The contribution of gene flow, selection, and genetic drift to five thousand years of human allele frequency change.

Genomic time series from experimental evolution studies and ancient DNA datasets offer us a chance to directly observe the interplay of various evolutionary forces. We show how the genome-wide variance in allele frequency change between two time points can be decomposed into the contributions of gene flow, genetic drift, and linked selection. In closed populations, the contribution of linked selection is identifiable because it creates covariances between time intervals, and genetic drift does not. However, repeated gene flow between populations can also produce directionality in allele frequency change, creating covariances. We show how to accurately separate the fraction of variance in allele frequency change due to admixture and linked selection in a population receiving gene flow. We use two human ancient DNA datasets, spanning around 5,000 y, as time transects to quantify the contributions to the genome-wide variance in allele frequency change. We find that a large fraction of genome-wide change is due to gene flow. In both cases, after correcting for known major gene flow events, we do not observe a signal of genome-wide linked selection. Thus despite the known role of selection in shaping long-term polymorphism levels, and an increasing number of examples of strong selection on single loci and polygenic scores from ancient DNA, it appears to be gene flow and drift, and not selection, that are the main determinants of recent genome-wide allele frequency change. Our approach should be applicable to the growing number of contemporary and ancient temporal population genomics datasets.

Uncovering ghost introgression through genomic analysis of a distinct eastern Asian hickory species.

Ghost introgression, or the transfer of genetic material from extinct or unsampled lineages to sampled species, has attracted much attention. However, conclusive evidence for ghost introgression, especially in plant species, remains scarce. Here, we newly assembled chromosome-level genomes for both Carya sinensis and Carya cathayensis, and additionally re-sequenced the whole genomes of 43 C. sinensis individuals as well as 11 individuals representing 11 diploid hickory species. These genomic datasets were used to investigate the reticulation and bifurcation patterns within the genus Carya (Juglandaceae), with a particular focus on the beaked hickory C. sinensis. By combining the D-statistic and BPP methods, we obtained compelling evidence that supports the occurrence of ghost introgression in C. sinensis from an extinct ancestral hickory lineage. This conclusion was reinforced through the phylogenetic network analysis and a genome scan method VolcanoFinder, the latter of which can detect signatures of adaptive introgression from unknown donors. Our results not only dispel certain misconceptions about the phylogenetic history of C. sinensis but also further refine our understanding of Carya's biogeography via divergence estimates. Moreover, the successful integration of the D-statistic and BPP methods demonstrates their efficacy in facilitating a more precise identification of introgression types.

Secondary Contact, Introgressive Hybridization, and Genome Stabilization in Sticklebacks.

Advances in genomic studies have revealed that hybridization in nature is pervasive and raised questions about the dynamics of different genetic and evolutionary factors following the initial hybridization event. While recent research has proposed that the genomic outcomes of hybridization might be predictable to some extent, many uncertainties remain. With comprehensive whole-genome sequence data, we investigated the genetic introgression between 2 divergent lineages of 9-spined sticklebacks (Pungitius pungitius) in the Baltic Sea. We found that the intensity and direction of selection on the introgressed variation has varied across different genomic elements: while functionally important regions displayed reduced rates of introgression, promoter regions showed enrichment. Despite the general trend of negative selection, we identified specific genomic regions that were enriched for introgressed variants, and within these regions, we detected footprints of selection, indicating adaptive introgression. Geographically, we found the selection against the functional changes to be strongest in the vicinity of the secondary contact zone and weaken as a function of distance from the initial contact. Altogether, the results suggest that the stabilization of introgressed variation in the genomes is a complex, multistage process involving both negative and positive selection. In spite of the predominance of negative selection against introgressed variants, we also found evidence for adaptive introgression variants likely associated with adaptation to Baltic Sea environmental conditions.

Divergent Selection in Low Recombination Regions Shapes the Genomic Islands in Two Incipient Shorebird Species.

