Читать книгу Fundamentals of Conservation Biology - Malcolm L. Hunter Jr. - Страница 102

Populations that lack genetic diversity may also experience problems (e.g. low fertility and high mortality among offspring, etc.) even in environments that are not changing (Fig. 5.7). A loss of fitness associated with genetic uniformity often develops from breeding between closely related individuals, an outcome known as “inbreeding depression.” It is a well‐known phenomenon in zoos, where populations of captive animals are often small, and mating among close relatives can be unavoidable (Ralls et al. 1988) (Fig. 5.8). Inbreeding affects traits important for fitness. Reproductive biology is particularly sensitive. For example, female marmoset monkeys inbred in captive situations develop fused genital labia and cannot copulate but are otherwise reproductively healthy (Isachenko et al. 2002). Plant and animal breeders who breed individuals that are genetically similar to one another to promote desirable characteristics that they share, such as a preferred color or resistance to a certain disease, can also promote inbreeding indirectly.

Figure 5.7 Relationships between reproductive fitness and genetic diversity summarized across many studies by Reed and Frankham (2003). The strength of the relationship is measured by the correlation coefficient, which ranges from −1 when higher fitness is associated with lower genetic diversity (and vice versa) to +1 when higher fitness is associated with higher genetic variation (and vice versa). If there was no relationship then most studies would report correlations between fitness and genetic diversity around zero but as this figure clearly indicates relationships tend to be quite positive (averaging about 0.4).

(Reed and Frankham 2003/John Wiley & Sons)

Figure 5.8 Juvenile mortality in 44 species of mammals (16 ungulates, 16 primates, 10 rodents, one marsupial, and an elephant shrew) bred in captivity. Open bars represent mortality rates with inbred parents; black bars represent mortality rates from matings between unrelated parents. Species are arranged from left to right by increasing mortality from unrelated parents. Numbers on the tops of the bars are the sample size. (

Data from Ralls and Ballou 1983)

There are three general explanations for relatively low fitness in genetically uniform populations. First, there is more homozygosity in genetically uniform populations, and this may lead to the expression of deleterious alleles that are usually recessive and suppressed in heterozygous individuals. Hip dysplasia in purebred dogs is a widely known current example. At one time, inbreeding within the royal families of Europe resulted in many family members having a split upper lip. An example of inbreeding that increases the expression of a maladaptive trait in a wild species is provided in Fig. 5.9. These traits are widespread in many populations (for example, as many as 1 in 20 people carry the gene for cystic fibrosis, or 5%) but the two recessives rarely combine at random to produce the condition (p² = 0.05 × 0.05 = 0.0025 or 2.5 in 1000 offspring). The problem is small populations. If two carriers happen to be present in a small group then inbreeding greatly amplifies the likelihood that the deleterious form of a particular gene will be inherited from both the mother and father and be expressed in the offspring. Some alleles, called lethal recessives, have mortal effects when they come together in a homozygous recessive individual.

Figure 5.9 Deformities resulting from population isolation and inbreeding, in this case in white‐tailed deer from an abandoned military installation (Seneca Army Depot). When the depot was created in 1941, a 24‐mile (39 km) fence was erected around its perimeter, isolating a small herd of white‐tailed deer, some of which had white coats. These deer are not albino, but instead carry a set of recessive genes for all‐white coats. The isolation of the herd has caused high levels of inbreeding and widespread expression of this unusual coat color. The coat color is maladaptive as it makes the deer highly conspicuous to would‐be predators, particularly deer hunters.

(BrianAdler/Wikimedia Commons/Public domain)

Second, heterozygous individuals may be more fit in terms of phenotypic characteristics than homozygous individuals, a phenomenon known as heterosis. For example, evidence suggests that heterozygous animals tend to be more resistant to disease, grow faster, and survive longer than homozygotes (Frankel 2013). This effect seems to be present, but not as strong, among plants (Ledig 1986).

The third reason is closely tied to the “evolutionary potential” issue discussed in the preceding section. In a population dominated by heterozygotes there will be more genetic variability among offspring (some heterozygotes, some homozygous dominants, and some homozygous recessives). In a changing environment perhaps at least some of the young will have the right combinations of alleles to survive. In other words, from an evolutionary perspective it may be preferable not to put all your eggs in one basket or all your zygotes into one genotype.

