In and out of Madagascar : dispersal to peripheral islands, insular speciation and diversification of Indian Ocean daisy trees (Psiadia, Asteraceae)

This study was supported by the European Union’s HOTSPOTS Training Network (MEST-2005-020561)Madagascar is surrounded by archipelagos varying widely in origin, age and structure. Although small and geologically young, these archipelagos have accumulated disproportionate numbers of unique lineages in comparison to Madagascar, highlighting the role of waif-dispersal and rapid in situ diversification processes in generating endemic biodiversity. We reconstruct the evolutionary and biogeographical history of the genus Psiadia (Asteraceae), a plant genus with near equal numbers of species in Madagascar and surrounding islands. Analyzing patterns and processes of diversification, we explain species accumulation on peripheral islands and aim to offer new insights on the origin and potential causes for diversification in the Madagascar and Indian Ocean Islands biodiversity hotspot. Our results provide support for an African origin of the group, with strong support for non-monophyly. Colonization of the Mascarenes took place by two evolutionary distinct lineages from Madagascar, via two independent dispersal events, each unique for their spatial and temporal properties. Significant shifts in diversification rate followed regional expansion, resulting in co-occurring and phenotypically convergent species on high-elevation volcanic slopes. Like other endemic island lineages, Psiadia have been highly successful in dispersing to and radiating on isolated oceanic islands, typified by high habitat diversity and dynamic ecosystems fuelled by continued geological activity. Results stress the important biogeographical role for Rodrigues in serving as an outlying stepping stone from which regional colonization took place. We discuss how isolated volcanic islands contribute to regional diversity by generating substantial numbers of endemic species on short temporal scales. Factors pertaining to the mode and tempo of archipelago formation and its geographical isolation strongly govern evolutionary pathways available for species diversification, and the potential for successful diversification of dispersed lineages, therefore, appears highly dependent on the timing of arrival, as habitat and resource properties change dramatically over the course of oceanic island evolution.Publisher PDFPeer reviewe

Ancestral area reconstruction using the dispersal-extinction-cladogenesis model.

<p>Inset map shows the Madagascar and Indian Ocean Islands biodiversity hotspot (dashed line) and the distribution and number of species of <i>Psiadia</i> (negative values indicate recorded extinctions of putative members of the genus). Contours of smaller islands have been enlarged and highlighted for clarity. Branch colors follow the designated geographic areas on the inset map. Bold node numbers indicate differences in optimal resolution between reconstruction using the dec-model and statistical Dispersal-Vicariance analyses. Asterisks highlight nodes for which multiple equally probable solutions were retrieved using Lagrange and/or S-DIVA. Arrows indicate dispersal events between designated regions. Node numbers refer to per-clade results listed in <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0042932#pone.0042932.s004" target="_blank">Table S3</a>. Geographic coverage is indicated by capitals following taxon names. Broken branches lead to nodes with low posterior probabilities (<90) obtained in BEAST.</p

Lineage through time curves (with 95% confidence intervals) for clades A and B.

<p>Black lines: individual empirical curves from the BEAST analysis. Blue (clade A) and red (clade B) lines demarcate 95% confidence intervals generated using a constant rates model. Included rate shifts (*) and 95% HPD intervals shown as described in text and <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0042932#pone-0042932-g003" target="_blank">Figure 3</a>.</p

Results of relaxed Bayesian dating and diversification rate shift analyses for selected nodes.

<p>Notes: Values in Ma. Node numbers refer to symbols used in <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0042932#pone-0042932-g003" target="_blank">Figure 3</a>. Abbreviations: HPD – Highest Posterior Density interval; PP – Posterior Probability; MRCA – Most Recent Common Ancestor; SG – Slowinski-Guyer; RC – Relative Cladogenesis.</p

ERM nodal probabilities obtained in whole-tree tests for diversification rate-variation using SYMMETREE.

<p>Notes: Tests were conducted on the consensus tree obtained with MrBayes and the two separate pruned ingroup clades of clade A and B, and the MCC chronogram obtained with BEAST.</p

Chronogram for <i>Psiadia</i> s.l. and results of diversification rate shift analyses.

<p>Broken branches lead to nodes with low posterior probabilities (<90) obtained in BEAST. Arrows indicate rate shifts associated with results obtained using SYMMETREE (rate shift box A, B & C: Δ1, Δ2 and SG) and the Relative Cladogenesis test (RC1 & RC2). Numbered nodes 1–4 indicate calibrated nodes. Numbered Nodes 5–10 refer to key events in the evolutionary history of <i>Psiadia</i>, as discussed in text. Bars: blue, <i>Psiadia</i> clade A & B; grey, other taxa contained with <i>Psiadia</i>-clades; white, outgroup taxa. Abbreviations: Re (Réunion), Mu (Mauritius), Ro (Rodrigues), Md (Madagascar), So (South Africa), Sa (Saudi Arabia), Ta (Tanzania), My (Mayotte), Th (Thailand), Pa (Paraguay), Au (Australia), Ml (Malawi), Co (Congo-Kinshasa), Et (Ethiopia), Ou (Outgroups).</p

Results of birth-death likelihood (BDL) analyses of lineage diversification.

<p>Notes: Analyses were conducted using the ultrametric tree obtained in BEAST. All outgroups and intermittent taxa were pruned to obtain the ingroup clades A and B. Abbreviations: Pb – pure birth; Bd – birth-death; DDX – exponential density dependent; DDL – logistic density dependent; Yule2rate – Yule with 2 rates; Yule3rate – Yule with 3 rates; LH – log-likelihood; r1/r2/r3 – net diversification rates; a – extinction fraction; xp – rate change parameter DDX model; k – carrying capacity parameter DDL model; st1/st2 – timing of rate shift (mya); AIC – Akaike information criterion; ΔAICrc  =  difference between the best rate constant and rate variable models.</p