Inbreeding affects evolutionary responses
We explored the consequences of small population size and the concomitant process of genetic erosion of populations to address two fundamental questions: (i) How do the effects of genetic drift and inbreeding affect the stress perception of populations? (ii) To what extent does genetic erosion impede evolutionary adaptation to stressful environments of such populations? These questions are important as many fragmented populations currently suffer both from genetic erosion and changing and deteriorating environmental conditions (e.g. climate change, chemical pollution), which endanger their persistence.
The evidence presented here shows that generally the fitness reduction because of inbreeding increases significantly under stress and that this effect becomes amplified as inbreeding coefficients increase (Bijlsma et al. 2000; Armbuster and Reed 2005; Fox and Reed 2011). This phenomenon causes populations to be much more sensitive to environmental stress, making it still harder to cope with the rapid deteriorating environmental conditions. This increases the extinction risk of inbred populations greatly (Bijlsma et al. 2000). The increased sensitivity to environmental stress of genetically eroded populations signifies that effects of human-induced stress cannot properly be evaluated without taking this phenomenon into account. Given its importance, further investigations are called for to understand the causation and consequences of the synergistic interaction between inbreeding and stress.
Small populations are also subject to loss of genetic variation due to genetic drift. The available data show that this, in general, also holds for adaptive variation. The decrease in standing genetic variation in small populations could potentially decrease evolutionary responses. This is well supported by the experimental evidence for traits that are not or only marginally related to fitness for which genetically eroded populations showed significantly reduced selection responses. There is also increasing evidence that this may also hold for fitness-related traits (Frankham et al. 1999; Willi and Hoffmann 2009; Bakker et al. 2010). This indicates that fragmentation and the accompanying genetic erosion will limit the evolutionary responses to stressful environmental conditions.
However, the effects of inbreeding depression and loss of adaptive variation are not independent. When a population is subjected to a novel environmental stress, the selection intensity will increase and the growth rate of the population will decrease and will often become negative initially leading to a decrease in population size that even may reach a critical low level because of selective deaths, the cost of selection (Haldane 1957; Gomulkiewicz and Holt 1995; Orr and Unckless 2008; Bell and Gonzalez 2009 and references therein). Only after adapted individuals have reached a sufficient high frequency in the stressed population, this trend will be reversed and the population will show a positive growth rate again. As such, persistence/extinction can be regarded as a race between adaptation and demographic decay (Maynard Smith 1989; Bell and Gonzalez 2009). In the presence of increased inbreeding depression under stress, the extra reduction in individual fitness is expected to reduce population numbers and growth rates much further, making adaptive recovery a great deal more difficult. Thus, the increased cost of inbreeding under stress coupled with the cost of adaptation is expected to limit adaptation and severely increase the extinction probability of small populations. In this process, inbreeding plays a pivotal role. The interaction between inbreeding depression and reduced levels of genetic variation will critically limit evolutionary responses. One has to realize that the dynamics of the adaptive responses may differ considerably depending on whether the environmental changes occur gradually or abruptly.
Chevin et al. (2010) recently published a stimulating paper in which they expanded the evolutionary model by Lynch and Lande (1993) by including phenotypic plasticity. What they did not (yet) include were, among others, genetic drift and inbreeding. As inbreeding increases the sensitivity to stress and decreases fitness, it is expected to increase the environmental sensitivity to selection considerably. Moreover, inbreeding can significantly impair plastic responses (Auld and Relyea 2010). Based on the model of Chevin et al. (2010), it is expected that the joint effects of inbreeding would be that the critical maximum rate of environmental change that allows long-term persistence would become decreased. This effect will even be strengthened if inbreeding makes plasticity more costly. We advocate that future modeling of the persistence of biodiversity in changing environments preferably should include the effects of genetic erosion.
Some general remarks
Our inferences are restricted to species that are liable to inbreeding depression. Clearly not all species will suffer in the same way: normally selfing species will show little loss in fitness upon inbreeding, while species that normally outcross will show much higher levels of inbreeding depression. We have focused solely on the effects of genetic erosion and have not discussed nongenetic factors, nor did we discuss possible positive effects of fragmentation and geographic isolation in the context of the buildup of local races and possible speciation events (Howard 1993). These issues go beyond the framework of this paper.
