Inbreeding depression

Inbreeding is more likely to occur in small populations simply because there is a greater chance that an individual will mate with a relative. In a diploid species, inbreeding increases the likelihood that an individual will have two alleles that are identical by descent at any given locus, and it therefore has the effect of increasing homozygosity at all loci. For this reason, the inbreeding coefficient F is based on heterozygosity deficits (Equation 3.15). This relationship between inbreeding and heterozygosity also means that the rate at which heterozygosity is lost from a population following drift (1/(2Ne); Chapter 3) is equal to the rate at which inbreeding accumulates, and this can be expressed as:

where AF equals the increment in inbreeding that will occur from one generation to the next (see also Box 7.2). In the absence of immigrants, inbreeding will therefore accumulate at a rate that is inversely proportional to population size (Figure 7.5).

Box 7.2 Inbreeding and genetic diversity

In outcrossing species, a small Ne, low genetic diversity and high inbreeding go hand in hand. Discussions may focus explicitly on only one or two of these topics, but it is important to remember that, over time, populations with small effective sizes will simultaneously experience an increase in inbreeding and a decrease in genetic diversity. This relationship can be shown by the following equation:

where Ht and H0 represent heterozygosity at generation t and generation 0, respectively, and F is the inbreeding coefficient (Frankham, Ballou and Briscoe, 2002). We were introduced to the first part of this equation in Chapter 3 (Equation 3.14) as a way to estimate the rate at which heterozygosity will be lost from a population. By expanding this equation to include the inbreeding coefficient, we can see how drift, which is strongly influenced by population size, will simultaneously reduce genetic diversity and promote inbreeding.

Inbreeding threatens the survival of small populations when it leads to a reduction in fitness, a phenomenon that is known as inbreeding depression. There are two ways in which this can occur. The first of these is known as dominance, so-called because the favourable alleles at a locus are usually dominant and the deleterious alleles have been maintained within the populations because they are recessive. The increased homozygosity that results from inbreeding means that deleterious alleles are more likely to occur as homozygotes; when this happens their effects cannot be masked by the dominant favourable allele, which results in inbreeding depression. The second phenomenon that can lead to inbreeding depression is known as overdominance, or heterozygote advantage, which means that individuals that are heterozygous at a particular locus have a higher

Number of generations

Figure 7.5 The increase over time in the inbreeding coefficients (F) of five populations of different sizes, all of which were outbred completely at time zero (F — 0) and all of which are closed to immigrants. The rate at which inbreeding levels increase within a population is inversely proportional to its effective size

Number of generations

Figure 7.5 The increase over time in the inbreeding coefficients (F) of five populations of different sizes, all of which were outbred completely at time zero (F — 0) and all of which are closed to immigrants. The rate at which inbreeding levels increase within a population is inversely proportional to its effective size fitness than individuals that are homozygous for either allele. In Chapter 3 we were introduced to sickle cell anaemia, a classic example of overdominance in which heterozygotes benefit from a high resistance to malaria.

Inbreeding depression can be quantified using the following equation:

where Xj is the fitness value of a particular trait in inbred offspring and XO is the fitness value of that same trait in outbred offspring. We can work through this equation by looking at the trait of survival in golden lion tamarins (Leontopithecus rosalia). In one study, the average survival of outbred offspring was found to be 0.829, whereas the average survival of inbred offspring was 0.474 (Dietz and Baker, 1993). The level of inbreeding depression revealed by this trait is therefore S = 1 - (0.474/ 0.829) = 1 - 0.572 = 0.428. Some other examples of inbreeding depression are shown in Table 7.4.

