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Systematic Biology Volume 58 Number 6, pp. 547–661 58 Number Volume Systematic Biology Volume 58, Number 6 December 2009 CONTENTS Systematic Biology REGULAR ARTICLES Species Tree Discordance Traces to Phylogeographic Clade Boundaries in North American Fence A JOURNAL OF THE Lizards ( Sceloporus ) Adam D. Leaché ........................................................................................................................................................................ 547 Society of Systematic Biologists The Use and Validity of Composite Taxa in Phylogenetic Analysis Véronique Campbell and François-Joseph Lapointe .................................................................................................................. 560 Radiation of Extant Cetaceans Driven by Restructuring of the Oceans Mette E. Steeman, Martin B. Hebsgaard, R. Ewan Fordyce, Simon Y. W. Ho, Daniel L. Rabosky, Rasmus Nielsen, Carsten Rahbek, Henrik Glenner, Martin V. Sørensen, and Eske Willerslev ........................................................................... 573 Taxon Selection under Split Diversity Bui Quang Minh, Steffen Klaere, and Arndt von Haeseler ...................................................................................................... 586 Estimating Trait-Dependent Speciation and Extinction Rates from Incompletely Resolved Phylogenies Richard G. FitzJohn, Wayne P. Maddison, and Sarah P. Otto ................................................................................................. 595 Reticulation, Data Combination, and Inferring Evolutionary History: An Example from Danthonioideae (Poaceae) Michael D. Pirie, Aelys M. Humphreys, Nigel P. Barker, and H. Peter Linder ....................................................................... 612 Heritability of Extinction Rates Links Diversifi cation Patterns in Molecular Phylogenies and Fossils BIOLOGY SYSTEMATIC Daniel L. Rabosky ..................................................................................................................................................................... 629 Testing Species-Level Diversifi cation Hypotheses in Madagascar: The Case of Microendemic Brookesia Leaf Chameleons Ted M. Townsend, David R. Vieites, Frank Glaw, and Miguel Vences .................................................................................... 641 BOOK REVIEWS Stephen Jay Gould: Refl ections on His View of Life David A. Morrison .................................................................................................................................................................... 657 Systematics and Taxonomy of Australian Birds R. Terry Chesser ........................................................................................................................................................................ 659 December 2009 Cover Illustration: Much less familiar than their larger and more colorful cousins, the diminutive leaf chameleons of the genus Brookesia are nonetheless one of the most speciose reptile groups in Madagascar. Although these leaf-litter inhabitants are distributed across most of the island, individual species often have very restricted distributions. In this issue, Townsend and co-authors use distributional data combined with a dated multi-gene phylogeny of this group to test recent hypotheses proposed to explain the generally high level of faunal and fl oral microendemism on the island. Their results fi nd no support for watershed-contraction or riverine-barrier mediated diversifi cation in this group, although a montane-refuge hypothesis is consistent with some fi ndings. However, species-level divergences in this group are much older than the Pliocene–Pleistocene ages previously proposed. Photos by Frank Glaw. VOLUME 58 ONLINE ISSN 1076-836X DECEMBER 2009 PRINT ISSN 1063-5157 oxford NUMBER 6 Published on behalf of the Society of Systematic Biologists http:// systbiol.org/ Syst. Biol. 58(6):641–656, 2009 c The Author(s) 2009. Published by Oxford University Press, on behalf of the Society of Systematic Biologists. All rights reserved. For Permissions, please email: [email protected] DOI:10.1093/sysbio/syp073 Advance Access publication on November 11, 2009 Testing Species-Level Diversification Hypotheses in Madagascar: The Case of Microendemic Brookesia Leaf Chameleons 1, 2 3 4 TED M. TOWNSEND ∗,DAVID R. VIEITES ,FRANK GLAW , AND MIGUEL VENCES 1Department of Biology, San Diego State University, 5500 Campanile Drive, San Diego, CA 92182-4164, USA; 2 Museo Nacional de Ciencias Naturales, Consejo Superior de Investigaciones Cient´ıficas,C/ Jos´eGutierrez Abascal n◦2, 28006, Madrid, Spain; 3Zoologische Staatssammlung, M¨unchhausenstr. 21, 81247 M¨unchen,Germany; and 4Technical University of Braunschweig, Zoological Institute, Spielmannstr. 