Evolutionary patterns of range size, abundance and species richness in Amazonian trees

24 Amazonian tree species vary enormously in their total abundance and range size, while 25 Amazonian tree genera vary greatly in species richness. Here, we construct a phylogenetic 26 hypothesis that represents half of Amazonian tree genera in order to analyse evolutionary 27 patterns of range size, abundance, and species richness. We find several clear, broad-scale 28 patterns. Firstly, there is significant phylogenetic signal for all three characteristics, i.e. closely 29 related genera tend to have similar numbers of species and similar mean range size and 30 abundance. Additionally, the species richness of genera shows a significant, negative relationship 31 with the mean range size and abundance of their constituent species, while mean range size and 32 abundance are significantly, positively correlated. These correlations are stronger in the raw data, 33 but still significant when using phylogenetically independent contrasts. We suggest that tree 34 stature and/or other phylogenetically related biological traits underlie these results. Lineages 35 comprised of small-statured trees show greater species richness and smaller range sizes and 36 abundances. Lastly, the phylogenetic signal that we evidence for range size suggests that should 37 many small ranged species go extinct, greater phylogenetic diversity may be lost than expected if 38 range size were distributed randomly across the phylogeny. 39 40 41


Introduction
Some Amazonian tree species attain incredibly high abundance (tens to hundreds of millions of mature individuals), while most have small populations sizes, numbering in the thousands to tens of thousands (ter Steege et al. 2013).Similarly, the range of some Amazonian tree species extends across the entire Amazon basin, while most are restricted to much smaller areas (Kristiansen et al. 2009).A similar imbalance is observed in species to genus ratios.Over half of all Amazonian tree species belong to genera with 100 or more species, while the majority of genera (52%) have ten or fewer species (Gentry 1993).Recent studies have begun to document variation in the range size (Feeley & Silman 2009) and abundance (ter Steege et al. 2013) of Amazonian tree species and in the species richness of Amazonian tree genera (Baker et al. 2014), but these studies have largely failed to find causal factors to explain the variation (although see Baker et al. 2014).Here, we explore broad-scale evolutionary patterns for these characteristics for the first time using a newly derived, genus-level phylogeny that covers half of all Amazonian tree genera.

Methods
We intersected a list of all Neotropical tree genera (from ctfs.arnarb.harvard.edu/webatlas/neotropicaltree)with a list of Amazonian plant species (Feeley & Silman 2009) in order to generate a list of Amazonian tree species.The Feeley and Silman (2009) dataset additionally includes estimates of range size for all species.We obtained estimates for the total abundance of Amazonian tree species from ter Steege et al. (2013)  We obtained sequences of the rbcL plastid gene for 631 Amazonian angiosperm tree genera (Table S1), with 568 sequences coming from Genbank (www.ncbi.nlm.nih.gov/genbank/) and an additional 64 genera being newly sequenced following protocols outlined in Baraloto et al. (2012).We obtained sequences of the matK plastid gene from Genbank for 452 of the 631 genera with rbcL data (Table S1).Sequences were aligned using the MAFFT software (Katoh & Standley 2013) and then manually checked and edited.Preliminary phylogenetic analyses allowed us to exclude sequences from GenBank that likely represent taxonomic misidentifications.
We estimated an initial phylogeny using maximum likelihood analysis in RAxML v8.0.0 (Stamatakis, Hoover & Rougemont 2008), on the CIPRES web server (www.phylo.org).We included sequences of Amborella trichopoda (Amborellaceae) and Nymphaea alba (Nymphaeaceae) as outgroups.This initial tree was used as a starting point for simultaneous topology and divergence time estimation in the software BEAST v1.82 (Drummond & Rambaut 2007).We implemented fossil-based age constraints for 25 nodes distributed across the phylogeny (see Table S2).
For each genus in the phylogeny, we calculated the mean range size and abundance for all constituent species in the Feeley and Silman (2009) et al. (2013).We considered the number of species for each genus in the Feeley and Silman (2009) dataset as an estimate of the species richness of that genus in the Amazon.As an alternative estimate, we used the Neotropical species richness estimates for genera in Gentry   1993).We assessed correlations amongst these genus-level characteristics, both in the raw data and using phylogenetically independent contrasts.We tested for phylogenetic signal for each of these genus-level characteristics using Pagel's λ (Freckleton, Harvey & Pagel 2002).Under Brownian motion evolution, where trait values drift randomly over evolutionary time and where the phylogenetic relationships of taxa perfectly predict the covariance among taxa for trait values, the expected value of λ is one.When the phylogenetic relationships of taxa do not predict the covariance at all, the expected value of λ is zero.We compared the fit of different values for λ (one, zero and the maximum likelihood estimate) using the Akaike information criterion (AIC).
In order to determine which lineages may be responsible for significant phylogenetic signal for a given characteristic (e.g.mean range size of genera), we used the following approach.We first estimated the ancestral value at each node in the phylogeny using maximum likelihood ancestral state reconstruction (Schluter et al. 1997).We then randomised the tips of the phylogeny 1000 times, reconstructed ancestral values at nodes each time, and compared the observed reconstructed value to that across the randomisations.If the observed value for a node was greater than that in 97.5% of the randomisations, we considered the lineage descending from that node to show significantly high values for the trait, while if the observed value was lower than 2.5% of the randomisations, we considered the lineage to show significantly low values.The phylogeny derived from these sequences spans from the Magnoliids to the Asterids, thus encompassing all major lineages of angiosperms (Fig. 1).Most orders and families were monophyletic in the phylogeny with the notable (previously known) exceptions of Olacaceae and Icacinaceae, while the large-scale phylogenetic relationships are largely in agreement with those from recent, angiosperm-wide phylogenetic analyses (e.g.Magallón et al. 2015).

