Estimation of contemporary effective population size in plant populations: Limitations of genomic datasets.

Effective population size (N e) is a pivotal evolutionary parameter with crucial implications in conservation practice and policy. Genetic methods to estimate N e have been preferred over demographic methods because they rely on genetic data rather than time-consuming ecological monitoring. Methods based on linkage disequilibrium (LD), in particular, have become popular in conservation as they require a single sampling and provide estimates that refer to recent generations. A software program based on the LD method, GONE, looks particularly promising to estimate contemporary and recent-historical N e (up to 200 generations in the past). Genomic datasets from non-model species, especially plants, may present some constraints to the use of GONE, as linkage maps and reference genomes are seldom available, and SNP genotyping is usually based on reduced-representation methods. In this study, we use empirical datasets from four plant species to explore the limitations of plant genomic datasets when estimating N e using the algorithm implemented in GONE, in addition to exploring some typical biological limitations that may affect N e estimation using the LD method, such as the occurrence of population structure. We show how accuracy and precision of N e estimates potentially change with the following factors: occurrence of missing data, limited number of SNPs/individuals sampled, and lack of information about the location of SNPs on chromosomes, with the latter producing a significant bias, previously unexplored with empirical data. We finally compare the N e estimates obtained with GONE for the last generations with the contemporary N e estimates obtained with the programs currentNe and NeEstimator.

Low-frequency somatic mutations are heritable in tropical trees Dicorynia guianensis and Sextonia rubra.

Somatic mutations potentially play a role in plant evolution, but common expectations pertaining to plant somatic mutations remain insufficiently tested. Unlike in most animals, the plant germline is assumed to be set aside late in development, leading to the expectation that plants accumulate somatic mutations along growth. Therefore, several predictions were made on the fate of somatic mutations: mutations have generally low frequency in plant tissues; mutations at high frequency have a higher chance of intergenerational transmission; branching topology of the tree dictates mutation distribution; and exposure to UV (ultraviolet) radiation increases mutagenesis. To provide insights into mutation accumulation and transmission in plants, we produced two high-quality reference genomes and a unique dataset of 60 high-coverage whole-genome sequences of two tropical tree species, Dicorynia guianensis (Fabaceae) and Sextonia rubra (Lauraceae). We identified 15,066 de novo somatic mutations in D. guianensis and 3,208 in S. rubra, surprisingly almost all found at low frequency. We demonstrate that 1) low-frequency mutations can be transmitted to the next generation; 2) mutation phylogenies deviate from the branching topology of the tree; and 3) mutation rates and mutation spectra are not demonstrably affected by differences in UV exposure. Altogether, our results suggest far more complex links between plant growth, aging, UV exposure, and mutation rates than commonly thought.

High intraspecific growth variability despite strong evolutionary legacy in an Amazonian forest.

Tree growth is key to species performance. However, individual growth variability within species remains underexplored for a whole community, and the role of species evolutionary legacy and local environments remains unquantified. Based on 36 years of diameter records for 7961 trees from 138 species, we assessed individual growth across an Amazonian forest. We related individual growth to taxonomy, topography and neighbourhood, before exploring species growth link to functional traits and distribution along the phylogeny. We found most variation in growth among individuals within species, even though taxonomy explained a third of the variation. Species growth was phylogenetically conserved up to the genus. Traits of roots, wood and leaves were good predictors of growth, suggesting their joint selection during convergent evolutions. Neighbourhood crowding significantly decreased individual growth, although much of inter-individual variation remains unexplained. The high intraspecific variation observed could allow individuals to respond to the heterogeneous environments of Amazonian forests.

Higher local intra- than interspecific variability in water- and carbon-related leaf traits among Neotropical tree species.

