Adaptive introgression: a plant perspective Suarez-Gonzalez, Adriana; Lexer, Christian; Cronk, Quentin C. B.
Biology letters (2005),
03/2018, Letnik:
14, Številka:
3
Journal Article
Recenzirano
Odprti dostop
Introgression is emerging as an important source of novel genetic variation, alongside standing variation and mutation. It is adaptive when such introgressed alleles are maintained by natural ...selection. Recently, there has been an explosion in the number of studies on adaptive introgression. In this review, we take a plant perspective centred on four lines of evidence: (i) introgression, (ii) selection, (iii) phenotype and (iv) fitness. While advances in genomics have contributed to our understanding of introgression and porous species boundaries (task 1), and the detection of signatures of selection in introgression (task 2), the investigation of adaptive introgression critically requires links to phenotypic variation and fitness (tasks 3 and 4). We also discuss the conservation implications of adaptive introgression in the face of climate change. Adaptive introgression is particularly important in rapidly changing environments, when standing genetic variation and mutation alone may only offer limited potential for adaptation. We conclude that clarifying the magnitude and fitness effects of introgression with improved statistical techniques, coupled with phenotypic evidence, has great potential for conservation and management efforts.
The genic view of the process of speciation is based on the notion that species isolation may be achieved by a modest number of genes. Although great strides have been made to characterize ...'speciation genes' in some groups of animals, little is known about the nature of genic barriers to gene flow in plants. We review recent progress in the characterization of genic species barriers in plants with a focus on five 'model' genera: Mimulus (monkey flowers); Iris (irises); Helianthus (sunflowers); Silene (campions); and Populus (poplars, aspens, cottonwoods). The study species in all five genera are diploid in terms of meiotic behaviour, and chromosomal rearrangements are assumed to play a minor role in species isolation, with the exception of Helianthus for which data on the relative roles of chromosomal and genic isolation factors are available. Our review identifies the following key topics as being of special interest for future research: the role of intraspecific variation in speciation; the detection of balancing versus directional selection in speciation genetic studies; the timing of fixation of alleles of major versus minor effects during plant speciation; the likelihood of adaptive trait introgression; and the identification and characterization of speciation genes and speciation gene networks.
Natural hybrid zones have proven to be precious tools for understanding the origin and maintenance of reproductive isolation (RI) and therefore species. Most available genomic studies of hybrid zones ...using whole‐ or partial‐genome resequencing approaches have focused on comparisons of the parental source populations involved in genome admixture, rather than exploring fine‐scale patterns of chromosomal ancestry across the full admixture gradient present between hybridizing species. We have studied three well‐known European ‘replicate’ hybrid zones of Populus alba and P. tremula, two widespread, ecologically divergent forest trees, using up to 432 505 single‐nucleotide polymorphisms (SNPs) from restriction site‐associated DNA (RAD) sequencing. Estimates of fine‐scale chromosomal ancestry, genomic divergence and differentiation across all 19 poplar chromosomes revealed strikingly contrasting results, including an unexpected preponderance of F₁ hybrids in the centre of genomic clines on the one hand, and genomically localized, spatially variable shared variants consistent with ancient introgression between the parental species on the other. Genetic ancestry had a significant effect on survivorship of hybrid seedlings in a common garden trial, pointing to selection against early‐generation recombinants. Our results indicate a role for selection against recombinant genotypes in maintaining RI in the face of apparent F₁ fertility, consistent with the intragenomic ‘coadaptation’ model of barriers to introgression upon secondary contact. Whole‐genome resequencing of hybridizing populations will clarify the roles of specific genetic pathways in RI between these model forest trees and may reveal which loci are affected most strongly by its cyclic breakdown.