As more and more studies of inbreeding accumulate in the literature, it is becoming apparent that inbreeding depression is actually far more widespread than was previously believed. The recent proliferation of inbreeding studies is partially attributable to the increasing accessibility of molecular data. In the past, inbreeding depression was typically inferred from lengthy investigations that sought to compare the overall fitness of inbred versus outbred individuals. Studies such as these have proved invaluable to our understanding of inbreeding in wild

Table 7.4 Some examples of inbreeding depression in a variety of taxonomic groups. Adapted from Crnokrak and Roff (1999) and references therein

Species

Trait

Xo

Xi

S

Cooper's hawk (Accipiter cooperii)

Clutch size

4

3.7

0.075

Mexican jay (Aphelocoma ultramarina)

Nestling survival

0.33

0.086

0.739

Lion (Panthera leo)

Sperm mobility

91

61

0.330

Anubis baboon (Papio anubis)

% Offspring viability

84.2

50

0.406

Tree snail (Arianta arbustorum)

Number of clutches

17

13.6

0.200

Common adder (Vipera berus)

Brood size

10

7

0.300

Yellow trout lily (Erythronium americanum)

Seed production

41.2

10.5

0.745

Blue gilia (Gilia achilleifolia)

% Seedling establishment

100

69

0.310

populations, but they have several drawbacks. In the first place, a lack of pedigree information, combined with the high frequency of extra-pair fertilizations in many wild populations, can make it difficult to determine whether individuals are outbred or inbred. Futhermore, not all species lend themselves to the intensity of study that is needed before data such as those presented in Table 7.4 can be accumulated; particularly problematic is the fact that field studies are typically limited to a short period of time -- often a single breeding season -- and the data collected during this period may not accurately reflect an individual's life-time fitness. Longer-term studies can sometimes be conducted under laboratory or captive conditions, but inbreeding depression may be greatly reduced in captive populations; according to one review, inbreeding depression is on average 6.9 times higher for mammals in the wild compared with mammals that are kept in captivity (Crnokrak and Roff, 1999). Some of these problems may be circumvented by a shortcut that uses molecular data and individual fitness components to look for heterozygosity fitness correlations.

Heterozygosity fitness correlations

Heterozygosity fitness correlations (HFCs) are based on two principles: first, multilocus heterozygosity values can be used as a measure of inbreeding; and second, inbreeding depression leads to a reduction in fitness. If we combine these two principles, we reach the conclusion that inbreeding depression should be characterized by a correlation between low heterozygosity and reduced fitness. This is most commonly tested for by comparing observed heterozygosity values with one or more individual fitness components such as rate or percentage of seed germination, growth rate, time to reproduction, the number of flowers, fruits or seeds, sperm quality or volume, and longevity.

Although caution should be used when interpreting results that are based on a limited number of loci (Pemberton, 2004), a number of studies have suggested that

Correlation coefficient, r

Figure 7.6 Distribution of the correlation coefficients (r) from a meta-analysis of heterozygosity fitness correlations. The mean correlation between heterozygosity (or equivalent measure of genetic diversity) and fitness was 0.432. Adapted from Reed and Frankham (2003) and references therein a correlation between heterozygosity and fitness is indeed a useful measure of inbreeding depression. In one study, a meta-analysis was conducted on 34 data sets, each based on a minimum of three populations. Each data set was examined to see if there was a correlation between the genetic diversity of a population and its overall fitness. Twenty-eight of the data sets showed a positive correlation between fitness and genetic diversity. The median correlation was 0.440 (Figure 7.6), which the author felt was substantial considering that the meta-analysis incorporated a diversity of species and a variety of methods for estimating both fitness and genetic diversity (Reed and Frankham, 2003). Some examples of inbreeding depression inferred from HFCs are given in Table 7.5.

A particularly detailed study of heterozygosity and fitness was conducted on a wild population of red deer (Cervus elaphus) on the Isle of Rum (Figure 7.7). This population has been monitored intensively since 1971, and these long-term records provide reliable measures of fitness based on the number of calves that each individual produced over its lifetime. Heterozygosity values were calculated using between six and nine microsatellite markers, and an analysis of the data showed that lifetime breeding success was positively correlated with heterozygosity in both males and females (Slate et al., 2000). Another in-depth study was conducted on a large metapopulation of the Glanville fritillary butterfly (Melitaea cinxia) on the Aland islands in southwest Finland. This metapopulation consists of many small populations that breed in about 1600 meadows of different sizes and varying distances from one another. There is an average of 200 extinctions and 114

