Hybridization and speciation dynamic of Quercus petraea and Quercus robur

Les chênes sessiles et pédonculés sont deux espèces sympatriques interfertiles occupant des places distinctes dans la succession écologique. Elles constituent pour cela un bon modèle pour l’étude de la spéciation écologique. Malgré leur écologie contrastée, les deux espèces de chênes coexistent naturellement dans de nombreuses forêts, rendant possible l’étude de leur système de reproduction intra- et interspécifique. Des travaux précédents ont suggéré que l’hybridation entre ces deux espèces serait fréquence-dépendante. Elle dépendrait de la proportion de pollen allospécifique (c'est-à-dire de pollen de l’autre espèce) que reçoit l’arbre mère étudié. Ce phénomène d’hybridation fréquence-dépendante est appelé effet Hubbs, du nom d’un ichtyologue qui découvrit ce mécanisme en 1955. Mon travail a consisté à étudier, dans une parcelle mixte de chênes, les barrières à l’hybridation qui permettent la coexistence de ces deux espèces. Pour cela, j’ai effectué une étude de paternité de grande ampleur (près de 3500 individus typés sur 12 marqueurs microsatellites). Tout d’abord, je me suis intéressée à la délimitation des deux espèces en appliquant pour la première fois in situ le critère d’interfertilité. Je me suis ensuite concentrée sur les facteurs qui influencent l’hybridation au travers d’une modélisation des croisements à l’échelle de l’individu. Les résultats montrent que le maintien de ces deux espèces est régi par deux composantes environnementales importantes : la fréquence de chaque espèce et leur distribution, qui influencent la quantité de pollen reçue. Grâce à cette étude empirique et à l’approche de modélisation de ces croisements, nous avons désormais une bien meilleure vision de l’effet de l’environnement sur l’hybridation. J’ai par la suite comparé les caractéristiques du système de reproduction de chaque espèce (dispersion du pollen et fécondité mâle) en cherchant si un lien existait avec leur stratégie écologique. Les résultats suggèrent que les différences de dynamique écologique pourraient être à l’origine de la spéciation du fait de l’existence de compromis différents en termes d’allocation de ressources mais qu’à plus court terme la stabilité de l’environnement est essentielle au maintien des espèces.Quercus petraea and Q. robur are two interfertile sympatric species. They occupy distinct stages during forest succession and constitute therefore good models for ecological speciation studies. Despite their differences, they often grow together in mixed stands, allowing the study of their intra- and interspecific reproductive system. Hybridization between these two oak species has been suggested to be frequency-dependent. The effect of the relative species abundance on hybridization is known as the “Hubbs’ effect”, from the name of an ichthyologist who described this mechanism in 1955. My work was to study the processes that limit hybridization between these two species, thereby allowing their coexistence. I conducted an extensive paternity analysis (almost 3500 individuals genotyped at 12 microsatellite markers). First, I tried to delimitate the two oak species by applying for the first time in situ the interfertility criterion. Then, I focused on interspecific crosses by studying those factors influencing hybridization. Results showed that the maintenance of these two species depends on the frequency of each species and their distribution, as both factors influence the quantity of pollen received by female flowers. Thanks to this empirical study and to this modeling approach, we have now a much better view of environmental effects on hybridization. I then compared the characteristics of the reproductive system of each species (pollen dispersal and male fertility) in relation with their ecological strategies. The results suggest that differences in species ecological dynamics are at the origin of the speciation process but that at a finer scale the stability of the environment is crucial for species’ maintenance

Lagache2012

Lagache201

Data from: Fine-scale environmental control of hybridization in oaks

Natural hybridization is attracting much interest in modern speciation and conservation biology studies, but the underlying mechanisms remain poorly understood. In particular, it is unclear why environmental changes often increase hybridization rates. To study this question, we surveyed mating events in a mixed oak stand and developed a spatially-explicit individual-based hybridization model. This model, where hybridization is frequency dependent, pollen is non-limiting and which allows immigrant pollen to compete with local pollen, takes into account species-specific pollen dispersal and sexual barriers to hybridization. The consequences of pollen limitation on hybridization were studied using another simple model. The results indicate that environmental changes could increase hybridization rates through two distinct mechanisms. First, by disrupting the spatial organisation of communities, they should decrease the proportion of conspecific pollen available for mating, thus increasing hybridization rates. Second, by decreasing the density of conspecifics, they should increase pollen limitation and thus hybridization rates, as a consequence of chance pollination predominating over deterministic pollen competition. Altogether, our results point to a need for considering hybridization events at the appropriate level of organisation and provide new insights into why hybridization rates generally increase in disturbed environments

