Comparative Phyloclimatic Analysis and Evolution of Ecological Niches in the Scimitar Babblers (Aves: Timaliidae: <em>Pomatorhinus</em>)

<div><p>We present the first extensive and integrative analysis of niche evolution based on climatic variables and a dated molecular phylogeny of a heterogeneous avian group of Southeast Asian scimitar babblers of the genus <em>Pomatorhinus</em>. The four main clades of scimitar babblers have species that co-occur in similar areas across southern Asia but some have diverged at different timeframes, with the most recently evolved clade harboring the highest number of species. Ecological niche models and analysis of contributing variables within a phylogenetic framework indicate instances of convergent evolution of members of different clades onto similar ecological parameter space, as well as divergent evolution of members from within clades. <em>Pomatorhinus</em> species from different clades occupying Himalayan foothills show convergence towards similar climatic tolerances, whereas within a clade, allopatric sister-species occurring in the Himalayas have diverged to occupy different climatic parameter spaces. Comparisons of climatic tolerances of Himalayan foothills taxa with species distributed further south in Assam/Burma and Burma/Thailand indicate convergence towards similar parameter spaces in several climatic variables. Niche overlap was observed to be lower among species of the youngest clade (<em>ruficollis</em>) and higher among species of older clades (<em>ferruginosus</em>). Analysis of accumulation of ecological disparity through time indicates rapid divergence within recent time frames. As a result, Himalayan taxa originating at different temporal scales within the four main scimitar babbler clades have differentiated ecologically only in recently diverged taxa. Our study suggests that the repeated orogenic and climatic fluctuations of the Pliocene and Pleistocene within mainland Southeast Asia served as an important ecological speciation driver within scimitar babblers, by providing opportunities for rapid geographic expansion and filling of novel environmental niches.</p> </div

History of evolution of climatic tolerances <i>Pomatorhinus</i> scimitar babblers.

<p>The maximum a posteriori chronogram topology produced by the BEAST analysis and the PNO profiles of four ecological variables have been integrated to represent the reconstruction of mean climatic tolerances based on 100 random samples of the PNO profiles at internal nodes. Panel (a) depicts the evolution of Isothermality (Bio3), (b) reconstructs Temperature Seasonality (Bio4), while (c) summarized the evolution of Precipitation of the warmest quarter (Bio18), and (d) of Precipitation of the coldest quarter (Bio19). Members of the four main <i>Pomatorhinus</i> clades are colored red (<i>ruficollis</i>), blue (<i>schisticeps</i>), yellow (<i>ferruginosus</i>), and green (<i>hypoleucos</i>). The three letter codes abbreviating the specific epithets of each species are positioned at the mean of the 80% central density. Taxa occupying Himalayan foothills are denoted by open triangles, Assam/Burma highlands by open circles, and Burma/Thailand highlands are represented by open squares. Overlapping internal nodes indicate convergent climatic origins, while crossing branches of the phylogenetic tree indicate convergent niche evolution among taxa from different clades. See also <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0055629#pone.0055629.s003" target="_blank">Figure S3</a> for plots of evolution of climatic tolerances of all 10 bioclimatic variables used in niche modeling algorithm of the present study.</p

Summary of input data and MAXENT model parameters.

<p>Summary of number of occurrence points and MAXENT modeling algorithm variable contributions and model AUC scores for 29 species of Southeast Asian <i>Pomatorhinus</i> scimitar babblers. For taxa with 10–12 occurrence points, a cross-validation sampling has been employed in MAXENT and averages are being reported throughout the table. Taxa are grouped by clades identified through the phylogenetic analysis outlined in <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0055629#pone-0055629-g003" target="_blank">Figure 3</a>. Species abbreviations reflect the first three letters of their specific epithet, and taxa annotated by open triangles occupy Himalayan foothills, while open circles and open squares denote species occupying highlands at lower latitudes (Assam/Burma and Burma/Thailand, respectively). Variable abbreviations are given in brackets and are referenced throughout the main text and the supplementary materials. Variable contributions to overall model performance greater than 25% are indicated in bold and darkened boxes.</p

Phylogenetic hypothesis and chronogram of scimitar babbler relationships.

