Adaptive Gene Flow Research Articles

Patterns and effects of gene flow on adaptation across spatial scales: implications for management.

Gene flow can have rapid effects on adaptation and is an important evolutionary tool available when undertaking biological conservation and restoration. This tool is underused partly because of the perceived risk of outbreeding depression and loss of mean fitness when different populations are crossed. In this article, we briefly review some theory and empirical findings on how genetic variation is distributed across species ranges, describe known patterns of gene flow in nature with respect to environmental gradients, and highlight the effects of gene flow on adaptation in small or stressed populations in challenging environments (e.g., at species range limits). We then present a case study involving crosses at varying spatial scales among mountain populations of a trigger plant (Stylidium armeria: Stylidiaceae) in the Australian Alps to highlight how some issues around gene flow effects can be evaluated. We found evidence of outbreeding depression in seed production at greater geographic distances. Nevertheless, we found no evidence of maladaptive gene flow effects in likelihood of germination, plant performance (size), and performance variance, suggesting that gene flow at all spatial scales produces offspring with high adaptive potential. This case study demonstrates a path to evaluating how increasing sources of gene flow in managed wild and restored populations could identify some offspring with high fitness that could bolster the ability of populations to adapt to future environmental changes. We suggest further ways in which managers and researchers can act to understand and consider adaptive gene flow in natural and conservation contexts under rapidly changing conditions.

Genomic architecture controls multivariate adaptation to climate change.

As climate change advances, environmental gradients may decouple, generating novel multivariate environments that stress wild populations. A commonly invoked mechanism of evolutionary rescue is adaptive gene flow tracking climate shifts, but gene flow from populations inhabiting similar conditions on one environmental axis could cause maladaptive introgression when populations are adapted to different environmental variables that do not shift together. Genomic architecture can play an important role in determining the effectiveness and relative magnitudes of adaptive gene flow and insitu adaptation. This may have direct consequences for how species respond to climate change but is often overlooked. Here, we simulated microevolutionary responses to environmental change under scenarios defined by variation in the polygenicity, linkage, and genetic redundancy of two independent traits, one of which is adapted to a gradient that shifts under climate change. We used these simulations to examine how genomic architecture influences evolutionary outcomes under climate change. We found that climate-tracking (up-gradient) gene flow, though present in all scenarios, was strongly constrained under scenarios of lower linkage and higher polygenicity and redundancy, suggesting insitu adaptation as the predominant mechanism of evolutionary rescue under these conditions. We also found that high polygenicity caused increased maladaptation and demographic decline, a concerning result given that many climate-adapted traits may be polygenic. Finally, in scenarios with high redundancy, we observed increased adaptive capacity. This finding adds to the growing recognition of the importance of redundancy in mediating insitu adaptive capacity and suggests opportunities for better understanding the climatic vulnerability of real populations.

Reproductive isolation in a three-way contact zone.

Contact zones between divergent forms within a species provide insight into the role of gene flow in adaptation and speciation. Previous work has focused on contact zones involving only two divergent forms, but in nature, many more than two populations may overlap simultaneously and experience gene flow. Patterns of introgression in wild populations are, therefore, likely much more complicated than is often assumed. We begin to address this gap in current knowledge by investigating patterns of divergence and introgression across a complex natural contact zone. We use phenotypic and genomic data to confirm the existence of a three-way contact zone among divergent freshwater resident, saltwater resident and saltwater migratory three-spined stickleback (Gasterosteus aculeatus) on the island of North Uist, Scottish Western Isles. We find evidence for hybridization, mostly between saltwater resident and saltwater migratory forms. Despite hybridization, genomic analyses reveal pairwise islands of divergence between all forms that are maintained across the contact zone. Genomic cline analyses also provide evidence for selection and/or hybrid incompatibilities in divergent regions. Divergent genomic regions occur across multiple chromosomes and involve many known adaptive loci and several chromosomal inversions. We also identify distinct immune gene expression profiles between forms, but no evidence for transgressive expression in hybrids. Our results suggest that reproductive isolation is maintained in this three-way contact zone, despite some hybridization, and that reduced recombination in chromosomal inversions may play an important role in maintaining this isolation.

