Population size is not genetic quality

Abstract

Inbreeding depression is a phenomenon largely taken for granted among evolutionary geneticists (Conner & Hartl, 2004). For conservation biologists, the most important source of inbreeding comes when small population size leads to nonrandom mating among genotypes, either because available mates are related or because drift has reduced heterozygosity. Either process leads to the over-expression of homozygotes throughout the genome. Because many of the resultant homozygotes will express deleterious phenotypes, inbreeding is expected to widely lead to reductions in phenotypic values and fitness for individuals spawned from such unions. Inbreeding itself does not lead to reductions in allelic diversity. Rather, it enables selection to more effectively weed out deleterious recessives, and linkage disequilibrium drags along alleles at linked loci, so that over time we often see declining genetic diversity in inbreeding populations. On the whole, populations with measurable inbreeding are predicted to have lower average fitness than comparable populations with random mating (i.e. ‘inbreeding depression’), because of the expression of deleterious homozygotes rather than secondarily reduced allelic diversity (Conner & Hartl, 2004). Inbreeding level is variable; it may be severe, as when populations are so small so as to necessitate mating among close relatives, or may be subtle in any situation that results in a nonrandom association of mates. Thus, even populations of moderate, but not effectively infinite, size may experience some of the deleterious effects of inbreeding. It seems obvious, then, that inbreeding is not a good thing for most populations (though there are certainly many taxa, especially plants, that make due with high levels of inbreeding). If inbreeding reduces fitness, should not we expect inbreeding to be one of the many factors that hasten the demise of declining populations? As Reed, Nicholas & Stratton (2007a,b) point out, the causal relationship between inbreeding and extinction risk is not clear. In extremely small populations, the very ones expected to be highly inbred, realities of demography and stochasticity are expected to blink out a population before inbreeding can make its mark (Lande, 1988). In somewhat larger populations, density-dependent mortality might lead to situations in which population dynamics are largely unaffected by the level of inbreeding. In such cases, inbreeding might correlate with, but not contribute to, population growth (or decline) rates. It is exactly these kinds of populations – declining, but not perilously small – for which management decisions have a reasonable chance of protecting both the numbers of a species and its genetic potential. Reed et al. (2007a) set out to test whether genetic diversity and inbreeding have measurable impacts on population dynamics of two species of wolf spiders across a range of population sizes. Using a 3-year dataset that they recently published in Conservation Genetics (Reed et al., 2007b), they analyze a new independent variable, population growth, to discern whether inbreeding or genetic quality impacts population dynamics. Their analyses clearly show that habitat quality (as measured by prey capture rate) and population size impacts population growth rate. The effect of population size is most obvious (and significant) in years with low prey capture rate, leading the authors to the conclusion that inbreeding (or ‘genetic quality,’ or ‘genetic diversity’) impacts population dynamics under stressful situations. As a generality, I agree with the expectation that genetic factors will have negative effects on population growth, especially under stressful conditions. However, I found myself questioning whether this impressive dataset and analysis demonstrate such links. Moreover, I think it is critical to distinguish different genetic phenomena, their origins and their expected consequences. Inbreeding might affect population growth rate through at least two distinct paths. For populations with little history of inbreeding and thus a wealth of deleterious recessives, inbreeding depression is expected to lower mean fitness (for populations with a history of inbreeding, as with many plant breeding systems, past selection would have reduced the number of deleterious recessives so that inbreeding depression is less marked). Inbreeding depression might also result from a reduction of heterozygosity at overdominant loci (Conner & Hartl, 2004). This reduction in mean fitness should lead to declines in the population growth rate unless density-dependent mortality results in