Hybrid speciation driven by multilocus introgression of ecological traits.

Hybridization allows adaptations to be shared among lineages and may trigger the evolution of new species1,2. However, convincing examples of homoploid hybrid speciation remain rare because it is challenging to demonstrate that hybridization was crucial in generating reproductive isolation3. Here we combine population genomic analysis with quantitative trait locus mapping of species-specific traits to examine a case of hybrid speciation in Heliconius butterflies. We show that Heliconius elevatus is a hybrid species that is sympatric with both parents and has persisted as an independently evolving lineage for at least 180,000 years. This is despite pervasive and ongoing gene flow with one parent, Heliconius pardalinus, which homogenizes 99% of their genomes. The remaining 1% introgressed from the other parent, Heliconius melpomene, and is scattered widely across the H. elevatus genome in islands of divergence from H. pardalinus. These islands contain multiple traits that are under disruptive selection, including colour pattern, wing shape, host plant preference, sex pheromones and mate choice. Collectively, these traits place H. elevatus on its own adaptive peak and permit coexistence with both parents. Our results show that speciation was driven by introgression of ecological traits, and that speciation with gene flow is possible with a multilocus genetic architecture.

Introgression of an All-Stage and Broad-Spectrum Powdery Mildew Resistance Gene Pm3VS from Dasypyrum villosum Chromosome 3V into Wheat.

Powdery mildew, caused by Blumeria graminis f. sp. tritici (Bgt), is a serious disease that threatens wheat production globally. It is imperative to explore novel resistance genes to control this disease by developing and planting resistant varieties. Here, we identified a wheat-Dasypyrum villosum 3V (3D) disomic substitution line, NAU3815 (2n = 42), with a high level of powdery mildew resistance at both the seedling and adult-plant stages. Subsequently, NAU3815 was used to generate recombination between chromosomes 3V and 3D. Through genomic in situ hybridization (GISH), fluorescence in situ hybridization (FISH), and 3VS- and 3VL-specific markers analysis, four introgression lines were developed from the selfing progenies of 3V and 3D double monosomic line NAU3816, which was derived from the F1 hybrids of NAU3815/NAU0686. There were t3VS (3D) ditelosomic substitution line NAU3817, t3VL (3D) ditelosomic substitution line NAU3818, homozygous T3DL·3VS translocation line NAU3819, and homozygous T3DS·3VL translocation line NAU3820. Powdery mildew tests of these lines confirmed the presence of an all-stage and broad-spectrum powdery mildew resistance gene, Pm3VS, located on chromosome arm 3VS. When compared with the recurrent parent NAU0686 plants, the T3DL·3VS translocation line NAU3819 showed no obvious negative effect on yield-related traits. However, the introduction of the T3DL·3VS translocated chromosome had a strong effect on reducing the flag-leaf length. Consequently, the T3DL·3VS translocation line NAU3819 provides a new germplasm in breeding for both resistance and plant architecture.

Past human expansions shaped the spatial pattern of Neanderthal ancestry.

The worldwide expansion of modern humans (Homo sapiens) started before the extinction of Neanderthals (Homo neanderthalensis). Both species coexisted and interbred, leading to slightly higher introgression in East Asians than in Europeans. This distinct ancestry level has been argued to result from selection, but range expansions of modern humans could provide an alternative explanation. This hypothesis would lead to spatial introgression gradients, increasing with distance from the expansion source. We investigate the presence of Neanderthal introgression gradients after past human expansions by analyzing Eurasian paleogenomes. We show that the out-of-Africa expansion resulted in spatial gradients of Neanderthal ancestry that persisted through time. While keeping the same gradient orientation, the expansion of early Neolithic farmers contributed decisively to reducing the Neanderthal introgression in European populations compared to Asian populations. This is because Neolithic farmers carried less Neanderthal DNA than preceding Paleolithic hunter-gatherers. This study shows that inferences about past human population dynamics can be made from the spatiotemporal variation in archaic introgression.