The evidence presented here mostly comes from laboratory experiments, and the situation undoubtedly will be more complex in nature. However, our findings suggest that inbreeding depression is a key factor in the adaptive process, and the magnitude of inbreeding depression generally increases in the wild. Therefore, we are confident that inbreeding depression also plays a pivotal role in the adaptive process in nature. Moreover, population sizes in nature fluctuate considerably in time. This will on average deflate the effective population size (Ne) and strengthen the effects of genetic drift.
Future prospects and practical approaches
Since the 1980s, conservation genetics has recognized the need to avert the negative effects of genetic erosion as it does increase the extinction probability of species (Frankham et al. 2002). Here, we showed that genetic erosion, and particularly inbreeding depression, will also significantly impair the adaptive potential to (future) stressful challenges, like climate change and pollution. This leads to two questions that we will shortly address: (i) How can we identify populations that are threatened by genetic erosion? (ii) How can we alleviate the negative effects of genetic erosion and decrease extinction probabilities?
The first question implies that we need methods that reveal when populations are genetically eroded and suffer from inbreeding depression. Although individual inbreeding can be detected in nature using pedigrees, estimates of the inbreeding coefficients and the related fitness effects are difficult to determine at the population level. In many investigations, Wright’s fixation index FIS is used as a measure of the level of inbreeding. However, this is incorrect as in small randomly mating populations, FIS will be always zero, even though biparental inbreeding increases the inbreeding coefficient (f) continuously (Keller and Waller 2002; Biebach and Keller 2010). In this situation, population-specific FST can be used to infer the level of inbreeding and offers a convenient way to estimate the average level of inbreeding in a population (Vitalis et al. 2001; Biebach and Keller 2010; and references therein). Both the rate of loss of variation and the rate of inbreeding critically depend on the genetically effective population size (Ne). Neutral molecular markers, such of microsatellite loci, are currently the markers of choice to study the genetics of populations and allow estimation of important parameters that contribute to loss of genetic variation and the rate of inbreeding. In combination with constantly improving estimation procedures, it is now feasible to estimate these parameters, like effective population size, inbreeding coefficient and migration rate, with increasing accuracy. This makes it possible to evaluate the genetic risks of the population under investigation and to device effective management decisions (Palstra and Ruzzante 2008; Biebach and Keller 2010; Luikart et al. 2010).
Comparing the performance of small versus large populations for several fitness traits, known to be affected by inbreeding, does facilitate the detection of populations that suffer from inbreeding depression. This approach has been successfully applied to several species, leading to management measures to alleviate the genetic problems (Westemeier et al. 1998; Madsen et al. 1999; Vilà et al. 2003; Hedrick and Fredrickson 2010). However, the performance of a population also depends on ecological and environmental factors, which may confound the genetic effects. Recent developments in landscape genetics may help to entangle the different factors contributing to the endangerment of populations (Segelbacher et al. 2010).
Although neutral molecular markers provide crucial information about the dynamics of neutral genetic variation and the level of inbreeding, we are also highly interested in the dynamics and loss of adaptive variation. Unfortunately, there is only a weak correlation between molecular genetic diversity and quantitative genetic variation (Hedrick 2001; Gilligan et al. 2005), and thus the levels of neutral variation are not predictive for the levels of adaptive variation. Also, heterozygosity at these markers shows little correlation with the inbreeding coefficient (Pemberton 2004). However, the rapid advances in genomic techniques promise to solve these problems. In the near future, molecular tools will allow us to obtain the complete sequence of any species. It is expected that this will enable us to successfully address hot topics like the genetic basis of inbreeding depression, the structure and amount of adaptive variation, the level of local adaptation and the causes of G×E interactions (Allendorf et al. 2010; Kristensen et al. 2010; Ouborg et al. 2010). This would greatly advance our understanding of genetic processes in small populations and the dynamics of biodiversity in a changing world.