Understanding the genetics of biological diversification across micro‐ and macro‐evolutionary time scales is a vibrant field of research for molecular ecologists as rapid advances in sequencing ...technologies promise to overcome former limitations. In palms, an emblematic, economically and ecologically important plant family with high diversity in the tropics, studies of diversification at the population and species levels are still hampered by a lack of genomic markers suitable for the genotyping of large numbers of recently diverged taxa. To fill this gap, we used a whole genome sequencing approach to develop target sequencing for molecular markers in 4,184 genome regions, including 4,051 genes and 133 non‐genic putatively neutral regions. These markers were chosen to cover a wide range of evolutionary rates allowing future studies at the family, genus, species and population levels. Special emphasis was given to the avoidance of copy number variation during marker selection. In addition, a set of 149 well‐known sequence regions previously used as phylogenetic markers by the palm biological research community were included in the target regions, to open the possibility to combine and jointly analyse already available data sets with genomic data to be produced with this new toolkit. The bait set was effective for species belonging to all three palm sub‐families tested (Arecoideae, Ceroxyloideae and Coryphoideae), with high mapping rates, specificity and efficiency. The number of high‐quality single nucleotide polymorphisms (SNPs) detected at both the sub‐family and population levels facilitates efficient analyses of genomic diversity across micro‐ and macro‐evolutionary time scales.
In the context of potential interspecific gene flow, the integrity of species will be maintained by reproductive barriers that reduce genetic exchange, including traits associated with prezygotic ...isolation or poor performance of hybrids. Hybrid zones can be used to study the importance of different reproductive barriers, particularly when both parental species and hybrids occur in close spatial proximity. We investigated the importance of barriers to gene flow that act early vs. late in the life cycle of European Populus by quantifying the prevalence of homospecific and hybrid matings within a mosaic hybrid zone. We obtained genotypic data for 11 976 loci from progeny and their maternal parents and constructed a Bayesian model to estimate individual admixture proportions and hybrid classes for sampled trees and for the unsampled pollen parent. Matings that included one or two hybrid parents were common, resulting in admixture proportions of progeny that spanned the whole range of potential ancestries between the two parental species. This result contrasts strongly with the distribution of admixture proportions in adult trees, where intermediate hybrids and each of the parental species are separated into three discrete ancestry clusters. The existence of the full range of hybrids in seedlings is consistent with weak reproductive isolation early in the life cycle of Populus. Instead, a considerable amount of selection must take place between the seedling stage and maturity to remove many hybrid seedlings. Our results highlight that high hybridization rates and appreciable hybrid fitness do not necessarily conflict with the maintenance of species integrity.
Molecular ecologists increasingly require ‘universal’ genetic markers that can easily be transferred between species. The distribution of cross‐species transferability of nuclear microsatellite loci ...is highly uneven across taxa, being greater in animals and highly variable in flowering plants. The potential for successful cross‐species transfer appears highest in species with long generation times, mixed or outcrossing breeding systems, and where genome size in the target species is small compared to the source. We discuss the implications of these findings and close with an outlook on potential alternative sources of cross‐species transferable markers.
Recent advances in population genomics have triggered great interest in the genomic landscape of divergence in taxa with ‘porous’ species boundaries. One important obstable of previous studies of ...this topic was the low genomic coverage achieved. This issue can now be overcome by the use of ‘next generation’ or short‐read DNA‐sequencing approaches capable of assaying many thousands of single nucleotide polymorphisms (SNPs) in divergent species. We have scanned the ‘porous’ genomes of Populus alba and Populus tremula, two ecologically divergent hybridizing forest trees, using >38 000 SNPs assayed by restriction site associated DNA (RAD) sequencing. Windowed analyses indicate great variation in genetic divergence (e.g. the proportion of fixed SNPs) between species, and these results are unlikely to be strongly biased by genomic features of the Populus trichocarpa reference genome used for SNP calling. Divergence estimates were significantly autocorrelated (P < 0.01; Moran's I up to 0.6) along 11 of 19 chromosomes. Many of these autocorrelations involved low divergence blocks, thus suggesting that allele sharing was caused by recurrent gene flow rather than shared ancestral polymorphism. A conspicuous low divergence block of three megabases was detected on chromosome XIX, recently put forward as an incipient sex chromosome in Populus, and was largely congruent with introgression of mapped microsatellites in two natural hybrid zones (N > 400). Our results help explain the origin of the ‘genomic mosaic’ seen in these taxa with ‘porous’ genomes and suggest rampant introgression or extensive among‐species conservation of an incipient plant sex chromosome. RAD sequencing holds great promise for detecting patterns of divergence and gene flow in highly divergent hybridizing species.