Integrating sex-bias into studies of archaic introgression on chromosome X.

Evidence of interbreeding between archaic hominins and humans comes from methods that infer the locations of segments of archaic haplotypes, or 'archaic coverage' using the genomes of people living today. As more estimates of archaic coverage have emerged, it has become clear that most of this coverage is found on the autosomes- very little is retained on chromosome X. Here, we summarize published estimates of archaic coverage on autosomes and chromosome X from extant human samples. We find on average 7 times more archaic coverage on autosomes than chromosome X, and identify broad continental patterns in this ratio: greatest in European samples, and least in South Asian samples. We also perform extensive simulation studies to investigate how the amount of archaic coverage, lengths of coverage, and rates of purging of archaic coverage are affected by sex-bias caused by an unequal sex ratio within the archaic introgressors. Our results generally confirm that, with increasing male sex-bias, less archaic coverage is retained on chromosome X. Ours is the first study to explicitly model such sex-bias and its potential role in creating the dearth of archaic coverage on chromosome X.

Methods to detect and characterize introgression.

Introgression, also known as introgressive hybridization, refers to the process that genetic components from the gene pool of one population transfer to the other via constant backcrossing. Introgression is widespread in nature, which plays important roles in increasing genetic diversity and improving adaptability to the environment, and in turn, influences the evolutionary progress of animals, plants and humans. Being as an important evolutionary event, researchers pay great attention to the detection of introgression, the introgression direction, the introgression timing, the pattern of introgression and so on. With the rapid development of high-throughput sequencing technologies, methods to detect and characterize introgression based on genome-wide data are continuously developed. In this review, we summarize a series of methods for introgression detection, and introduce the design principles and applications of these methods. We also discuss the maintenance and selection of gene segments after introgression. This review provides a relatively comprehensive reference for the studies on introgression.

Introgression from extinct species facilitates adaptation to its vacated niche.

Anthropogenic disturbances of ecosystems are causing a loss of biodiversity at an unprecedented rate. Species extinctions often leave ecological niches underutilized, and their colonization by other species may require new adaptation. In Lake Constance, on the borders of Germany, Austria and Switzerland, an endemic profundal whitefish species went extinct during a period of anthropogenic eutrophication. In the process of extinction, the deep-water species hybridized with three surviving whitefish species of Lake Constance, resulting in introgression of genetic variation that is potentially adaptive in deep-water habitats. Here, we sampled a water depth gradient across a known spawning ground of one of these surviving species, Coregonus macrophthalmus, and caught spawning individuals at greater depths (down to 90 m) than historically recorded. We sequenced a total of 96 whole genomes, 11-17 for each of six different spawning depth populations (4, 12, 20, 40, 60 and 90 m), to document genomic intraspecific differentiation along a water depth gradient. We identified 52 genomic regions that are potentially under divergent selection between the deepest (90 m) and all shallower (4-60 m) spawning habitats. At 12 (23.1%) of these 52 loci, the allele frequency pattern across historical and contemporary populations suggests that introgression from the extinct species potentially facilitates ongoing adaptation to deep water. Our results are consistent with the syngameon hypothesis, proposing that hybridization between members of an adaptive radiation can promote further niche expansion and diversification. Furthermore, our findings demonstrate that introgression from extinct into extant species can be a source of evolvability, enabling rapid adaptation to environmental change, and may contribute to the ecological recovery of ecosystem functions after extinctions.

Molecular Cytogenetic Analysis of the Introgression between Agropyron cristatum P Genome and Wheat Genome.

