Sarah W. Fitzpatrick

Genetic rescue to the rescue

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.

Geographical variation in genetic structure of an Atlantic Coastal Forest frog reveals regional differences in habitat stability

Climatic oscillations throughout the Pleistocene combined with geological and topographic complexity resulted in extreme habitat heterogeneity along the Atlantic coast of Brazil. Inferring how these historic landscape patterns have structured the current diversity of the regions biota is important both for our understanding of the factors promoting diversification, as well as the conservation of this biodiversity hotspot. Here we evaluate potential historical scenarios of diversification in the Atlantic Coastal Forest of Brazil by investigating the population genetic structure of a frog endemic to the region. Using mitochondrial and nuclear sequences, we generated a Bayesian population‐level phylogeny of the Thoropa miliaris species complex. We found deep genetic divergences among five geographically distinct clades. Southern clades were monophyletic and nested within paraphyletic northern clades. Analyses of historical demographic patterns suggest an overall north to south population expansion, likely associated with regional differences in habitat stability during the Pliocene and early Pleistocene. However, genetic structure among southern populations is less pronounced and likely represents more recent vicariant events resulting from Holocenic sea‐level oscillations. Our analyses corroborate that the Atlantic Coastal Forest has been a biogeographically dynamic landscape and suggest that the high diversity of its fauna and flora resulted from a combination of climatic and geologic events from the Pliocene to the present.

Adaptive divergence despite strong genetic drift: genomic analysis of the evolutionary mechanisms causing genetic differentiation in the island fox (Urocyon littoralis)

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.

Locally adapted traits maintained in the face of high gene flow

Gene flow between phenotypically divergent populations can disrupt local adaptation or, alternatively, may stimulate adaptive evolution by increasing genetic variation. We capitalised on historical Trinidadian guppy transplant experiments to test the phenotypic effects of increased gene flow caused by replicated introductions of adaptively divergent guppies, which were translocated from high- to low-predation environments. We sampled two native populations prior to the onset of gene flow, six historic introduction sites, introduction sources and multiple downstream points in each basin. Extensive gene flow from introductions occurred in all streams, yet adaptive phenotypic divergence across a gradient in predation level was maintained. Descendants of guppies from a high-predation source site showed high phenotypic similarity with native low-predation guppies in as few as ~12 generations after gene flow, likely through a combination of adaptive evolution and phenotypic plasticity. Our results demonstrate that locally adapted phenotypes can be maintained despite extensive gene flow from divergent populations.

Gene flow from an adaptively divergent source causes rescue through genetic and demographic factors in two wild populations of Trinidadian guppies

Genetic rescue, an increase in population growth owing to the infusion of new alleles, can aid the persistence of small populations. Its use as a management tool is limited by a lack of empirical data geared toward predicting effects of gene flow on local adaptation and demography. Experimental translocations provide an ideal opportunity to monitor the demographic consequences of gene flow. In this study we take advantage of two experimental introductions of Trinidadian guppies to test the effects of gene flow on downstream native populations. We individually marked guppies from the native populations to monitor population dynamics for 3 months before and 26 months after gene flow. We genotyped all individuals caught during the first 17 months at microsatellite loci to classify individuals by their genetic ancestry: native, immigrant, F1 hybrid, F2 hybrid, or backcross. Our study documents a combination of demographic and genetic rescue over multiple generations under fully natural conditions. Within both recipient populations, we found substantial and long‐term increases in population size that could be attributed to high survival and recruitment caused by immigration and gene flow from the introduction sites. Our results suggest that low levels of gene flow, even from a divergent ecotype, can provide a substantial demographic boost to small populations, which may allow them to withstand environmental stochasticity.

Parallelism Isn't Perfect: Could Disease and Flooding Drive a Life-History Anomaly in Trinidadian Guppies?

Nonparallel evolution, where independent populations occupy similar environments but show phenotypic differences, can uncover previously ignored selective factors. We investigated a nonparallelism in the life-history strategy of a Trinidadian guppy population, a system famous for parallel adaptation to differences in predation risk. We tested the hypothesis that high mortality drives an observed fast life-history pattern (i.e., earlier maturation and more frequent reproductive events) that is atypical for a low-predation environment. Using mark-recapture techniques, we compared neighboring low-predation populations, finding significantly higher mortality rates in the population with atypical life-history traits. Mortality was elevated during the wet season, when flooding was common. Moreover, individuals from the anomalous population were more likely to transition from healthy to infected disease states. Our results stand out against previous patterns observed in this system, indicating that higher mortality caused by disease and flooding may have selected for a faster life history. Thus, we highlight that even in systems famous for parallel adaptation, variation in selective pressures can result in nonparallel phenotypic evolution.