BACKGROUND AND AIMS: Intraspecific variability in leaf water-related traits remains little explored despite its potential importance in the context of increasing drought frequency and severity. Studies comparing intra- and interspecific variability of leaf traits often rely on inappropriate sampling designs that result in non-robust estimates, mainly owing to an excess of the species/individual ratio in community ecology or, on the contrary, to an excess of the individual/species ratio in population ecology. METHODS: We carried out virtual testing of three strategies to compare intra- and interspecific trait variability. Guided by the results of our simulations, we carried out field sampling. We measured nine traits related to leaf water and carbon acquisition in 100 individuals from ten Neotropical tree species. We also assessed trait variation among leaves within individuals and among measurements within leaves to control for sources of intraspecific trait variability. KEY RESULTS: The most robust sampling, based on the same number of species and individuals per species, revealed higher intraspecific variability than previously recognized, higher for carbon-related traits (47-92 and 4-33 % of relative and absolute variation, respectively) than for water-related traits (47-60 and 14-44 % of relative and absolute variation, respectively), which remained non-negligible. Nevertheless, part of the intraspecific trait variability was explained by variation of leaves within individuals (12-100 % of relative variation) or measurement variations within leaf (0-19 % of relative variation) and not only by individual ontogenetic stages and environmental conditions. CONCLUSIONS: We conclude that robust sampling, based on the same number of species and individuals per species, is needed to explore global or local variation in leaf water- and carbon-related traits within and among tree species, because our study revealed higher intraspecific variation than previously recognized.

Selection in space and time: Individual tree growth is adapted to tropical forest gap dynamics.

Tropical forest dynamics are driven by growth and survival strategies of tree species in relation to treefall gaps; however, the ecological and evolutionary roles of intraspecific variation in the response to forest gaps remain unexplored. Here, we associated genomic data of three related tree species of the genus Symphonia in a French Guiana forest with (1) each individual tree's growth potential, and (2) with its light and competition environment estimated based on 33 years of forest monitoring in plots covering 120 ha. We show that individual trees within species have genetically determined growth strategies that are adapted to the local light and competition environments, which are shaped by the time since the last treefall. Within species, fast-growing genotypes are more frequent in light-enriched environments and slow-growing genotypes in more shaded environments. Forest gap dynamics is thus a strong selection driver that shapes adaptive strategies and maintains genetic variation within tropical tree species.

Topography drives microgeographic adaptations of closely related species in two tropical tree species complexes.

Closely related tree species that grow in sympatry are abundant in rainforests. However, little is known of the ecoevolutionary processes that govern their niches and local coexistence. We assessed genetic species delimitation in closely related sympatric species belonging to two Neotropical tree species complexes and investigated their genomic adaptation to a fine-scale topographic gradient with associated edaphic and hydrologic features. Combining LiDAR-derived topography, tree inventories, and single nucleotide polymorphisms (SNPs) from gene capture experiments, we explored genome-wide population genetic structure, covariation of environmental variables, and genotype-environment association to assess microgeographic adaptations to topography within the species complexes Symphonia (Clusiaceae), and Eschweilera (Lecythidaceae) with three species per complex and 385 and 257 individuals genotyped, respectively. Within species complexes, closely related tree species had different realized optima for topographic niches defined through the topographic wetness index or the relative elevation, and species displayed genetic signatures of adaptations to these niches. Symphonia species were genetically differentiated along water and nutrient distribution particularly in genes responding to water deprivation, whereas Eschweilera species were genetically differentiated according to soil chemistry. Our results suggest that varied topography represents a powerful driver of processes modulating tropical forest biodiversity with differential adaptations that stabilize local coexistence of closely related tree species.

Topography shapes the local coexistence of tree species within species complexes of Neotropical forests.

Forest inventories in Amazonia include around 5000 described tree species belonging to more than 800 genera. Numerous species-rich genera share genetic variation among species because of recent speciation and/or recurrent hybridisation, forming species complexes. Despite the key role that tree species complexes play in understanding Neotropical diversification, and their need to exploit a diversity of niches, little is known about the mechanisms that allow local coexistence of tree species complexes and their species in sympatry. In this study, we explored the fine-scale distribution of five tree species complexes and 22 species within these complexes. Combining forest inventories, botanical determination, and LiDAR-derived topographic data over 120 ha of permanent plots in French Guiana, we used a Bayesian modelling framework to test the role of fine-scale topographic wetness and tree neighbourhood on the occurrence of species complexes and the relative distribution of species within complexes. Species complexes of Neotropical trees were widely spread across the topographic wetness gradient at the local scale. Species within complexes showed pervasive niche differentiation along with topographic wetness and competition gradients. Similar patterns of species-specific habitat preferences were observed within several species complexes: species more tolerant to competition for resources grow in drier and less fertile plateaus and slopes. If supported by partial reproductive isolation of species and adaptive introgression at the species complex level, our results suggest that both species-specific habitat specialisation within species complexes and the broad ecological distribution of species complexes might explain the success of these species complexes at the regional scale.