Signatures Of Divergent Selection Research Articles

Pollinator and habitat-mediated selection as potential contributors to ecological speciation in two closely related species.

In ecological speciation, incipient species diverge due to natural selection that is ecologically based. In flowering plants, different pollinators could mediate that selection (pollinator-mediated divergent selection) or other features of the environment that differ between habitats of 2 species could do so (environment-mediated divergent selection). Although these mechanisms are well understood, they have received little rigorous testing, as few studies of divergent selection across sites of closely related species include both floral traits that influence pollination and vegetative traits that influence survival. This study employed common gardens in sites of the 2 parental species and a hybrid site, each containing advanced generation hybrids along with the parental species, to test these forms of ecological speciation in plants of the genus Ipomopsis. A total of 3 vegetative traits (specific leaf area, leaf trichomes, and photosynthetic water-use efficiency) and 5 floral traits (corolla length and width, anther insertion, petal color, and nectar production) were analyzed for impacts on fitness components (survival to flowering and seeds per flower, respectively). These traits exhibited strong clines across the elevational gradient in the hybrid zone, with narrower clines in theory reflecting stronger selection or higher genetic variance. Plants with long corollas and inserted anthers had higher seeds per flower at the Ipomopsis tenuituba site, whereas selection favored the reverse condition at the Ipomopsis aggregata site, a signature of divergent selection. In contrast, no divergent selection due to variation in survival was detected on any vegetative trait. Selection within the hybrid zone most closely resembled selection within the I. aggregata site. Across traits, the strength of divergent selection was not significantly correlated with width of the cline, which was better predicted by evolvability (standardized genetic variance). These results support the role of pollinator-mediated divergent selection in ecological speciation and illustrate the importance of genetic variance in determining divergence across hybrid zones.

Genetic divergences and hybridization within the Sebastes inermis complex.

The Sebastes inermis complex includes three sympatric species (Sebastes cheni, viz Sebastes inermis, and Sebastes ventricosus) with clear ecomorphological differences, albeit incomplete reproductive isolation. The presence of putative morphological hybrids (PMH) with plausibly higher fitness than the parent species indicates the need to confirm whether hybridization occurs within the complex. In this sense, we assessed the dynamics of genetic divergence and hybridization within the species complex using a panel of 10 microsatellite loci, and sequences of the mitochondrial control region (D-loop) and the intron-free rhodopsin (RH1) gene. The analyses revealed the presence of three distinct genetic clusters, large genetic distances using D-loop sequences, and distinctive mutations within the RH1 gene. These results are consistent with the descriptions of the three species. Two microsatellite loci had signatures of divergent selection, indicating that they are linked to genomic regions that are crucial for speciation. Furthermore, nonsynonymous mutations within the RH1 gene detected in S. cheni and "Kumano" (a PMH) suggest dissimilar adaptations related to visual perception in dim-light environments. The presence of individuals with admixed ancestry between two species confirmed hybridization. The presence of nonsynonymous mutations within the RH1 gene and the admixed ancestry of the "Kumano" morphotype highlight the potential role of hybridization in generating novelties within the species complex. We discuss possible outcomes of hybridization within the species complex, considering hybrid fitness and assortative mating. Overall, our findings indicate that the genetic divergence of each species is maintained in the presence of hybridization, as expected in a scenario of speciation-with-gene-flow.

The role of genomic signatures of directional selection and demographic history in the population structure of a marine teleost with high gene flow

Recent studies have uncovered patterns of genomic divergence in marine teleosts where panmixia due to high gene flow has been the general paradigm. These signatures of divergent selection are often impacted by structural variants, acting as "supergenes" facilitating local adaptation. The highly dispersing European plaice (Pleuronectes platessa)-in which putative structural variants (i.e., inversions) have been identified-has successfully colonized the brackish water ecosystem of the Baltic Sea. Thus, the species represents an ideal opportunity to investigate how the interplay of gene flow, structural variants, natural selection, past demographic history, and gene flow impacts on population (sub)structuring in marine systems. Here, we report on the generation of an annotated draft plaice genome assembly in combination with population sequencing data-following the salinity gradient from the Baltic Sea into the North Sea together with samples from Icelandic waters-to illuminate genome-wide patterns of divergence. Neutral markers pointed at large-scale panmixia across the European continental shelf associated with high gene flow and a common postglacial colonization history of shelf populations. However, based on genome-wide outlier loci, we uncovered signatures of population substructuring among the European continental shelf populations, i.e., suggesting signs of ongoing selection. Genome-wide selection analyses (xp-EHH) and the identification of genes within genomic regions of recent selective sweeps-overlapping with the outlier loci-suggest that these represent the signs of divergent selection. Our findings provide support for genomic divergence driven by local adaptation in the face of high gene flow and elucidate the relative importance of demographic history versus adaptive divergence in shaping the contemporary population genetic structure of a marine teleost. The role of the putative inversion(s) in the substructuring-and potentially ongoing adaptation-was seemingly not substantial.