Speciation in the face of gene flow is usually associated with a heterogeneous genomic landscape of divergence in nascent species pairs. However, multiple factors, such as divergent selection and local recombination rate variation, can influence the formation of these genomic islands. Examination of the genomic landscapes of species pairs that are still in the early stages of speciation provides an insight into this conundrum. In this study, population genomic analyses were undertaken using a wide range of sampling and whole-genome resequencing data from 96 unrelated individuals of Kentish plover (Charadrius alexandrinus) and white-faced plover (Charadrius dealbatus). We suggest that the two species exhibit varying levels of population admixture along the Chinese coast and on the Taiwan Island. Genome-wide analyses for introgression indicate that ancient introgression had occurred in Taiwan population, and gene flow is still ongoing in mainland coastal populations. Furthermore, we identified a few genomic regions with significant levels of interspecific differentiation and local recombination suppression, which contain several genes potentially associated with disease resistance, coloration, and regulation of plumage molting and thus may be relevant to the phenotypic and ecological divergence of the two nascent species. Overall, our findings suggest that divergent selection in low recombination regions may be a main force in shaping the genomic islands in two incipient shorebird species.

Inference of Locus-Specific Population Mixtures from Linked Genome-Wide Allele Frequencies.

Admixture between populations and species is common in nature. Since the influx of new genetic material might be either facilitated or hindered by selection, variation in mixture proportions along the genome is expected in organisms undergoing recombination. Various graph-based models have been developed to better understand these evolutionary dynamics of population splits and mixtures. However, current models assume a single mixture rate for the entire genome and do not explicitly account for linkage. Here, we introduce TreeSwirl, a novel method for inferring branch lengths and locus-specific mixture proportions by using genome-wide allele frequency data, assuming that the admixture graph is known or has been inferred. TreeSwirl builds upon TreeMix that uses Gaussian processes to estimate the presence of gene flow between diverged populations. However, in contrast to TreeMix, our model infers locus-specific mixture proportions employing a hidden Markov model that accounts for linkage. Through simulated data, we demonstrate that TreeSwirl can accurately estimate locus-specific mixture proportions and handle complex demographic scenarios. It also outperforms related D- and f-statistics in terms of accuracy and sensitivity to detect introgressed loci.

Phylogenetic Conflict Between Species Tree and Maternally Inherited Gene Trees in a Clade of Emberiza Buntings (Aves: Emberizidae).

Different genomic regions may reflect conflicting phylogenetic topologies primarily due to incomplete lineage sorting and/or gene flow. Genomic data are necessary to reconstruct the true species tree and explore potential causes of phylogenetic conflict. Here, we investigate the phylogenetic relationships of 4 Emberiza species (Aves: Emberizidae) and discuss the potential causes of the observed mitochondrial non-monophyly of Emberiza godlewskii (Godlewski's bunting) using phylogenomic analyses based on whole genome resequencing data from 41 birds. Analyses based on both the whole mitochondrial genome and ~39 kilobases from the non-recombining W chromosome reveal sister relationships between each the northern and southern populations of E. godlewskii with E. cioides and E. cia, respectively. In contrast, the monophyly of E. godlewskii is reflected by the phylogenetic signal of autosomal and Z chromosomal sequence data as well as demographic inference analyses, which-in combination-support the following tree topology: ([{E. godlewskii, E. cia}, E. cioides], E. jankowskii). Using D-statistics, we detected multiple gene flow events among different lineages, indicating pervasive introgressive hybridization within this clade. Introgression from an unsampled lineage that is sister to E. cioides or introgression from an unsampled mitochondrial + W chromosomal lineage of E. cioides into northern E. godlewskii may explain the phylogenetic conflict between the species tree estimated from genome-wide data versus mtDNA/W tree topologies. These results underscore the importance of using genomic data for phylogenetic reconstruction and species delimitation.

Complex Polyploids: Origins, Genomic Composition, and Role of Introgressed Alleles.