Climate-driven past and present interspecies gene flow may have contributed to shape microscale adaptation capacity in Tillandsia lomas in hyperarid south American desert systems

Epiarenic (sand-growing) Tillandsia vegetation in the hyperarid and arid region of the Chilean-Peruvian Atacama Desert represents an extreme case of adaptation in plant species-poor ecosystems. The involved species exist at the limit of terrestrial life and form mono/oligo-specific and very characteristic structures within the landscape. Covering thousands of square kilometers they represent the major carbon sink in the hyperarid Atacama core. The various Tillandsia species and respective vegetation may have evolved and adapted independently to this extreme environment. The most abundant vicariant diploid species are T. landbeckii in Chile and T. purpurea in Peru. Spatio-temporally varying distribution range overlaps may have caused potentially adaptive gene flow between different species leading to present day gene pools. Using species distribution modelling we explored the idea that from Last Glacial Maximum (LGM) onwards both species shifted their distribution ranges, which resulted in the formation of varying suture zones from Peru towards northern Chile. We further explored genetic data from a Tillandsia loma vegetation in Southern Peru with three sympatrically growing species exemplifying inter-species gene flow crossing even ploidy levels. This mechanism highlights a strategy to evolve and adapt more rapidly to environmental changes in extreme arid and hyperarid habitats and provides an opportunity for Tillandsia populations to efficiently conserve new genotypes via subsequent clonal propagation.

The wave of gene advance under diverse systems of mating.

Mating systems will influence gene spread across the natural distribution of a plant species. Existing theories have not fully explored the role of mating systems on the wave of advance of an advantageous gene. Here, we develop a theory to account for the rate of spread of both advantageous and neutral genes under different mating systems, based on migration-selection processes. We show that a complex relationship exists between selfing rate and the speed of gene spread. The interaction of selfing with gametophytic selection shapes the traveling wave of the advantageous gene. Selfing can impede (or enhance) the spread of an advantageous gene in the presence (or absence) of gametophytic selection. The interaction of selfing with recombination shapes the spread of a neutral gene. Linkage disequilibrium, mainly generated by selfing, enhances the traveling wave of the neutral gene that is tightly linked with the selective gene. Recombination gradually breaks down the genetic hitchhiking effects along the direction of advantageous gene spread, yielding decreasing waves of advance of neutral genes. The stochastic process does not alter the pattern of selfing effects except for increasing the uncertainty of the waves of advance of both advantageous and neutral genes. This theory helps us to explain how mating systems act as a barrier to spread of adaptive and neutral genes, and to interpret species cohesion maintained by a low level of adaptive gene flow.

Female toads engaging in adaptive hybridization prefer high-quality heterospecifics as mates.

Hybridization-interbreeding between species-is generally thought to occur randomly between members of two species. Contrary to expectation, female plains spadefoot toads (Spea bombifrons) can increase their evolutionary fitness by preferentially mating with high-quality males of another species, the Mexican spadefoot toad (Spea multiplicata). Aspects of Mexican spadefoot males' mating calls predict their hybrid offspring's fitness, and plains spadefoot females prefer Mexican spadefoot males on the basis of these attributes, but only in populations and ecological conditions where hybridization is adaptive. By selecting fitness-enhancing mates of another species, females increase hybridization's benefits and exert sexual selection across species. Nonrandom mating between species can thereby increase the potential for adaptive gene flow between species so that adaptive introgression is not simply happenstance.

