Christian Parisod

Hybridization and speciation

Hybridization has many and varied impacts on the process of speciation. Hybridization may slow or reverse differentiation by allowing gene flow and recombination. It may accelerate speciation via adaptive introgression or cause near‐instantaneous speciation by allopolyploidization. It may have multiple effects at different stages and in different spatial contexts within a single speciation event. We offer a perspective on the context and evolutionary significance of hybridization during speciation, highlighting issues of current interest and debate. In secondary contact zones, it is uncertain if barriers to gene flow will be strengthened or broken down due to recombination and gene flow. Theory and empirical evidence suggest the latter is more likely, except within and around strongly selected genomic regions. Hybridization may contribute to speciation through the formation of new hybrid taxa, whereas introgression of a few loci may promote adaptive divergence and so facilitate speciation. Gene regulatory networks, epigenetic effects and the evolution of selfish genetic material in the genome suggest that the Dobzhansky–Muller model of hybrid incompatibilities requires a broader interpretation. Finally, although the incidence of reinforcement remains uncertain, this and other interactions in areas of sympatry may have knock‐on effects on speciation both within and outside regions of hybridization.

Evolutionary consequences of autopolyploidy

Autopolyploidy is more common in plants than traditionally assumed, but has received little attention compared with allopolyploidy. Hence, the advantages and disadvantages of genome doubling per se compared with genome doubling coupled with hybridizations in allopolyploids remain unclear. Autopolyploids are characterized by genomic redundancy and polysomic inheritance, increasing effective population size. To shed light on the evolutionary consequences of autopolyploidy, we review a broad range of studies focusing on both synthetic and natural autopolyploids encompassing levels of biological organization from genes to evolutionary lineages. The limited evidence currently available suggests that autopolyploids neither experience strong genome restructuring nor wide reorganization of gene expression during the first generations following genome doubling, but that these processes may become more important in the longer term. Biogeographic and ecological surveys point to an association between the formation of autopolyploid lineages and environmental change. We thus hypothesize that polysomic inheritance may provide a short-term evolutionary advantage for autopolyploids compared to diploid relatives when environmental change enforces range shifts. In addition, autopolyploids should possess increased genome flexibility, allowing them to adapt and persist across heterogeneous landscapes in the long run.

Epigenetic variation in mangrove plants occurring in contrasting natural environment.

Background Epigenetic modifications, such as cytosine methylation, are inherited in plant species and may occur in response to biotic or abiotic stress, affecting gene expression without changing genome sequence. Laguncularia racemosa, a mangrove species, occurs in naturally contrasting habitats where it is subjected daily to salinity and nutrient variations leading to morphological differences. This work aims at unraveling how CpG-methylation variation is distributed among individuals from two nearby habitats, at a riverside (RS) or near a salt marsh (SM), with different environmental pressures and how this variation is correlated with the observed morphological variation. Principal Findings Significant differences were observed in morphological traits such as tree height, tree diameter, leaf width and leaf area between plants from RS and SM locations, resulting in smaller plants and smaller leaf size in SM plants. Methyl-Sensitive Amplified Polymorphism (MSAP) was used to assess genetic and epigenetic (CpG-methylation) variation in L. racemosa genomes from these populations. SM plants were hypomethylated (14.6% of loci had methylated samples) in comparison to RS (32.1% of loci had methylated samples). Within-population diversity was significantly greater for epigenetic than genetic data in both locations, but SM also had less epigenetic diversity than RS. Frequency-based (GST) and multivariate (βST) methods that estimate population structure showed significantly greater differentiation among locations for epigenetic than genetic data. Co-Inertia analysis, exploring jointly the genetic and epigenetic data, showed that individuals with similar genetic profiles presented divergent epigenetic profiles that were characteristic of the population in a particular environment, suggesting that CpG-methylation changes may be associated with environmental heterogeneity. Conclusions In spite of significant morphological dissimilarities, individuals of L. racemosa from salt marsh and riverside presented little genetic but abundant DNA methylation differentiation, suggesting that epigenetic variation in natural plant populations has an important role in helping individuals to cope with different environments.