Introgression allows polyploid species to acquire new genomic content from diploid progenitors or from other unrelated diploid or polyploid lineages, contributing to genetic diversity and facilitating adaptive allele discovery. In some cases, high levels of introgression elicit the replacement of large numbers of alleles inherited from the polyploid's ancestral species, profoundly reshaping the polyploid's genomic composition. In such complex polyploids, it is often difficult to determine which taxa were the progenitor species and which taxa provided additional introgressive blocks through subsequent hybridization. Here, we use population-level genomic data to reconstruct the phylogenetic history of Betula pubescens (downy birch), a tetraploid species often assumed to be of allopolyploid origin and which is known to hybridize with at least four other birch species. This was achieved by modeling polyploidization and introgression events under the multispecies coalescent and then using an approximate Bayesian computation rejection algorithm to evaluate and compare competing polyploidization models. We provide evidence that B. pubescens is the outcome of an autoploid genome doubling event in the common ancestor of B. pendula and its extant sister species, B. platyphylla, that took place approximately 178,000-188,000 generations ago. Extensive hybridization with B. pendula, B. nana, and B. humilis followed in the aftermath of autopolyploidization, with the relative contribution of each of these species to the B. pubescens genome varying markedly across the species' range. Functional analysis of B. pubescens loci containing alleles introgressed from B. nana identified multiple genes involved in climate adaptation, while loci containing alleles derived from B. humilis revealed several genes involved in the regulation of meiotic stability and pollen viability in plant species.

Multi-generation genetic contributions of immigrants reveal cryptic elevated and sex-biased effective gene flow within a natural meta-population.

Impacts of immigration on micro-evolution and population dynamics fundamentally depend on net rates and forms of resulting gene flow into recipient populations. Yet, the degrees to which observed rates and sex ratios of physical immigration translate into multi-generational genetic legacies have not been explicitly quantified in natural meta-populations, precluding inference on how movements translate into effective gene flow and eco-evolutionary outcomes. Our analyses of three decades of complete song sparrow (Melospiza melodia) pedigree data show that multi-generational genetic contributions from regular natural immigrants substantially exceeded those from contemporary natives, consistent with heterosis-enhanced introgression. However, while contributions from female immigrants exceeded those from female natives by up to three-fold, male immigrants' lineages typically went locally extinct soon after arriving. Both the overall magnitude, and the degree of female bias, of effective gene flow therefore greatly exceeded those which would be inferred from observed physical arrivals, altering multiple eco-evolutionary implications of immigration.

Assessing the risk of climate maladaptation for Canadian polar bears.

The Arctic is warming four times faster than the rest of the world, threatening the persistence of many Arctic species. It is uncertain if Arctic wildlife will have sufficient time to adapt to such rapidly warming environments. We used genetic forecasting to measure the risk of maladaptation to warming temperatures and sea ice loss in polar bears (Ursus maritimus) sampled across the Canadian Arctic. We found evidence for local adaptation to sea ice conditions and temperature. Forecasting of genome-environment mismatches for predicted climate scenarios suggested that polar bears in the Canadian high Arctic had the greatest risk of becoming maladapted to climate warming. While Canadian high Arctic bears may be the most likely to become maladapted, all polar bears face potentially negative outcomes to climate change. Given the importance of the sea ice habitat to polar bears, we expect that maladaptation to future warming is already widespread across Canada.

Broken Ring Speciation in California Mygalomorph Spiders (Nemesiidae, Calisoga).

AbstractIdealized ring species, with approximately continuous gene flow around a geographic barrier but singular reproductive isolation at a ring terminus, are rare in nature. A broken ring species model preserves the geographic setting and fundamental features of an idealized model but accommodates varying degrees of gene flow restriction over complex landscapes through evolutionary time. Here we examine broken ring species dynamics in Calisoga spiders, which, like the classic ring species Ensatina salamanders, are distributed around the Central Valley of California. Using nuclear and mitogenomic data, we test key predictions of common ancestry, ringlike biogeography, biogeographic timing, population connectivity, and terminal overlap. We show that a ring complex of populations shares a single common ancestor, and from an ancestral area in the Sierra Nevada mountains, two distributional and phylogenomic arms encircle the Central Valley. Isolation by distance occurs along these distributional arms, although gene flow restriction is also evident. Where divergent lineages meet in the South Coast Ranges, we find rare lineage sympatry, without evidence for nuclear gene flow and with clear evidence for morphological and ecological divergence. We discuss general insights provided by broken ring species and how such a model could be explored and extended in other systems and future studies.