Intraspecific diversification of the crop wild relative Brassica cretica Lam. using demographic model selection

BackgroundCrop wild relatives (CWRs) contain genetic diversity, representing an invaluable resource for crop improvement. Many of their traits have the potential to help crops to adapt to changing conditions that they experience due to climate change. An impressive global effort for the conservation of various CWR will facilitate their use in crop breeding for food security.The genus Brassica is listed in Annex I of the International Treaty on Plant Genetic Resources for Food and Agriculture. Brassica oleracea (or wild cabbage), a species native to southern and western Europe, has become established as an important human food crop plant because of its large reserves stored over the winter in its leaves.Brassica cretica Lam. (Bc) is a CWR in the brassica group and B. cretica subsp. nivea (Bcn) has been suggested as a separate subspecies. The species Bc has been proposed as a potential gene donor to brassica crops, including broccoli, cabbage, cauliflower, oilseed rape, etc.ResultsWe sequenced genomes of four Bc individuals, including two Bcn and two Bc. Demographic analysis based on our whole-genome sequence data suggests that populations of Bc are not isolated. Classification of the Bc into distinct subspecies is not supported by the data. Using only the non-coding part of the data (thus, the parts of the genome that has evolved nearly neutrally), we find the gene flow between different Bc population is recent and its genomic diversity is high.ConclusionsDespite predictions on the disruptive effect of gene flow in adaptation, when selection is not strong enough to prevent the loss of locally adapted alleles, studies show that gene flow can promote adaptation, that local adaptations can be maintained despite high gene flow, and that genetic architecture plays a fundamental role in the origin and maintenance of local adaptation with gene flow. Thus, in the genomic era it is important to link the selected demographic models with the underlying processes of genomic variation because, if this variation is largely selectively neutral, we cannot assume that a diverse population of crop wild relatives will necessarily exhibit the wide-ranging adaptive diversity required for further crop improvement.

Genomic architecture of parallel ecological divergence: Beyond a single environmental contrast.

The study of parallel ecological divergence provides important clues to the operation of natural selection. Parallel divergence often occurs in heterogeneous environments with different kinds of environmental gradients in different locations, but the genomic basis underlying this process is unknown. We investigated the genomics of rapid parallel adaptation in the marine snail Littorina saxatilis in response to two independent environmental axes (crab-predation versus wave-action and low-shore versus high-shore). Using pooled whole-genome resequencing, we show that sharing of genomic regions of high differentiation between environments is generally low but increases at smaller spatial scales. We identify different shared genomic regions of divergence for each environmental axis and show that most of these regions overlap with candidate chromosomal inversions. Several inversion regions are divergent and polymorphic across many localities. We argue that chromosomal inversions could store shared variation that fuels rapid parallel adaptation to heterogeneous environments, possibly as balanced polymorphism shared by adaptive gene flow.

Interspecific introgression mediates adaptation to whole genome duplication

Adaptive gene flow is a consequential phenomenon across all kingdoms. Although recognition is increasing, there is no study showing that bidirectional gene flow mediates adaptation at loci that manage core processes. We previously discovered concerted molecular changes among interacting members of the meiotic machinery controlling crossover number upon adaptation to whole-genome duplication (WGD) in Arabidopsis arenosa. Here we conduct a population genomic study to test the hypothesis that adaptation to WGD has been mediated by adaptive gene flow between A. arenosa and A. lyrata. We find that A. lyrata underwent WGD more recently than A. arenosa, suggesting that pre-adapted alleles have rescued nascent A. lyrata, but we also detect gene flow in the opposite direction at functionally interacting loci under the most extreme levels of selection. These data indicate that bidirectional gene flow allowed for survival after WGD, and that the merger of these species is greater than the sum of their parts.

Genetic Affinities among Southern Africa Hunter-Gatherers and the Impact of Admixing Farmer and Herder Populations.