<p>Ultrametric time calibrated topology based on the analysis of mitochondrial sequence data from 29 scimitar babbler taxa sampled in the study of Reddy and Moyle <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0055629#pone.0055629-Reddy2" target="_blank">[17]</a>. Horizontal grey bars at nodes represent 95% confidence intervals around node heights as generated in the program BEAST, and calibrated using a normally distributed prior on ND2 mutation rates (see Methods). Nodal support above 95% Bayesian posterior probability is indicated by an asterisk. The four main clades are highlighted in grey and labeled with their respective taxonomic designation. Taxa annotated by open triangles occupy Himalayan foothills, while open circles and open squares denote species occupying highlands at lower latitudes (Assam/Burma and Burma/Thailand, respectively).</p

Niche overlap values between and within clades of <i>Pomatorinus</i> babblers.

<p>Summary of geographic niche overlap values as calculated by the <i>D</i> (above diagonal) and <i>I</i> (below diagonal) statistics as outlined in Warren et al. <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0055629#pone.0055629-Phillips1" target="_blank">[49]</a>. Species are grouped by clades identified through the phylogenetic analysis outlined in <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0055629#pone-0055629-g003" target="_blank">Figure 3</a>. Species abbreviations reflect the first three letters of their specific epithet, and taxa annotated by open triangles occupy Himalayan foothills, while open circles and open squares denote species occupying highlands at lower latitudes (Assam/Burma and Burma/Thailand, respectively). Boxed values represent overlap comparisons between taxa within their respective clades. Overlap values ranging from 0.11–0.50 are highlighted in light grey, while values above 0.50 are highlighted in dark grey.</p

Predicted niche occupancy (PNO) profiles for the four clades of <i>Pomatorhinus</i> scimitar babblers.

<p>Horizontal axes represent the Isothermality (Bio3 - the tolerance of diurnal temperature range divided by the annual temperature range, all multiplied by 100) parameter space divided into 50 equally spaced bins, while vertical axes denote the total suitability of the isothermality index of each species over its entire geographic range (see Methods). Specific epithets have been reduced to three letter codes for brevity. Taxa annotated by open triangles occupy Himalayan foothills, while open circles and open squares denote species occupying highlands at lower latitudes (Assam/Burma and Burma/Thailand, respectively). Overlapping peaks of PNO profiles indicate similar climatic tolerances, while the overall breadth of the profile denotes the degree of specificity in climatic tolerance. See also <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0055629#pone.0055629.s002" target="_blank">Figure S2</a> for PNO graphs of all 10 bioclimatic variables used in the niche modeling algorithm of the 4 <i>Pomatorhinus</i> clades and their constituent species.</p

Plots of accumulation of relative ecological disparity through time (DTT).

<p>Plot summarizes all 29 Southeast Asian <i>Pomatorhinus</i> scimitar babblers (solid line) compared with mean disparity as simulated under 1000 replicates of an unconstrained model of Brownian Evolution (dashed line). Disparity plots start out in the left side or the graph (root of topology) at a value of 1 and end on the right (all extant taxa) at a value of 0. Disparity represents the mean of the square pairwise differences between all terminal taxa defined at each node (see Methods). The same four bioclimatic variables as in <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0055629#pone-0055629-g006" target="_blank">Figure 6</a> (Isothermality, Temperature Seasonality, Precipitation of Warmest Quarter, Precipitation of Coldest Quarter) are represented in distinct panels. The morphological disparity index (MDI) value represent the overall difference in disparity between the observed and the unconstrained null hypothesis.</p

Map illustrating the geographic region of <i>Pomatorhinus</i> scimitar babblers.

<p>Sampled occurrence points used in ecological niche model analyses are indicated by red dots. Overlap of resulted ecological niche models of the 29 species included in the study ranges from highest species density indicated in blue hues (maximum of 14 species), while areas of single species occurrence are denoted in light green. Note that disjunct geographic areas such as the islands of the Philippines and Sulawesi do offer climatic conditions suitable for scimitar babblers, although no taxa presently occur in these areas. See also <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0055629#pone.0055629.s001" target="_blank">Figure S1</a> for a summary of ecological niche models of each of the 29 <i>Pomatorhinus</i> species.</p

Supp Fig 1

Average Standard Deviation of Split Frequencies plot

TreeBASE S11986

Nexus file of the final 6-gene data set