Impact of transposable elements on the organization and function of allopolyploid genomes

Transposable elements (TEs) represent an important fraction of plant genomes and are likely to play a pivotal role in fuelling genome reorganization and functional changes following allopolyploidization. Various processes associated with allopolyploidy (i.e. genetic redundancy, bottlenecks during the formation of allopolyploids or genome shock following genome merging) may allow accumulation of TE insertions. Our objective in carrying out a survey of the literature and a comparative analysis across different allopolyploid systems is to shed light on the structural, epigenetic and functional modifications driven by TEs during allopolyploidization and subsequent diploidization. The available evidence indicates that TE proliferation in the short or the long term after allopolyploidization may be restricted to a few TEs, in specific polyploid systems. By contrast, data indicate major structural changes in the TE genome fraction immediately after allopolyploidization, mainly through losses of TE sequences as a result of recombination. Emerging evidence also suggests that TEs are targeted by substantial epigenetic changes, which may impact gene expression and genome stability. Furthermore, TEs may directly or indirectly support the evolution of new functionalities in allopolyploids during diploidization. All data stress allopolyploidization as a shock associated with drastic genome reorganization. Mechanisms controlling TEs during allopolyploidization as well as their impact on diploidization are discussed.

Rapid structural and epigenetic reorganization near transposable elements in hybrid and allopolyploid genomes in Spartina

*Transposable elements (TE) induce structural and epigenetic alterations in their host genome, with major evolutionary implications. These alterations are examined here in the context of allopolyploid speciation, on the recently formed invasive species Spartina anglica, which represents an excellent model to contrast plant genome dynamics following hybridization and genome doubling in natural conditions. *Methyl-sensitive transposon display was used to investigate the structural and epigenetic dynamics of TE insertion sites for several elements, and to contrast it with comparable genome-wide methyl-sensitive amplified polymorphism analyses. *While no transposition burst was detected, we found evidence of major structural and CpG methylation changes in the vicinity of TE insertions accompanying hybridization, and to a lesser extent, genome doubling. Genomic alteration appeared preferentially in the maternal subgenome, and the environment of TEs was specifically affected by large maternal-specific methylation changes, demonstrating that TEs fuel epigenetic alterations at the merging of diverged genomes. *Such genome changes indicate that nuclear incompatibilities in Spartina trigger immediate alterations, which are TE-specific with an important epigenetic component. Since most of this reorganization is conserved after genome doubling that produced a fertile invasive species, TEs certainly play a central role in the shock-induced dynamics of the genome during allopolyploid speciation.

Glacial in situ survival in the Western Alps and polytopic autopolyploidy in Biscutella laevigata L. (Brassicaceae).

Past climatic changes and especially the ice ages have had a great impact on both the distribution and the genetic composition of plant populations, but whether they promoted speciation is still controversial. The autopolyploid complex Biscutella laevigata is a classical example of polyploidy linked to glaciations and is an interesting model to explore migration and speciation driven by climate changes in a complex alpine landscape. Diploid taxa survived the last glacial maximum in several never‐glaciated areas and autotetraploids are clearly dominant in the central parts of the Alps; however, previous range‐wide studies failed to identify their diploid ancestor(s). This study highlights the phylogeographical relationships of maternal lineages in the Western Alps and investigates the polyploidy process using plastid DNA sequences (trnS‐trnG and trnK‐intron) combined with plastid DNA length polymorphism markers, which were transferable among Brassicaceae species. Twenty‐one distinct plastid DNA haplotypes were distinguished in 67 populations densely sampled in the Western Alps and main lineages were identified by a median‐joining network. The external Alps harboured high levels of genetic diversity, while the Central Alps contained only a subset of haplotypes due to postglacial recolonization. Several haplotypes were restricted to local peripheral refugia and evidence of in situ survival in central nunataks was detected by the presence of highly differentiated haplotypes swamped by frequent ones. As hierarchical genetic structure pointed to an independent evolution of the species in different biogeographical districts, and since tetraploids displayed haplotypes belonging to different lineages restricted to either the northern or the southern parts of the Alpine chain, polytopic autopolyploidy was also apparent in the Western Alps.