Southern African indigenous groups, traditionally hunter-gatherers (San) and herders (Khoekhoe), are commonly referred to as “Khoe-San” populations and have a long history in southern Africa. Their ancestors were largely isolated up until ∼2,000 years ago before the arrival of pastoralists and farmers in southern Africa. Assessing relationships among regional Khoe-San groups has been challenging due to admixture with immigrant populations that obscure past population affinities and gene flow among these autochthonous communities. We re-evaluate a combined genome-wide data set of previously published southern Africa Khoe-San populations in conjunction with novel data from Khoe-San individuals collected in Xade (Central Kalahari Game Reserve, Botswana) prior to their resettlement outside the reserve. After excluding regions in the genome that trace their ancestry to recent migrant groups, the genetic diversity of 20 Khoe-San groups fitted an isolation-by-distance model. Even though isolation-by-distance explained most genetic affinities between the different autochthonous groups, additional signals of contact between Khoe-San groups could be detected. For instance, we found stronger genetic affinities, than what would be explained by isolation-by-distance gene flow, between the two geographically separated Khoe-San groups, who speak branches of the Kx’a-language family (ǂHoan and Ju). We also scanned the genome-wide data for signals of adaptive gene flow from farmers/herders into Khoe-San groups and identified a number of genomic regions potentially introduced by the arrival of the new groups. This study provides a comprehensive picture of affinities among Khoe-San groups, prior to the arrival of recent migrants, and found that these affinities are primarily determined by the geographic landscape.

Recent Adaptive Acquisition by African Rainforest Hunter-Gatherers of the Late Pleistocene Sickle-Cell Mutation Suggests Past Differences in Malaria Exposure

The hemoglobin βS sickle mutation is a textbook case in which natural selection maintains a deleterious mutation at high frequency in the human population. Homozygous individuals for this mutation develop sickle-cell disease, whereas heterozygotes benefit from higher protection against severe malaria. Because the overdominant βS allele should be purged almost immediately from the population in the absence of malaria, the study of the evolutionary history of this iconic mutation can provide important information aboutthehistory of human exposure to malaria. Here, we sought to increase our understanding of the origins and time depth of theβS mutation in populations with different lifestyles and ecologies, and we analyzed the diversity of HBB in 479 individuals from 13 populations of African farmers and rainforest hunter-gatherers. Using an approximate Bayesian computation method, we estimated the age of the βS allele while explicitly accounting for population subdivision, past demography, and balancing selection. When the effects of balancing selection are taken into account, our analyses indicate a single emergence of βS in the ancestors of present-day agriculturalist populations ∼22,000 years ago. Furthermore, we show that rainforest hunter-gatherers have more recently acquired the βS mutation from the ancestors of agriculturalists through adaptive gene flow during the last ∼6,000 years. Together, our results provide evidence for a more ancient exposure to malarial pressures among the ancestors of agriculturalists than previously appreciated, and they suggest that rainforest hunter-gatherers have been increasingly exposed to malaria during the last millennia.

Rapid evolution of a skin-lightening allele in southern African KhoeSan

Skin pigmentation is under strong directional selection in northern European and Asian populations. The indigenous KhoeSan populations of far southern Africa have lighter skin than other sub-Saharan African populations, potentially reflecting local adaptation to a region of Africa with reduced UV radiation. Here, we demonstrate that a canonical Eurasian skin pigmentation gene, SLC24A5, was introduced to southern Africa via recent migration and experienced strong adaptive evolution in the KhoeSan. To reconstruct the evolution of skin pigmentation, we collected phenotypes from over 400 ≠Khomani San and Nama individuals and high-throughput sequenced candidate pigmentation genes. The derived causal allele in SLC24A5, p.Ala111Thr, significantly lightens basal skin pigmentation in the KhoeSan and explains 8 to 15% of phenotypic variance in these populations. The frequency of this allele (33 to 53%) is far greater than expected from colonial period European gene flow; however, the most common derived haplotype is identical among European, eastern African, and KhoeSan individuals. Using four-population demographic simulations with selection, we show that the allele was introduced into the KhoeSan only 2,000 y ago via a back-to-Africa migration and then experienced a selective sweep (s = 0.04 to 0.05 in ≠Khomani and Nama). The SLC24A5 locus is both a rare example of intense, ongoing adaptation in very recent human history, as well as an adaptive gene flow at a pigmentation locus in humans.