Population transcriptomic sequencing reveals allopatric divergence and local adaptation in Pseudotaxus chienii (Taxaceae)

BackgroundElucidating the effects of geography and selection on genetic variation is critical for understanding the relative importance of adaptation in driving differentiation and identifying the environmental factors underlying its occurrence. Adaptive genetic variation is common in tree species, especially widely distributed long-lived species. Pseudotaxus chienii can occupy diverse habitats with environmental heterogeneity and thus provides an ideal material for investigating the process of population adaptive evolution. Here, we characterize genetic and expression variation patterns and investigate adaptive genetic variation in P. chienii populations.ResultsWe generated population transcriptome data and identified 13,545 single nucleotide polymorphisms (SNPs) in 5037 unigenes across 108 individuals from 10 populations. We observed lower nucleotide diversity (π = 0.000701) among the 10 populations than observed in other gymnosperms. Significant negative correlations between expression diversity and nucleotide diversity in eight populations suggest that when the species adapts to the surrounding environment, gene expression and nucleotide diversity have a reciprocal relationship. Genetic structure analyses indicated that each distribution region contains a distinct genetic group, with high genetic differentiation among them due to geographical isolation and local adaptation. We used FST outlier, redundancy analysis, and latent factor mixed model methods to detect molecular signatures of local adaptation. We identified 244 associations between 164 outlier SNPs and 17 environmental variables. The mean temperature of the coldest quarter, soil Fe and Cu contents, precipitation of the driest month, and altitude were identified as the most important determinants of adaptive genetic variation. Most candidate unigenes with outlier signatures were related to abiotic and biotic stress responses, and the monoterpenoid biosynthesis and ubiquitin-mediated proteolysis KEGG pathways were significantly enriched in certain populations and deserve further attention in other long-lived trees.ConclusionsDespite the strong population structure in P. chienii, genomic data revealed signatures of divergent selection associated with environmental variables. Our research provides SNPs, candidate unigenes, and biological pathways related to environmental variables to facilitate elucidation of the genetic variation in P. chienii in relation to environmental adaptation. Our study provides a promising tool for population genomic analyses and insights into the molecular basis of local adaptation.

Urbanization without isolation: the absence of genetic structure among cities and forests in the tiny acorn ant Temnothorax nylanderi.

Urban alteration of neutral and adaptive evolutionary processes is still underexplored. Using a genome-wide SNP dataset, we investigated (i) urban-induced modifications of population demography, genetic diversity and population structure and (ii) signature of divergent selection between urban and forest populations in the ant species, Temnothorax nylanderi. Our results did not reveal an impact of urbanization on neutral processes since we observed: (i) analogous genetic diversity among paired urban/forest sites and two control populations; (ii) weak population genetic structure explained neither by habitat (urban versus forest) nor by geography; (iii) a remarkably similar demographic history across populations with an ancestral growth followed by a recent decline, regardless of their current habitat or geographical location. The micro-geographical home range of ants may explain their resilience to urbanization. Finally, we detected 19 candidate loci discriminating urban/forest populations and associated with core cellular components, molecular function or biological process. Two of these loci were associated with a gene ontology term that was previously found to belong to a module of co-expressed genes related to caste phenotype. These results call for transcriptomics analyses to identify genes associated with ant social traits and to infer their potential role in urban adaptation.

