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

Sylvain Schmitt, Niklas Tysklind, Géraldine Derroire, Myriam Heuertz, Bruno Hérault

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Sylvain Schmitt, Niklas Tysklind, Géraldine Derroire, Myriam Heuertz, Bruno Hérault. Topography shapes the local coexistence of tree species within species complexes of Neotropical forests. Oecologia, 2021, 173, pp.1491-1498. 10.1007/s00442-021-04939-2. hal-03231179

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

--Manuscript Draft--

<table><tr><td>Manuscript Number:</td><td>OECO-D-20-00296R3</td></tr><tr><td>Full Title:</td><td>Topography shapes the local coexistence of tree species within species complexes of Neotropical forests</td></tr><tr><td>Article Type:</td><td>Population ecology – original research</td></tr><tr><td>Corresponding Author:</td><td>Sylvain Schmitt, PhD<br>CNRS: Centre National de la Recherche Scientifique<br>Kourou, FRENCH GUIANA</td></tr><tr><td>Order of Authors:</td><td>Sylvain Schmitt, PhD<br>Niklas Tysklind, PhD<br>Géraldine Derroire, PhD<br>Myriam Heuertz, PhD<br>Bruno Hérault, PhD</td></tr><tr><td>Response to Reviewers:</td><td>Reviewer #2: The authors have successfully addressed all the comments and suggestions made in the last review.<br>&gt; Thank you again for the thorough comments on our manuscript.</td></tr><tr><td>Funding Information:</td><td>Agence Nationale de la Recherche (ANR-10-LABEX-0025) Not applicable</td></tr><tr><td>Abstract:</td><td>Forest inventories in Amazonia include around 5,000 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 120ha 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 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.</td></tr></table>
Sylvain Schmitt
69, route d'Arcachon
33610 Cestas, France

Avril 7, 2020

**Object:** Submission of a manuscript to Oecologia

Dear Editor,

We would like to submit an original research article entitled "Topography shapes the local coexistence of tree species within species complexes of Neotropical forests" for consideration to publish in Oecologia. In this manuscript, we present an original research addressing the effect of topography on the distribution of species complexes and the local coexistence of species within species complexes based on a large inventories of 22 species within 5 species complexes associated to fine-scale topographic and neighbor crowding data.

Lowland Amazonia includes numerous species-rich tree genera sharing a large amount of genetic variation either because of recent common ancestry and/or recurrent hybridization, forming species complexes. Despite the key role that species complexes play in understanding Neotropical diversification, and the need for exploiting a diversity of niches for species complexes to thrive, little is known about local coexistence of Neotropical species complexes in sympatry. Combining full forest inventories, high-quality botanical determination, and LiDAR-derived topographic data over 120ha of permanent plots, we used a Bayesian modelling framework to test the role of fine-scale topography and tree neighbourhood on the presence of species complexes and the relative distribution of species within complexes. Species complexes of Neotropical trees were widely spread across topography at the local-scale, while species within species complexes showed pervasive niche differentiation along topographic position, water accumulation, and competition gradients. Our results suggest that both habitat specialisation of species within species complexes and the broad ecological distribution of species complexes might explain the success of these Neotropical species complexes at the regional scale

We believe that this manuscript would be a valuable contribution to Oecologia and attract a large readership as our results contribute to shed some light on species coexistence within the understudied Neotropical species complexes.

We have no conflicts of interest to disclose.

Thank you for your consideration.

Sincerely,
Sylvain Schmitt,
on behalf of the co-authors
# Topography shapes the local coexistence of tree species within species complexes of Neotropical forests

Sylvain Schmitt<sup>1,2,*</sup>, Niklas Tysklind<sup>3</sup>, Géraldine Derroire<sup>4</sup>, Myriam Heuertz<sup>2</sup>,

