scholarly journals The maintenance of standing genetic variation: gene flow versus selective neutrality in Atlantic stickleback fish

Author(s):  
Quiterie Haenel ◽  
Laurent Guerard ◽  
Andrew MacColl ◽  
Daniel Berner

Adaptation to derived habitats often occurs from standing genetic variation (SGV). The maintenance within ancestral populations of genetic variants favorable in derived habitats is commonly ascribed to long-term antagonism between purifying selection and gene flow resulting from hybridization across habitats. A largely unexplored alternative idea based on quantitative genetic models of polygenic adaptation is that variants favored in derived habitats are neutral in ancestral populations when their frequency is relatively low. To explore the latter, we first identify genetic variants important to the adaptation of threespine stickleback fish to a rare derived habitat – nutrient-depleted acidic lakes – based on whole-genome sequence data. Sequencing marine stickleback from six locations across the Atlantic ocean then allows us to infer that the frequency of these derived variants in the ancestral habitat is unrelated to the likely opportunity for gene flow of these variants from acidic-adapted populations. This result is consistent with the selective neutrality of derived variants within the ancestor. Our study thus supports an underappreciated explanation for the maintenance of SGV, and calls for a better understanding of the fitness consequences of adaptive genetic variation across habitats and genomic backgrounds.

Author(s):  
Brian Huntley

Species’ distributions, population sizes, and community composition are affected, directly and indirectly, by climatic changes, leading to changes in location, extent, and/or quality of distributions, range fragmentation or coalescence, and temporal discontinuities in suitable conditions. Quaternary fossil records document these responses, emphasizing individualism of species’ responses and impermanence of communities. Recent observations document similar changes attributable to recent climatic changes, including rapid decreases and increases in ranges and/or populations. Both also document extinctions associated with rapid climatic changes. Modelling studies predict substantial changes in species’ distributions, population sizes, and communities in response to future climatic changes. Implicit assumptions that genetic variation enabling adaptation is ubiquitous throughout species’ ranges, or that gene flow may be sufficiently rapid to allow adaptation, may be invalid. Work is needed to investigate spatial structuring of adaptive genetic variation and rates of gene flow, and to develop new models. Without this, species extinction risks may be severely underestimated.


2016 ◽  
Vol 113 (29) ◽  
pp. 8064-8071 ◽  
Author(s):  
Victoria L. Sork ◽  
Paul F. Gugger ◽  
Jin-Ming Chen ◽  
Silke Werth

Phylogeography documents the spatial distribution of genetic lineages that result from demographic processes, such as population expansion, population contraction, and gene movement, shaped by climate fluctuations and the physical landscape. Because most phylogeographic studies have used neutral markers, the role of selection may have been undervalued. In this paper, we contend that plants provide a useful evolutionary lesson about the impact of selection on spatial patterns of neutral genetic variation, when the environment affects which individuals can colonize new sites, and on adaptive genetic variation, when environmental heterogeneity creates divergence at specific loci underlying local adaptation. Specifically, we discuss five characteristics found in plants that intensify the impact of selection: sessile growth form, high reproductive output, leptokurtic dispersal, isolation by environment, and the potential to evolve longevity. Collectively, these traits exacerbate the impact of environment on movement between populations and local selection pressures—both of which influence phylogeographic structure. We illustrate how these unique traits shape these processes with case studies of the California endemic oak, Quercus lobata, and the western North American lichen, Ramalina menziesii. Obviously, the lessons we learn from plant traits are not unique to plants, but they highlight the need for future animal, plant, and microbe studies to incorporate its impact. Modern tools that generate genome-wide sequence data are now allowing us to decipher how evolutionary processes affect the spatial distribution of different kinds of genes and also to better model future spatial distribution of species in response to climate change.


2020 ◽  
Author(s):  
Lisa Cooper ◽  
Lynsey Bunnefeld ◽  
Jack Hearn ◽  
James M Cook ◽  
Konrad Lohse ◽  
...  

AbstractPopulation divergence and gene flow are key processes in evolution and ecology. Model-based analysis of genome-wide datasets allows discrimination between alternative scenarios for these processes even in non-model taxa. We used two complementary approaches (one based on the blockwise site frequency spectrum (bSFS), the second on the Pairwise Sequentially Markovian Coalescent (PSMC)) to infer the divergence history of a fig wasp, Pleistodontes nigriventris. Pleistodontes nigriventris and its fig tree mutualist Ficus watkinsiana are restricted to rain forest patches along the eastern coast of Australia, and are separated into northern and southern populations by two dry forest corridors (the Burdekin and St. Lawrence Gaps). We generated whole genome sequence data for two haploid males per population and used the bSFS approach to infer the timing of divergence between northern and southern populations of P. nigriventris, and to discriminate between alternative isolation with migration (IM) and instantaneous admixture (ADM) models of post divergence gene flow. Pleistodontes nigriventris has low genetic diversity (π = 0.0008), to our knowledge one of the lowest estimates reported for a sexually reproducing arthropod. We find strongest support for an ADM model in which the two populations diverged ca. 196kya in the late Pleistocene, with almost 25% of northern lineages introduced from the south during an admixture event ca. 57kya. This divergence history is highly concordant with individual population demographies inferred from each pair of haploid males using PSMC. Our analysis illustrates the inferences possible with genome-level data for small population samples of tiny, non-model organisms and adds to a growing body of knowledge on the population structure of Australian rain forest taxa.


