraser D.J. Effective/census population size ratio estimation: a compendium and appraisal. Ecol. Evol. 2012, 2:2357-2365.
61. Palstra F.P., Ruzzante D.E. Genetic estimates of contemporary effective population size: what can they tell us about the importance of genetic stochasticity for wild population persistence?. Mol. Ecol. 2008, 17:3428-3447.
62. Perfeito L., Sousa A., Bataillon T., Gordo I. Rates of fitness decline and rebound suggest pervasive epistasis. Evolution 2013, 10.1111/evo.12234.
63. Piou C., Prévost E. A demo-genetic individual-based model for Atlantic salmon populations: model structure, parameterization and sensitivity. Ecol. Model. 2012, 231:37-52.
64. Pressey R.L., Bottrill M.C. Opportunism, threats, and the evolution of systematic conservation planning. Conserv. Biol. 2008, 22:1340-1345.
65. Prout T. How well does opposing selection maintain variation?. Evolutionary Genetics: From Molecules to Morphology 2000, 157-181. Cambridge University Press, New York. R.S. Singh, C.B. Krimbas (Eds.).
66. Reed D.H., Bryant E.H. Experimental test of minimum viable population size. Anim. Conserv. 2000, 3:7-14.
67. Reed T.E., Schindler D.E., Hague M.J., Patterson D.A., Meir E., Waples R.S., Hinch S.G. Time to evolve? Potential evolutionary responses of Fraser River sockeye salmon to climate change and effects on persistence. PLoS One 2011, 6(6):e20380.
68. Robertson A. Selection for heterozygotes in small populations. Genetics 1962, 47:1291-1300.
69. Rodríguez-Ramilo S.T., Pérez-Figuero A., Fernández B., Fernández J., Caballero A. Mutation-selection balance accounting for genetic variation for viability in Drosophila melanogaster as deduced from an inbreeding and artificial selection experiment. J. Evol. Biol. 2004, 17:528-541.
70. Roff D.A. The maintenance of phenotypic and genetic variation in threshold traits by frequency-dependent selection. J. Evol. Biol. 1998, 11:513-529.
71. Saccheri I., Kuussaari M., Kankare M., Vikman P., Fortelius W., Hanski I. Inbreeding and extinction in a butterfly metapopulation. Nature 1998, 392:491-494.
72. Shaffer M.K. Minimum viable populations size for species conservation. Bioscience 1981, 31:131-134.
73. Simmons M.J., Crow J.F. Mutations affecting fitness in Drosophila populations. Annu. Rev. Genet. 1977, 11:49-78.
74. Soulé M.E. Thresholds for survival: maintaining fitness and evolutionary potential. Conservation Biology: An Evolutionary-Ecological Perspective 1980, 151-169. Sinauer, Sunderland, MA. M.E. Soulé, B.A. Wilcox (Eds.).
75. Soulé M.E. What is conservation biology?. Bioscience 1985, 35:727-734.
76. Viable Populations for Conservation 1987, Cambridge University Press, Cambridge. M.E. Soulé (Ed.).
77. Spielman D., Brook B.W., Frankham R. Most species are not driven to extinction before genetic factors impact them. Proc. Nat. Acad. Sci. U.S.A. 2004, 101:15261-15264.
78. Traill L.W., Bradshaw C.J.A., Brook B.W. Minimum viable population size: a meta-analysis of 30years of published estimates. Biol. Conserv. 2007, 139:159-166.
79. Vilas C., Miguel E.S., Amaro R., Garcia C. Relative contribution of inbreeding depression and eroded adaptive diversity to extinction risk in small populations of shore campion. Conserv. Biol. 2006, 20:229-238.
80. e/N ratio. Mol. Ecol. 2002, 11:1029-1037.
81. Waples, R.S., Luikart, G., Faulkner, J.R., Tallmon, D.A., 2013. Simple life-history traits explain key effective population size ratios across diverse taxa. Proc. Roy. Soc. Lond. B 280, doi.org/10.1098/rspb.2013.1339.
82. White G.M., Boshier D.H., Powell W. Increased pollen flow counteracts fragmentation in a tropical dry forest: An example from Swietenia humilis Zaccarini. Proc. Nat. Acad. Sci. U.S.A. 2002, 99:2038-2042.
83. Woodworth L.M., Montgomery M.E., Briscoe D.A., Frankham R. Rapid genetic deterioration in captivity: causes and conservation implications. Conserv. Genet. 2002, 3:277-288.
84. Wright, S., 1969. Evolution and the Genetics of Populations. 2. The Theory of Gene Frequencies. University of Chicago Press, Chicago, IL.
85. Zeigler, S.L., Che-Castaldo, J.P., Neel, M.C., 2013. Actual and potential use of population viability analyses in recovery of plant species listed under the U.S. Endangered Species Act. Conserv. Biol. doi:10.1111/cobi.12130.