Bruno Hérault<sup>5,6,7</sup>

<sup>1</sup> CNRS, UMR EcoFoG (Agroparistech, Cirad, INRAE, Université des Antilles, Université de la Guyane), Campus Agronomique, 97310 Kourou, French Guiana; <sup>2</sup> Univ. Bordeaux, INRAE, BIOGECO, 69 route d'Arcachon, 33610 Cestas France; <sup>3</sup> INRAE, UMR EcoFoG (Agroparistech, CNRS, Cirad, Université des Antilles, Université de la Guyane), Campus Agronomique, 97310 Kourou, French Guiana; <sup>4</sup> Cirad, UMR EcoFoG (Agroparistech, CNRS, INRAE, Université des Antilles, Université de la Guyane), Campus Agronomique, 97310 Kourou, French Guiana; <sup>5</sup> CIRAD, UPR Forêts et Sociétés, Yamoussoukro, Côte d'Ivoire; <sup>6</sup> Forêts et Sociétés, Univ Montpellier, CIRAD, Montpellier, France; <sup>7</sup> Institut National Polytechnique Félix Houphouët-Boigny, INP-HB, Yamoussoukro, Côte d'Ivoire; *Corresponding author: Sylvain Schmitt <sylvain.m.schmitt@gmail.com></text>

## Authors' contributions

NT and SS conceived the ideas; SS, BH, and NT designed methodology; SS and BH analysed model outputs; SS, NT and MH led the writing of the manuscript. All authors contributed critically to the drafts and gave final approval for publication.
Abstract

Forest inventories in Amazonia include around 5,000 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 120ha 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 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.

## Keywords

species distribution; syngameon; habitat specialisation; Paracou

## Introduction

Tropical forests shelter the highest level of biodiversity worldwide (Gaston 2000), as already showcased by Connell (1978). Lowland Amazonian forest inventory plots include around 5,000 identified tree species belonging to 810 genera (ter Steege et al. 2013); thus many genera are species-rich. To understand the processes leading to such diversity, it is pivotal to understand what ecological mechanisms lead to the relative success of these species-rich genera. Among them, many have been shown to have a higher level of genetic polymorphism than species-poor genera, oftentimes sharing haplotypes among species, which is likely related to introgression among congeneric species (Caron et al. 2019). Indeed, interspecific hybrids occur in 16% of plant genera, and more often so in species-rich genera (Whitney et al. 2010).

Species that are morphologically similar, or have blurry morphological differences, and/or share large amounts of genetic variation due to recent common ancestry and/or hybridisation are defined as species complexes (Pernès and Lourd 1984; Brown et al 1995). Species complexes can result from adaptive radiation and segregation among species in the
use of environmental gradients, through a combination and reshuffling of genetic features
among species in hybrid swarms (Seehausen 2004). These processes may multiply the
number of potential ecological niches, in turn reducing competition among the species and
helping the species gain reproductive isolation (Runemark et al. 2019). The establishment
of a hybrid or derived species requires some degree of reproductive isolation from its
progenitors to avoid becoming an evolutionary melting pot. Nevertheless, simulations
suggest that low hybridisation success among congeneric species promotes the coexistence
of species in the community by allowing for the persistence of rare species through
hybridisation (Cannon and Lerdau 2015). Furthermore, the way we perceive the role of
genetic connectivity among populations and species is quickly changing, as a growing body
of literature supports that species-specific adaptations may be maintained or even
maximised despite high levels of gene flow, especially if selective pressures are spatially
and/or temporally variable (Tigano and Friesen 2016).

When closely related but distinct species that live in sympatry are connected by limited, but
recurrent, interspecific gene flow, they are called a syngameon (Suarez-Gonzalez et al.
2018). Syngameons are particular in that they evolve responding to two contrasting
evolutionary pressures, those acting at the species level maximizing species-level
adaptations to a niche that reduces competition among species, and those acting at the
syngameon level which benefit all constituent species. Syngameons as a whole might thus
have a selective advantage, decreasing the overall risk of genus extinction, maximising
population size, all the while allowing adaptation of their distinct species to specific niches
and reducing competition among species (Cannon and Lerdau 2015). Consequently, and in
juxtaposition to other types of species complexes, syngameons are not necessarily a transitional or incipient phase of a process towards complete speciation but may be a highly successful evolutionary status *per se* (Cannon and Petit 2019). In one of the best known syngameons, the European white oak, the constituent species lack private cpDNA haplotypes indicating extensive hybridisation (Petit et al. 2002), but each of its constituent species includes unique portions of the genome that remain divergent (Hipp et al. 2019). Moreover, each species has unique ecological preferences, including drought and cold tolerance, and adaptation to alkaline soils (Leroy et al. 2019; Cannon and Petit 2019). The maintenance of the different species is orchestrated, in part, by the genes allowing their survival according to their ecological niche preferences (Leroy et al. 2019).