2019 ◽  
Author(s):  
Xin Zhou ◽  
Lu Zhang ◽  
Ziming Weng ◽  
David L. Dill ◽  
Arend Sidow

AbstractVariant discovery in personal, whole genome sequence data is critical for uncovering the genetic contributions to health and disease. We introduce a new approach, Aquila, that uses linked-read data for generating a high quality diploid genome assembly, from which it then comprehensively detects and phases personal genetic variation. Assemblies cover >95% of the human reference genome, with over 98% in a diploid state. Thus, the assemblies support detection and accurate genotyping of the most prevalent types of human genetic variation, including single nucleotide polymorphisms (SNPs), small insertions and deletions (small indels), and structural variants (SVs), in all but the most difficult regions. All heterozygous variants are phased in blocks that can approach arm-level length. The final output of Aquila is a diploid and phased personal genome sequence, and a phased VCF file that also contains homozygous and a few unphased heterozygous variants. Aquila represents a cost-effective evolution of whole-genome reconstruction that can be applied to cohorts for variation discovery or association studies, or to single individuals with rare phenotypes that could be caused by SVs or compound heterozygosity.


2020 ◽  
Author(s):  
Erik R Funk ◽  
Garth M Spellman ◽  
Kevin Winker ◽  
Jack J Withrow ◽  
Kristen C Ruegg ◽  
...  

Abstract Understanding how gene flow affects population divergence and speciation remains challenging. Differentiating one evolutionary process from another can be difficult because multiple processes can produce similar patterns, and more than one process can occur simultaneously. Although simple population models produce predictable results, how these processes balance in taxa with patchy distributions and complicated natural histories is less certain. These types of populations might be highly connected through migration (gene flow), but can experience stronger effects of genetic drift and inbreeding, or localized selection. Although different signals can be difficult to separate, the application of high-throughput sequence data can provide the resolution necessary to distinguish many of these processes. We present whole-genome sequence data for an avian species group with an alpine and arctic tundra distribution to examine the role that different population genetic processes have played in their evolutionary history. Rosy-finches inhabit high elevation mountaintop sky islands and high-latitude island and continental tundra. They exhibit extensive plumage variation coupled with low levels of genetic variation. Additionally, the number of species within the complex is debated, making them excellent for studying the forces involved in the process of diversification, as well as an important species group in which to investigate species boundaries. Total genomic variation suggests a broadly continuous pattern of allele frequency changes across the mainland taxa of this group in North America. However, phylogenomic analyses recover multiple distinct, well supported, groups that coincide with previously described morphological variation and current species-level taxonomy. Tests of introgression using D-statistics and approximate Bayesian computation reveal significant levels of introgression between multiple North American taxa. These results provide insight into the balance between divergent and homogenizing population genetic processes and highlight remaining challenges in interpreting conflict between different types of analytical approaches with whole-genome sequence data. [ABBA-BABA; approximate Bayesian computation; gene flow; phylogenomics; speciation; whole-genome sequencing.]


2021 ◽  
Vol 12 (1) ◽  
Author(s):  
Quiterie Haenel ◽  
Krista B. Oke ◽  
Telma G. Laurentino ◽  
Andrew P. Hendry ◽  
Daniel Berner

AbstractHow ecological divergence causes strong reproductive isolation between populations in close geographic contact remains poorly understood at the genomic level. We here study this question in a stickleback fish population pair adapted to contiguous, ecologically different lake and stream habitats. Clinal whole-genome sequence data reveal numerous genome regions (nearly) fixed for alternative alleles over a distance of just a few hundred meters. This strong polygenic adaptive divergence must constitute a genome-wide barrier to gene flow because a steep cline in allele frequencies is observed across the entire genome, and because the cline center closely matches the habitat transition. Simulations confirm that such strong divergence can be maintained by polygenic selection despite high dispersal and small per-locus selection coefficients. Finally, comparing samples from near the habitat transition before and after an unusual ecological perturbation demonstrates the fragility of the balance between gene flow and selection. Overall, our study highlights the efficacy of divergent selection in maintaining reproductive isolation without physical isolation, and the analytical power of studying speciation at a fine eco-geographic and genomic scale.