The second question, in essence, involves (i) alleviating inbreeding depression and restoring adaptive genetic variation and (ii) increasing population sizes to a level at which genetic erosion will be minimal. These issues have been regularly discussed in the field of conservation genetics. We will discuss these issues here briefly, while further ideas can be found elsewhere (e.g. Frankham et al. 2002; Sgrò et al. 2011). Table 1 presents the outline of a three-step program of interventions that will alleviate the problems caused by genetic erosion. Improving gene flow and connectivity between the population fragments that previously formed a single large population is the first step. It is now well documented that influx of migrants in genetically eroded populations rapidly decreases inbreeding depression, increases genetic diversity and positively affects population growth (Westemeier et al. 1998; Madsen et al. 1999; Vilà et al. 2003; Hedrick and Fredrickson 2010). This process of genetic rescue will be only successful in the long term if gene flow levels stay high as otherwise genetic erosion will arise again (Liberg et al. 2005; Biebach and Keller 2010). Genetic rescue often raises concerns about outbreeding depression (Edmands 2007). Unless the environment has changed drastically since a population became fragmented and the population fragments have become locally adapted, outbreeding depression is not expected to be a problem at this scale as increased connectivity only restores the previous situation. This step is expected to decrease both the genetic and demographic risks of populations.
Table 1. Management measures to improve the genetic constitution of fragmented and genetically eroded populations in three steps.
|1. Increase gene flow between fragments and/or increase connectivity||As populations in habitat fragments are expected to be fixed for different (mildly) deleterious alleles, this measure will immediately decrease inbreeding depression levels; it will increase genetic variation levels; local adaptation in general will not be a problem as it restores former undivided conditions and establishes a metapopulation with sufficient gene flow levels.|
|2. Increase habitat and/or population size||This measure will decrease the impact of genetic drift and inbreeding; it will buffer the genetic erosion of populations that will occur in the future; it will mitigate the cost of selection upon adaptation.|
|3. Facilitate genetic exchange with more distant populations and populations from different habitats||This measure will mitigate inbreeding depression even more; it will boost the level of genetic diversity; it will supplement adaptive genetic variants not yet present in the population; this will facilitate evolutionary responses in the future. Dangers: this measure may disrupt local adaptation and cause outbreeding depression; if the total population size is large enough, recombination and selection may nullify this loss of fitness over the generations.|
Even so promoting gene flow will cancel the negative effects of genetic erosion, the total (meta)population size often is still limited, and genetic erosion might arise again. Therefore, to ensure long-term viability, in a second phase of the rescue process, it would be advisable to increase population size to a level at which genetic erosion is expected to be minimized. This could be achieved by increasing the habitat size or by improving the quality of the habitat (e.g., by removing edge effects) so it can sustain larger numbers of individuals. This action would decrease genetic risks even further and, in addition, make the population more resistant against environmental stochasticity (Lande 1993).
If required, gene flow between more distant and (slightly) different habitats could be promoted as a third step. This step will increase genetic diversity even further by an influx of genetic variants that may not have been present in the target population. Such an intervention is expected to facilitate adaptive response in the (near) future. For instance, importing immigrants from the warmer regions (e.g., lower latitudes) of a species distribution into the cooler regions may improve the ability of the receiving population to cope with ongoing climate change. A drawback of this action is that the immigrants might be maladapted and disrupt local adaptation, thereby causing outbreeding depression (Edmands 2007; Frankham et al. 2011). However, Frankham et al. (2011) showed that when a careful decision procedure is followed, the probability of outbreeding depression to occur might be considerably lower than generally anticipated. Moreover, after a hybridization event, recombination and natural selection can overcome the initial decrease in fitness and improve fitness to levels higher than before hybridization within a few generations (Edmands et al. 2005; Erickson and Fenster 2006). This suggests that outbreeding depression might only be a temporal problem. If the receiving population is healthy and sufficiently large, it is expected to be able to cope with this short-term problem. Nevertheless, great care should be taken before implementing this third step.