Similarly, Neotropical tree species show pervasive species-habitat associations (Fine et al. 2004; Esteves and Vicentini 2013). Specifically, congeneric species pairs may have contrasting preferences for topography and soil type (Itoh et al. 2003; Allié et al. 2015; Lan et al. 2016), and sometimes may grow in the same abiotic habitat but segregate according to light access (Yamasaki et al. 2013). Habitat specialisation may thus support congeneric species coexistence in sympatry. Among Neotropical congeneric tree species, many share genetic variation (Caron et al. 2019), which leads us to hypothesise that they may operate as syngameons.

Despite the key role of plant species complexes and syngameons in Neotropical ecology, diversification, and evolution (Pinheiro et al. 2018), little is known of the ecological drivers creating and maintaining diversity within Neotropical species complexes (Baraloto et al.
2012; Levi et al., 2019; ter Steege et al. 2013; Cannon and Petit 2019). Particularly, the generality of niche specialisation along environmental gradients among species within species complexes, as a potential driver of speciation and maintenance of species complexes, has not been addressed.

Here, we assessed the relative importance of the abiotic environment and biotic interactions in shaping species distribution within and among species complexes. We took advantage of the Paracou study site with more than 75,000 censused and geolocated individual trees in a highly diverse tropical forest site located in French Guiana, within the Guiana Shield in Amazonia. The Paracou site encompasses a diversity of micro-habitats through topographic variation ranging from seasonally flooded bottomlands to drier plateaus (Gourlet-Fleury et al. 2004) and displays variation in canopy gap size distribution (Goulamoussene 2016) and forest turn-over (Ferry et al. 2010). Combining tree inventories and LiDAR-derived topographic data, we used Bayesian modelling to address the following questions: (1) Are species complexes widely spread across biotic and abiotic environments, *i.e.* as generalists, or do they occupy specific niches, *i.e.* as specialists? (2) Do species within complexes also behave as generalists, *i.e.* do they occur throughout the environmental niche of species complexes, or does the biotic and abiotic environment favour niche differentiation within species complexes, *i.e.* do species within complexes have a narrower environmental niche than the complex? We considered as generalist those species whose variation in abundance does not imply a shift of species dominance along the environmental gradient, whereas we considered species as specialist those species whose variation in abundance implied a shift of species dominance along the gradient.
# Material and Methods

## Study site

The study was conducted in the northernmost part of the Guiana Plateau region, at the Paracou field station in French Guiana. The site is characterised by an average of 3,102 mm annual rainfall and a mean air temperature of 25.7 °C (Aguilos et al. 2018). Old tropical forest with an exceptional richness (e.g. over 750 woody species) develops in this area across a succession of small hills rising to 10–40 m a.s.l. (Gourlet-Fleury et al. 2004). A logging experiment was conducted in the Paracou station in 1986 (details in Hérault and Piponiot, 2018). We used seven undisturbed permanent inventory plots from Paracou (i.e., six plots of 6.25 ha and one of 25 ha) which have been censused (i.e. diameter at breast height > 10 cm) every 1-2 years since 1984.

## Species complexes

The literature about syngameons is concentrated on temperate models (Levi et al. 2019b), and, to the best of our knowledge, no studies have inventoried species complexes in Amazonia or in the Paracou community (Pinheiro et al. 2018). From the Paracou database, we identified five species complexes based on evidence for low (phylo-)genetic resolution or plastid DNA sharing in the clade (Gonzalez et al. 2009; Baraloto et al. 2012; Caron et al. 2019): *Eschweilera clade Parvifolia* (Lecythidaceae; Chave et al. unpublished; Heuertz et al.
2020); *Licania* (Chrysobalanaceae; Bardon et al. 2016); *Iryanthera* (Myristicaceae); *Symphonia* (Clusiaceae; Torroba-Balmori et al. 2017); and *Talisia* (Sapindaceae). We removed species with less than ten individuals in Paracou in 2015, which resulted in five species complexes each including two to nine species (Table 1). The species in the five species complexes are dispersed by animals (*Eschweilera* see Prance and Mori 1993; *Iryanthera* see Howe 1983; *Licania* see Hammond et al. 1995, *Symphonia* see Forget et al. 2007; *Talisia* see Julliot 1996 and Théry and Larpin 1993). In addition, *Eschweilera*, *Licania*, and *Talisia* share haplotypes between species pairs (Caron et al. 2019) and *Symphonia* shows introgression between species pairs (Schmitt 2020), suggesting interspecific gene flow characteristic of syngameons. The Paracou community might include other species complexes. Nevertheless, our selection illustrates the phylogenetic diversity of species complexes in Paracou (see supplementary material S8), and the identified species complexes include species that are locally abundant and hyperdominant at the regional level (ter Steege et al. 2013), illustrating their significant ecological role in the Neotropics.