Signatures of divergent selection for cold tolerance in maize

Divergently selected genotypes can be used for detecting the genomic regions affecting the selected trait (selection signature). Moreover, the genetic distances (GDs) among divergently selected lines can be correlated with the agronomic performances of the crosses among them. Using as source the maize F2 of B73 × IABO78, we previously conducted four cycles of divergent recurrent selection and three cycles of divergent selection in inbreeding for cold tolerance at germination. We finally obtained 10 lines selected for low (L) and 10 lines selected for high (H) cold tolerance, which exhibited a notable divergence for both the selected and associated traits. Herein, we investigated the 20 lines and the 28 single diallel crosses among eight random lines (four L and four H); the main objectives were to identify the putative regions controlling the selected and associated traits and to study the relationships between crosses performances and GDs among their parental lines. Allele frequencies at 932 recombination blocks based on 19,220 polymorphic SNPs were obtained for the two lines’ groups; the F ST calculated across sliding windows indicated 18 regions highly divergent between groups. The increasing alleles for cold tolerance were contributed by both parents, consistently with the transgressive segregations previously found. Several regions associated to DG also affected various agronomic traits. The cross performances showed some relationships with the genetic distances among parental lines for traits affected by dominance, provided that all crosses were considered, while these relationships vanished when only L × H crosses were examined.

Cunningham's skinks show low genetic connectivity and signatures of divergent selection across its distribution.

Establishing corridors of connecting habitat has become a mainstay conservation strategy to maintain gene flow and facilitate climate‐driven range shifts. Yet, little attention has been given to ascertaining the extent to which corridors will benefit philopatric species, which might exhibit localized adaptation. Measures of genetic connectivity and adaptive genetic variation across species’ ranges can help fill this knowledge gap. Here, we characterized the spatial genetic structure of Cunningham's skink (Egernia cunninghami), a philopatric species distributed along Australia's Great Dividing Range, and assessed evidence of localized adaptation. Analysis of 4,274 SNPs from 94 individuals sampled at four localities spanning 500 km and 4° of latitude revealed strong genetic structuring at neutral loci (mean F ST ± SD = 0.603 ± 0.237) among the localities. Putatively neutral SNPs and those under divergent selection yielded contrasting spatial patterns, with the latter identifying two genetically distinct clusters. Given low genetic connectivity of the four localities, we suggest that the natural movement rate of this species is insufficient to keep pace with spatial shifts to its climate envelope, irrespective of habitat availability. In addition, our finding of localized adaptation highlights the risk of outbreeding depression should the translocation of individuals be adopted as a conservation management strategy.

Genome-wide discovery of single nucleotide polymorphisms (SNPs) and single nucleotide variants (SNVs) in deep-sea mussels: Potential use in population genomics and cross-species application

The present study aimed to generate genome-wide single nucleotide polymorphisms (SNPs) for the deep-sea mussel Bathymodiolus platifrons via a combination of genome survey sequencing and the type IIB endonuclease restriction-site associated DNA (2b-RAD) sequencing, assess the potential use of SNPs in detecting fine-sale population genetic structure and signatures of divergent selection, as well as their cross-species application in other bathymodioline mussels. Genome survey sequencing was conducted for one individual of B. platifrons. De novo assembly resulted in 781,720 sequences with a scaffold N50 of 2.9kb. Using these sequences as a reference, 9307 genome-wide SNPs were identified by 2b-RAD for 28 B. platifrons individuals collected from a seep and a vent population. Among these SNPs, nine outliers showed significant evidence for divergent selection, and their positions in the genes or scaffolds were identified. The FST estimated based on the putative neutral SNPs was low (0.0126) indicating the two B. platifrons populations having a high genetic connectivity. However, the permutation test detected significant differences (P<0.00001), indicating the two populations having clearly detectable genetic differentiation. The Bayesian clustering analyses and principle component analyses (PCA) performed based on either the putative neutral or outlier SNPs also showed that these two populations were genetically differentiated. In addition, 2b-RAD was also conducted to detect 10,199, 6429, and 3811 single nucleotide variants (SNVs) respectively in the bathymodioline mussels Bathymodiolus japonicus, Bathymodiolus aduloides and Idas sp. with different phylogenetic distances from B. platifrons. Overall, our study has demonstrated the feasibility and effectiveness of combining genome survey sequencing and 2b-RAD to rapidly generate genomic resources for use in fine-scale population genetic studies, and various cross-species applications.

Rapid evolution of chemosensory receptor genes in a pair of sibling species of orchid bees (Apidae: Euglossini).