Agropyron cristatum (2n = 4x = 28, PPPP) is an important wild relative of common wheat (Triticum aestivum L., 2n = 6x = 42). A previous report showed that the wheat-A. cristatum 6P translocation line WAT655 carrying A. cristatum 6PS (0.81-1.00) exhibited high resistance to prevalent physiological races of stripe rust (CYR32 and CYR33). In this study, three disease resistance-related transcripts, which were mapped to A. cristatum 6PS (0.81-1.00) through the analysis of specific molecular markers, were acquired from among A. cristatum full-length transcripts. The BC5F2 and BC5F2:3 genetic populations of the translocation line WAT655 were analyzed by using three disease resistance-related gene markers, A. cristatum P genome-specific markers, and fluorescence in situ hybridization (FISH). The results revealed that the introgression between A. cristatum P genome and wheat genome was observed in progenies of the genetic populations of the translocation line WAT655 and the physical positions of the three genes were considerably adjacent on A. cristatum 6PS (0.81-1.00) according to the FISH results. Additionally, kompetitive allele-specific PCR (KASP) markers of the three genes were developed to detect and acquire 24 breeding lines selected from the progenies of the distant hybridization of wheat and A. cristatum, which showed resistance to physiological races of stripe rust (CYR32 and CYR33) and other desirable agronomic traits according to the field investigation. In conclusion, this study not only provides new insights into the introgression between A. cristatum P genome and wheat genome but also provides the desirable germplasms for breeding practice.

Phylogenomic assessment of the role of hybridization and introgression in trait evolution.

Trait evolution among a set of species-a central theme in evolutionary biology-has long been understood and analyzed with respect to a species tree. However, the field of phylogenomics, which has been propelled by advances in sequencing technologies, has ushered in the era of species/gene tree incongruence and, consequently, a more nuanced understanding of trait evolution. For a trait whose states are incongruent with the branching patterns in the species tree, the same state could have arisen independently in different species (homoplasy) or followed the branching patterns of gene trees, incongruent with the species tree (hemiplasy). Another evolutionary process whose extent and significance are better revealed by phylogenomic studies is gene flow between different species. In this work, we present a phylogenomic method for assessing the role of hybridization and introgression in the evolution of polymorphic or monomorphic binary traits. We apply the method to simulated evolutionary scenarios to demonstrate the interplay between the parameters of the evolutionary history and the role of introgression in a binary trait's evolution (which we call xenoplasy). Very importantly, we demonstrate, including on a biological data set, that inferring a species tree and using it for trait evolution analysis in the presence of gene flow could lead to misleading hypotheses about trait evolution.

Hybridization with mountain hares increases the functional allelic repertoire in brown hares.

Brown hares (Lepus europaeus Pallas) are able to hybridize with mountain hares (L. timidus Linnaeus) and produce fertile offspring, which results in cross-species gene flow. However, not much is known about the functional significance of this genetic introgression. Using targeted sequencing of candidate loci combined with mtDNA genotyping, we found the ancestral genetic diversity in the Finnish brown hare to be small, likely due to founder effect and range expansion, while gene flow from mountain hares constitutes an important source of functional genetic variability. Some of this variability, such as the alleles of the mountain hare thermogenin (uncoupling protein 1, UCP1), might have adaptive advantage for brown hares, whereas immunity-related MHC alleles are reciprocally exchanged and maintained via balancing selection. Our study offers a rare example where an expanding species can increase its allelic variability through hybridization with a congeneric native species, offering a route to shortcut evolutionary adaptation to the local environmental conditions.

Morphological ghosts of introgression in Darwin's finch populations.

Many species of plants, animals, and microorganisms exchange genes well after the point of evolutionary divergence at which taxonomists recognize them as species. Genomes contain signatures of past gene exchange and, in some cases, they reveal a legacy of lineages that no longer exist. But genomic data are not available for many organisms, and particularly problematic for reconstructing and interpreting evolutionary history are communities that have been depleted by extinctions. For these, morphology may substitute for genes, as exemplified by the history of Darwin's finches on the Galápagos islands of Floreana and San Cristóbal. Darwin and companions collected seven specimens of a uniquely large form of Geospiza magnirostris in 1835. The populations became extinct in the next few decades, partly due to destruction of Opuntia cactus by introduced goats, whereas Geospiza fortis has persisted to the present. We used measurements of large samples of G. fortis collected for museums in the period 1891 to 1906 to test for unusually large variances and skewed distributions of beak and body size resulting from introgression. We found strong evidence of hybridization on Floreana but not on San Cristóbal. The skew is in the direction of the absent G. magnirostris We estimate introgression influenced 6% of the frequency distribution that was eroded by selection after G. magnirostris became extinct on these islands. The genetic residuum of an extinct species in an extant one has implications for its future evolution, as well as for a conservation program of reintroductions in extinction-depleted communities.