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The species richness of genera is negatively correlated with mean range size (r = -0.40,p < 0.001) and mean abundance (r = -0.38,p < 0.001).These relationships are weaker, but still significant, when using phylogenetically independent contrasts (PICs), indicating that phylogenetically related traits partially underlie the correlations (mean range size PICs: r = -0.28,p < 0.001; mean abundance PICs: r = -0.24,p < 0.001; Fig. 2).Meanwhile, mean range size and abundance of genera are strongly positively correlated, using both the raw data and PICs (r = 0.44, p < 0.001; PICs: r = 0.43, p < 0.001).All of the genus-level characteristics show significant phylogenetic signal, but less than what would be expected under a Brownian motion model of evolution (Table 1).
Significant phylogenetic signal for these characteristics is driven by significantly high or low values in many lineages (Fig. 1, Table S3).Diverse lineages in the Magnoliids and the Asterids show high species richness and low mean range size and abundance, including the Lamiales and multiple lineages in the Rubiaceae and Solanales.One marked exception to the general pattern in the Asterids is Lecythidaceae, which shows low species richness and high abundance.All results concerning species richness were highly similar when analyses alternatively used species richness estimates from Gentry (1993).

Discussion
Our analyses have revealed that fundamental characteristics of Amazonian tree genera, such as their species richness and mean range size, show strong relationships with phylogeny (Fig. 1) and with each other (Fig. 2).Closely related genera have similar numbers of species and are comprised of species with similar range sizes and abundances, while the species richness of genera shows a significant negative correlation with mean range size and abundance.This Many of the lineages in our study that show high species richness and small geographic ranges (e.g.Myrtaceae, Melastomataceae, Rubiaceae, Asterales, Solanales, and Lamiales) tend to be small in stature.Previous studies have shown a positive relationship between the height of Amazonian trees and their range size (Kristiansen et al. 2009, Ruokolainen et al. 2002).Such a relationship may be due to larger-statured trees being able to disperse their seeds greater distances, likely through greater fecundity, which would increase the chances that at least some seeds make it a long distance and would, for animal-dispersed species, potentially attract more dispersers.Increased dispersal ability would also increase gene flow among distant populations, which, in turn, could reduce opportunities for allopatric isolation and contribute to reduced diversification.Smaller statured trees may also have shorter generation times, which could contribute to increased diversification (Baker et al. 2014).Thus, small-stature may be a biological trait that spurs diversification and may also underlie the negative correlation between mean range size and species richness of genera.
Small-statured lineages also show lower abundances, although this is partly, if not entirely, explained by the abundance estimates being derived from tree plots that survey individuals >10 cm diameter at breast height (ter Steege et al. 2013).In any case, we are keen to emphasise that the genus-level characteristics that we studied here do not represent biological traits per se, but rather reflect underlying biological traits that are driving the observed phylogenetic signal and correlations.Traits other than tree stature (e.g.dispersal syndrome) may also show phylogenetic signal and be responsible for the observed correlations; large-scale compilations of trait data for

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Preprints | https://doi.org/10.7287/peerj.preprints.2043v1| CC-BY 4.0 Open Access | rec: 15 May 2016, publ: 15 May 2016 Meanwhile, diverse lineages in the Rosids show low species richness and high mean range size and abundance, including Euphorbiaceae, Salicaceae and Moraceae.Within the Rosids, the PeerJ Preprints | https://doi.org/10.7287/peerj.preprints.2043v1| CC-BY 4.0 Open Access | rec: 15 May 2016, publ: 15 May 2016 exception to this pattern is found in multiple lineages in the Myrtales, including the Melastomataceae, which show a pattern similar to most lineages in the Asterids.The Leguminosae (Fabaceae), the most genus-rich family in our dataset, does not show any significant departures from null expectations, although individual lineages therein show low species richness and high mean range size.Within the monocots, the Arecaceae show significantly low mean range size, while one lineage (Iriartea with Socratea) shows significantly high abundance.
negative relationship is pervasive across multiple phylogenetic scales.At a broad scale, we found that various lineages in the Rosids are comprised of genera that show low species richness and high mean range size and abundance, while lineages in the Magnoliids and Asterids show the opposite pattern.PeerJ Preprints | https://doi.org/10.7287/peerj.preprints.2043v1| CC-BY 4.0 Open Access | rec: 15 May 2016, publ: 15 May 2016 Amazonian trees are clearly needed to advance our understanding of these patterns.PeerJ Preprints | https://doi.org/10.7287/peerj.preprints.2043v1| CC-BY 4.0 Open Access | rec: 15 May 2016, publ: 15 May 2016

Figure 1 :
Figure 1: Phylogeny of 631 Amazonian tree genera with terminal branches coloured according
and ter Steege et al. (2013) datasets.Of the 631 genera in the phylogeny, 493 had an abundance estimate for at least one species in ter Steege