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Fior, S.

Publications and source records attributed to Fior, S..

10 recordsLinked to original sources

Soil heterogeneity and pleiotropy contribute to polygenic soil adaptation during postglacial range expansion in an alpine plant

1) Plants colonized new abiotic environments during postglacial range expansions. Little is known about whether populations adapt to different soil conditions during range expansion and, if so, which mechanisms underlie presumably polygenic adaptation. It remains unclear how pleiotropy and soil heterogeneity contribute to such adaptation. 2) We studied 43 populations of Dianthus sylvestris with characterized soil conditions along its postglacial range expansion in the Alps. We leveraged genome-wide data and variation in multiple soil variables to identify polygenic signatures of selection in soil-associated alleles using environmental association analysis, generalized dissimilarity models, and polygenic scores. 3) We found signatures of selection in 814 single nucleotide polymorphisms (SNPs) and the largest magnitude of allele frequency change in candidate SNPs associated with K, Mg, and Al. Candidate genes showed higher pleiotropy than randomly sampled genes. We found soil heterogeneity shaping the populations adaptive genetic variation in the landscape. 4) Our results suggest that populations of D. sylvestris adapted to contrasting soil chemical properties during postglacial range expansion through polygenic adaptation. Pleiotropy likely plays an important role in polygenic adaptation to novel selective pressures and soil heterogeneity is an important factor contributing to the maintenance of adaptive genetic variation.

evolutionary biology↗

Adaptation across a precipitation gradient from niche center to niche edge

Evaluating the potential for species to adapt to changing climate relies on an appreciation of current patterns of adaptive variation and selection, which might vary in intensity across a species niche, affecting our inference of where adaptation might be most important in the future. Here we investigate the genetic basis of adaptation in Lactuca serriola, the wild relative of the common lettuce, growing along a steep precipitation gradient in Israel approaching the species arid niche limit, and used candidate loci to inform predictions of its past and future adaptive evolution. Environmental association analyses combined with generalized dissimilarity models revealed 98 candidate genes showing non-linear shifts in allele frequencies across the gradient, with a large proportion under strong directional selection near the dry niche edge. Selection acts on genes with separate suites of biological functions, specifically related to osmotic stress and phenological adjustments at the dry edge, and related to biotic interactions at the niche center. The adaptive genetic composition of populations, as inferred through polygenic risk scores, indicates that intensified selection may be the key determinant of the dry niche edge. However, inference of past and future evolutionary change suggests larger adaptive shifts in the mesic part of the range, which is most affected by climate change. Our study highlights that non-linear spatial variation in selection has implications for predicting past and future responses to climate change.

genomics↗

Trait evolution linked to climatic shifts contributes to adaptive divergence in an alpine carnation (Dianthus sylvestris)

Populations expanding to new habitats may encounter novel selection regimes which can lead to ecotype formation. In the Alps, elevation corresponds to steep ecological gradients, along which ecotype formation has occurred in many species. The majority of alpine plant species are perennial and little is known about how selection acts across different stages of their life-cycles and how fitness trade-offs shape adaptive processes in perennials. We investigated how selection at opposite ends of elevational gradients has driven ecotype formation in Dianthus sylvestris, a perennial herb that expanded its ecological niche to low elevation habitats after the Last Glacial Maximum. Through a multi-year reciprocal transplant experiment including parental populations and recombinant crosses we assessed fitness under natural conditions and dissect how adaptation is mediated by different fitness components with inherent trade-offs, and pinpoint the contribution of growth and reproductive traits to this process. We show that the evolution of local adaptation proceeded by selection acting primarily through reproduction and survival at low and high elevation, respectively. At low elevation the primary contribution to adaptation was third year reproduction, concomitant with a left skewed age distribution. At high elevation the contribution to adaptation and the age distribution were more dispersed across the life cycle. We found that large, early flowering plants have a consistent fitness advantage. This was mediated by direct selection favoring large size through reproductive output at low elevation, and early flowering through the probability to produce seeds at high elevation. Our results indicate that the selection regime imposed by the warm low elevation habitat led to the evolution of an ecotype exhibiting a life-history strategy characterized by high investment in rapid growth and early reproduction. In contrast, the high elevation strategy favors high investment in self-maintenance. Our results suggest that weakening of a key fitness trade-off associated with resource allocation contributed to the evolution of distinct ecotypes in this perennial plant species.