## Environmental variables

We consider the environment experienced by an individual to be composed of abiotic and biotic factors. We explored several topographic and biotic descriptors of Paracou plots (relative elevation, slope, curvature, topographic ruggedness index, topographic wetness index, elevation, canopy height and neighbourhood crowding index, see supplementary material S1). We chose topographic wetness index and neighbourhood crowding index as two little-correlated (Pearson's r = 0.12) environmental descriptors to depict the
distribution of species complexes and that of species within complexes along the distribution of light, water, and nutrients.

The topographic wetness index (TWI), which was correlated to other topographic variables, identifies water accumulation areas and is thus critical for species distribution at local scale in tropical ecosystems (Ferry et al. 2010; Allié et al. 2015). TWI was derived from a 1-m resolution digital elevation model built based on data from a LiDAR campaign done in 2015 using SAGA-GIS (Conrad et al. 2015).

The neighbourhood crowding index (NCI; Uriarte et al. 2004), which was correlated to canopy height, was calculated from field censuses and used as a descriptor of the biotic interactions among trees. Although we recognise their potential non-negligible role in explaining species distributions, other biotic effects, such as variance in herbivory pressure and pathogen species richness, were not directly included into our analyses. The neighbourhood crowding index NCIᵢ for each tree individual i was calculated with the following formula:

$$NCI_i = \sum_{j|\delta_{i,j}<20m} DBH_j^2 \cdot \exp(-\frac{1}{4}\delta_{i,j}) \quad (1)$$

where DBHⱼ is the diameter of neighbouring tree j and δᵢⱼ its distance to individual tree i. NCIᵢ is computed for neighbours at a distance δᵢⱼ of up to 20m because NCI showed negligible effect beyond 20m in preliminary analysis. The size effect of neighbours was taken as their squared DBH, and hence proportional to their basal area. The distance effect
of neighbours was set to -1/4, corresponding to neighbours beyond 20m having less than 1% effect compared to the effect of neighbours at 0m.

## Analyses

### Distribution of complexes

The distribution of each species complex was inferred separately. We considered the occurrences of all individuals from species belonging to the species complex as presences, and all occurrences of trees belonging to other species as pseudo-absences. The presence of each species complex $Presence_{species complex_k}$ was inferred with a logistic regression within a Bernoulli distribution (which corresponds to the best model form among several forms tested, see supplementary material S2 and S3):

$$ Presence_{species complex_k} \sim Bernoulli[\logit^{-1}(\alpha_k + \beta_k * X_k + \gamma_k * X_k^2)] \quad (2) $$

were $X$ is the matrix of environmental descriptors (TWI and NCI), $\alpha$ is the intercept, $\beta$ is a vector representing the slope of environmental descriptors and $\gamma$ is a vector representing the quadratic form of effects of environmental descriptors for every species complex $k$ (see supplementary material S9 and S10).
Distribution of species

Joint distributions of species were inferred within each species complex. We used a softmax regression within a conjugated Dirichlet Process and Multinomial distribution to infer the distribution of species jointly and not independently:

$$ \text{Presence}_{\text{species}_i|\text{species complex}_k} \sim \text{Dirichlet Multinomial}(\text{softmax}(\alpha_i + \beta_i * X_i + \gamma_i * X_i^2))(3) $$

were *Presence*<sub>species<sub>i</sub>|species complex<sub>k</sub></sub> represents the species *i* for every individual as a simplex of 0s and 1s (i.e. 0 for all other species from the species complex and 1 for the considered species), *X* is the matrix of environmental descriptors (i.e. TWI and NCI), *α* is the vector of species intercepts, *β* is a matrix representing the slope of environmental descriptors and *γ* is a matrix representing the quadratic form of effects of environmental descriptor for every species *i* of the species complex *k* (see supplementary material S9 and S10).

