ReviewGenetics and extinction
Introduction
There is ongoing controversy about the importance of genetic factors in extinction risk. Biological extinctions are due to the combined effects of deterministic (habitat loss, over exploitation, introduced species and pollution) and stochastic (demographic, environmental, genetic and catastrophic) factors (Shaffer, 1981). Prior to 1970, genetic factors were rarely mentioned as causes of extinction. Frankel, 1970, Frankel, 1974 was primarily responsible for proposing that loss of genetic diversity elevated extinction risk, especially by compromising evolutionary response to environmental change. Frankel and Soulé (1981) added the deleterious effects of inbreeding to the argument, and they presumed that genetic factors had an important role in causing extinctions. Later, the issue of mutation accumulation was introduced by Lande (1995) and Lynch et al. (1995). Outbreeding between diverged populations may also lead to deleterious effects on reproductive fitness (outbreeding depression), but its effects are clearly less important overall than that of inbreeding depression (Frankham et al., 2002). It is most probable when populations that are highly differentiated genetically are crossed. I will not consider this issue in detail here.
Genetic factors affect extinction risk because threatened species have small and/or declining populations (IUCN, 2004), and in such populations inbreeding and loss of genetic diversity are unavoidable (Frankham et al., 2002). The relationships between population size, loss of genetic diversity and inbreeding in closed random mating populations are described by the following equation:where Ht is heterozygosity (Hardy–Weinberg expected heterozygosity, or gene diversity) at generation t, H0 initial heterozygosity, Ne the genetically effective population size and F the inbreeding coefficient. Since the middle term in the equation is approximately this equation predicts an exponential decay of genetic diversity with generations that occurs at greater rates in smaller than larger populations (Fig. 1). The inbreeding coefficient equals the proportionate loss of genetic diversity. The rate of decay in genetic diversity and the increase in inbreeding depend upon the genetically effective population size, rather than the actual or census size. The effective size is typically much smaller than the number of potentially breeding adults in populations, averaging an order of magnitude lower than census population sizes (Frankham, 1995a).
A major controversy erupted over the role of genetic factors in extinction risk following Lande, 1988) paper in Science. He was interpreted as saying that most species are driven to extinction before genetic factors have time to impact them (the ‘Lande scenario’; Pimm, 1991, Young, 1991, Wilson, 1992, Caro and Laurenson, 1994, Caughley, 1994, Dobson, 1999, Elgar and Clode, 2001). The effectiveness of natural selection in reducing the frequency of the deleterious alleles (purging) that cause inbreeding depression has been an important part of this controversy (Lande, 1988, Hedrick, 1994).
A second controversy about the impact of inbreeding on reproductive fitness began in the late 1970s in relation to captive animals (see Ralls et al., 1979), and in the 1990s spread to scepticism about whether inbreeding depression affected species in wild habitats (see Caro and Laurenson, 1994, Caughley, 1994, Craig, 1994, Merola, 1994). A third controversy has erupted concerning the role of mutation accumulation in extinction risk for sexually reproducing species (Charlesworth et al., 1993, Lande, 1995, Lynch et al., 1995).
The purpose of this review is to examine evidence on the impacts of inbreeding depression, loss of genetic diversity and mutational accumulation on extinction risk.
Section snippets
Effects of inbreeding on fitness in outbreeding species
Inbreeding has long been known to reduce reproduction and survival in naturally outbreeding species (inbreeding depression). Darwin (1876) provided the first compelling evidence on this, based on comparisons of the progeny of self and cross-fertilization in 57 species of plants. Selfing reduced seed production by an average of 41% and height by 13%. Not all species showed inbreeding depression for all characters studied, but virtually all showed it for most reproductive fitness characters.
Loss of evolutionary potential
Loss of genetic diversity in small populations is expected to increase extinction risk by adversely affecting the ability of populations to evolve to cope with environmental change (evolutionary potential). Environmental change is experienced by essentially all species, whether it be due to global climate change, new or changed diseases, pests and parasites, new predators, climatic cycles, etc. (Frankham and Kingslover, 2004). Evolutionary changes have been documented in many species in natural
Mutation accumulation and meltdown
In large populations, deleterious alleles are kept at low frequencies due to the balance between mutation and natural selection. However, in small populations, selection is less effective and mildly deleterious alleles become selectively neutral, with their fate being determined by genetic drift (Lande, 1995, Lynch et al., 1995). Consequently, some of these mildly deleterious alleles increase in frequency and reduce reproductive fitness. Over long time spans, sufficient alleles could drift to
Consequences of ignoring genetic factors
There is compelling evidence that inbreeding and loss of genetic variation contribute to extinction risk in captive populations, very strong evidence that they contribute in wild populations in nature, and evidence that most species are not driven to extinction before genetic factors impact them, as documented above. Thus, there is sufficient evidence to consider the controversies regarding the contribution of genetic factors to extinction risk as resolved.
However, does this matter in the
Future directions
There are several areas where essential information is lacking, or controversial, or limited in scope, as follows:
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There is a great need for information on the impact of genetic factors on extinction risk for taxa that regularly inbreed or are asexual, haplo-diploid or polyploid.
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There is a need for much more information on the extent of inbreeding depression for the full life cycle for a broad range of outbreeding taxa in the wild. Additional information is required on the impacts of inbreeding
Conclusions
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Inbreeding and loss of genetic diversity contribute to extinction risk in small laboratory populations.
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Inbreeding depression contributes to extinction risk in most wild populations of naturally outbreeding species and loss of genetic diversity is expected to contribute in the long-term.
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Ignoring genetic factors may lead to inappropriate recovery strategies.
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Any study of extinction risk or minimum viable population sizes that excludes genetic factors will underestimate the true threat.
Acknowledgements
This manuscript is based upon my presentation at the Okazaki Biological Conference on the Biology of Extinction in January 2004. I thank Yoh Iwasa and Stuart Pimm for inviting me, the National Institute for Basic Biology, Okazaki, Japan for travel funds, and Barry Brook and Julian O’Grady for comments on the manuscript. The research from my laboratory has been funded by Australian Research Council and Macquarie University Research grants. This is publications number 410 of the Key Centre for
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