Table 7.5 Species in which a positive correlation has been found between heterozygosity and fitness (HFCs). Inbreeding depression is inferred from a combination of reduced fitness and low heterozygosity values

Species

Characteristic

Reference

Soay sheep (Ovis aries)

Pocket gopher (Thomomys bottae)

Butterfly blue (Scabiosa columbaria), a perennial plant

Common mussel (Mytilus edulis)

American chestnut (Castanea dentata)

Dainty damselfly (Coenagrion scitulum)

Common toad (Bufo bufo)

Higher parasite-mediated mortality in individuals with low heterozygosity Metabolic cost of burrowing is higher in individuals with low heterozygosity Populations were less able to compete with Bromus grass when heterozygosity was low Improved immune response in highly heterozygous individuals Higher growth rates in highly heterozygous individuals Heterozygosity positively correlated with body size and mating success Inverse correlation between heterozygosity and number of observed physical abnormalities in developing tadpoles

Coltman et al. (1999)

Hildner and Soule (2004)

Pluess and Stocklin (2004)

Carissan-Lloyd, Pipe and

Beaumont (2004) Stilwell et al. (2003)

Carchini et al. (2001)

Hitchings and Beebee (1998)

Figure 7.7 Male red deer (Cervus elaphus) on the Isle of Rum. Lifetime breeding success in this population is positively correlated with heterozogosity. Photograph provided by Jon Slate and reproduced with permission

re-colonizations each year. In this study, females were sampled from 42 populations of varying size and isolation, and characterized at eight loci (seven allozymes and one microsatellite). Heterozygosity was lower, and hence inbreeding was higher, in small populations, a result that was not surprising because some of the smallest populations consist entirely of full-siblings. In addition, these small populations showed evidence of inbreeding depression in the form of reduced egg hatching success, larval survival and female longevity, plus a longer pupal period that increases the likelihood of pupae being parasitized. When 7/42 populations went extinct during the second year of the study, it became apparent that the risk of a population becoming extinct was inversely proportional to its overall heterozygosity and hence directly proportional to its level of inbreeding. This study was the first to demonstrate that inbreeding in the wild can cause populations to become extinct (Saccheri et al., 1998).

Purging

Inbreeding does not automatically lead to inbreeding depression. One way in which inbreeding depression can be avoided is through the purging of deleterious alleles. As we know, inbreeding increases the homozygosity of recessive deleterious alleles, which means that the associated deleterious traits are more likely to be expressed. These traits then will be selected against, which can lead to elimination (purging) of the deleterious alleles from the population. This process is particularly effective against alleles that are lethal in the homozygous state. However, purging is unlikely to have much effect on alleles that are only mildly deleterious, which instead may become fixed within a small population following genetic drift. Furthermore, purging cannot ameliorate the effects of inbreeding that are associated with overdominance, and can be counteracted by the introduction of novel deleterious alleles following mutation. The effectiveness of purging therefore remains a subject of debate, in part because purging is more often inferred than unequivocally demonstrated. In the absence of empirical evidence, it is often provided as a default explanation for the survival of species that have been through extremely small bottlenecks, such as Pere David's deer (Elaphurus davidianus). This deer is undoubtedly one of the most inbred mammals in the world because the global population was reduced to 13 individuals in the 19th century. Nevertheless, the deer are now thriving and show little evidence of inbreeding depression, possibly because purging eliminated lethal recessives during at least one of the bottlenecks.

More precise evidence for purging was sought in a review of 28 experimental studies of mammals, insects, molluscs and plants in which inbreeding depression had been estimated over multiple generations of experimentally inbred strains. Inbreeding depression initially increased over several generations, but after a while the situation started to reverse in a number of species when fitness levels rebounded. The most likely explanation for this reduction in inbreeding depression is the purging of deleterious alleles, although it is also possible that the increase in fitness reflected adaptation to laboratory conditions (Crnokrak and Barrett, 2002). In insects, there is some evidence that purging is responsible for the relatively low levels of inbreeding that have been found in haplodiploid compared with diploid species, because purging of genetic load can be accomplished relatively easily through the production of haploid males whose deleterious recessive alleles cannot be masked (Henter, 2003).