Genome‐wide association to fine‐scale ecological heterogeneity within a continuous population of Biscutella laevigata (Brassicaceae)

Gene flow, drift and selection can be detected through different signatures across the genome and the landscape. Genetic discontinuities along with their correlation to environmental features can be used to tease out isolation-by-distance and isolation-by-time from processes related to selection. Using spatial statistics (spatial autocorrelation methods, canonical correspondence analysis and partial Mantel tests) dealing with genome-wide amplified fragment length polymorphism (AFLP) under unlikely Hardy-Weinberg assumptions, this study investigates 124 individuals within a continuous population of the autopolyploid Biscutella laevigata (Brassicaceae). Fine-scale spatial genetic structure was strong and the mosaic-like distribution of AFLP genotypes was consistently associated with habitat factors, even when controlled for geographical distances. The use of multivariate analyses enabled separation of the factors responsible for the repartition of the genetic variance and revealed a composite effect of isolation by distance, phenological divergence and local adaptation to habitats characterised by different solar radiation regimes. These results suggest that the immigrant inviability barrier facilitated the maintenance of adapted subpopulations to distinct environmental conditions at the local scale.

Transposable elements and microevolutionary changes in natural populations.

Transposable elements (TEs) usually represent the most abundant and dynamic fraction of genomes in almost all living organisms. The overall capacity of such ‘junk DNA’ to induce mutations and foster the reorganization of functional genomes suggests that TE may be of central evolutionary significance. However, to what extent TE dynamics drive and is driven by the evolutionary trajectory of host taxa remains poorly known. Further work addressing the fate of TE insertions in natural populations is necessary to shed light on their impact on microevolutionary processes. Here, we highlight methodological approaches (i.e. transposon displays and high‐throughput sequencing), tracking TE insertions across large numbers of individuals and discuss their pitfalls and benefits for molecular ecology surveys.

Origin and expansion of the allotetraploid Aegilops geniculata, a wild relative of wheat

*This study reconstructs the phylogeography of Aegilops geniculata, an allotetraploid relative of wheat, to discuss the impact of past climate changes and recent human activities (e.g. the early expansion of agriculture) on the genetic diversity of ruderal plant species. *We combined chloroplast DNA (cpDNA) sequencing, analysed using statistical parsimony network, with nonhierarchical K-means clustering of amplified fragment length polymorphism (AFLP) genotyping, to unravel patterns of genetic structure across the native range of Ae. geniculata. The AFLP dataset was further explored by measurement of the regional genetic diversity and the detection of isolation by distance patterns. *Both cpDNA and AFLP suggest an eastern Mediterranean origin of Ae. geniculata. Two lineages have spread independently over northern and southern Mediterranean areas. Northern populations show low genetic diversity but strong phylogeographical structure among the main peninsulas, indicating a major influence of glacial cycles. By contrast, low genetic structuring and a high genetic diversity are detected in southern Mediterranean populations. Finally, we highlight human-mediated dispersal resulting in substantial introgression between resident and migrant populations. *We have shown that the evolutionary trajectories of ruderal plants can be similar to those of wild species, but are interfered by human activities, promoting range expansions through increased long-distance dispersal and the creation of suitable habitats.

Gene flow between wheat and wild relatives: empirical evidence from Aegilops geniculata, Ae. neglecta and Ae. triuncialis.

Gene flow between domesticated species and their wild relatives is receiving growing attention. This study addressed introgression between wheat and natural populations of its wild relatives (Aegilops species). The sampling included 472 individuals, collected from 32 Mediterranean populations of three widespread Aegilops species (Aegilops geniculata, Ae. neglecta and Ae. triuncialis) and compared wheat field borders to areas isolated from agriculture. Individuals were characterized with amplified fragment length polymorphism fingerprinting, analysed through two computational approaches (i.e. Bayesian estimations of admixture and fuzzy clustering), and sequences marking wheat‐specific insertions of transposable elements. With this combined approach, we detected substantial gene flow between wheat and Aegilops species. Specifically, Ae. neglecta and Ae. triuncialis showed significantly more admixed individuals close to wheat fields than in locations isolated from agriculture. In contrast, little evidence of gene flow was found in Ae. geniculata. Our results indicated that reproductive barriers have been regularly bypassed during the long history of sympatry between wheat and Aegilops.