Environmental descriptors were all scaled to the unit in order to ease model inference and compare the strength of the effects among environmental descriptors. A Bayesian method was used to infer parameters of all models using stan language (Carpenter et al. 2017, see supplementary material S6 and S7) and the rstan package (Stan Development Team 2018) in the R environment (R Core Team 2020).
## Results

The topographic wetness index (TWI) and the neighbourhood crowding index (NCI) had null or weak effects on the probability of occurrence of species complexes, with the exception of an effect of TWI on the probability of occurrence of the *Eschweilera* clade *Parvifolia*, *Licania*, and *Iryanthera* (Fig. 1) species complexes. Wetter habitats (TWI>4) resulted in an increasing probability of occurrence of the species complex *Iryanthera* but a decreasing probability of occurrence of the species complexes *Licania* and *Eschweilera* clade *Parvifolia* (Fig. 1). However, the ranking of species complexes for probability of occurrence did not change significantly along the TWI gradient.

Conversely, the *TWI* strongly influenced the relative probability of occurrence of species within species complexes, with shifts in species dominance. The effect of the *NCI* was substantial, but did not shift species dominance within species complexes. For instance, the relative probability of occurrence of species *Iryanthera hostmanii*, *Eschweilera coriacea*, and *Symphonia globulifera* increased with water accumulation (TWI) while it decreased for *I. sagotiana*, *E. sagotiana*, and *S. sp1* (Fig. 2 and supplementary material S11). The change of relative probability of occurrence along the *TWI* gradient led to a shift of dominance among the aforementioned species within the *Symphonia*, *Eschweilera* clade *Parvifolia*, and *Iryanthera* species complexes, revealing a strong effect of topography. Similarly, the relative probability of occurrence of species *Licania membranacea*, *Eschweilera sagotiana*, and *Symphonia sp1* increased with neighbourhood crowding (NCI) while it decreased for *L. alba*, *E. coriacea*, and *S. globulifera* (Fig. 2 and supplementary material S11). Thus, two species
complexes, *Symphonia* and *Eschweilera* clade *Parvifolia*, included species with opposed
preferences along environmental gradients defined through *TWI* and *NCI*. For instance, *S. sp1*, more tolerant to neighbourhood crowding (high NCI), grows preferentially in drier
habitats such as plateaus (low TWI), while *S. globulifera* grows preferentially with
decreased neighbourhood crowding (low NCI) and dominates in wet habitat such as
bottomlands (high TWI).

Discussion

Understanding the eco-evolutionary processes that underlie the origin and maintenance of
species complexes, such as how species within species complexes exploit differential
ecological niches (Runemark et al. 2019), is paramount to further our knowledge of
Neotropical diversification processes (Pinheiro et al. 2018). Nevertheless, the ecological
processes governing the distribution of species complexes in the Neotropics have received
relatively little attention (Baraloto et al. 2012; ter Steege et al. 2013; Levi et al. 2019). Here,
we show that species complexes of Neotropical trees span the full range of the studied
topographic wetness and competition gradients, and are thus widely spread throughout
light, water, and nutrient habitats at the fine spatial scale. Conversely, most species within
species complexes show pervasive niche differentiation along topographic position, water
accumulation, and competition gradients. Habitat preferences along topographic wetness
and competition gradients were coordinated among species within several species
complexes: species that are more tolerant to competition for resources grow in drier and
less fertile plateaus and slopes, as opposed to wet and fertile bottom-lands, where species
that are less tolerant to competition for resources are more frequently found. Consequently,
our results suggest that the ecologically broad distribution of species complexes combined
with the habitat specialisation of species within species complex might explain the success
of these Neotropical species complexes at the regional scale (ter Steege et al. 2013). This
appreciation of the ecological abundance of species and their species complexes does not
yet consider reproductive biology and interspecific gene flow. For this statement to hold
more broadly, it is necessary to assume at least partial reproductive isolation of species and
evolutionary adaptation of species to the fine-scale habitat structure, but with occasional
adaptive introgression between species at the species complex level.