Because purging may be an effective way to reduce inbreeding depression, it has been suggested in the past that deliberate inbreeding can be used as a conservation management tool to rid small populations of deleterious alleles. However, many biologists believe that the risks associated with this outweigh the potential benefits, since it is extremely difficult to predict the efficacy of purging. This unpredictability has been illustrated by a number of studies, including an experiment in which inbreeding depression was monitored over ten generations of inbreeding in three subspecies of wild mice: Peromyscus polionotus subgriseus, P. p. rhoadsi and P p. leucocephalus. Although comparable breeding programmes were set up for all three subspecies, the results were inconsistent. Over time, P. p. rhoadsi showed a reduction in inbreeding depression, P. p. leucocephalus showed an increase in inbreeding depression, and P. p. subgriseus showed no change. These differences may depend at least partially on whether or not populations had experienced previous bouts of inbreeding and purging in the wild, although this is unlikely to be the only relevant factor (Lacy and Ballou, 1998). Results such as these mean that many conservation biologists view deliberate attempts at purging to be a fairly desperate strategy for reducing inbreeding depression.

Self-fertilization

So far we have been looking at inbreeding depression in species that reproduce solely by outcrossing. We will now turn our attention to self-fertilization (or selfing), which involves the fusion of gametes that have been produced by the same individual and is therefore the most extreme form of inbreeding. Around 40 % of all flowering plant species are capable of self-fertilization. We might expect selfing plants to exhibit high levels of inbreeding depression, but in fact they are often less prone to inbreeding depression than outcrossing species. This may be because they are more adept at purging deleterious alleles, although, as with obligately out-crossing species, purging seems to be more effective in some populations than in others.

In the eelgrass (Zostera marina), for example, selfing plants produce seeds more frequently and in larger numbers than outcrossing plants (Rhode and Duffy, 2004). In the wild daffodil Narcissus longispathus, on the other hand, inbreeding

Figure 7.8 Narcissus longispathus (Amaryllidaceae), a rare self-compatible trumpet daffodil restricted to a few mountain ranges in southeastern Spain. Photograph by Spencer C.H. Barrett and reproduced with permission

depression can be pronounced (Figure 7.8). This is a herb that is endemic to a few mountain ranges in southeastern Spain and can reproduce by either self-fertilization or outcrossing. In one study, heterozygosity was found to be much higher in parental plants than in seedlings, a discrepancy that is taken as evidence for strong selection against inbred offspring (Barrett, Cole and Herrera, 2004). This is therefore an example of self-fertilization leading to inbreeding depression in the form of high seedling mortality. Despite these obvious drawbacks, the authors of this study suggest that self-fertilization is maintained in this species because it allows prolific reproduction during the founding of new populations, even if mates are unavailable.

Many hermaphrodite animals are capable of both outcrossing and self- fertilization, including a number of tapeworm, snail and ascidian species. The parasitic tapeworm Schistocephalus solidus has a complex life cycle, with a copepod (freshwater zooplankton) as its first intermediate host, the three-spined stickleback (Gasterosteus aculeatus) as its second intermediate host, and one of several fish-eating bird species as its final host. Researchers who were interested in whether or not selfing led to inbreeding depression in this parasite used microsatellite data to compare the genotypes of adults and offspring to establish whether juveniles were the product of self-fertilization (one parent) or outcrossing (two parents). They then discovered that outcrossed parasites produced a significantly more intense infection than selfed parasites, and as a result they were more likely to progress in their life cycle to the point where they could reach their final host. Despite an advantage to outcrossing, this species nevertheless maintains an ability to self-fertilize, presumably for reproductive assurance because there is no guarantee that a tapeworm will be able to find a partner with which to outcross (Christen and Milinski, 2003).

