Restoring gene flow into small, isolated populations can alleviate genetic load and decrease extinction risk (i.e., genetic rescue), yet gene flow is rarely augmented as a conservation strategy. Due ...to this discrepancy between opportunity and action, a recent call was made for widespread genetic rescue attempts. However, several aspects of augmenting gene flow are poorly understood, including the magnitude and duration of beneficial effects and when deleterious effects are likely to occur. We discuss the remaining uncertainties of genetic rescue in order to promote and direct future research and to hasten progress toward implementing this potentially powerful conservation strategy on a broader scale.
Genetic rescue has helped prevent the extinction of several populations, yet augmented gene flow is rarely used as a conservation strategy.Recent calls have been made for a paradigm shift in the conservation of small, isolated populations away from managing populations in isolation and toward widespread restoration of gene flow.Several aspects of genetic rescue remain poorly understood.Genetic rescue is inherently an eco-evolutionary process, and successful genetic rescue attempts have been part of comprehensive conservation plans that consider habitat, life history, and genetics.Genomics is being increasingly used in the implementation and monitoring of genetic rescue attempts.
Genetic rescue to the rescue Whiteley, Andrew R.; Fitzpatrick, Sarah W.; Funk, W. Chris ...
Trends in ecology & evolution (Amsterdam),
January 2015, 2015-Jan, 2015-01-00, 20150101, Letnik:
30, Številka:
1
Journal Article
Recenzirano
•Genetic rescue is difficult to detect at the population level.•Recent studies show genetic rescue is a more powerful tool than has been appreciated.•Genomics provide a useful way to advance genetic ...rescue research and application.
Genetic rescue can increase the fitness of small, imperiled populations via immigration. A suite of studies from the past decade highlights the value of genetic rescue in increasing population fitness. Nonetheless, genetic rescue has not been widely applied to conserve many of the threatened populations that it could benefit. In this review, we highlight recent studies of genetic rescue and place it in the larger context of theoretical and empirical developments in evolutionary and conservation biology. We also propose directions to help shape future research on genetic rescue. Genetic rescue is a tool that can stem biodiversity loss more than has been appreciated, provides population resilience, and will become increasingly useful if integrated with molecular advances in population genomics.
The unprecedented rate of extinction calls for efficient use of genetics to help conserve biodiversity. Several recent genomic and simulation-based studies have argued that the field of conservation ...biology has placed too much focus on conserving genome-wide genetic variation, and that the field should instead focus on managing the subset of functional genetic variation that is thought to affect fitness. Here, we critically evaluate the feasibility and likely benefits of this approach in conservation. We find that population genetics theory and empirical results show that conserving genome-wide genetic variation is generally the best approach to prevent inbreeding depression and loss of adaptive potential from driving populations toward extinction. Focusing conservation efforts on presumably functional genetic variation will only be feasible occasionally, often misleading, and counterproductive when prioritized over genome-wide genetic variation. Given the increasing rate of habitat loss and other environmental changes, failure to recognize the detrimental effects of lost genome-wide genetic variation on long-term population viability will only worsen the biodiversity crisis.
Gene flow is an enigmatic evolutionary force because it can limit adaptation but may also rescue small populations from inbreeding depression 1–3. Several iconic examples of genetic rescue—increased ...population growth caused by gene flow 4, 5—have reversed population declines 6, 7. However, concerns about outbreeding depression and maladaptive gene flow limit the use of human-mediated gene flow in conservation 8, 9. Rescue effects of immigration through demographic and/or genetic mechanisms have received theoretical and empirical support, but studies that monitor initial and long-term effects of gene flow on individuals and populations in the wild are lacking. Here, we used individual-based mark-recapture, multigenerational pedigrees, and genomics to test the demographic and evolutionary consequences of manipulating gene flow in two isolated, wild Trinidadian guppy populations. Recipient and source populations originated from environments with different predation, flow, and resource regimes 10. We documented 10-fold increases in population size following gene flow and found that, on average, hybrids lived longer and reproduced more than residents and immigrants. Despite overall genomic homogenization, alleles potentially associated with local adaptation were not entirely swamped by gene flow. Our results suggest that genetic rescue was caused not just by increasing individual genetic diversity, rather new genomic variation from immigrants combined with alleles from the recipient population resulted in highly fit hybrids and subsequent increases in population size. Contrary to the classic view of maladaptive gene flow, our study reveals conditions under which immigration can produce long-term fitness benefits in small populations without entirely swamping adaptive variation.