8, 38106 Braunschweig, Germany; ∗Correspondence to be sent to: Department of Biology, San Diego State University, 5500 Campanile Drive, San Diego, CA 92182-4164, USA; E-mail: [email protected]. Abstract.—Madagascar’s flora and fauna are remarkable both for their diversity and supraspecific endemism. Moreover, many taxa contain large numbers of species with limited distributions. Several hypotheses have been proposed to explain this high level of microendemism, including 1) riverine barrier, 2) mountain refuge, and 3) watershed contraction hypotheses, the latter 2 of which center on fragmentation due to climatic shifts associated with Pliocene/Pleistocene glaciations. The Malagasy leaf chameleon genus Brookesia is a speciose group with a high proportion of microendemic taxa, thus making it an excellent candidate to test these vicariance scenarios. We used mitochondrial and nuclear sequence data to construct a Brookesia phylogeny, and temporal concordance with Pliocene/Pleistocene speciation scenarios was tested by estimating divergence dates using a relaxed-clock Bayesian method. We strongly reject a role for Pliocene/Pleistocene climatic fluctuations in species-level diversification of Brookesia. We also used simulations to test the spatial predictions of the watershed contraction model in a phylogenetic context, independent of its temporal component, and found no statistical support for this model. The riverine barrier model is likewise a qualitatively poor fit to our data, but some rela- tionships support a more ancient mountain refuge effect. We assessed support for the 3 hypotheses in a nonphylogenetic context by examining altitude and species richness and found a significant positive correlation between these variables. This is consistent with a mountain refuge effect but does not support the watershed contraction or riverine barrier models. Finally, we find repeated higher level east-west divergence patterns 1) between the 2 sister clades comprising the Brookesia minima group and 2) within the clade of larger leaf chameleons, which shows a basal divergence between western and eastern/northern sister clades. Our results highlight the central role of phylogeny in any meaningful tests of species-level diversification theories. [Biogeography; Chamaeleonidae; phylogeny; Pleistocene glaciation; relaxed clock; speciation; Squamata.] Once part of the southern supercontinent of Gond- Nussbaum et al. 1998; Vences and Glaw 2002, 2003; wana, Madagascar, is currently situated some 400 km Wood et al. 2007). In other groups, the major evolu- off the southeastern shore of Africa and is famous tionary splits consistently separate a clade occurring for a remarkable flora and fauna that are increasingly roughly in the northern fifth of Madagascar from a more threatened by loss of habitat and other human-induced southern clade, with examples found in chameleons, changes. Madagascar’s last subaerial connections to geckos, skinks, and mouse lemurs (Yoder and Heckman Africa and India date to approximately 160 and 90 mil- 2006; Boumans et al. 2007). As a general pattern, the lion years ago, respectively (Storey et al. 1995), although spatial distribution of species richness in some higher limited dispersal to and from other continents may have taxonomic groups may have been shaped by a latitudi- been possible over land bridges or small sea barriers in nal and altitudinal middomain effect (Lees et al. 1999). the Late Cretaceous or Paleocene (Briggs 2003; Noonan Nonetheless, even within the major bioclimatic regions, and Chippindale 2006; Van Bocxlaer et al. 2007; van species-level local endemism is high, and a major goal der Meijden et al. 2007). This long history of isolation of researchers has been to uncover the causes of this has contributed greatly to the remarkable degree of pattern (Goodman and Benstead 2003 and references floral and faunal endemism of Madagascar (Goodman therein; Vences et al. 2009). and Benstead 2003), which amounts to 100% in native amphibians and 92% in nonmarine nonavian reptiles (Glaw and Vences 2007). Potential Climatic and Geographic Barriers In terrestrial vertebrates, the majority of species diver- In their study of biogeographic patterns in the leaf sity corresponds to a limited number of endemic clades chameleons (genus Brookesia) of northern Madagascar, that colonized most of the available bioclimatic regions, Raxworthy and Nussbaum (1995) recognized 5 rainfor- including the eastern rainforests, central highlands, est regions delimited largely by altitudinal differences western dry deciduous forests, and southern arid spiny and intervening dry forests and characterized by a high forests. There are several sister-taxon pairs that follow degree of
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