50/500 or 100/1000 debate not about time frame

26 06 2014

Not enough individualsAs you might recall, Dick Frankham, Barry Brook and I recently wrote a review in Biological Conservation challenging the status quo regarding the famous 50/500 ‘rule’ in conservation management (effective population size [Ne] = 50 to avoid inbreeding depression in the short-term, and Ne = 500 to retain the ability to evolve in perpetuity). Well, it inevitably led to some comments arising in the same journal, but we were only permitted by Biological Conservation to respond to one of them. In our opinion, the other comment was just as problematic, and only further muddied the waters, so it too required a response. In a first for me, we have therefore decided to publish our response on the arXiv pre-print server as well as here on ConservationBytes.com.

50/500 or 100/1000 debate is not about the time frame – Reply to Rosenfeld

cite as: Frankham, R, Bradshaw CJA, Brook BW. 2014. 50/500 or 100/1000 debate is not about the time frame – Reply to Rosenfeld. arXiv: 1406.6424 [q-bio.PE] 25 June 2014.

The Letter from Rosenfeld (2014) in response to Jamieson and Allendorf (2012) and Frankham et al. (2014) and related papers is misleading in places and requires clarification and correction, as follows:

  1. “Census population size (the MVP) may be anywhere from 5 to 10 times the effective population size”: this is far too low for highly fecund species, such as fish where it is typically 1000 or more (Palstra & Ruzzante 2008; Frankham et al. 2014).
  2. “Frankham and associates … goals focus on recovery targets needed for long-term persistence in perpetuity, rather than short-term prevention of extinction…”: Incorrect: the Ne = 50 (or 100) that is a major focus of our paper (including in the title) deals explicitly with avoiding inbreeding depression in the short-term and thus avoiding immediate extinctions. Furthermore, the five-generations duration we recommend is most definitely ‘short-term’. Frankham and colleagues have also done many laboratory and modelling experiments on inbreeding and extinction and reviewed the field several times, concluding that the inbreeding avoidance we recommend applies to short-term management time frames (see Frankham 2005; Frankham et al. 2010 for references).
  3. “Frankham et al. (2014) do not appear to dispute the case made by Jamieson and Allendorf (2012) that most endangered species are rapidly declining as a consequence of human impacts … that increase mortality and that the effects of inbreeding and reduced evolutionary potential are secondary.”: this is misleading; some are, but typically it is a synergy of deterministic and stochastic effects (including genetic ones) that cannot be arbitrarily disentangled, as established by several independent approaches (described and referenced in Frankham et al. 2014). First, population viability analyses for many real, threatened species revealed that inclusion of inbreeding depression in stochastic-demographic models resulted in median reductions of 30-40% in median times to extinction – such reductions are clearly not “secondary” (Brook et al. 2002; O’Grady et al. 2006). Second, the related view that other factors typically drive species to extinction before genetic factors can impact them has been refuted, based on > 170 comparisons of genetic diversity in threatened and closely related non-threatened species (Spielman et al. 2004; Evans & Sheldon 2008; Flight 2010). Third, empirical field studies, where relative contributions could be partitioned, have also demonstrated large effects of inbreeding and loss of genetic diversity on extinction risk (Newman & Pilson 1997; Saccheri et al. 1998; Nieminenet al. 2001; Vilas et al. 2006). Fourth, gene flow into inbred populations with low genetic diversity typically leads to large genetic rescue effects on fitness, especially in natural outbreeding species (Tallmon et al. 2004; Frankham, unpublished data). Fifth, small populations of self-incompatible species with so few S alleles that they are functionally extinct become capable of sexual reproduction when outcrossing adds new S alleles, as observed in the Illinois population of the Lakeside daisy and in Florida ziziphus (DeMauro 1993; Weekley et al. 2002; Gitzendanner et al. 2012).
  4. “… much of this debate concerns the time scale over which to plan for recovery and persistence … rather than the science”: while there are substantial areas of agreement between the groups, Jamieson and Allendorf disagree with our revision from 50/500 to 100/1000 (Franklin et al. 2014).
  5. “However, long-term PVAs that account for evolutionary potential are not at all incompatible with PVAs over shorter time horizons that identify priority threats to persistence and interim recovery targets.” We did not say otherwise.
  6. Neither our paper, nor our previous work related to the issue (e.g., Traill et al. 2010) “… implicitly link long-term MVPs in the thousands to a triage approach that may explicitly write off extremely rare species that are costly to recover”, as suggested by Jamieson and Allendorf (2012) and repeated by Rosenfeld (2014). Frankham et al. (2014) did not discuss triage, which is essentially “smart decision making” (Bottrill et al. 2008).
  7. Finally, framing the question of short- or long-term management of extinction risk as mutually exclusive goals is moot if the ultimate outcome is extinction. Separating the two time frames is therefore fallacious.


