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Quantitative Genetics in Conservation Biology

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Quantitative Genetics in Conservation Biology Genet. Res., Camb.(1999), 74, pp. 237–244. Printed in the United Kingdom # 1999 Cambridge University Press 237 Quantitative genetics in conservation biology RICHARD FRANKHAM* Key Centre for Biodiersity and Bioresources, Department of Biological Sciences, Macquarie Uniersity, NSW 2109, Australia (Receied 29 March 1999 and in reised form 18 June 1999) Summary Most of the major genetic concerns in conservation biology, including inbreeding depression, loss of evolutionary potential, genetic adaptation to captivity and outbreeding depression, involve quantitative genetics. Small population size leads to inbreeding and loss of genetic diversity and so increases extinction risk. Captive populations of endangered species are managed to maximize the retention of genetic diversity by minimizing kinship, with subsidiary efforts to minimize inbreeding. There is growing evidence that genetic adaptation to captivity is a major issue in the genetic management of captive populations of endangered species as it reduces reproductive fitness when captive populations are reintroduced into the wild. This problem is not currently addressed, but it can be alleviated by deliberately fragmenting captive populations, with occasional exchange of immigrants to avoid excessive inbreeding. The extent and importance of outbreeding depression is a matter of controversy. Currently, an extremely cautious approach is taken to mixing populations. However, this cannot continue if fragmented populations are to be adequately managed to minimize extinctions. Most genetic management recommendations for endangered species arise directly, or indirectly, from quantitative genetic considerations. threatened (critically endangered, endangered or vul- 1. Loss of biodiversity nerable) (IUCN, 1996; Primack, 1998). Projected The biological diversity of the planet is rapidly being extinction rates per decade, based on a range of depleted due to loss of habitat, overexploitation, different methods, range from 1–5%to8–11% introduced species and pollution. A large but unknown (World Conservation Monitoring Centre, 1992). All number of species have gone to extinction, and many reputable conservation authorities project major fu- others have been reduced to the point where they ture extinctions. require benign human intervention to save them from Loss of habitat is currently the most important extinction (World Conservation Monitoring Centre, factor causing loss of biodiversity, but global climate 1992; Lawton & May, 1995). change due to pollution may overtake it in the future. There have been almost 900 recorded extinctions At small population size, additional stochastic factors since 1600, the majority being of island forms (see (demographic, environmental, catastrophic and gen- Primack, 1998). The rate of extinctions has generally etic) come into play and accelerate the decline to increased over time (Smith et al., 1993). Many other extinction. These stochastic factors operate in a species have gone extinct due to habitat loss before negative feedback leading species to spiral downwards they were described. towards extinction (‘the extinction vortex’). The scale of current threat is immense. Of all species, 25% of mammals, 11% of birds, 20% of reptiles, 25% of amphibians, 34% of fish, 32% of 2. What is an endangered species? gymnosperms and 9% of angiosperms are listed as Mace & Lande (1991) defined objective criteria for classifying species as in danger of extinction, based on * e-mail: rfrankha!RNA.bio.mq.edu.au population biology principles. They defined endanger- Downloaded from https://www.cambridge.org/core. IP address: 170.106.202.8, on 23 Sep 2021 at 19:38:47, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.1017/S001667239900405X R. Frankham 238 ment as a high probability of extinction in a short 4. Relationship between genetics and extinctions time. For example, critically endangered was defined as having at least a 50% probability of extinction The assumption underlying genetic concerns in con- within 10 years, or three generations, whichever is the servation biology is that inbreeding and loss of genetic longer. diversity increase the risk of extinction (Frankel & Surrogate measures were devised to classify species Soule! , 1981). While this is a logical extension from into these categories; these were based on population observed effects of inbreeding on reproductive fitness decline, area of occupancy, population size and and impacts of reduced genetic diversity on ability to decline, or population size alone. One of the criteria evolve, direct evidence has been limited and the issue was clearly influenced by genetic