•New gene flow into small, isolated guppy populations led to increases in abundance•Mark-recapture and pedigree data show high hybrid survival and reproductive success•Candidate adaptive alleles resist introgression more than neutral expectations•Gene flow can rescue small populations without erasing adaptive variation
Gene flow can limit adaptation but may also rescue small populations. Fitzpatrick et al. document genetic rescue in small populations of Trinidadian guppies. Wild pedigrees and mark-recapture data reveal high hybrid fitness and maintenance of putative adaptive alleles, suggesting assisted gene flow may be an effective conservation strategy.
Environmental change can expose populations to unfamiliar stressors, and maladaptive responses to those stressors may result in population declines or extirpation. Although gene flow is classically ...viewed as a cause of maladaptation, small and isolated populations experiencing high levels of drift and little gene flow may be constrained in their evolutionary response to environmental change. We provide a case study using the model Trinidadian guppy system that illustrates the importance of considering gene flow and genetic drift when predicting (mal)adaptive response to acute stress. We compared population genomic patterns and acute stress responses of inbred guppy populations from headwater streams either with or without a recent history of gene flow from a more diverse mainstem population. Compared to “no‐gene flow” analogues, we found that populations with recent gene flow showed higher genomic variation and increased stress tolerance—but only when exposed to a stress familiar to the mainstem population (heat shock). All headwater populations showed similar responses to a familiar stress in headwater environments (starvation) regardless of gene flow history, whereas exposure to an entirely unfamiliar stress (copper sulfate) showed population‐level variation unrelated to environment or recent evolutionary history. Our results suggest that (mal)adaptive responses to acutely stressful environments are determined in part by recent evolutionary history and in part by previous exposure. In some cases, gene flow may provide the variation needed to persist, and eventually adapt, in the face of novel stress.
Abstract
Restoring gene flow among fragmented populations is discussed as a potentially powerful management strategy that could reduce inbreeding depression and cause genetic rescue. Yet, examples of ...assisted migration for genetic rescue remain sparse in conservation, prompting several outspoken calls for its increased use in genetic management of fragmented populations. We set out to evaluate the extent to which this strategy is underused and to determine how many imperiled species would realistically stand to benefit from genetic rescue, focusing on federally threatened or endangered vertebrate species in the United States. We developed a “genetic rescue suitability index (GR index)” based on concerns about small population problems relative to risks associated with outbreeding depression and surveyed the literature for 222 species. We found that two-thirds of these species were good candidates for consideration of assisted migration for the purpose of genetic rescue according to our suitability index. Good candidate species spanned all taxonomic groups and geographic regions, though species with more missing data tended to score lower on the suitability index. While we do not recommend a prescriptive interpretation of our GR index, we used it here to establish that assisted migration for genetic rescue is an underused strategy. For example, we found in total, “genetic rescue” was only mentioned in 11 recovery plans and has only been implemented in 3 of the species we surveyed. A potential way forward for implementation of this strategy is incorporating genetic rescue as a priority in USFWS recovery documentation. In general, our results suggest that although not appropriate for all imperiled species, many more species stand to benefit from a conservation strategy of assisted migration for genetic rescue than those for which it has previously been considered or implemented.
Detecting recent demographic changes is a crucial component of species conservation and management, as many natural populations face declines due to anthropogenic habitat alteration and climate ...change. Genetic methods allow researchers to detect changes in effective population size (Ne) from sampling at a single timepoint. However, in species with long lifespans, there is a lag between the start of a decline in a population and the resulting decrease in genetic diversity. This lag slows the rate at which diversity is lost, and therefore makes it difficult to detect recent declines using genetic data. However, the genomes of old individuals can provide a window into the past, and can be compared to those of younger individuals, a contrast that may help reveal recent demographic declines. To test whether comparing the genomes of young and old individuals can help infer recent demographic bottlenecks, we use forward‐time, individual‐based simulations with varying mean individual lifespans and extents of generational overlap. We find that age information can be used to aid in the detection of demographic declines when the decline has been severe. When average lifespan is long, comparing young and old individuals from a single timepoint has greater power to detect a recent (within the last 50 years) bottleneck event than comparing individuals sampled at different points in time. Our results demonstrate how longevity and generational overlap can be both a hindrance and a boon to detecting recent demographic declines from population genomic data.