Water availability strongly impacts population genetic patterns of an imperiled Great Plains endemic fish

Genetic, demographic, and environmental processes affect natural populations synergistically, and understanding their interplay is crucial for the conservation of biodiversity. Stream fishes in metapopulations are particularly sensitive to habitat fragmentation because persistence depends on dispersal and colonization of new habitat but dispersal is constrained to stream networks. Great Plains streams are increasingly fragmented by water diversion and climate change, threatening connectivity of fish populations in this ecosystem. We used seven microsatellite loci to describe population and landscape genetic patterns across 614 individuals from 12 remaining populations of Arkansas darter (Etheostoma cragini) in Colorado, a candidate species for listing under the U.S. Endangered Species Act. We found small effective population sizes, low levels of genetic diversity within populations, and high levels of genetic structure, especially among basins. Both at- and between-site landscape features were associated with genetic diversity and connectivity, respectively. Available stream habitat and amount of continuous wetted area were positively associated with genetic diversity within a site, while stream distance and intermittency were the best predictors of genetic divergence among sites. We found little genetic contribution from historic supplementation efforts, and we provide a set of management recommendations for this species that incorporate a conservation genetics perspective.

Gene Flow Constrains and Facilitates Genetically Based Divergence in Quantitative Traits

Theory predicts that gene flow will decrease phenotypic differences among populations. Correlational studies have in some cases documented constraining effects of gene flow on phenotypic divergence and/or have also provided evidence for local differentiation despite high gene flow. However, correlative studies are unable to evaluate how gene flow affects genetically based phenotypic divergence or the extent to which gene flow constrains adaptive divergence. Translocation experiments using Trinidadian guppies provided an opportunity to test the effects of new gene flow on quantitative traits in native recipient populations. We measured a suite of traits in guppies reared in common garden environments before and multiple generations following gene flow from guppies that originated from a different environment. We interpreted our results in light of a priori predictions based on evolutionary theory and extensive background information about guppies and our focal populations. Although we could not include a spatiotemporal control that would allow us to be certain that the observed changes were directly caused by gene flow, we found that post-gene flow populations showed genetically based shifts in most traits. Whether traits shifted in predicted adaptive directions or whether they became more or less similar to the source population depended on the trait and initial conditions of the population. Our study provided a rare opportunity to test how recent gene flow affects genetically based changes in traits with known adaptive significance, and our results attest to the complex interactions between gene flow and selection.

Sex, Mitochondria, and Genetic Rescue

Genetic rescue is a potentially effective management tool to offset the effects of reduced genetic diversity in imperiled populations. However, implementation requires complex choices. Here we address the consequences of introducing males versus females, highlighting the possibility that introduced females might lead to maladapted mitonuclear genomes and reduced offspring fitness.

An experimental test of alternative population augmentation scenarios: Population Augmentation

Human land use is fragmenting habitats worldwide and inhibiting dispersal among previously connected populations of organisms, often leading to inbreeding depression and reduced evolutionary potential in the face of rapid environmental change. To combat this augmentation of isolated populations with immigrants is sometimes used to facilitate demographic and genetic rescue. Augmentation with immigrants that are genetically and adaptively similar to the target population effectively increases population fitness, but if immigrants are very genetically or adaptively divergent, augmentation can lead to outbreeding depression. Despite well-cited guidelines for the best practice selection of immigrant sources, often only highly divergent populations remain, and experimental tests of these riskier augmentation scenarios are essentially nonexistent. We conducted a mesocosm experiment with Trinidadian guppies (Poecilia reticulata) to test the multigenerational demographic and genetic effects of augmenting 2 target populations with 3 types of divergent immigrants. We found no evidence of demographic rescue, but we did observe genetic rescue in one population. Divergent immigrant treatments tended to maintain greater genetic diversity, abundance, and hybrid fitness than controls that received immigrants from the source used to seed the mesocosms. In the second population, divergent immigrants had a slightly negative effect in one treatment, and the benefits of augmentation were less apparent overall, likely because this population started with higher genetic diversity and a lower reproductive rate that limited genetic admixture. Our results add to a growing consensus that gene flow can increase population fitness even when immigrants are more highly divergent and may help reduce uncertainty about the use of augmentation in conservation.