evolutionary biology↗

Life history traits mediate elevational adaptation in a perennial alpine plant

O_LISpatially divergent natural selection drives adaptation to contrasting environments and the evolution of ecotypes. Understanding this process in perennial plants is challenging because natural selection acts on multiple life history traits linked by fitness trade-offs. C_LIO_LIIn a multi-year reciprocal transplant experiment of high and low elevation populations of the alpine carnation Dianthus carthusianorum in the Central Alps, we tested how different stages of the life cycle contribute to adaptation. Moreover, we used matrix population models to infer the specific contributions of individual life stages to fitness, coupled with trade-off analyses. C_LIO_LIWe found genotype x environment interactions consistent with elevational adaptation both in single fitness components linked to reproduction and survival, and in integrative fitness estimates. Adaptation at low elevation is driven by early reproduction, in contrast to an opposite strategy at high elevation. Adaptive life-history differences between populations originating from low and high elevations are mediated by environmental effects on plant growth and trade-offs between reproduction and survival. C_LIO_LIOur work reveals elevational ecotypes of the perennial alpine plant D. carthusianorum that express alternative life history strategies in response to climatic differences shaping resource allocation. C_LI

evolutionary biology↗

Sequential colonization events with restricted gene flow in a widespread European carnation species

The key questions relating to the evolutionary processes underlying plant colonization success pertain to the geographic origin of the source population(s), the location of the migration routes, the extent to which genetic diversity is reduced via founder effects, and the extent of gene flow among populations during expansion. However, these questions must still be addressed for perennial herbaceous plants with large geographic distributions. We investigated the colonization history of Dianthus carthusianorum (the Carthusian Pink), one of the most widespread European carnation species. We called genome-wide 236,964 SNPs from a large sample across the D. carthusianorum distribution range, and used up-to-date population genomics approaches (approximate Bayesian computation Random-Forest method, ABC-RF) to infer population demographic history. Spatial genetic structure and diversity analyses and demographic inferences indicated successive East-West colonization events by the Carthusian Pink. ABC-RF also revealed gene flow during colonization, but only among geographically close populations. This study provides important insights into the colonization processes of herbaceous perennial species belonging to one of Europes most diverse plant genera.

evolutionary biology↗

Unravelling drivers of local adaptation through Evolutionary Functional-Structural Plant modelling

O_LILocal adaptation to contrasting environmental conditions along environmental gradients is a widespread phenomenon in plant populations, yet we lack a mechanistic understanding of how individual agents of selection contribute to local adaptation. C_LIO_LIHere, we developed a novel evolutionary functional-structural plant (E-FSP) model that simulates local adaptation of virtual plants along an environmental gradient. First, we validate the model by testing if it can recreate two elevational ecotypes of Dianthus carthusianorum occurring in the Swiss Alps. Second, we use the E-FSP model to disentangle the relative contribution of abiotic (temperature) and biotic (competition and pollination) selection pressures to elevational adaptation in D. carthusianorum. C_LIO_LIThe model reproduced the qualitative differences between the elevational ecotypes in two phenological (germination and flowering time) and one morphological trait (stalk height), as well as qualitative differences in four performance variables that emerge from GxE interactions (flowering time, number of stalks, rosette area and seed production). Our results suggest that elevational adaptation in D. carthusianorum is predominantly driven by the abiotic environment. C_LIO_LIOur approach shows how E-FSP models incorporating physiological, ecological and evolutionary mechanisms can be used in combination with experiments to examine hypotheses about patterns of adaptation observed in the field. C_LI

evolutionary biology↗

Climate-induced range shifts drive adaptive response via spatio-temporal sorting of alleles

Quaternary climate fluctuations drove many species to shift their geographic ranges, in turn shaping their genetic structures. Recently, it has been argued that adaptation may have accompanied species range shifts via the "sieving" of genotypes during colonisation and establishment. However, this has not been directly demonstrated, and knowledge remains limited on how different evolutionary forces, that are typically investigated separately, interacted to jointly mediate species responses to past climatic change. Here, through whole-genome resequencing of over 1200 individuals of the carnation Dianthus sylvestris coupled with integrated population genomic and gene-environment models, we reconstruct the past neutral and adaptive landscape of this species as it was shaped by the Quaternary glacial cycles. We show that adaptive responses emerged concomitantly with the post-glacial range shifts and expansions of this species in the last 20 thousand years. This was due to the spatial sorting of adaptive alleles through time, as populations expanded out of restrictive glacial refugia into the broader and more heterogeneous range of habitats available in the present-day inter-glacial. Our results reveal a tightly-linked interplay of migration and adaptation under past climate-induced range shifts that has acted to shape the spatial patterns of adaptive genetic variation we see in the species today.