Species complexes are widely spread across habitats

The general null or weak effects of our considered biotic and abiotic environmental
variables on the abundance distribution of species complexes suggest that species
complexes are widely spread throughout light, water, and nutrient gradients at the local
scale, and that the species complexes thus behave as generalists that appear to benefit from
the evolutionary advantages typical of generalists. Topographic wetness index (TWI)
indicates the topographic position where water accumulates. Neighbourhood crowding
index (NCI) represents competition with neighbours and thus access to light, water, and
nutrients. TWI and NCI had no effect on the distribution of species complexes, at the
exception of a weak effect of high TWI increasing the abundance of *Iryanthera*, and
increasing the abundances of *Licania*, and *Eschweilera clade Parvifolia*. This results
emphasises the generality of the widespread distribution of species complexes throughout
light, water, and nutrients gradients with either segregated species with ecological preferences or generalist species.

The higher abundance of the *Iryanthera* species complex in wet habitats has already been evidenced experimentally (Baraloto et al. 2007). Increased or decreased abundance of species complexes at high *TWI* values might be due to variations in species complex-specific adaptations to a more constraining habitat, for example anoxia in water-logged soils.

## Species show pervasive niche differentiation within species complexes

The repeated observation of species relative abundance variation within species complexes along biotic and abiotic environmental gradients represents evidence for pervasive niche differentiation of species within four locally abundant species complexes. Indeed, species within *Iryanthera*, *Licania*, *Symphonia*, and *Eschweilera* clade *Parvifolia* species complexes are segregated along a gradient from wet to drier habitats and a gradient from low to increased neighbourhood crowding.

Habitat segregation along topography and wetness gradients corresponds to the well-known bottomland to plateau gradient observed in Amazonia (Kraft et al. 2008; Ferry et al. 2010). Species within species complexes segregate between seasonally flooded habitats with frequent soil anoxia but increased soil fertility and drier uphill habitats with a higher risk of drought and reduced fertility, whereas few species grow preferentially in intermediate habitats (e.g. *Licania membranacea*, Fig. 2). Indeed, water-use strategies and
edaphic conditions are known to shape divergent habitat associations between congeneric
species pairs (Baltzer et al. 2005). Our results are in agreement with previous evidence of
species-habitat association with topography among sympatric congeneric species at local
scale (Itoh et al. 2003; Allié et al. 2015; Lan et al. 2016; but see Baldeck et al. 2013b). We
tested here topography in our study but not edaphic properties. Besides covariation with
topography, edaphic properties have independent effects on the species distribution
(Baldeck et al. 2013a), which may increase species niche differentiation within species
complexes.

Species within species complexes segregate also between high neighbourhood crowding
conditions that result in a decreased access to light, water, and nutrients and low
neighbourhood crowding conditions where competition for resources is lower. Yamasaki et
al. (2010) already evidenced segregation according to access to light between two
congeneric species at local scale, but that grew in the same topography. In our study, *S. sp1*,
*I. sagotiana*, *E. sagotiana*, and *T. hexaphylla* showed more tolerance to competition for
resources (i.e. high *NCI*) and grow in drier and less fertile habitats (i.e. low *TWI*), whereas
*S. globulifera*, *I. hostmannii*, and *E. coriacea* that grow in wet habitats also grow
preferentially with less competition for resources. To the best of our knowledge, previous
studies have shown segregation of species according to topography or light, independently
but not together, which opens avenues for future studies on their joint effects.
**Conclusion**

We found Neotropical tree species complexes to be widespread across habitats at local scale, while the species composing them showed pervasive habitat differentiation along topography and competition gradients. The pervasive niche differentiation among species within several species complexes might be related to parallel adaptation to local environment resulting in replicated functional strategies (Baraloto et al. 2007, Baltzer et al. 2005), with several diversification events across taxa (e.g. Fine et al. (2014) for Protiae). Habitat specialisation reduces competition among the species and thus helps the species gain reproductive isolation for their establishment within species complexes (Runemark et al. 2019). Meanwhile, porous genomes allow for the transfer of adaptive genes through potentially rapid introgression (Cannon and Scher 2017) that may benefit one or several species, allowing for coevolution at the species complex level (Cannon and Lerdau 2015). Consequently, if habitat specialisation allows at least partial reproductive isolation and if porous genomes allow adaptive introgression, our results suggest that both habitat specialisation of species within species complexes and the widespread distribution of species complexes might explain the success of these Neotropical species complexes at the regional scale (ter Steege et al. 2013).