Protocol for detecting introgressed archaic variants with SPrime.

The SPrime program detects the variants in current-day populations that were introgressed from an archaic source in the past. It is optimized for detecting introgression from Neanderthals and Denisovans in modern humans. We provide a protocol for detecting Neanderthal and Denisovan introgression in 1000 Genomes Project data, specifically focusing on the CHB (Han Chinese in Beijing) population. For complete details on the use and execution of this protocol, please refer to Browning et al. (2018).

Inferring archaic introgression from hominin genetic data.

Questions surrounding the timing, extent, and evolutionary consequences of archaic admixture into human populations have a long history in evolutionary anthropology. More recently, advances in human genetics, particularly in the field of ancient DNA, have shed new light on the question of whether or not Homo sapiens interbred with other hominin groups. By the late 1990s, published genetic work had largely concluded that archaic groups made no lasting genetic contribution to modern humans; less than a decade later, this conclusion was reversed following the successful DNA sequencing of an ancient Neanderthal. This reversal of consensus is noteworthy, but the reasoning behind it is not widely understood across all academic communities. There remains a communication gap between population geneticists and paleoanthropologists. In this review, we endeavor to bridge this gap by outlining how technological advancements, new statistical methods, and notable controversies ultimately led to the current consensus.

The timing of human adaptation from Neanderthal introgression.

Admixture has the potential to facilitate adaptation by providing alleles that are immediately adaptive in a new environment or by simply increasing the long-term reservoir of genetic diversity for future adaptation. A growing number of cases of adaptive introgression are being identified in species across the tree of life, however the timing of selection, and therefore the importance of the different evolutionary roles of admixture, is typically unknown. Here, we investigate the spatio-temporal history of selection favoring Neanderthal-introgressed alleles in modern human populations. Using both ancient and present-day samples of modern humans, we integrate the known demographic history of populations, namely population divergence and migration, with tests for selection. We model how a sweep placed along different branches of an admixture graph acts to modify the variance and covariance in neutral allele frequencies among populations at linked loci. Using a method based on this model of allele frequencies, we study previously identified cases of adaptive Neanderthal introgression. From these, we identify cases in which Neanderthal-introgressed alleles were quickly beneficial and other cases in which they persisted at low frequency for some time. For some of the alleles that persisted at low frequency, we show that selection likely independently favored them later on in geographically separated populations. Our work highlights how admixture with ancient hominins has contributed to modern human adaptation and contextualizes observed levels of Neanderthal ancestry in present-day and ancient samples.

Implications of emmer (Triticum dicoccon Schrank) introgression on bread wheat response to heat stress.

Wheat is sensitive to heat stress, particularly during grain filling, and this reduces grain yield. Ancestral wheat species, such as emmer wheat (Triticum dicoccon Schrank), represent potential sources of new genetic diversity for traits that may impact wheat responses to heat stress. However, the diversity available in emmer wheat has only been explored superficially. Recently developed emmer derived hexaploid wheat genotypes were evaluated for physiological, phenological and agronomic traits in a multi-environment, multi-season strategy. The emmer-based hexaploid lines were developed from crosses and backcrosses to 9 hexaploid recurrent parents and these genotypes and 7 commercial cultivars were evaluated under two times of sowing (E1 and E2) in the field for three consecutive years (2014-2016). The materials were genotyped using a 90 K SNP platform and these data used to estimate the contribution of emmer wheat to the progeny. Significant phenotypic and genetic variation for traits were observed. Higher temperature during reproductive development and grain filling reduced trait expression. Emmer progeny with greater trait values than their recurrent parents and commercial cultivars in both environments were found. Derivatives with higher physiological trait values yielded well in both environments; as indicated by the clustering of genotypes. The emmer wheat parent contributed between 1 and 43 % of the genome of the emmer-based hexaploid progeny, and progeny with greater emmer contribution had superior trait values in both environments. These results showed a positive effect of direct emmer introgression on wheat performance under heat stress. Mitigation of high temperature stress through the introgression of favorable alleles from wheat close relatives into modern wheat cultivars is possible.