evolutionary biology↗

A target capture approach for phylogenomic analyses at multiple evolutionary timescales in rosewoods (Dalbergia spp.) and the legume family (Fabaceae)

Understanding the genetic changes associated with the evolution of biological diversity is of fundamental interest to molecular ecologists. The assessment of genetic variation at hundreds or thousands of unlinked genetic loci forms a sound basis to address questions ranging from micro-to macro-evolutionary timescales, and is now possible thanks to advances in sequencing technology. Major difficulties are associated with i) the lack of genomic resources for many taxa, especially from tropical biodiversity hotspots, ii) scaling the numbers of individuals analyzed and loci sequenced, and iii) building tools for reproducible bioinformatic analyses of such datasets. To address these challenges, we developed a set of target capture probes for phylogenomic studies of the highly diverse, pantropically distributed and economically significant rosewoods (Dalbergia spp.), explored the performance of an overlapping probe set for target capture across the legume family (Fabaceae), and built a general-purpose bioinformatics pipeline. Phylogenomic analyses of Dalbergia species from Madagascar yielded highly resolved and well supported hypotheses of evolutionary relationships. Population genomic analyses identified differences between closely related species and revealed the existence of a potentially new species, suggesting that the diversity of Malagasy Dalbergia species has been underestimated. Analyses at the family level corroborated previous findings by the recovery of monophyletic subfamilies and many well-known clades, as well as high levels of gene tree discordance, especially near the root of the family. The new genomic and bioinformatics resources will hopefully advance systematics and ecological genetics research in legumes, and promote conservation of the highly diverse and endangered Dalbergia rosewoods.

genomics↗

Polygenic routes lead to parallel altitudinal adaptation in Heliosperma pusillum (Caryophyllaceae)

Understanding how organisms adapt to the environment is a major goal of modern biology. Parallel evolution - the independent evolution of similar phenotypes in different populations - provides a powerful framework to investigate the evolutionary potential of populations, the constraints of evolution, its repeatability and therefore its predictability. Here, we quantified the degree of gene expression and functional parallelism across replicated ecotype formation in Heliosperma pusillum (Caryophyllaceae), and gained insights into the architecture of adaptive traits. Population structure analyses and demographic modelling support a previously formulated hypothesis of parallel polytopic divergence of montane and alpine ecotypes. We detect a large proportion of differentially expressed genes (DEGs) underlying divergence within each replicate ecotype pair, with a strikingly low amount of shared DEGs across pairs. Functional enrichment of DEGs reveals that the traits affected by significant expression divergence are largely consistent across ecotype pairs, in strong contrast to the non-shared genetic basis. The remarkable redundancy of differential gene expression indicates a polygenic architecture for the diverged adaptive traits. We conclude that polygenic traits appear key to opening multiple routes for adaptation, widening the adaptive potential of organisms.

evolutionary biology↗

Identifying loci under selection via explicit demographic models

Adaptive genetic variation is a function of both selective and neutral forces. To accurately identify adaptive loci, it is thus critical to account for demographic history. Theory suggests that signatures of selection can be inferred using the coalescent, following the premise that genealogies of selected loci deviate from neutral expectations. Here, we build on this theory to develop an analytical framework to identify Loci under Selection via explicit Demographic models (LSD). Under this framework, signatures of selection are inferred through deviations in demographic parameters, rather than through summary statistics directly, and demographic history is accounted for explicitly. Leveraging on the property of demographic models to incorporate directionality, we show that LSD can provide information on the environment in which selection acts on a population. This can prove useful in elucidating the selective processes underlying local adaptation, by characterising genetic trade-offs and extending the concepts of antagonistic pleiotropy and conditional neutrality from ecological theory to practical application in genomic data. We implement LSD via Approximate Bayesian Computation and demonstrate, via simulations, that LSD has i) high power to identify selected loci across a large range of demographic-selection regimes, ii) outperforms commonly applied genome-scan methods under complex demographies, and iii) accurately infers the directionality of selection for identified candidates. Using the same simulations, we further characterise the behaviour of isolation-with-migration models conducive to the study of local adaptation under regimes of selection. Finally, we demonstrate an application of LSD by detecting loci and characterising genetic trade-offs underlying flower colour in Antirrhinum majus.

evolutionary biology↗