Molecular divergence in tropical tree populations occupying environmental mosaics

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The maintenance of diversity in Amazonia: a subtle combination of chance and determinism

Two main theories are evoked to explain community assembly and the maintenance of high diversity across tropical rainforest landscapes: Neutralism and Determinism. The contrast between the neutralist and the determinist theories of community assembly is quite comparable to the contrast between neutral and adaptive (molecular) evolution of populations.
Under the unified neutral theory of biodiversity (Hubbell 2001), meta-community dynamics is governed by the speciation-extinction equilibrium in which the size of populations changes randomly (‘ecological drift’), eventually leading to extinction, and populations exchange individuals according with dispersal distance between them (Ricklefs, 2006). Thus, species assemblages are random subsets of the available pool of species able to spread in a given area (Tuomisto & Ruokolainen 1997). Even if this model is often unrealistic (Ricklefs, 2006), it accounts for most of the observed patterns of species abundance in tropical communities, suggesting that neutral process play a crucial role in community assembly (Chaves et al., 2003). From an evolutionary point of view, populations may evolve neutrally (under the combination of random mutation, migration, genetic drift and demographic events). In theory, populations may diverge into separate species if gene flow is restricted, either by a biogeographic barrier, or by the geographic distance between populations (also called isolation-by-distance). In such cases of allopatric speciation, the probability to observe a given species in a given area is thus a function of the dispersal abilities of the neighborhood populations of this species (Latimer et al. 2005). The great diversity observed in Amazonia, by comparison with temperate forests, is commonly explained by differences in speciation-extinction rates that are themselves dependent on the size of the climatically similar area. The main hypothesis is that there is a positive relationship between an ecoclimatic zone and the geographic range size of a species. Subsequently, two main hypotheses could explain the great diversity of the tropics: ‘museum’ and ‘cradle’ (Chown & Gaston 2000, Mittelbach et al. 2007, Arita & Vazquez-Domingez 2008). The ‘museum’ hypothesis postulates that there is a negative relationship between the geographic range size of a species and its likelihood of extinction. This is because large ranges should buffer species against extinction by reducing the probability of range wide catastrophes and because large population sizes would minimize the chance of extinction due to stochastic reasons. Because large species range sizes are typical of the tropics, tropics should act as a museum of diversity with low extinction rates with older taxa by comparison with temperate zones. The ‘cradles’ hypothesis postulates that there is a positive relationship between the geographic range size of a species and the likelihood of its speciation. This is because species with larger ranges are more likely to undergo allopatric speciation resulting from isolations-by-distance or isolations by biogeographic barriers. Tropic may thus be viewed as cradles of diversity, with high speciation rates.
In the ‘environmental filtering’ theory, species assemblages are controlled by determinist factors involving abiotic and biotic interactions (Wright 2002). In particular, habitat heterogeneity (Terborgh et al. 2002) and local interactions (mainly competition and predation) are commonly evoked as important drivers of diversity in tropical landscapes. Environmental filtering exerted by both abiotic and biotic factors would have led to niche partitioning and habitat specialization in tropical rainforest trees. From an evolutionary point of view, the evolution of populations and the divergence between species may have been driven by selective pressures exerted by environmental heterogeneity (sympatric speciation). Moreover, habitat heterogeneity is associated to disturbance gradients (particularly logging, and tree-fall gaps). Under the disturbance hypothesis, species diversity is enhanced by intermediate levels of disturbance, as observed in French Guiana (Molino et al. 2001). Another determinist hypothesis evokes density-dependant mortality around mother trees. This hypothesis was formulated by Janzen (1970) who observed a decrease in seedlings mortality with the distance to the mother trees, probably due to allelopathic chemical compounds or to density-dependent predation. This process leads to ‘gaps of regeneration’ around mother trees, allowing the installation of other tree species and preventing mono-specific assembly. However, this process remains poorly understood and documented.
Neutrality and determinism probably act in pair in governing species evolution and assembly structuring (Gravel et al. 2006, Jabot et al. 2008), and their relative effects probably vary across geographical scales and study areas (Gravel et al. 2006, Jabot et al. 2008). In the following section, I will focus on spatial heterogeneity in tropical landscapes (and particularly that observed at local scales) without, however, excluding the existence of neutral processes.