The evolutionary mechanisms generating the tremendous biodiversity of islands have long fascinated evolutionary biologists. Genetic drift and divergent selection are predicted to be strong on islands ...and both could drive population divergence and speciation. Alternatively, strong genetic drift may preclude adaptation. We conducted a genomic analysis to test the roles of genetic drift and divergent selection in causing genetic differentiation among populations of the island fox (Urocyon littoralis). This species consists of six subspecies, each of which occupies a different California Channel Island. Analysis of 5293 SNP loci generated using Restriction‐site Associated DNA (RAD) sequencing found support for genetic drift as the dominant evolutionary mechanism driving population divergence among island fox populations. In particular, populations had exceptionally low genetic variation, small Nₑ (range = 2.1–89.7; median = 19.4), and significant genetic signatures of bottlenecks. Moreover, islands with the lowest genetic variation (and, by inference, the strongest historical genetic drift) were most genetically differentiated from mainland grey foxes, and vice versa, indicating genetic drift drives genome‐wide divergence. Nonetheless, outlier tests identified 3.6–6.6% of loci as high FST outliers, suggesting that despite strong genetic drift, divergent selection contributes to population divergence. Patterns of similarity among populations based on high FST outliers mirrored patterns based on morphology, providing additional evidence that outliers reflect adaptive divergence. Extremely low genetic variation and small Nₑ in some island fox populations, particularly on San Nicolas Island, suggest that they may be vulnerable to fixation of deleterious alleles, decreased fitness and reduced adaptive potential.
Population genetic connectivity is influenced by multiple abiotic and biotic attributes, including geography, dispersal ability, and life history, which may lead to different patterns of population ...structure of organisms occupying similar habitats. We investigated how differences in dispersal ability and biogeographic gradients correspond with population structuring of 3 aquatic insect species found within naturally fragmented interdunal wetlands along the eastern shoreline of Lake Michigan in midwestern USA. Interdunal wetlands are small, highly fragmented, and patchily distributed along the eastern coast of Lake Michigan, USA. Our focal species, Anax junius (Drury, 1773), Notonecta undulata Say, 1832, and Caenis amica Hagen, 1861 were chosen as high, intermediate, and low dispersers, respectively. We hypothesized that all insect populations experience isolation by distance with relatively low gene flow among sites, but that the strength of isolation by distance varies with dispersal ability. We used cytochrome c oxidase subunit I sequence data to confirm species identification and restriction enzyme-association DNA sequencing for population genomic analyses. Our cytochrome c oxidase subunit I data revealed that Caenis populations consisted of multiple species split along a latitudinal gradient. Restriction site-association DNA sequencing data showed that A. junius displayed strong isolation by distance, where N. undulata did not. Additionally, both A. junius and N. undulata populations displayed 2 genetic clusters along the coastline, and genetic diversity increased along with latitude. These results indicate that biogeographical variables, such as latitude and covarying abiotic factors, may be stronger predictors of population structure than dispersal ability and that inference of population structure within aquatic macroinvertebrates should be on a species-specific basis.
Adaptation to environmental change requires that populations harbor the necessary genetic variation to respond to selection. However, dispersal‐limited species with fragmented populations and reduced ...genetic diversity may lack this variation and are at an increased risk of local extinction. In freshwater fish species, environmental change in the form of increased stream temperatures places many cold‐water species at‐risk. We present a study of rainbow darters (Etheostoma caeruleum) in which we evaluated the importance of genetic variation on adaptive potential and determined responses to extreme thermal stress. We compared fine‐scale patterns of morphological and thermal tolerance differentiation across eight sites, including a unique lake habitat. We also inferred contemporary population structure using genomic data and characterized the relationship between individual genetic diversity and stress tolerance. We found site‐specific variation in thermal tolerance that generally matched local conditions and morphological differences associated with lake‐stream divergence. We detected patterns of population structure on a highly local spatial scale that could not be explained by isolation by distance or stream connectivity. Finally, we showed that individual thermal tolerance was positively correlated with genetic variation, suggesting that sites with increased genetic diversity may be better at tolerating novel stress. Our results highlight the importance of considering intraspecific variation in understanding population vulnerability and stress response.
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