PerspectiveGenetics in conservation management: Revised recommendations for the 50/500 rules, Red List criteria and population viability analyses
Introduction
Conservation biology is a crisis discipline requiring urgent management for threatened species often with inadequate information (Soulé, 1985). As most species have inadequate information on which to base effective intervention decisions, conservation action is frequently opportunistic, seeking compromise under competing demands, and/or politically expediency (Pressey and Bottrill, 2008). For example, parcels of land offered for sale require that decisions to purchase for conservation must be made promptly (McDonald-Madden et al., 2008). Given limited resources and sparse information for most threatened species, scientific generalisations are often required. Some authors have criticised these (Flather et al., 2011), but the alternative is usually unscientific conservation decisions made at the political and bureaucratic levels, especially in poorer countries and for non-charismatic species (Brook et al., 2011).
The International Union for Conservation of Nature and Natural Resources (IUCN) recognises the need to conserve biodiversity at three level: genetic diversity, species and ecosystems (McNeely et al., 1990), with genetic issues being involved in all three (Frankham et al., 2010). We concentrate on the first two. Species are usually driven to extinction by a combination of systematic human-associated threats (habitat loss, over-exploitation, introduced species, pollution and climate change) and stochastic events associated with small population size (demographic, ecological and genetic stochasticity, and catastrophes) (Shaffer, 1981), typically interacting in a synergistic feedback (Brook et al., 2008) termed the ‘extinction vortex’ (Gilpin and Soulé, 1986). In this Perspective we focus on controversial aspects of genetic stochasticity (see Glossary in Appendix A1), primarily encompassing inbreeding depression, and reduced evolutionary potential (Frankham et al., 2010, Jamieson and Allendorf, 2012).
Inbreeding and loss of genetic diversity are unavoidable in small, closed, sexually reproducing populations, and accumulate in a ratchet-like manner over generations for diploid random-mating populations, as follows (Wright, 1969):where Ht is heterozygosity at generation t (for neutral variation), H0 initial heterozygosity, Ne genetically effective population size and F the inbreeding coefficient (with generation zero defined as having F = 0). In naturally outbreeding species, this typically results in inbreeding depression (unless they have already experienced it) and reduced ability to evolve (Frankham et al., 2010).
To work, generalizations depend on different taxa responding similarly, or at least groups of them doing so. While ecologists typically emphasise species distinctiveness (e.g. Flather et al., 2011), evolutionary and conservation geneticists usually focus on the similarity of evolutionary processes across species with similar breeding systems. For example, across most major taxa: (i) inbreeding has consistently deleterious effects on fitness in wild outbreeding diploid and polyploid species (Crnokrak and Roff, 1999), (ii) population mean genetic diversity, mean fitness and population size are positively correlated (Frankham, 2012), (iii) heritabilities (genetic variation as a proportion of phenotypic variation) are lower for fitness than for quantitative traits peripherally related to fitness (Mousseau and Roff, 1987, Falconer and Mackay, 1996), (iv) non-additive genetic variation is greater for fitness than peripheral traits (Frankham et al., 2010), and (v) mutation rates for quantitative characters are relatively similar (Houle et al., 1996). Consequently, generalisations are often justifiable for genetic issues in conservation biology (see also Appendix A2).
Our focus is on three genetic issues relating to generalisations. First, an effective population size of at least 50 (Franklin, 1980, Soulé, 1980) has been long recommended as a ‘rule’ for avoiding inbreeding depression in the short term. Second, Ne = 500 has been considered sufficient to retain evolutionary potential in perpetuity (Franklin, 1980, Lande and Barrowclough, 1987). These two issues had important roles in the development and implementation of the IUCN Red List categorisation system for threatened species (Mace et al., 2008), especially criterion C that relates to population size (Appendix A3). Third, minimum viable population sizes (MVP; Shaffer, 1981) provide estimates of the sizes required for species to persist with high probability in the long-term. Given that over 30 years have elapsed since the classic Ne = 50 and Ne = 500 recommendations were proposed, and their tenacity in conservation management circles, we now ask whether current evidence supports them, and how they might be modified. Jamieson and Allendorf (2012) reviewed these issues, but we reach different conclusions to them on several important issues.