BackgroundInsects rely more on chemical signals (semiochemicals) than on any other sensory modality to find, identify, and choose mates. In most insects, pheromone production is typically regulated through biosynthetic pathways, whereas pheromone sensory detection is controlled by the olfactory system. Orchid bees are exceptional in that their semiochemicals are not produced metabolically, but instead male bees collect odoriferous compounds (perfumes) from the environment and store them in specialized hind-leg pockets to subsequently expose during courtship display. Thus, the olfactory sensory system of orchid bees simultaneously controls male perfume traits (sender components) and female preferences (receiver components). This functional linkage increases the opportunities for parallel evolution of male traits and female preferences, particularly in response to genetic changes of chemosensory detection (e.g. Odorant Receptor genes). To identify whether shifts in pheromone composition among related lineages of orchid bees are associated with divergence in chemosensory genes of the olfactory periphery, we searched for patterns of divergent selection across the antennal transcriptomes of two recently diverged sibling species Euglossa dilemma and E. viridissima.ResultsWe identified 3185 orthologous genes including 94 chemosensory loci from five different gene families (Odorant Receptors, Ionotropic Receptors, Gustatory Receptors, Odorant Binding Proteins, and Chemosensory Proteins). Our results revealed that orthologs with signatures of divergent selection between E. dilemma and E. viridissima were significantly enriched for chemosensory genes. Notably, elevated signals of divergent selection were almost exclusively observed among chemosensory receptors (i.e. Odorant Receptors).ConclusionsOur results suggest that rapid changes in the chemosensory gene family occurred among closely related species of orchid bees. These findings are consistent with the hypothesis that strong divergent selection acting on chemosensory receptor genes plays an important role in the evolution and diversification of insect pheromone systems.Electronic supplementary materialThe online version of this article (doi:10.1186/s12862-015-0451-9) contains supplementary material, which is available to authorized users.

Interspecific gene flow and maintenance of species integrity in oaks

Oak species show a wide variation in morphological and physiological characters, and species boundaries between closely related species are often not clear-cut. Still, despite frequent interspecific gene flow, oaks maintain distinct morphological and physiological adaptations. In sympatric stands, spatial distribution of species with different ecological requirements is not random but constrained by soil and other microenvironmental factors. Pre-zygotic isolation (e.g. cross incompatibilities, asynchrony in flowering, pollen competition) and post-zygotic isolation (divergent selection) contribute to the maintenance of species integrity in sympatric oak stands. The antagonistic effects of interspecific gene flow and divergent selection are reflected in the low genetic differentiation between hybridizing oak species at most genomic regions interspersed by regions with signatures of divergent selection (outlier regions). In the near future, the availability of high-density genetic linkage maps anchored to scaffolds of a sequenced Q. robur genome will allow to characterize the underlying genes in these outlier regions and their putative role in reproductive isolation between species. Reciprocal transplant experiments of seedlings between parental environments can be used to characterize selection on outlier genes. High transferability of gene-based markers will enable comparative outlier screens in different oak species.

Extensive linkage disequilibrium and parallel adaptive divergence across threespine stickleback genomes

Population genomic studies are beginning to provide a more comprehensive view of dynamic genome-scale processes in evolution. Patterns of genomic architecture, such as genomic islands of increased divergence, may be important for adaptive population differentiation and speciation. We used next-generation sequencing data to examine the patterns of local and long-distance linkage disequilibrium (LD) across oceanic and freshwater populations of threespine stickleback, a useful model for studies of evolution and speciation. We looked for associations between LD and signatures of divergent selection, and assessed the role of recombination rate variation in generating LD patterns. As predicted under the traditional biogeographic model of unidirectional gene flow from ancestral oceanic to derived freshwater stickleback populations, we found extensive local and long-distance LD in fresh water. Surprisingly, oceanic populations showed similar patterns of elevated LD, notably between large genomic regions previously implicated in adaptation to fresh water. These results support an alternative biogeographic model for the stickleback radiation, one of a metapopulation with appreciable bi-directional gene flow combined with strong divergent selection between oceanic and freshwater populations. As predicted by theory, these processes can maintain LD within and among genomic islands of divergence. These findings suggest that the genomic architecture in oceanic stickleback populations may provide a mechanism for the rapid re-assembly and evolution of multi-locus genotypes in newly colonized freshwater habitats, and may help explain genetic mapping of parallel phenotypic variation to similar loci across independent freshwater populations.