Evidence for low fitness due to loss of genetic variation has slowly been accumulating for a diverse suite of species (Frankham et al. 2014). Good examples are lions (Packer et al. 1991), song sparrows (Keller et al. 1994), adders (Madsen et al. 1996), and Fennoscandian arctic foxes (Norén et al. 2016). Because inbreeding is particularly germane in captive populations, conservation biologists who work with captive populations of wild species that are endangered or extinct in the wild and those who manage rare breeds of domestic species strive to minimize inbreeding depression. We will return to genetic management of populations later in this chapter.

A loss of fitness can also occur when mating occurs between individuals that are too genetically dissimilar, a phenomenon called outbreeding depression (Schaal and Leverich 2005). Many species have a large range that includes quite different environments even though the populations comprising them are often adjacent and exchanging genes through dispersal and interbreeding. Consider the peregrine falcon that breeds on every continent except Antarctica. Birds breeding in southern Africa have had to adapt to a very different environment from those in, say, arctic Canada, India, or Japan. They do this through development of co‐adapted gene complexes, which is to say suites of alleles that work well together and “fit” the animal to its particular environment. So what happens when you cross‐breed individuals from different environments (something that has been done extensively with peregrine falcons)? These gene complexes can be broken up with the end result being offspring that are adapted to nowhere in particular and whose fitness is thereby depressed everywhere. This is the essence of outbreeding depression, which is mostly a concern in captive‐bred species where individuals from very different origins can be “thrown together” in breeding programs. In nature individuals rarely travel the distances that would break up co‐adapted gene complexes. Examples of outbreeding depression are diverse and include translocations of ibex to restore populations in the Tatra Mountains of Slovakia (Fig. 5.10), common frogs (Sagvik et al. 2005), salmonid fishes (Lehnert et al. 2014), and orangutans (Banes et al. 2016). It is important to note that inbreeding and outbreeding are part of the same continuum from breeding with close relatives to breeding with completely unrelated individuals, with many species breeding systems defined along a narrow part of the gradient, hemmed in between the depression caused by inbreeding and outbreeding (Brys and Jacquemyn 2016).

Figure 5.10 Outbreeding depression among ibex. When an ibex population of the Tatra Mountains of Slovakia was extirpated, conservationists replaced it with animals from nearby Austria (Capra ibex ibex), and later added ibex from Turkey (Capra ibex aegagrus) and the Sinai (Capra ibex nubiana). The offspring of these subspecific crosses mated in the fall rather than the winter as the Austrian ibex had, and their young were born during the winter, rather than spring, and died. The reintroduction failed; worse, it caused the whole population to disappear. This is one of the subspecies involved in the dysfunctional crosses: Capra ibex ibex.

(Daniele Faieta/Flickr/CC BY 4.0)

Although outbreeding depression usually refers to intraspecific mating, botanists also use the term to refer to a loss of fitness that occurs when individuals of two closely related species interbreed, what zoologists would call hybridization. (Recall that botanists often do not use the reproductive isolation definition of species described in Chapter 3.) Interspecific outbreeding depression or hybridization is a problem among some rare plants that may be exposed to large amounts of pollen from closely related common species (e.g. Rieseberg and Gerber 1995).

In the case of some rare plants suffering from inbreeding, a little outbreeding may be “the cure.” Consider the seabluff catchfly; outbred individuals may be more fit than offspring from selfing or local pollination and hence more valuable for translocation efforts (Kephart 2004). Genetic rescue is the technical term used to describe mitigating the effects of inbreeding through outbreeding. Evidently a small amount of gene flow has immediate and lasting impacts on reducing inbreeding (Frankham 2016) although caution is urged in its application (Waller 2015). In summary, inbreeding and outbreeding may lead to a loss of fitness because: (1) inbreeding generates more homozygotes (some of which may express recessive deleterious alleles lurking in the population); and (2) with outbreeding, adaptive genetic differences among populations are lost through intermixing. It must be emphasized that these are both generalizations that do not necessarily apply to all species. For example, endangered red wolves are not apparently vulnerable to inbreeding depression (Brzeski et al. 2014) whereas arctic foxes very much are (Norén et al. 2016); sensitivities may even vary within different populations of the same species (Fenster and Galloway 2000).