Neandertal introgression and accumulation of hypomorphic mutations in the neuropeptide S (NPS) system promote attenuated functionality.

The neuropeptide S (NPS) system plays an important role in fear and fear memory processing but has also been associated with allergic and inflammatory diseases. Genes for NPS and its receptor NPSR1 are found in all tetrapods. Compared to non-human primates, several non-synonymous single-nucleotide polymorphisms (SNPs) occur in both human genes that collectively result in functional attenuation, suggesting adaptive mechanisms in a human context. To investigate historic and geographic origins of these hypomorphic mutations and explore genetic signs of selection, we analyzed ancient genomes and worldwide genotype frequencies of four prototypic SNPs in the NPS system. Neandertal and Denisovan genomes contain exclusively ancestral alleles for NPSR1 while all derived alleles occur in ancient genomes of anatomically modern humans, indicating that they arose in modern Homo sapiens. Worldwide genotype frequencies for three hypomorphic NPSR1 SNPs show significant regional homogeneity but follow a gradient towards increasing derived allele frequencies that supports an out-of-Africa scenario. Increased density of high-frequency polymorphisms around the three NPSR1 loci suggests weak or possibly balancing selection. A hypomorphic mutation in the NPS precursor, however, was detected at high frequency in Eurasian Neandertal genomes and shows genetic signatures indicating that it was introgressed into the human gene pool, particularly in Southern Europe, by interbreeding with Neandertals. We discuss potential evolutionary scenarios including behavior and immune-based natural selection.

Resistance to pirimiphos-methyl in West African Anopheles is spreading via duplication and introgression of the Ace1 locus.

Vector population control using insecticides is a key element of current strategies to prevent malaria transmission in Africa. The introduction of effective insecticides, such as the organophosphate pirimiphos-methyl, is essential to overcome the recurrent emergence of resistance driven by the highly diverse Anopheles genomes. Here, we use a population genomic approach to investigate the basis of pirimiphos-methyl resistance in the major malaria vectors Anopheles gambiae and A. coluzzii. A combination of copy number variation and a single non-synonymous substitution in the acetylcholinesterase gene, Ace1, provides the key resistance diagnostic in an A. coluzzii population from Côte d'Ivoire that we used for sequence-based association mapping, with replication in other West African populations. The Ace1 substitution and duplications occur on a unique resistance haplotype that evolved in A. gambiae and introgressed into A. coluzzii, and is now common in West Africa primarily due to selection imposed by other organophosphate or carbamate insecticides. Our findings highlight the predictive value of this complex resistance haplotype for phenotypic resistance and clarify its evolutionary history, providing tools to for molecular surveillance of the current and future effectiveness of pirimiphos-methyl based interventions.

Predicted structural differences of four fertility-related Y-chromosome proteins in Macaca mulatta, M. fascicularis, and their Indochinese hybrids.