considerations. is controversial. In a highly influential paper, Lande Effective population sizes of less than 50, 500 or 2000 (1988) argued that random demographic and en- were involved in critically endangered, endangered vironmental events would drive small wild populations and vulnerable classifications, respectively. When to extinction before genetic factors came into play (see translating these to actual census sizes, a Ne\N ratio also Caro & Laurenson, 1994; Caughley, 1994). of 0n2 was assumed. With revision, these principles Do genetic problems contribute to the endanger- formed the basis of revised IUCN (the World ment and extinction of wild populations? Inbreeding Conservation Union) categories of risk (IUCN, 1994, has been shown to increase extinction rates in 1996). laboratory populations of Drosophila and mice under conditions where non-genetic factors could be excluded (Frankham, 1995b). Further, simulation 3. Genetic concerns in conservation biology studies by Mills & Smouse (1994) have shown that Sir Otto Frankel was largely responsible for the genetic factors are likely to contribute to extinctions recognition of genetic factors in conservation biology even when demographic and environmental sto- (Frankel, 1970, 1974; Frankel & Soule! , 1981). Frankel chasticity and catastrophes are operating. Saccheri et was also a major figure in efforts to conserve genetic al.(1998) provided direct evidence for the involvement diversity for crop plants (see Frankel et al., 1995). of inbreeding and genetic diversity in extinctions of The concerns of Frankel and others have led to the wild butterfly populations in Finland. identification of nine major genetic issues in con- Several indirect lines of evidence indicate that the servation biology (Frankham, 1995a): butterfly results are likely to apply to other species (Frankham & Ralls, 1998). Genetics may contribute (1) Inbreeding depression affecting reproductive to the extinction proneness of island populations. fitness. Island populations have lower genetic diversity than (2) Loss of genetic diversity reducing the ability of mainland populations (Frankham, 1997) and many species to adapt in response to environmental are inbred to levels where captive populations show change. elevated extinction risk from inbreeding (Frankham, (3) Fragmentation of populations and reduction in 1998). Notably, endemic island populations that are migration. more prone to extinction than non-endemic popu- (4) Accumulation and loss of deleterious mutations. lations have lower genetic diversity and higher (5) Genetic adaptation to captivity and its adverse inbreeding levels than non-endemic populations. Since effects on reintroduction success. there are no demographic or environmental reasons to (6) Outbreeding depression. predict higher extinction rates in endemic than non- (7) Taxonomic uncertainties. endemic island populations, genetic factors, or their (8) Use of genetics to understand aspects of species interaction with environmental and demographic biology important to conservation. stochasticity are probably involved in the differences (9) Use of genetic markers in forensics. in extinction rates. The first six of these involve primarily, or solely, Ratios of effective to census population sizes average quantitative genetics. Even the resolution of taxo- only 0n11, much lower than previously suspected nomic uncertainties involves inferences about the (Frankham, 1995c). Consequently, genetic concerns probable fitness of crosses between populations. become important at larger population sizes than IUCN, the premier international conservation previously believed. A majority of endangered species body, has recognized the importance of genetic issues have lower genetic diversity than non-endangered in conservation. They have designated genetic di- species (Frankham, 1995a; Haig & Avise, 1996), versity, along with species diversity and ecosystem which would not be expected if ecological factors diversity, as requiring conservation (McNeely et al., drove populations to extinction before genetic factors 1990). Genetics contributes not only to the con- became important. Experimental populations of a servation of genetic diversity, but also to the con- wild plant with reduced genetic variation showed servation of species. higher extinction rates than populations with normal Downloaded from https://www.cambridge.org/core. IP address: 170.106.202.8, on 23 Sep 2021 at 19:38:47, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.1017/S001667239900405X Quantitatie genetics in conseration biology 239 levels when both were planted in the field(Newman & regime designed to adapt endangered species to Pilson, 1997). Finally, genetic factors appear to be tolerate inbreeding was devised by Templeton & Read implicated in declines
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