Environmental heterogeneity across forests landscapes

At continental and regional scales, both precipitations and the intensity of the dry season are the main causes of climatic variations across the Amazonian forest landscape: while temperatures are quite homogeneous, precipitations show large variations among regions (ranging from 1000 to 3000 mm per year, figure 17) with a precipitation gradient that increases from Southeast to Northwest Amazonia (Mayle & Power 2008). Moreover, the intensity of the dry season is more pronounced at the extreme of the gradients, where precipitations are the most abundant. French Guiana also exhibits a large gradient of precipitations that increases from west to east, figure 18 (Wagner 2011).

Consequences of spatial heterogeneity on population evolution & species divergence

As quickly evoked previously (‘3.The maintenance of diversity in Amazonia’), population evolution is driven by a combination of neutral (mutation, recombination, genetic drift, migration, reproduction, demography) and adaptive (natural selection) processes. Populations may diverge into new species, either due to isolation-by-distance that may be caused by populations isolation into refuges or biogeographic barriers (allopatric speciation), or by local adaptation to habitat heterogeneity (sympatric speciation). However, the drivers of populations evolution and speciation processes in tropical rainforest trees are poorly known, partly because the boundaries of species are often confused, and many species are organized in species complexes, with incomplete reproductive isolation between species and cryptic species (Cavers & Dick 2013).
At regional scale, many phylogeographic analyses revealed patterns of genetic divergence structured by the biogeographic history of the species, and mainly dispersal constraints that occurred during tertiary and quaternary. For example, Jacaranda copaia is widespread in the Amazon basin and comprises two sub-species: one subspecies widespread from Central America to Bolivia and another one distributed in the Guiana shield. In a recent study, Scotti-Saintagne et al. (2012) showed that the geographical patterns of genetic diversity in these two Jacaranda copaia sub-species were largely shaped by Pleistocene climatic changes that isolated ancestral species into refuges, with a center of diversification in Central Amazonia probably due to a secondary contact zone. Moreover, the absence of cross-Andean disjunction suggested that the Andean uplift was not a barrier to dispersal, probably because Jacaranda copaia is a wind-dispersed pioneer species, favored by canopy gaps and disturbances, and able to tolerate relatively dry conditions. Another example is provided by the Carapa species complex (Duminil et al. 2006, Scotti-Saintagne et al. 2012). Scotti-Saintagne et al. suggested that the biogeographic history of two Carapa species was a combination of tertiary and quaternary events, including Pliocene Andean uplifts, and then late Miocene development of Amazon drainage, but was also influenced by hybridization and introgressions during the Quaternary, figure 28.

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Evidences of adaptation in temperate and tropical plant populations