We critique and make recommendations (Table 1) on (i) the Ne = 50 and 500 rules, (ii) how best to translate Ne into census population size (N), (iii) the genetic consequences of fragmented populations, and (iv) the treatment of genetic issues in PVA and their effect on estimation of MVPs. Finally, we (v) evaluate the implications of these for the IUCN Red List categorisation system.
Section snippets
Population size required to avoid inbreeding depression in the short term: Ne = 50?
Soulé (1980) and Franklin (1980) proposed Ne = 50 as sufficient to prevent inbreeding depression in naturally outbreeding diploid species in the short term, and most authors, including Jamieson and Allendorf (2012) still endorse this value. However, specifying the duration as ‘short term’ is too vague, because it can mean different things in different disciplines. Since Soulé and Franklin had ∼5 generations in mind (from discussions with RF), we recommend that 5 generations be used (because
Population size required to maintain evolutionary potential in perpetuity: Ne = 500?
Franklin (1980) argued that additive quantitative genetic variation (VA), rather than single-locus variation determined the ability to evolve. He concluded that Ne = 500 was sufficient to retain evolutionary potential in perpetuity, based on the equilibrium between adding genetic variation by mutation (Vm), and losing VA/(2Ne) per generation by random genetic drift for a quantitative trait that is either unaffected by selection or subject to stabilising selection (typical of peripheral
Extrapolating from effective (Ne) to census (N) population sizes
Ne discussed above need to be converted into mean (adult) census population sizes (N) per generation for conservation managers. Information on the Ne/N ratio is required for this conversion, but comprehensive estimates that encompass all relevant variables are only available for ∼100 species (Frankham, 1995, Palstra and Ruzzante, 2008, Palstra and Fraser, 2012). Accordingly, most conversions have been based on average Ne/N (0.10–0.14; Frankham, 1995, Palstra and Ruzzante, 2008). Palstra and
Fragmented populations and connectivity
So far, we have considered only single, approximately random-mating closed populations. However, free-ranging wild species usually have fragmented distributions, with population structures varying from effectively single random-mating populations (fragmented spatially, but connected by gene flow), through partially connected fragments and meta-populations, to completely isolated subpopulations; each circumstance has different genetic consequences in relation to genotype frequencies, genetic
How well is genetics incorporated into PVAs and MVPs?
Minimum viable population (MVP) sizes required for long-term population persistence are commonly determined using population viability analysis (PVA) simulation models (Traill et al., 2007). Ideally these models should include all systematic and stochastic variables potentially affecting population viability. But how much is genetics considered in most PVAs?
There is now extensive evidence that genetic factors influence extinction risk (Frankham, 2005, Frankham et al., 2010, Allendorf et al.,
Relationships between Ne = 100, Ne = 1000, MVP and IUCN Red List criteria
MVPs identify populations that are relatively safe from all threats. If available and based on adequate data, a species-specific PVA is the most comprehensive guide to the likely persistence for a species, or population. If this is not available, or a PVA yields results of doubtful validity, or a species falls into the Data Deficient category of the IUCN Red List, then Ne ⩽ 100 indicates that it likely faces serious genetic threats after 5 or more generations, whereas Ne ⩾ 1000 indicates little or
Conclusions
Based on our review of recent theoretical and empirical evidence, we conclude that the oft-cited Ne = 50 rule for avoiding (minimising) inbreeding depression in the short-term (5 generations), and Ne = 500 proposed for maintaining evolutionary potential in perpetuity, need to be at least doubled, as do the genetically derived IUCN Red List population-size thresholds for Criterion C. Further, population viability analyses need to incorporate more realistic genetic risks by routinely including
Acknowledgments
We thank G. Cooke, M. Eldridge, C. Fenster, I. Franklin, P. Hedrick, W. Hill, A. Hoffmann, C. Lees, G. Mace, D. Spielman, M. Soulé, Y. Willi and five anonymous reviewers for comments on the manuscript. C.J.A.B. and B.W.B. are supported by Australian Research Council Future Fellowships.
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