Heterozygosity, Fitness and Inbreeding Depression in Natural Populations

Heterozygosity, fitness and inbreeding depression in natural populations

Inbreeding is mating between close relatives and can depress components of reproductive fitness thus having detrimental effects on the populations survival, a phenomenon known as inbreeding depression. There are two principal theories for the mechanism of inbreeding depression. The partial dominance hypothesis (Charlesworth and Charlesworth, 1987) suggests that inbreeding increases the frequency of homozygous combinations of deleterious recessive alleles due to the increased chance of offspring inheriting alleles identical by decent from both heterozygous parents. This is shown in figure 1 and results in a reduction of population fitness.

Figure 1 Adapted from Madsen (1996)

However the overdominance hypothesis suggests that because inbreeding increases homozygotes it reduces the overall frequency of the superior heterozygote's relative to Hardy Weinberg ratios if the population was randomly mating. This results in the loss of the heterozygote advantage and in a decrease in fitness (Charlesworth and Charlesworth 1987).

Both hypotheses are likely to be correct and that a combination of the two causes an overall increase in homozygotes and decrease in heterozygotes of the offspring relative to that of the population as a whole if it were mating randomly and in Hardy Weinberg frequencies. As a result there is a loss of genetic diversity, superior heterozygotes and increase in recessive mutations which leads to the loss in the populations' evolutionary adaptability to cope and evolve to environmental change. This is indicated by the following equation for loss of neutral genetic variation in a random mating population:

Hg / H0 = [1 - 1 / (2Ne) ]g = 1 -F (Frankham 2002)

Where Hg is the heterozygosity at generation g, H0 the initial heterozygosity, Ne the long-term effective population size and F the inbreeding coefficient. As stated by Frankham (2005), 'the effects of inbreeding and loss of genetic variability are usually inseparable'.

In small populations such as those of threatened species, inbreeding becomes inevitable as matings between close relatives become unavoidable resulting in an increase in homozygotes for recessive deleterious mutations which may become fixed at some loci. However, inbreeding is rarer in larger populations typically of non threatened species. This is due to a wider choice in mating partners and wider genetic diversity. The heterozygote advantage can be retained and recessive deleterious alleles are kept rare by selection even though the population may carry many of them. This is because they will rarely be inherited from both parents by offspring and so the population is fitter.

There have been many studies done on domestic or captive-bred populations to document the detrimental effects of inbreeding depression (Ralls and Ballou 1983, 1988). Inbreeding reduces reproduction and survival in essentially all well studied species and is virtually unavoidable in captive populations due to their small population sizes. For example, in forty captive populations belonging to thiry-eight species there was an average increase of 33% for mortality in inbred matings (Ralls et al 1988). Fewer studies have been done on natural wild populations due to difficulties in monitoring the populations such as establishing the relatedness between individuals in a breeding pair. Many studies have therefore focused on juvenile traits due to difficulties obtaining complete life history data and also identifying parameters that reflect their lifetime reproductive success.

Inbreeding has deleterious effects on reproductive fitness in all well studied species of naturally outbreeding animals and plants and so they exhibit inbreeding depression. Greenwood (1978) found that inbreeding pairs have lower breeding success resulting from higher nesting mortality than normal pairs in the great tit (Parsus major) and so inbreeding depression occurs. When Crnokrak and Roff (1999) analysed 169 estimates of inbreeding depression for 137 traits they detected statistically significant levels of inbreeding depression in the wild approximately 54% of the time when species are known to be inbred. They also demonstrated that the cost of inbreeding depression under natural conditions is much higher than under captive conditions by comparing data to the estimates zoo species published by Ralls et al (1988). This may be because wild environments are typically more stressful that in captive environments and that weak inbred young that would normally die in the wild would most likely survive in captivity with veterinary assistance (Ralls et al 1988).

Although inbreeding has been shown to have a detrimental impact on individual fitness, its contribution to extinction is still poorly understood and the relative impact of inbreeding on the viability of natural populations has been questioned.

Some think that ecological and demographic factors events ranging from annual variation in climate to catastrophes such as disease epidemics are the 'immediate importance than genetics in determining population viability'. They may typically drive populations to extinction before genetic factors can impact and so are of more significance (Lande 1988). For example, work on the endangered cheetah (Acinonyx jubatus) has emphasized the importance of environmental factors including habitat size and poachers on its mortality in the wild. Initial evidence seemed to show that the cheetah's endangerment in the wild and captivity was due to it exhibiting relatively low levels of genetic variability. The genetic variability was measured by polymorphism (P), the proportion of loci that vary in a population and heterozygosity (H), the proportion of loci which vary in the average individual. Reduced population heterozygosity is associated with inbreeding and therefore population reproductive fitness. O'Brien et al (1983, 1987);

Sub species P H

South African A. j. jubatus 0.02 0.0004

East African A. j. raineyi 0.04 0.014

Table 1: Results for genetic variability taken from O'Brien et al (1983, 1987)

These results were based on a genetic survey of 47 loci in 55 cheetahs from the two areas. The percentage polymorphism of 3.2% and average herterozygosity of 0.013 were also shown to be far lower than other mammalian populations of average 14.7% polymorphism and 0.036 heterozygosity (Nevo 1978) and so inbreeding depression was widely accepted as the explanation for its difficulties breeding.

However