Natural hybrid zones in forest trees provide systems to study the transfer of adaptive genetic variation by introgression. Previous landscape genomic studies in Populus trichocarpa, a keystone tree ...species, indicated genomic footprints of admixture with its sister species Populus balsamifera and identified candidate genes for local adaptation. Here, we explored the patterns of introgression and signals of local adaptation in P. trichocarpa and P. balsamifera, employing genome resequencing data from three chromosomes in pure species and admixed individuals from wild populations. Local ancestry analysis in admixed P. trichocarpa revealed a telomeric region in chromosome 15 with P. balsamifera ancestry, containing several candidate genes for local adaptation. Genomic analyses revealed signals of selection in certain genes in this region (e.g. PRR5, COMT1), and functional analyses based on gene expression variation and correlations with adaptive phenotypes suggest distinct functions of the introgressed alleles. In contrast, a block of genes in chromosome 12 paralogous to the introgressed region showed no signs of introgression or signatures of selection. We hypothesize that the introgressed region in chromosome 15 has introduced modular or cassette‐like variation into P. trichocarpa. These linked adaptive mutations are associated with a block of genes in chromosome 15 that appear to have undergone neo‐ or subfunctionalization relative to paralogs in a duplicated region on chromosome 12 that show no signatures of adaptive variation. The association between P. balsamifera introgressed alleles with the expression of adaptive traits in P. trichocarpa supports the hypothesis that this is a case of adaptive introgression in an ecologically important foundation species.
Studies of the strength and nature of reproductive isolation (RI) between species can greatly contribute to our understanding of speciation. Although the role of RI in speciation is well recognized, ...there is a dearth of information on the contributions of different barriers between related plant species. Here, we estimated multiple components of RI between two Mediterranean orchid sister species (Orchis mascula and Orchis pauciflora), disentangling the strength and absolute contributions of seven different isolating mechanisms. Our survey includes one prepollination, two postpollination prezygotic (pollen—stigma incompatibility, conspecific pollen precedence), two intrinsic postzygotic (embryo mortality and hybrid sterility) and two extrinsic postzygotic (hybrid habitat differentiation and hybrid pollination) isolating mechanisms. We found strong RI between the investigated species, although none of the barriers were able to completely impede gene flow. Five isolating mechanisms contributed positively to the maintenance of species boundaries. Contrary to most surveys of isolating mechanisms, our data speak against a clear predominance of prepollination or of prezygotic barriers but confirm the emerging pattern of multiple barriers contributing to the maintenance of species integrity. These findings suggest an allopatric condition during early phases of species divergence. We discuss our data in the wider context of previous studies carried out in this orchid group by using a comparative approach.
Interspecific hybridization may enhance the capacity of populations to adapt to changing environments, and has practical implications for reforestation. We use genome‐wide estimates of admixture and ...phenotypic traits for trees in a common garden to examine the extent and direction of gene flow across a Picea hybrid zone, testing assumptions of the bounded hybrid superiority and tension zone models of hybrid zone maintenance. Seeds were collected from the ecological transition zone spanning from maritime to continental climates across the Picea sitchensis–P. glauca contact zone, and 721 trees were planted in a common garden experiment within the hybrid zone. Individuals were genotyped using a panel of 384 candidate‐gene single nucleotide polymorphisms (SNPs) putatively associated with adaptive traits in Picea, and phenotyped at age ten for height and autumn cold hardiness. Low interspecific heterozygosity in hybrids indicated that intrinsic reproductive barriers were too weak to prevent widespread recombination, although introgression appeared asymmetric with P. sitchensis dominating the zone. Whereas marker‐based hybrid index was strongly correlated with climate and geography, phenotypic traits exhibited weak or no significant clines. Our results indicated that exogenous selection appeared to play a strong role in the distribution and structure of this hybrid zone, indicative of an environmentally determined bounded hybrid superiority model of hybrid zone maintenance, although endogenous mechanisms could not be ruled out. This study provides insight into the mechanisms underlying adaptation across ecologically transitional hybrid zones that will ultimately provide an additional tool in managing these economically important tree species.
PDF
