Another potential problem that may affect the success of translocations is outbreeding depression. We know from the earlier section on genetic rescue that when two genetically divergent individuals reproduce heterosis may occur, which results in progeny whose fitness is higher than the average fitness of either parental population. This can happen through the masking of deleterious alleles or by overdominance associated with increased heterozygosity. In some cases, however, the fitness of the progeny will be lower than that of either parent, in which case outbreeding depression has occurred. Two genetic factors can lead to outbreeding depression. The first is the loss of locally adapted genotypes. If individuals from two populations that are each adapted to their natal environments hybridize, their offspring will contain a mixture of alleles that may not be well suited to either environment. When this occurs, outbreeding depression will be evident in the first generation of offspring.
Immigrant x Native
Heterosis in F
Loss of locally adapted alleles in F1 = outbreeding depression
Heterosis in F
Heterosis in subsequent generations (through dominance or overdominance) = genetic rescue
Breakdown of coadapted gene complex in subsequent generations = outbreeding depression
Figure 7.11 Some outcomes that may result from matings between immigrant and native individuals. Note that genetic rescue assumes that the native population was experiencing some level of inbreeding depression prior to the mating between natives and immigrants
The second genetic cause of outbreeding depression is the loss of positive epistatic interactions. Epistasis refers to the interaction of genes from multiple loci and their collective influence on particular traits. The group of loci involved in an epistatic interaction is known as a co-adapted gene complex, and if this complex is broken up through recombination then outbreeding depression may result. Because the set of chromosomes from each parental lineage will remain intact in their offspring (the F1 generation), outbreeding depression may not be evident immediately and in fact fitness may increase temporarily because the F1 generation will have high heterozygosity values. By the F2 generation, however, recombination will have disrupted adaptive gene combinations, causing a sudden reduction in fitness (Figure 7.11). This process was evident in the tidepool copepod Tigriopus californicus when broods representing both pure populations and interpopulation hybrids were raised under different conditions of temperature and salinity. As is typical following the disruption of co-adapted gene complexes, adverse affects were not evident in the F1 of interpopulation hybrids, but the fitness of the F2 generation was substantially reduced (Edmands and Deimler, 2004).
Although theoretically well established, the extent to which outbreeding depression threatens the survival of wild populations remains a matter of debate; some researchers maintain that its importance is overstated, whereas others believe that it is a widespread phenomenon that would be detected more often if appropriate studies were conducted. Outbreeding depression has been documented most commonly in plants because their relatively low dispersal rates, which are often combined with local adaptation to particular environmental conditions, mean that plants can show genetic differentiation over both small and large spatial scales. Under these conditions, outbreeding depression may result when individuals from either distant or neighbouring populations interbreed (see Box 7.3).
In wild populations of the herbaceous scarlet gilia (Ipomopsis aggregata), matings between parents separated by only 100 m produced offspring with a reduced lifetime fitness that was caused by outbreeding depression, although not surprisingly the decline in fitness depended in part on environmental heterogeneity and the associated selection regimes (Waser, Price and Shaw, 2000). Effects at an even finer spatial scale were found in Nelson's larkspur (Delphinium nelsonii) when flowers were hand-pollinated using pollen from between 1 m and 30 m away. Progeny from intermediate crossing distances (3 m and 10 m) grew approximately twice as large as the progeny that resulted from crossings between either nearby or more distant plants. This was presumably because pollen from intermediate distances did not adversely affect the fitness of offspring, whereas pollen from plants that were 1 m or 30 m away led to inbreeding depression and outbreeding depression, respectively (Waser and Price, 1994).
The potential importance of outbreeding depression to conservation management was illustrated by a study of the Mediterranean perennial herb Anchusa crispa, which is endemic to sandy seashores on the islands of Corsica and Sardinia. Populations are small and patchy and have extremely low levels of heterozygosity. The performance of inbred (from the same patch) and outcrossed (from different patches in the same population) plants was evaluated in greenhouse experiments. Although the plants that were produced after two generations of selfing produced fewer seeds than outcrossed plants, they also produced more clusters of flowers and had significantly higher survival rates, and therefore the overall fitness of inbred plants was substantially higher than that of outcrossed plants. In this case, outbreeding depression seemed to be more of a hazard than inbreeding depression, and the authors of this study suggested that inbreeding may have purged deleterious alleles in this species, and furthermore may actually be favoured because of the adaptation conferred by homozygous alleles in different populations (Quilichini, Debussche and Thompson, 2001). Although this was a greenhouse experiment that needs to be verified by studies of wild populations, these preliminary results suggest that conservation of A. crispa would not be well served by the introduction of novel alleles into small, inbred populations.