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Brook, B.W., Tonkyn, D.W., O’Grady, J.J., Frankham, R., 2002. Contribution of inbreeding to extinction risk in threatened  species. Conservation Ecology 6(1), 16. www.consecol.org/vol16/iss11/art16.

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Evans, S.R., Sheldon, B.C., 2008. Interspecific patterns of genetic diversity in birds: correlations with extinction risk. Conservation Biology 22, 1016-1025. doi:10.1111/j.1523-1739.2008.00972.x

Flight, P.A., 2010. Phylogenetic comparative methods strengthen evidence for reduced genetic diversity among endangered tetrapods. Conservation Biology 24, 1307-1315. doi:10.1111/j.1523-1739.2010.01498.x

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

Frankham, R., Ballou, J.D., Briscoe, D.A., 2010. Introduction to Conservation Genetics, 2nd edition. Cambridge University Press, Cambridge, U.K.

Frankham, R., Bradshaw, C.J.A., Brook, B.W., 2014. Genetics in conservation management: revised recommendations for the 50/500 rules, Red List criteria and population viability analyses. Biological Conservation 170, 56-63. doi:10.1016/j.biocon.2013.12.036

Franklin, I.R., Allendorf, F.W., Jamieson, I.G., 2014. The 50/500 rule is still valid – Reply to Frankham et al. Biological Conservation. doi:10.1016/j.biocon.2014.05.004

Gitzendanner, M.A., Weekley, C.W., Germain-Aubrey, C.C., Soltis, D.E., Soltis, P.S., 2012. Microsatellite evidence for high clonality and limited genetic diversity in Ziziphus celata (Rhamnaceae), an endangered, self-incompatible shrub endemic to the Lake Wales Ridge, Florida, USA. Conservation Genetics 13, 223-234. doi:10.1007/s10592-011-0287-9

Jamieson, I.G., Allendorf, F.W., 2012. How does the 50/500 rule apply to MVPs? Trends in Ecology and Evolution 27, 578-584. doi:10.1016/j.tree.2012.07.001

Newman, D., Pilson, D., 1997. Increased probability of extinction due to decreased genetic effective population size: experimental populations of Clarkia pulchella. Evolution 51, 354-362. doi:10.2307/2411107

Nieminen, M., Singer, M.C., Fortelius, W., Schöps, K., Hanksi, I., 2001. Experimental confirmation that inbreeding depression increases extinction risk in butterfly populations. American Naturalist 157, 237-244. doi:10.1086/318630

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

Palstra, F.P., Ruzzante, D.E., 2008. Genetic estimates of contemporary effective population size: what can they tell us about the importance of genetic stochasticity for wild population persistence? Molecular Ecology 17, 3428-3447.doi:10.1111/j.1365-294X.2008.03842.x

Rosenfeld, J.S., 50/500 or 100/1000? Reconciling short- and long-term recovery targets and MVPs. Biological Conservation. doi:10.1016/j.biocon.2014.05.005

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

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 USA 101, 15261-15264.doi:10.1073/pnas.0403809101

Tallmon, D.A., Luikart, G., Waples, R.S., 2004. The alluring simplicity and the complex reality of genetic rescue. Trends in Ecology and Evolution 19, 489-496. doi:10.1016/j.tree.2004.07.003

Traill, L.W., Brook, B.W., Frankham, R., Bradshaw, C.J.A., 2010. Pragmatic population viability targets in a rapidly changing world. Biological Conservation 143, 28-34.doi:10.1016/j.biocon.2009.09.001

Vilas, C., Miguel, E.S., Amaro, R., Garcia, C., 2006. Relative contribution of inbreeding depression and eroded adaptive diversity to extinction risk in small populations of shore campion. Conservation Biology 20, 229-238.doi:10.1111/j.1523-1739.2005.00275.x

Weekley, C.W., Kubisiak, T.L., Race, T.M., 2002. Genetic impoverishment and cross-incompatibility in remnant genotypes of Ziziphus celata (Rhamnaceae), a rare shrub endemic to the Lake Wales Ridge, Florida. Biodiversity and Conservation 11, 2027-2046. doi:10.1023/A:1020810800820



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