Inbreeding rate modifies the dynamics of genetic load in small populations

Abstract

The negative fitness consequences of close inbreeding are widely recognized, but predicting the long-term effects of inbreeding and genetic drift due to limited population size is not straightforward. As the frequency and homozygosity of recessive deleterious alleles increase, selection can remove (purge) them from a population, reducing the genetic load. At the same time, small population size relaxes selection against mildly harmful mutations, which may lead to accumulation of genetic load. The efficiency of purging and the accumulation of mutations both depend on the rate of inbreeding (i.e., population size) and on the nature of mutations. We studied how increasing levels of inbreeding affect offspring production and extinction in experimental Drosophila littoralis populations replicated in two sizes, N = 10 and N = 40. Offspring production and extinction were measured over 25 generations concurrently with a large control population. In the N = 10 populations, offspring production decreased strongly at low levels of inbreeding, then recovered only to show a consistent subsequent decline, suggesting early expression and purging of recessive highly deleterious alleles and subsequent accumulation of mildly harmful mutations. In the N = 40 populations, offspring production declined only after inbreeding reached higher levels, suggesting that inbreeding and genetic drift pose a smaller threat to population fitness when inbreeding is slow. Our results suggest that highly deleterious alleles can be purged in small populations already at low levels of inbreeding, but that purging does not protect the small populations from eventual genetic deterioration and extinction.

Severe Inbreeding Depression and No Evidence of Purging in an Extremely Inbred Wild Species-the Chatham Island Black Robin

“…; Pekkala et al. ). These conflicting results could reflect differences in experimental design, environmental conditions, or population sizes.…”

“…; Pekkala et al. ). Slow rates of inbreeding are expected to be less harmful on average than fast rates of inbreeding (i.e., relatively small populations where sib–sib matings are common) because it allows more time for selection to purge deleterious alleles and because a larger proportion of harmful mutations will be the target of selection (Wang et al.…”

On the genetic parameter determining the efficiency of purging: an estimate for Drosophila egg‐to‐pupae viability

“…Therefore, our estimate of d eNL implies that the relevance of purging should dramatically increase for population sizes above some value of the order of a few tens. Thus, it is not surprising that, although purging has often been reported under slow inbreeding, it has not been detected in many experiments dealing with very small lines or with close inbreeding, except regarding that ascribed to lethal or severely deleterious alleles (Hedrick, ; Latter et al ., ; Crnokrak & Barrett, ; Pedersen et al ., ; Swindell & Bouzat, ; Leberg & Firmin, ; Pekkala et al ., ).…”

No evidence for short‐term purging benefits of sexual selection in inbred red flour beetle populations

“…Apart from inbreeding rate, the relative effects of selection versus drift under inbreeding crucially depend on the mutational parameters of a population. These are, in general, still poorly understood and may differ largely among species, or even populations within species (Eyre‐Walker & Keightley, ), which could explain the mixed results of empirical studies (see Pekkala et al ., and Kennedy et al ., ), including discrepancies between this and earlier work investigating the effects of sexual selection on inbreeding load (Jarzębowska & Radwan, ; Michalczyk et al ., ).…”

“…For example, even if sexual selection assists natural selection in driving deleterious load from populations, very strong inbreeding may render the combined purging selection ineffective relative to drift. This notion is supported by simulation models showing that inbreeding rate should be negatively correlated with purging efficiency (e.g., Wang et al ., ; Caballero, Bravo & Wang, ), as well as by some (though not all) empirical studies analysing this relationship (reviewed in Pekkala et al ., ). In our study, very strong inbreeding (imposed via three generations of extreme bottlenecking by sib‐sib mating in Experiment I, and by maintaining breeding population size at the level of ten individuals throughout Experiment II) may have driven the populations below the level of fitness depression that could be rescued by sexual selection.…”