Genetic Drift: Bottleneck Effect and the Case of the Bearded Vulture

Although widely distributed across southern Europe, Africa, and Asia, the bearded vulture (Gypaetus barbatus), also known as the "bone crusher," was hunted to extinction in the European Alps in the early 1900s. This soaring scavenger, with a nearly nine-foot wingspan, takes its names from the black bristles at the base of its bill (which look like a beard) and the fact that it consumes bones (by dropping bones from carrion onto hard ground and then swooping down to suck out the marrow). Blamed for the loss of lambs, goats, and even small children throughout the Alps, that region's wild population was lost in the early 1900s, but many bearded vultures remained alive in zoos across Europe.

Thus, in the 1970s, biologists from the Frankfurt Zoological Society and elsewhere decided to try to reestablish a bearded vulture population in the Alps by introducing captive-bred birds into the wild. The reintroduction program is still underway today; in fact, since 1986, more than 120 bearded vultures have been released from captivity. About 60% to 65% of these birds are believed to have survived, and many have even reproduced (Hirzel et al., 2004). Although no one is exactly sure how many bearded vultures currently live in the Alps, the program is considered remarkably successful. However, some biologists have concerns about the project.

The problem with the bearded vulture project is not the size of the wild population; rather, it is the size of the captive population. At least that's what a team of European conservation biologists argued in a paper published in the journal Heredity (Gautschi et al., 2003). Today, there are only about 120 bearded vultures being kept in zoos and breeding centers across Europe, Asia, and the United States. Given these numbers, biologists are concerned that there is not enough genetic variability in the captive birds to keep either the captive or the wild population thriving over the long term.

Conservation biologists use effective population size (N_e) as a measure of the "genetic status" of a population: the greater the N_e, the less likely it is that the population will lose genetic variation due to genetic drift. Conservation biologists focus on maintaining as much genetic diversity in a population (and, therefore, as large an N_e) as possible. Without sufficient genetic variability, there is always the risk that a population will not be able to respond very well to new selective pressures caused by environmental change.

Because the current group of captive bearded vultures are descendants of a relatively small number of founder birds, their N_e is only about 20 to 30. However, as the authors of the Heredity paper explain, some conservation biologists think that this N_e needs to be as high as 500, maybe even 5,000, in order for the population to retain its evolutionary potential (Gautschi et al., 2003; Franklin & Frankham, 1998; Lynch & Lande, 1998). Boosting the N_e of the captive bearded vulture population from its current level to 500 (let alone 5,000) seems a bit daunting, but can anything actually be done to elevate the current numbers?

In order to answer this question, it is important to understand how scientists used a combination of pedigree data (historical information about the relatedness of all the captive birds) and microsatellite data to derive their estimated N_e of 20 to 30 individuals. First, they gathered pedigree data from what is known as a studbook, which is a database of information tracing the entire history of each individual in the captive population. (A studbook is maintained for each species bred in captivity.) Although the bearded vulture studbook has some data holes, with the geographic origins and relatedness of some of the founders remaining a mystery, it is complete enough that scientists were able to determine that all 120 captive birds descended from 36 founder birds, many of which were captured in regions of the former Soviet Union, Afghanistan, the Pyrenees, and Greece. Using this information, scientists calculated a range of N_e values from 19 to 30. They also noted that, because the studbook is incomplete, there is a chance that this range of seemingly small N_e values could be an overestimate if unknown founders came from the same geographic area and/or were related.

The next step was for scientists to calculate a DNA-based N_e estimate. To do so, they gathered blood samples from both wild and captive birds and extracted and amplified microsatellite regions of the DNA using a polymerase chain reaction (PCR). Microsatellites are, by and large, noncoding; scientists use the genetic variation at these loci as a proxy for potential genetic variation at other loci. Maintenance of the genetic variation at these loci (which are presumably not linked) would therefore indicate to scientists that the genetic diversity in other regions of the genome has been maintained. These other unknown loci may provide important variation on which natural selection may act. The scientists thus examined the variation among 14 microsatellite loci in the bearded vulture DNA, used the variation data to calculate the effective number of breeders (N_b), and used that as an equivalent of N_e. The DNA-derived estimates of N_e ranged from 23 to 27, which fall within the 19-30 range of pedigreed-derived N_e estimates.

While an N_e of 20 to 30 is quite low, especially if the goal is 500, more worrisome is the fact that the captive vultures appear to be losing, not gaining, genetic ground. In other words, their N_e is not even holding steady at 20 to 30. The authors of the Heredity article based this conclusion on two other variables conservation biologists often use (in addition to N_e) to gauge whether a population is genetically impoverished and, if so, to what extent: average heterozygosity and allelic diversity. In this context, heterozygosity is the frequency of heterozygotes at a particular locus; average heterozygosity is heterozygosity that is averaged over a series of loci (here, the 14 microsatellite loci). Similarly, allelic diversity is a measure of the number of alleles per locus; mean allelic diversity is allelic diversity that is averaged over a series of loci (again, in this case, the 14 microsatellite loci).

Even though the scientists determined that the captive bearded vulture population has more allelic diversity than the wild population and a comparable amount of heterozygosity, which might be interpreted as a good sign, allelic diversity in the captive population has declined over time. While the captive population doesn't seem to have lost much heterozygosity, through the use of a computer program developed for the Brookfield Zoo in Chicago by conservation biologist Robert Lacy, scientists have predicted that, given the captive population's current size and age structure, and assuming that eight birds will be released every year, the population will lose more than 10% of its initial heterozygosity over the next 200 years.

How does this loss of genetic variability (whether measured by changes in N_e or changes in heterozygosity) happen? As Gautschi et al. explain, genetic drift, arguably the most powerful evolutionary force at work in small populations, results from the random sampling of alleles from one generation to the next; eventually, alleles are lost and genetic variability declines.

Scientists predict that, unless something is done to increase the birds' N_e and stop the continuous decline of allelic diversity and heterozygosity, the day will come when the reintroduced wild vultures will be so genetically impoverished that, if selective pressures change, they will be at risk of extinction. Aside from recruiting additional founders to the captive population, scientists argue, the only other solution is to initiate some sort of back-and-forth gene flow between the captive and wild populations. In other words, instead of just reintroducing captive birds into the wild, why not also integrate some of the wild birds into the captive population as well? In theory, continuous gene flow between the populations would increase the effective population size and reduce genetic drift—not just in the captive population, but also in the wild population—thus slowing further loss of genetic variability.