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Genetic stochasticity, mean fitness of individuals and population dynamics

Keller, Biebach & Hoeck (2007) and McGowan, Wright & Hunt (2007) both emphasize the need for further research aimed at gaining a greater understanding of the relationship between inbreeding levels and population dynamics, as well as the implications of that relationship for conservation efforts. We fully agree with them that further study is needed and we thank them for their kind words suggesting that our research (Reed, Nicholas & Stratton, 2007a) is an excellent step towards a better understanding of how genetic factors interact with the environment to influence the risk of extinction in wild populations. Our data suggest that inbreeding stress interactions lower the mean fitness of individuals in more inbred populations, exacerbating the dangerous part of population fluctuations and increasing the risk of extinction. It has been demonstrated that smaller populations, as indicated through estimates of decreased genetic variation or through direct counts of individuals, have decreased values for numerous components of fitness relative to larger populations (Reed & Frankham, 2003; Reed, 2005, 2007). This is not surprising as population size and breeding structure influence fitness through several mechanisms: efficiency of selection, inbreeding depression, fixation of deleterious alleles and the loss of potentially adaptive alleles through drift, and the input of beneficial mutations (Reed, 2005, 2007). In the populations of spiders used in this study, we demonstrated directly that fecundity is lower in smaller populations (Reed, Nicholas & Stratton, 2007b) and, therefore, the potential growth rate is lower. We purposely shied away from using the terms inbreeding depression and random genetic drift, even though it seems obvious that is what is going on. Instead we used the term genetic quality. The term is not nebulous and does not rely on comparing individuals to some local optimum as stated by Brodie (2007). We define genetic quality precisely as a decrease in the mean fitness of an individual and fitness is measured relative to the other populations in the study. We chose this term specifically because, in practical terms, that is what matters to the central question we sought to answer: Does reduced mean fitness of individuals lead to changes in population dynamics that make those populations more vulnerable to extinction despite density-dependent mortality? The fact that the fate of alleles is more stochastic in smaller populations means that, all else being equal, smaller populations will be composed of individuals of lower average genetic quality. Brodie (2007) suggests that it is important to distinguish inbreeding from loss of genetic diversity. In our data, expected and observed heterozygosity are both excellent predictors of population fitness and the correlation between them is extremely high (r=0.99). It makes no difference which of these two variables is used in the models. Thus, whatever nonrandom mating is occurring within populations, it is almost identical among populations. The statistical techniques we used can only differentiate among independent variables that differ among populations; hence, we cannot comment on the effects of nonrandom mating on fitness in these populations. However, we can say that the differences in expected heterozygosity among these populations are almost certainly due to differential amounts of random genetic drift and therefore the differences in fitness are also due mostly to drift. Allelic richness, on the other hand, is a rather poor predictor of population fitness relative to expected heterozygosity levels (Table 1). Some believe that allelic richness is very important for the evolutionary potential of populations because the limit of selection response, over time frames where mutation is negligible, may be determined by the initial number of alleles (James, 1971; Hill & Rasbash, 1986). Nonetheless, because the rare alleles are mostly deleterious, it is not surprising that allelic richness is strongly correlated with expected heterozygosity (r=0.95), but that expected heterozygosity has much stronger support than models using allelic richness. Brodie (2007) also suggests that the most important aspect of many real-world conservation problems is the