PLoS Genetics ◽  
2021 ◽  
Vol 17 (12) ◽  
pp. e1009335
Author(s):  
Tyler S. Brown ◽  
Olufunmilayo Arogbokun ◽  
Caroline O. Buckee ◽  
Hsiao-Han Chang

Measuring gene flow between malaria parasite populations in different geographic locations can provide strategic information for malaria control interventions. Multiple important questions pertaining to the design of such studies remain unanswered, limiting efforts to operationalize genomic surveillance tools for routine public health use. This report examines the use of population-level summaries of genetic divergence (FST) and relatedness (identity-by-descent) to distinguish levels of gene flow between malaria populations, focused on field-relevant questions about data size, sampling, and interpretability of observations from genomic surveillance studies. To do this, we use P. falciparum whole genome sequence data and simulated sequence data approximating malaria populations evolving under different current and historical epidemiological conditions. We employ mobile-phone associated mobility data to estimate parasite migration rates over different spatial scales and use this to inform our analysis. This analysis underscores the complementary nature of divergence- and relatedness-based metrics for distinguishing gene flow over different temporal and spatial scales and characterizes the data requirements for using these metrics in different contexts. Our results have implications for the design and implementation of malaria genomic surveillance studies.


2021 ◽  
Author(s):  
Tyler Steven Brown ◽  
Aimee R. Taylor ◽  
Olufunmilayo Arogbokun ◽  
Caroline O. Buckee ◽  
Hsiao-Han Chang

Measuring gene flow between malaria parasite populations in different geographic locations can provide strategic information for malaria control interventions. Multiple important questions pertaining to the design of such studies remain unanswered, limiting efforts to operationalize genomic surveillance tools for routine public health use. This report evaluates numerically the ability to distinguish different levels of gene flow between malaria populations, using different amounts of real and simulated data, where data are simulated using parameters that approximate different epidemiological conditions. Specifically, using Plasmodium falciparum  whole genome sequence data and sequence data simulated for a metapopulation with different migration rates and effective population sizes, we compare two estimators of gene flow, explore the number of genetic markers and number of individuals required to reliably rank highly connected locations, and describe how these thresholds change given different effective population sizes and migration rates. Our results have implications for the design and implementation of malaria genomic surveillance efforts.


2019 ◽  
Author(s):  
Katharine L Korunes ◽  
Carlos A Machado ◽  
Mohamed AF Noor

AbstractBy shaping meiotic recombination, chromosomal inversions can influence genetic exchange between hybridizing species. Despite the recognized importance of inversions in evolutionary processes such as divergence and speciation, teasing apart the effects of inversions over time remains challenging. For example, are their effects on sequence divergence primarily generated through creating blocks of linkage-disequilibrium pre-speciation or through preventing gene flux after speciation? We provide a comprehensive look into the influence of chromosomal inversions on gene flow throughout the evolutionary history of a classic system: Drosophila pseudoobscura and D. persimilis. We use extensive whole-genome sequence data to report patterns of introgression and divergence with respect to chromosomal arrangements. Overall, we find evidence that inversions have contributed to divergence patterns between Drosophila pseudoobscura and D. persimilis over three distinct timescales: 1) pre-speciation segregation of ancestral polymorphism, 2) post-speciation ancient gene flow, and 3) recent gene flow. We discuss these results in terms of our understanding of evolution in this classic system and provide cautions for interpreting divergence measures in similar datasets in other systems.


2020 ◽  
Vol 375 (1806) ◽  
pp. 20190548 ◽  
Author(s):  
Yo Y. Yamasaki ◽  
Ryo Kakioka ◽  
Hiroshi Takahashi ◽  
Atsushi Toyoda ◽  
Atsushi J. Nagano ◽  
...  

Speciation is a continuous process. Although it is known that differential adaptation can initiate divergence even in the face of gene flow, we know relatively little about the mechanisms driving complete reproductive isolation and the genomic patterns of divergence and introgression at the later stages of speciation. Sticklebacks contain many pairs of sympatric species differing in levels of reproductive isolation and divergence history. Nevertheless, most previous studies have focused on young species pairs. Here, we investigated two sympatric stickleback species, Pungitius pungitius and P. sinensis , whose habitats overlap in eastern Hokkaido; these species show hybrid male sterility, suggesting that they may be at a late stage of speciation. Our demographic analysis using whole-genome sequence data showed that these species split 1.73 Ma and came into secondary contact 37 200 years ago after a period of allopatry. This long period of allopatry might have promoted the evolution of intrinsic incompatibility. Although we detected on-going gene flow and signatures of introgression, overall genomic divergence was high, with considerable heterogeneity across the genome. The heterogeneity was significantly associated with variation in recombination rate. This sympatric pair provides new avenues to investigate the late stages of the stickleback speciation continuum. This article is part of the theme issue ‘Towards the completion of speciation: the evolution of reproductive isolation beyond the first barriers’.


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