Conditionally Deleterious Mutation Load Accumulates in Genomic Islands of Local Adaptation but Can Be Purged with Sufficient Genotypic Redundancy.

AbstractLocal adaptation frequently evolves in patches or environments that are connected via migration. In these cases, genomic regions that are linked to a locally adapted locus experience reduced effective migration rates. Via individual-based simulations of a two-patch system, we show that this reduced effective migration results in the accumulation of conditionally deleterious mutations, but not universally deleterious mutations, adjacent to adaptive loci. When there is redundancy in the genetic basis of local adaptation (i.e., genotypic redundancy), turnover of locally adapted polymorphisms allows conditionally deleterious mutation load to be purged. The amount of mutational load that accumulates adjacent to locally adapted loci is dependent on redundancy, recombination rate, migration rate, population size, strength of selection, and the phenotypic effect size of adaptive alleles. Our results highlight the need to be cautious when interpreting patterns of local adaptation at the level of phenotype or fitness, as the genetic basis of local adaptation can be transient, and evolution may confer a degree of maladaptation to nonlocal environments.

Multigenerational Fitness Effects of Natural Immigration Indicate Strong Heterosis and Epistatic Breakdown in a Wild Bird Population.

AbstractThe fitness of immigrants and their descendants produced within recipient populations fundamentally underpins the genetic and population dynamic consequences of immigration. Immigrants can in principle induce contrasting genetic effects on fitness across generations, reflecting multifaceted additive, dominance, and epistatic effects. Yet full multigenerational and sex-specific fitness effects of regular immigration have not been quantified within naturally structured systems, precluding inference on underlying genetic architectures and population outcomes. We used four decades of song sparrow (Melospiza melodia) life history and pedigree data to quantify fitness of natural immigrants, natives, and their F1, F2, and backcross descendants and test for evidence of nonadditive genetic effects. Values of key fitness components (including adult lifetime reproductive success and zygote survival) of F1 offspring of immigrant-native matings substantially exceeded their parent mean, indicating strong heterosis. Meanwhile, F2 offspring of F1-F1 matings had notably low values, indicating surprisingly strong epistatic breakdown. Furthermore, magnitudes of effects varied among fitness components and differed between female and male descendants. These results demonstrate that strong nonadditive genetic effects on fitness can arise within weakly structured and fragmented populations experiencing frequent natural immigration. Such effects will substantially affect the net degree of effective gene flow and resulting local genetic introgression and adaptation.

Resource Variation Within and Between Patches: Where Exploitation Competition, Local Adaptation, and Kin Selection Meet.

AbstractIn patch- or habitat-structured populations, different processes can favor adaptive polymorphism at different scales. While spatial heterogeneity can generate spatially disruptive selection favoring variation between patches, local competition can lead to locally disruptive selection promoting variation within patches. So far, almost all theory has studied these two processes in isolation. Here, we use mathematical modeling to investigate how resource variation within and between habitats influences the evolution of variation in a consumer population where individuals compete in finite patches connected by dispersal. We find that locally and spatially disruptive selection typically act in concert, favoring polymorphism under a wider range of conditions than when in isolation. But when patches are small and dispersal between them is low, kin competition inhibits the emergence of polymorphism, especially when the latter is driven by local competition for resources. We further use our model to clarify what comparisons between trait and neutral genetic differentiation (QST/FST comparisons) can tell about the nature of selection. Overall, our results help us understand the interaction between two major drivers of polymorphism: locally and spatially disruptive selection, and how this interaction is modulated by the unavoidable effects of kin selection under limited dispersal.

Adaptive divergence, historical population dynamics, and simulation of suitable distributions for Picea Meyeri and P. Mongolica at the whole-genome level.