All methods confounded, the literature provides numerous molecular evidences of adaptive divergence in plant species, mainly across broad climatic gradients.
In Arabidopsis thaliana, a genome-wide association study revealed that fitness-related loci (growth and fruit production) exhibit signatures of local adaptation linked to climatic variables across Europe (Fournier-level et al. 2011), figure 59. In black spruce (Picea mariana), several genes involved in growth, response to constraints (cold and drought) show patterns of differentiation concordant with diversifying selection among both climatic and precipitation partitioning in Québec (Prunier et al. 2011). In Pinus pinaster, Eveno et al. (Eveno et al. 2007) analyzed the structure of genetic diversity across the maritime pine range for SNPs within genes candidates for drought stress tolerance. Several were identified as ‘outliers’ probably under diversifying selection. In Lobolly pine (Pinus taeda), several genes involved in responses to biotic and abiotic constraints were structured by aridity in the United States (Eckert et al. 2010). Similarly, Richardson et al. (Richardson et al. 2009) found that 70% of the genetic variations (obtained from anonymous AFLPs) is explained by climate in Pinus monticola inhabiting the west coast of USA.
Altitudinal gradients also provide molecular evidence of local adaptation. In white spruce, Namroud et al. (Namroud et al. 2008) found patterns of genetic differentiation concordant with divergent selection among populations of different elevations for genes involved in flowering time, oxidative stress and nitrogen uptake. In the coastal Catalonian montains, Jump et al. (Jump & Penuelas 2006) detected significant variation in gene frequencies related to temperatures in Fagus sylvatica. However, the question of plant adaptation to environmental conditions is highly neglected in tropical rainforests: there is, up to now, few study dealing with adaptation in tropical trees. Moreover, the great majority of studies that provides molecular evidence of adaptation in trees of temperate zones are focusing on broad climatic gradients acting at large spatial scales. On the contrary, only few studies have provided evidence of adaptation to local constraints (such as edaphic constraints among micro-habitats or local biotic constraints). Burgarella et al. (Burgarella et al. 2012) detected footprints of diversifying selection for taxol-related genes (involved in defense against predators) in Taxus baccata in Spain mountains. They suggested that local selective pressures exerted by predators and host-enemy co-evolution would have led to genetic divergence among uplands. In an original study, Manel et al. analyzed patterns of adaptation in a mountain plant (Arabis alpina) across geographical scales (Manel et al. 2010). Surprisingly, they found a higher proportion of loci of ecological relevance (Fst-based outliers) at local scale. At regional scales, temperature and precipitations were identified as the major drivers of allele distribution, but it was less clear at local scale in which environmental variations are characterized by topography-related variations rather than climatic ones. They suggested that there may be two different types of adaptive responses acting on A. alpina: a site-specific local adaptation (caused by topography-related variations) and a more general adaptive response at larger geographic scales (caused by large climatic gradient, including both temperatures and precipitations).

Table of contents :

INTRODUCTION – Evolution in Amazonia
1. Short overview of the Amazonian rainforest
2. The building of biodiversity in Amazonia
3. The maintenance of diversity in Amazonia: a subtle combination of chance and determinism
4. Spatial heterogeneity in the Amazonian rainforest
5. Tree species model, research questions and study sites
PART 1 – Molecular evolution: population genetics and genomics
1. Population evolution
2. Population differentiation: the complex interplay between gene flow, selection, and drift.
3. Neutral differentiation
4. Adaptive differentiation
5. Next generation sequencing / genotyping and new opportunities
PART II – Phenotypic evolution and quantitative genetics
1. Causes of phenotypic variation
2. Phenotypic evolution in populations
3. Phenotypic differentiation
1. Neutralism and adaptation in Eperua falcata
2. Open questions and perspectives
3. Importance of assessing genetic diversity in a changing world
Article n°1 ­ Molecular divergence in tropical tree populations occupying environmental mosaics
Article n° 2 ­ Genome scan reveals fine-scale genetic structure and suggests highly local adaptation in a Neotropical tree species (Eperua falcata, Fabaceae) Bioinformatic tools ‘
Rngs’: A suite of R functions to easily deal with next-generation (454-)sequencing data and post-process assembly and annotation results.
1. Introduction to bioinformatics
2. Short description of ‘Rngs’
3. Short overview of the functions
4. Detailed description of the functions
Article n°3 ­ High-throughput transcriptome sequencing and polymorphism discovery in four Neotropical tree species.
Article n°4 ­ Highly local environmental variability promotes intra-population divergence of quantitative traits: an example from tropical rainforest trees
Article n°5 ­ Local adaptation in tropical rainforest trees: response of E. falcata (Fabaceae) seedling populations from contrasted habitats to drought and to water-logging
Preliminary results ­ Reciprocal transplants


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