Inbreeding avoidance

A final testimony to the hazards associated with inbreeding are the lengths to which individuals will often go in order to avoid it. In Chapter 6 we were introduced to two important mechanisms of inbreeding avoidance. The first of these was sex-biased dispersal. If one sex is philopatric and the other disperses before reproducing, then the breeding males and females within a population or breeding group should not be related to each other. That is not to say that inbreeding avoidance is the only reason why sex-biased dispersal occurs, because other factors such as competition for territories or for mates may also come into play, but it is undoubtedly a driving force in some situations. One example of this was presented by a 9-year study of a savannah sparrow (Passerculus sandwichensis) population on an isolated archipelago in the Bay of Fundy, Canada. Both males and females were more likely to move to a different part of the island to breed if the parent of the opposite sex was still alive, presumably to reduce the risk of inbreeding (Wheelwright and Mauck, 1998).

Even when neither males nor females tend to disperse from their family groups, incestuous matings can often be avoided. A study that was published in 1995 reviewed data from a number of species that live in family groups and found that 18/19 avian species and 17/20 mammalian species showed a strong tendency to avoid mating with relatives (Emlen, 1995). This leads us to the second mechanism of inbreeding avoidance that was introduced in Chapter 6, and that is mate choice. If mates are chosen at least partially on the basis of inbreeding avoidance then species must have a basis for recognition. Some species will use phenotypic characters, for example the call of the American toad (Bufo americanus) is more similar in closely related individuals and can therefore be used as a cue to avoid inbreeding (Waldman, Rice and Honeycutt, 1992). Other species use olfactory

Table 7.6 Some examples of endangered or critically endangered species that had Nc <500 at their most recent assessment. These are not all necessarily doomed to extinction, but their risk is relatively high because of their low levels of genetic diversity and their often high levels of inbreeding. Sources: IUCN Red List 2003 and BirdLife International

Table 7.6 Some examples of endangered or critically endangered species that had Nc <500 at their most recent assessment. These are not all necessarily doomed to extinction, but their risk is relatively high because of their low levels of genetic diversity and their often high levels of inbreeding. Sources: IUCN Red List 2003 and BirdLife International

Species

Geographic range

Nc

Baishanzu fir (Abies beshanzuensis)

Baishanzu Mountain, China

5

Greenflower Indian mallow (Abutilon sandwicense)

Oahu, Hawaii

200-300

Bastard quiver tree (Aloe pillansii)

Namibia, South Africa

<200

Visayan wrinkled hornbill (Aceros waldeni)

Western Visayas, Philippines

120-160

Blue-eyed ground-dove (Columbina cyanopis)

Brazil

<250

Anegada ground iguana (Cyclura pinguis)

Virgin Islands

<200

Aruba Island rattlesnake (Crotalus durissus unicolor)

Caribbean

350

Javan rhinoceros (Rhinoceros sondaicus)

Java, Vietnam

<100

Ethiopian wolf (Canis simensis)

Ethiopia

400

cues, which may help them to identify genetically dissimilar mates, for example sand lizards prefer the odour of individuals that have distantly related MHC alleles (Olsson et al., 2003).

Of course, inbreeding avoidance is impossible in very small populations, but remember that inbreeding does not necessarily lead to inbreeding depression. A question that often appears in conservation genetics is how small a population must be if it is to avoid inbreeding depression. The work of animal breeders suggests that populations with an effective size of 50 or more should usually be able to avoid inbreeding depression and retain reproductive fitness (Franklin, 1980). However, this estimate refers to the short-term avoidance of inbreeding depression, and other studies suggest that an effective size ofbetween 500 and 1000 is necessary if populations are to maintain their long-term evolutionary potential (Franklin and Frankham, 1998). Note also that this is the effective population size, and if we accept that the average Ne/Nc ratio is 0.1 (Chapter 3), the minimum population census size necessary for long-term survival will be closer to 5000. Somewhat alarmingly, many species have a total Nc that is <500 (Table 7.6) and, although they are not all necessarily doomed to extinction, they are undoubtedly at a greater risk than large populations because of their relatively low levels of genetic diversity and their often high levels of inbreeding. In the next section we will look at how human management can help to reduce the risk of inbreeding through the introduction of novel genotypes.

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