The taxonomic classification of Picea meyeri and P. mongolica has long been controversial. To investigate the genetic relatedness, evolutionary history, and population history dynamics of these species, genotyping-by-sequencing (GBS) technology was utilized to acquire whole-genome single nucleotide polymorphism (SNP) markers, which were subsequently used to assess population structure, population dynamics, and adaptive differentiation. Phylogenetic and population structural analyses at the genomic level indicated that although the ancestor of P. mongolica was a hybrid of P. meyeri and P. koraiensis, P. mongolica is an independent Picea species. Additionally, P. mongolica is more closely related to P. meyeri than to P. koraiensis, which is consistent with its geographic distribution. There were up to eight instances of interspecific and intraspecific gene flow between P. meyeri and P. mongolica. The P. meyeri and P. mongolica effective population sizes generally decreased, and Maxent modeling revealed that from the Last Glacial Maximum (LGM) to the present, their habitat areas decreased initially and then increased. However, under future climate scenarios, the habitat areas of both species were projected to decrease, especially under high-emission scenarios, which would place P. mongolica at risk of extinction and in urgent need of protection. Local adaptation has promoted differentiation between P. meyeri and P. mongolica. Genotype‒environment association analysis revealed 96,543 SNPs associated with environmental factors, mainly related to plant adaptations to moisture and temperature. Selective sweeps revealed that the selected genes among P. meyeri, P. mongolica and P. koraiensis are primarily associated in vascular plants with flowering, fruit development, and stress resistance. This research enhances our understanding of Picea species classification and provides a basis for future genetic improvement and species conservation efforts.

Anti-predator defences are linked with high levels of genetic differentiation in frogs.

Predator-prey interactions have been suggested as drivers of diversity in different lineages, and the presence of anti-predator defences in some clades is linked to higher rates of diversification. Warning signals are some of the most widespread defences in the animal world, and there is evidence of higher diversification rates in aposematic lineages. The mechanisms behind such species richness, however, are still unclear. Here, we test whether lineages that use aposematism as anti-predator defence exhibit higher levels of genetic differentiation between populations, leading to increased opportunities for divergence. We collated from the literature more than 3000 pairwise genetic differentiation values across more than 700 populations from over 60 amphibian species. We find evidence that over short geographical distances, populations of species of aposematic lineages exhibit greater genetic divergence relative to species that are not aposematic. Our results support a scenario where the use of warning signals could restrict gene flow, and suggest that anti-predator defences could impact divergence between populations and potentially have effects at a macro-evolutionary scale.

Phylogenomic analyses re-examine the evolution of reinforcement and hypothesized hybrid speciation in Phlox wildflowers.

The tree of life is riddled with reticulate evolutionary histories, and some clades, such as the eastern standing Phlox, appear to be hotspots of hybridization. In this group, there are two cases of reinforcement and nine hypothesized hybrid species. Given their historical importance in our understanding of plant speciation, the relationships between these taxa and the role of hybridization in their diversification require genomic validation. Using phylogenomic analyses, we resolve the evolutionary relationships of the eastern standing Phlox and evaluate hypotheses about whether and how hybridization and gene flow played a role in their diversification. Our results provide novel resolution of the phylogenetic relationships in this group, including paraphyly across some taxa. We identify gene flow during one case of reinforcement and find genomic support for a hybrid lineage underlying one of the five hypothesized homoploid hybrid speciation events. Additionally, we estimate the ancestries of four allotetraploid hybrid species. Our results are consistent with hybridization contributing to diverse evolutionary outcomes within this group; although, not as extensively as previously hypothesized. This study demonstrates the importance of phylogenomics in evaluating hypothesized evolutionary histories of non-model systems and adds to the growing support of interspecific genetic exchange in the generation of biodiversity.

Scots pine - panmixia and the elusive signal of genetic adaptation.

Scots pine is the foundation species of diverse forested ecosystems across Eurasia and displays remarkable ecological breadth, occurring in environments ranging from temperate rainforests to arid tundra margins. Such expansive distributions can be favored by various demographic and adaptive processes and the interactions between them. To understand the impact of neutral and selective forces on genetic structure in Scots pine, we conducted range-wide population genetic analyses on 2321 trees from 202 populations using genotyping-by-sequencing, reconstructed the recent demography of the species and examined signals of genetic adaptation. We found a high and uniform genetic diversity across the entire range (global FST 0.048), no increased genetic load in expanding populations and minor impact of the last glacial maximum on historical population sizes. Genetic-environmental associations identified only a handful of single-nucleotide polymorphisms significantly linked to environmental gradients. The results suggest that extensive gene flow is predominantly responsible for the observed genetic patterns in Scots pine. The apparent missing signal of genetic adaptation is likely attributed to the intricate genetic architecture controlling adaptation to multi-dimensional environments. The panmixia metapopulation of Scots pine offers a good study system for further exploration into how genetic adaptation and plasticity evolve under gene flow and changing environment.