Genetic diversity increases insect herbivory on oak saplings

A growing body of evidence from community genetics studies suggests that ecosystem functions supported by plant species richness can also be provided by genetic diversity within plant species. This is not yet true for the diversity-resistance relationship as it is still unclear whether damage by insect herbivores responds to genetic diversity in host plant populations. We developed a manipulative field experiment based on a synthetic community approach, with 15 mixtures of one to four oak (Quercus robur) half-sib families. We quantified genetic diversity at the plot level by genotyping all oak saplings and assessed overall damage caused by ectophagous and endophagous herbivores along a gradient of increasing genetic diversity. Damage due to ectophagous herbivores increased with the genetic diversity in oak sapling populations as a result of higher levels of damage in mixtures than in monocultures for all families (complementarity effect) rather than because of the presence of more susceptible oak genotypes in mixtures (selection effect). Assemblages of different oak genotypes would benefit polyphagous herbivores via improved host patch location, spill over among neighbouring saplings and diet mixing. By contrast, genetic diversity was a poor predictor of the abundance of endophagous herbivores, which increased with individual sapling apparency. Plant genetic diversity may not provide sufficient functional contrast to prevent tree sapling colonization by specialist herbivores while enhancing the foraging of generalist herbivores. Long term studies are nevertheless required to test whether the effect of genetic diversity on herbivory change with the ontogeny of trees and local adaptation of specialist herbivores

Data from: Outlier loci highlight the direction of introgression in oaks

Loci considered to be under selection are generally avoided in attempts to infer past demographic processes as they do not fit neutral model assumptions. However, opportunities to better reconstruct some aspects of past demography might thus be missed. Here we examined genetic differentiation between two sympatric European oak species with contrasting ecological dynamics (Quercus robur and Q. petraea) with both outlier (i.e. loci possibly affected by divergent selection between species or by hitchhiking effects with genomic regions under selection) and non-outlier loci. We sampled 855 individuals in six mixed forests in France and genotyped them with a set of 262 SNPs enriched with markers showing high interspecific differentiation, resulting in accurate species delimitation. We identified between 13 and 74 interspecific outlier loci, depending on the coalescent simulation models and parameters used. Greater genetic diversity was predicted in Q. petraea (a late successional species) than in Q. robur (an early successional species) as introgression should theoretically occur predominantly from the resident species to the invading species. Remarkably, this prediction was verified with outlier loci but not with non-outlier loci. We suggest that the lower effective interspecific gene flow at loci showing high interspecific divergence has better preserved the signal of past asymmetric introgression towards Q. petraea caused by the species’ contrasting dynamics. Using markers under selection to reconstruct past demographic processes could therefore have broader potential than generally recognized

Non-additive effect of genetic diversity insect herbivores.

<p>(A) Test of the non-additive effect of genetic diversity on ectophagous insects. (B) Test of the non-additive effect of genetic diversity on endophagous insects. Semi transparent circles represent individual values per plot for net genetic diversity effect (NGDE, blue), complementarity effect (CE, red) and selection effect (SE, green). Solid black circled dots are the averaged values for all plots (grand mean) and each level of genetic diversity (GD). The ‘*’ symbol are for means value significantly different from zero.</p

Effect of mother tree identity on insect herbivores in monocultures.

<p>(A) Effect of mother tree identity on damage (% leaf area removed) due to ectophagous herbivores. (B) Effect of mother tree identity on the abundance of endophagous insect herbivores. Semi transparent coloured circles represent individual saplings. Darkest circles represent overlapping datapoints. Solid black circled dots indicate the mean values in monocultures for all saplings and all blocks. Same letter above two lines of dots indicates that the corresponding means were not significantly different (LMM and GLMM on monoculture plots).</p

Summary of <i>t</i> values from <i>t</i>-tests for net genetic diversity effect (NGDE), complementarity effect (CE) and selection effect (SE) on damage of ectophagous and abundance of endophagous (leaf-miners) insects, and on sapling height, for all mixtures (grand mean) and for each level of genetic diversity (GD).

<p>Significant t-values are in bold: (***) P-value <0.001, (**) 0.001< P-value <0.01, (*) 0.01< P-value <0.05.</p

Summary of the results of linear mixed models assessing the effect of sapling height (H), mother tree identity (MT), genetic diversity (GD) and genetic relatedness (GR) between oak saplings and their interactions on herbivory by ectophagous insects and on abundance of endophagous insects (leaf-miners).

<p>Results are given from LMM and Poisson GLMM for ectophagous and endophagous herbivores respectively.</p>a<p><i>df</i> degrees of freedom (numerator, denominator).</p>b<p>Log-likelihood R² were not estimated in case of significant H × GR and H × GD interactions.</p

Complete genotypes (826 samples and 262SNPs - Genalex format)

Complete genotypes (826 samples and 262SNPs - Genalex format