Species in the genus Macaca typically live in multimale-multifemale social groups with male macaques exhibiting some of the largest testis: body weight ratios among primates. Males are believed to experience intense levels of sperm competition. Several spermatogenesis genes are located on the Y-chromosome and, interestingly, occasional hybridization between two species has led to the introgression of the rhesus macaque (Macaca mulatta) Y-chromosome deep into the range of the long-tailed macaque (M. fascicularis). These observations have led to the prediction that the successful introgression of the rhesus Y-haplotype is due to functional differences in spermatogenesis genes compared to those of the native long-tailed Y-haplotype. We examine here four Y-chromosomal loci-RBMY, XKRY, and two nearly identical copies of CDY-and their corresponding protein sequences. The genes were surveyed in representative animals from north of, south of, and within the rhesus x long-tailed introgression zone. Our results show a series of non-synonymous amino acid substitutions present between the two Y-haplotypes. Protein structure modeling via I-TASSER revealed different folding patterns between the two species' Y-proteins, and functional predictions via TreeSAAP further reveal physicochemical differences as a result of non-synonymous substitutions. These differences inform our understanding of the evolution of primate Y-proteins involved in spermatogenesis and, in turn, have biomedical implications for human male fertility.

Genetic basis of vascular bundle variations in rice revealed by genome-wide association study.

The vascular bundles play important roles in transportation of photoassimilate, and the number, size, and capacity of vascular bundles influence the transportation efficiency. Dissecting the genetic basis may help to make better use of naturally occurring vascular bundle variations. Here, we conducted a genome-wide association study (GWAS) of the vascular bundle variations in a worldwide collection of 529 Oryza sativa accessions. A total of 42 and 93 significant association loci were identified in the neck panicle and flag leaf, respectively. The introgression lines showing extreme values of the target traits harbored at least one GWAS signal, indicating the reliability of the GWAS loci. Based on the data of near-isogenic lines and transgenic plants, Grain number, plant height, and heading date7 (Ghd7) was identified as a major locus for the natural variation of vascular bundles in the neck panicle at the heading stage. In addition, Narrow leaf1 (NAL1) was found to influence the vascular bundles in both the neck panicle and flag leaf, and the effects of the major haplotypes of NAL1 were characterized. The loci or candidate genes identified would help to improve vascular bundle system in rice breeding.

Primate phylogenomics uncovers multiple rapid radiations and ancient interspecific introgression.

Our understanding of the evolutionary history of primates is undergoing continual revision due to ongoing genome sequencing efforts. Bolstered by growing fossil evidence, these data have led to increased acceptance of once controversial hypotheses regarding phylogenetic relationships, hybridization and introgression, and the biogeographical history of primate groups. Among these findings is a pattern of recent introgression between species within all major primate groups examined to date, though little is known about introgression deeper in time. To address this and other phylogenetic questions, here, we present new reference genome assemblies for 3 Old World monkey (OWM) species: Colobus angolensis ssp. palliatus (the black and white colobus), Macaca nemestrina (southern pig-tailed macaque), and Mandrillus leucophaeus (the drill). We combine these data with 23 additional primate genomes to estimate both the species tree and individual gene trees using thousands of loci. While our species tree is largely consistent with previous phylogenetic hypotheses, the gene trees reveal high levels of genealogical discordance associated with multiple primate radiations. We use strongly asymmetric patterns of gene tree discordance around specific branches to identify multiple instances of introgression between ancestral primate lineages. In addition, we exploit recent fossil evidence to perform fossil-calibrated molecular dating analyses across the tree. Taken together, our genome-wide data help to resolve multiple contentious sets of relationships among primates, while also providing insight into the biological processes and technical artifacts that led to the disagreements in the first place.

Indonesian native goats (Capra hircus) reveal highest genetic frequency of mitochondrial DNA haplogroup B in the world.

The objective of this study was to determine mtDNA sequences of the 481 bp HV1 region from two Indonesian native goat breeds, Kacang and Marica, to confirm the phylogeographic distribution of caprine haplogroup B in Southeast Asia. Based on these sequences, 12 haplotypes were observed and categorized into the predominant haplogroup B and minority haplogroup A, indicating that Indonesian native goats present the highest frequency (0.950) of the haplogroup B in the world. These results strongly emphasize previous observations of the haplogroup B frequencies tending to increase southeastward in Southeast Asia. Additionally, this suggests that goats primary bred into Southeast Asia might predominantly carry haplogroup B. This could essentially contribute to the understanding of the origin, propagation route and/or introgression history of Southeast Asian goats.