Weak local adaptation to drought in seedlings of a widespread conifer.

Tree seedlings from populations native to drier regions are often assumed to be more drought tolerant than those from wetter provenances. However, intraspecific variation in drought tolerance has not been well-characterized despite being critical for developing climate change mitigation and adaptation strategies, and for predicting the effects of drought on forests. We used a large-scale common garden drought-to-death experiment to assess range-wide variation in drought tolerance, measured by decline of photosynthetic efficiency, growth, and plastic responses to extreme summer drought in seedlings of 73 natural populations of the two main varieties of Douglas-fir (Pseudotsuga menziesii var. menziesii and var. glauca). Local adaptation to drought was weak in var. glauca and nearly absent in menziesii. Var. glauca showed higher tolerance to drought but slower growth than var. menziesii. Clinal variation in drought tolerance and growth species-wide was mainly associated with temperature rather than precipitation. A higher degree of plasticity for growth was observed in var. menziesii in response to extreme drought. Genetic variation for drought tolerance in seedlings within varieties is maintained primarily within populations. Selective breeding within populations may facilitate adaptation to drought more than assisted gene flow.

Climatic variation allows montane willows to escape an adaptive trade-off.

Adaptive responses to climate change, based on heritable variation in stress tolerance, may be important for plant population persistence. It is unclear which populations will mount the strongest future adaptive responses. It may be fruitful to identify populations that have escaped trade-offs among performance traits, which can hinder adaptation. Barring strong genetic constraints, the extent of trade-offs may depend on spatial relationships among climate variables shaping different traits. Here, we test for climate-driven ecotypic variation and trade-offs among drought and freezing sensitivity, and growth, for Lemmon's willow (Salix lemmonii) in a common garden study of 90 genotypes from 38 sites in the Sierra Nevada, USA. Salix lemmonii exhibits ecotypic variation in leaf turgor loss point, a measure of drought sensitivity, from -0.95 to -0.74 MPa along a gradient of spring snowpack. We also find variation in spring freezing sensitivity with minimum May temperature. However, we find no trade-off, as the climatic gradients shaping these traits are spatially uncorrelated in our study region, despite being negatively correlated across the Sierra Nevada. Species may escape adaptive trade-offs in geographic regions where climate variables are spatially decoupled. These regions may represent valuable reservoirs of heritable adaptive phenotypic variation.

The opposed forces of differentiation and admixture across glacial cycles in the butterfly Aglais urticae.

Glacial cycles lead to periodic population interbreeding and isolation in warm-adapted species, which impact genetic structure and evolution. However, the effects of these processes on highly mobile and more cold-tolerant species are not well understood. This study aims to shed light on the phylogeographic history of Aglais urticae, a butterfly species with considerable dispersal ability, and a wide Palearctic distribution reaching the Arctic. Through the analysis of genomic data, four main genetic lineages are identified: European, Sierra Nevada, Sicily/Calabria/Peloponnese, and Eastern. The results indicate that the Sardo-Corsican endemic taxon ichnusa is a distinct species. The split between the relict lineages in southern Europe and the main European lineage is estimated to have happened 400-450 thousand years ago, with admixture observed during the Quaternary glacial cycles, and still ongoing, albeit to a much smaller extent. These results suggest that these lineages may be better treated as subspecific parapatric taxa. Ecological niche modelling supported the existence of both Mediterranean and extra-Mediterranean refugia during the glacial periods, with the main one located on the Atlantic coast. Nevertheless, gene flow between populations was possible, indicating that both differentiation and admixture have acted continuously across glacial cycles in this cold-tolerant butterfly, generally balancing each other but producing differentiated lineages in the southern peninsulas. We conclude that the population dynamics and the processes shaping the population genetic structure of cold-adapted species during the Quaternary ice ages may be different than those classically accepted for warm-adapted species.