Matching habitat choice promotes species persistence under climate change

Species may survive under contemporary climate change by either shifting their range or adapting locally to the warmer conditions. Theoretical and empirical studies recently underlined that dispersal, the central mechanism behind these responses, may depend on the match between an individuals’ phenotype and local environment. Such matching habitat choice is expected to induce an adaptive gene flow, but it now remains to be studied whether this local process could promote species’ responses to climate change. Here, we investigate this by developing an individual‐based model including either random dispersal or temperature‐dependent matching habitat choice. We monitored population composition and distribution through space and time under climate change. Relative to random dispersal, matching habitat choice induced an adaptive gene flow that lessened spatial range loss during climate warming by improving populations’ viability within the range (i.e. limiting range fragmentation) and by facilitating colonization of new habitats at the cold margin. The model even predicted range contraction under random dispersal but range expansion under optimal matching habitat choice. These benefits of matching habitat choice for population persistence mostly resulted from adaptive immigration decision and were greater for populations with larger dispersal distance and higher emigration probability. We also found that environmental stochasticity resulted in suboptimal matching habitat choice, decreasing the benefits of this dispersal mode under climate change. However population persistence was still better under suboptimal matching habitat choice than under random dispersal. Our results highlight the urgent need to implement more realistic mechanisms of dispersal such as matching habitat choice into models predicting the impacts of ongoing climate change on biodiversity.

Not just a migration problem: Metapopulations, habitat shifts, and gene flow are also important for fishway science and management

AbstractWorldwide, fishways are increasingly criticized for failing to meet conservation goals. We argue that this is largely due to the dominance of diadromous species of the Northern Hemisphere (e.g., Salmonidae) in the research that underpins the concepts and methods of fishway science and management. With highly diverse life histories, swimming abilities and spatial ecologies, most freshwater fish species do not conform to the stereotype imposed by this framework. This is leading to a global proliferation of fishways that are often unsuitable for native species. The vast majority of fish populations do not undertake extensive migrations between clearly separated critical habitats, yet the movement of individuals and the genetic information they carry is critically important for population viability. We briefly review some of the latest advances in spatial ecological modelling for dendritic networks to better define what it means to achieve effective fish passage at a barrier. Through a combination of critical habitat assessment and the modelling of metapopulations, climate change‐driven habitat shifts, and adaptive gene flow, we recommend a conceptual and methodological framework for fishway target‐setting and monitoring suitable for a wide range of species. In the process, we raise a number of issues that should contribute to the ongoing debate about fish passage research and the design and monitoring of fishways.

Genomics of local adaptation with gene flow.

Gene flow is a fundamental evolutionary force in adaptation that is especially important to understand as humans are rapidly changing both the natural environment and natural levels of gene flow. Theory proposes a multifaceted role for gene flow in adaptation, but it focuses mainly on the disruptive effect that gene flow has on adaptation when selection is not strong enough to prevent the loss of locally adapted alleles. The role of gene flow in adaptation is now better understood due to the recent development of both genomic models of adaptive evolution and genomic techniques, which both point to the importance of genetic architecture in the origin and maintenance of adaptation with gene flow. In this review, we discuss three main topics on the genomics of adaptation with gene flow. First, we investigate selection on migration and gene flow. Second, we discuss the three potential sources of adaptive variation in relation to the role of gene flow in the origin of adaptation. Third, we explain how local adaptation is maintained despite gene flow: we provide a synthesis of recent genomic models of adaptation, discuss the genomic mechanisms and review empirical studies on the genomics of adaptation with gene flow. Despite predictions on the disruptive effect of gene flow in adaptation, an increasing number of studies show that gene flow can promote adaptation, that local adaptations can be maintained despite high gene flow, and that genetic architecture plays a fundamental role in the origin and maintenance of local adaptation with gene flow.