Some of the issues associated with the regeneration of ecosystems fall under the heading of restoration genetics, an emerging field that combines restoration ecology with population genetics. A recent article by Hufford and Mazer (2003) highlighted some of the potential genetic pitfalls that can compromise the success of restoration programmes. We have discussed some of these in earlier sections of this and other chapters but will now briefly revisit them in the context of a specific conservation management technique. First, extreme founder effects should be avoided by screening for genotype diversity. This may be particularly important in plants that are capable of clonal reproduction, because in these species a founding population could include multiple individuals that have the same genotype. Restored eelgrass (Zostera marina) populations in southern California and New England were found to have significantly lower levels of genetic diversity than undisturbed populations because the founders were genetically depauperate, and this in turn led to inbreeding depression within the transplanted populations (Williams, 2001). A second concern is the genetic swamping of local genotypes, either through hybridization or through aggressive growth such as that exhibited by the invasive genotype of the common reed Phragmites australis in the USA (Chapter 5).
Although less well-studied and therefore somewhat controversial, a third potential genetic problem associated with ecosystem restoration is outbreeding depression following the mating of genetically dissimilar individuals. Projects that aim to restore biodiversity in intensively managed farmland often use seed mixtures of wildflowers that are produced by commercial suppliers, and that may have originated many miles from the site of restoration. The potential consequences of using seeds from distant sources were investigated in a study of three arable weed species: common corncockle (Agrostemma githago), red poppy (Papaver rhoeas) and white campion (Silene alba) (Keller, Kollmann and Edwards, 2000). Swiss plants were crossed with plants that originated in England, Germany and Hungary, and the fitness of the hybrids was compared with that of the parental plants. Outbreeding depression was indicated by reduced biomass in both the F2 generation of all red poppy crosses and in the F1 generation that was generated by a cross between Swiss and German corncockles. Seed mass decreased in the F2 generation of the white campion crosses and survival was reduced in both the F1 and F2 progeny of red poppies. Results such as these suggest that, whenever possible, habitats should be restored using seeds of relatively local origin. This should minimize the likelihood of both outbreeding depression and genetic swamping.
Outbreeding depression has been documented less frequently in animals, although some evidence has emerged from a number of recent studies. Hybrids between males and females from two different populations of pink salmon (Oncorhynchus gorbuscha) that are separated by around 1000 km showed a decreased survival in the F2 generation relative to either parental population, which is consistent with an epistatic model of outbreeding depression (Gilk et al., 2004). The male courtship song in offspring that were generated by interpopula-
tion crosses of the fruitfly Drosophila montana had a frequency different to that found in either parental population, which led to reduced mating success and lowered fitness, once again suggesting outbreeding depression (Aspi, 2000).
As with plants, outbreeding depression in animals may be more common following matings between individuals from populations that have undergone periods of inbreeding, for example matings between immigrants and natives in an inbred population of song sparrows (Melospiza melodia) showed signs of reduced fitness relative to the 'pure' native sparrows (Marr, Keller and Arcese, 2002). Because inbreeding is not uncommon in endangered species, the relevance of this to conservation is apparent. In the early 20th century the Kaziranga population of Indian rhinoceroses (Rhinoceros unicornis) underwent a severe bottleneck that was followed by a period of substantial inbreeding and purging of deleterious alleles. A captive breeding programme mated individuals from the Kaziranga and the Chitwan populations in an attempt to reduce inbreeding, but the offspring had a higher mortality rate than those in the inbred population, suggesting genetic incompatibility and outbreeding depression (Zschokke and Baur, 2002). In conclusion, although outbreeding depression may not be a common threat to the fitness of animal populations, a number of studies have shown it to be sufficiently detrimental, at least in the short term, to make it a point of consideration in translocation programmes. It is also a potential problem that should be kept in mind when species are maintained through captive breeding, a last resort approach in conservation biology that will be the subject of our final section.
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