**Acknowledgements**

We thank the University of Bordeaux for a PhD grant to Sylvain Schmitt. We are grateful to Pascal Petronelli and the CIRAD inventory team for their work on tree inventories and
botanical identification. This study was partially funded by an Investissement d'Avenir
grant of the ANR: CEBA (ANR-10-LABEX-0025).

Conflict of interest

The authors declare that they have no conflicts of interest.

Data accessibility

TWI and spatial positions of individuals were extracted from the Paracou Station database,
for which access is modulated by the scientific director of the station
(https://paracou.cirad.fr).

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<table><caption>Table 1: Identified species complexes with species including more than 10 individuals censused in the Paracou forest inventory. N represents the number of tree studied per species.</caption><thead><tr><th>Complex</th><th>Species</th><th>N</th></tr></thead><tbody><tr><td>Iryanthera</td><td>Iryanthera sagotiana</td><td>381</td></tr><tr><td>Iryanthera</td><td>Iryanthera hostmannii</td><td>335</td></tr><tr><td>Licania</td><td>Licania alba</td><td>1117</td></tr><tr><td>Licania</td><td>Licania membranacea</td><td>442</td></tr><tr><td>Licania</td><td>Licania canescens</td><td>164</td></tr><tr><td>Licania</td><td>Licania micrantha</td><td>139</td></tr><tr><td>Licania</td><td>Licania ovalifolia</td><td>95</td></tr><tr><td>Licania</td><td>Licania sprucei</td><td>76</td></tr><tr><td>Licania</td><td>Licania laxiflora</td><td>37</td></tr><tr><td>Licania</td><td>Licania parvifructa</td><td>12</td></tr><tr><td>Licania</td><td>Licania densiflora</td><td>6</td></tr><tr><td>Parvifolia</td><td>Eschweilera sagotiana</td><td>1208</td></tr><tr><td>Parvifolia</td><td>Eschweilera coriacea</td><td>500</td></tr><tr><td>Parvifolia</td><td>Eschweilera decolorans</td><td>84</td></tr><tr><td>Parvifolia</td><td>Eschweilera wachenheimii</td><td>19</td></tr><tr><td>Parvifolia</td><td>Eschweilera grandiflora</td><td>14</td></tr></tbody></table>
<table><tr><td>Parvifolia</td><td>Eschweilera pedicellata</td><td>14</td></tr><tr><td>Symphonia</td><td>Symphonia sp.1</td><td>382</td></tr><tr><td>Symphonia</td><td>Symphonia globulifera</td><td>71</td></tr><tr><td>Talisia</td><td>Talisia hexaphylla</td><td>60</td></tr><tr><td>Talisia</td><td>Talisia praealta</td><td>37</td></tr><tr><td>Talisia</td><td>Talisia simaboides</td><td>31</td></tr></table>
**Figure legends**

**Figure 1** Predicted probability of occurrence for studied species complexes in Paracou. Lines and shaded areas represent mean and the 95% confidence interval of projected probability of occurrence of species complexes depending on a) NCI (left) and b) TWI (right), with the other variable set to its mean value. Dashed lines represent the observed mean relative abundance of each species complex in Paracou. Species complexes are indicated by different colors

**Figure 2** Predicted relative probability of occurrence for species within five species complexes in Paracou a) Symphonia; b) Iryanthera; c) Talisai; d) Parvifolia; e) Licania. For each complex, projected relative probability of occurrence of species is shown depending on NCI (left) and TWI (right), with the other variable set to its mean value. Dashed line indicates the observed mean relative abundance of each species in Paracou. Species are identified by different colors.
<figure><img src="image_2.png" /><figcaption>Figure 1</figcaption></figure>
<figure><img src="image_3.png" /><figcaption>Figure 2</figcaption></figure>
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**Supplementary Material**

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