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Lizards As Model Organisms for Linking Phylogeographic and Speciation Studies

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Lizards As Model Organisms for Linking Phylogeographic and Speciation Studies Molecular Ecology (2010) 19, 3250–3270 doi: 10.1111/j.1365-294X.2010.04722.x INVITED REVIEW Lizards as model organisms for linking phylogeographic and speciation studies ARLEY CAMARGO,* BARRY SINERVO† and JACK W. SITES JR.* *Department of Biology and Bean Life Science Museum, Brigham Young University, Provo, UT 84602, USA, †Department of Ecology and Evolutionary Biology, University of California, Santa Cruz, CA 95064, USA Abstract Lizards have been model organisms for ecological and evolutionary studies from individual to community levels at multiple spatial and temporal scales. Here we highlight lizards as models for phylogeographic studies, review the published popula- tion genetics ⁄ phylogeography literature to summarize general patterns and trends and describe some studies that have contributed to conceptual advances. Our review includes 426 references and 452 case studies: this literature reflects a general trend of exponential growth associated with the theoretical and empirical expansions of the discipline. We describe recent lizard studies that have contributed to advances in understanding of several aspects of phylogeography, emphasize some linkages between phylogeography and speciation and suggest ways to expand phylogeographic studies to test alternative pattern-based modes of speciation. Allopatric speciation patterns can be tested by phylogeographic approaches if these are designed to discriminate among four alterna- tives based on the role of selection in driving divergence between populations, including: (i) passive divergence by genetic drift; (ii) adaptive divergence by natural selection (niche conservatism or ecological speciation); and (iii) socially-mediated speciation. Here we propose an expanded approach to compare patterns of variation in phylogeographic data sets that, when coupled with morphological and environmental data, can be used to discriminate among these alternative speciation patterns. [Correction made after online publication (28/07/2010): (minor deletion in the last line of the abstract)]. Keywords: adaptation, divergence, lizards, molecular markers, phylogeography, speciation Received 20 June 2009; revision accepted 10 May 2010 as families (Pough et al. 2004). Figure 1 depicts a phy- Introduction logenetic hypothesis from Townsend et al. (2004) that ‘Lizards’ are a paraphyletic group of non-avian reptiles summarizes relationships and distributions in these that, together with the odd ‘worm lizards’ (Amphisbae- major groups and while this arrangement has been nia) and the snakes (Serpentes), comprise the clade challenged (Lee et al. 2004; Vidal & Hedges 2005; Con- Squamata (Lee et al. 2004; Pough et al. 2004). The well- rad 2008), we present the hypothesis merely to acquaint supported clades Amphisbaenia and Serpentes are readers with some aspects of the evolutionary history of unambiguously nested within the Squamata but for the group. Lizards are widely distributed geographi- simplicity we refer to lizards as all squamates that do cally, occupy a wide range of habitats and are charac- not belong to these other clades. This group includes at terized by a striking range of morphologies, ecologies least 5354 species (The Reptile Database: http:// and body sizes (Pianka & Vitt 2003; Vitt & Caldwell www.reptile-database.org/ accessed on 15 February 2009). As a group, lizards show about 150 independent 2010) in about 25–26 crown clades usually recognized origins of lateral toe fringes (for sand running; Luke 1986), about 100 independent origins of viviparity (liz- Correspondence: Arley Camargo, Fax: +1 801 422 0090; ards + snakes; Blackburn 2006), multiple transitions to a E-mail: [email protected] snakelike body form with limb reduction (Greer 1991; Ó 2010 Blackwell Publishing Ltd LIZARD PHYLOGEOGRAPHY AND SPECIATION 3251 Chamaeleonidae (OW) Fig. 1 Schematic phylogeny of squa- ‘Agamidae’ (OW) mate reptiles showing relationships of IGUANIA major lizard clades with non-lizard taxa Hoplocercidae (NW-SA) (Amphisbaenia and Serpentes), modi- Polychrus (‘Polychrotidae’) fied from Townsend et al. (2004). The Crotaphytidae (NW-NA) geographic distributions of lizard lin- Iguanidae (NW+WP) eages are identified as follows: NW: Corytophanidae (NW-NA) New World; NA: North America; SA: Opluridae (MA) South America; CA: Central America; ‘Polychrotidae’ (NW) WP: West Pacific; MA: Madagascar; Tropidurinae OW: Old World; COSM: Cosmopolitan; Tropiduridae AS: Asia; EUAS: Eurasia; AF: Africa. Liolaeminae (NW-SA) The relationships within the clade Igua- Leiocephalinae nia were taken from Schulte et al. Anolis (‘Polychrotidae’) (2003). Phrynosomatidae (NW-NA) Anguidae (COSM) Helodermatidae (NW-NA) Xenosauridae (NW-CA) Varanidae (OW) Shinisauridae (OW-AS) Serpentes (COSM) Lacertidae (OW-EUAS) Amphisbaenia Teiidae (NW) Gymnophthalmidae (NW-SA) Cordylidae (OW-AF) Xantusiidae (NW-NA) Scincidae (COSM) Gekkonidae (COSM) Dibamidae (NA+AS) Wiens et al. 2006; Brandley et al. 2008) and multiple studies capable of discriminating among alternative origins of obligate parthenogenesis (Kearney et al. speciation patterns. Such questions can be framed in 2009). several alternative speciation contexts and we suggest Numerous symposia (Milstead 1967; Huey et al. 1983; that multi-disciplinary studies can highlight linkages of Vitt & Pianka 1994; Fox et al. 2003; Reilly et al. 2007) phylogeographic patterns to divergence processes and and texts (Roughgarden 1995; Pianka & Vitt 2003; Losos integrate some aspects of both phylogeographic 2009) have focused on lizards as model organisms, and pattern-based speciation studies to allow deeper because they share attributes relevant to the study of and more synthetic levels of inquiry. many biological processes and they are often abundant and easy to manipulate. In this review, we: (i) summa- Lizards as models for evolutionary studies rize some important aspects of lizard diversity and evo- lution; (ii) describe some advantages lizards offer as Lizards have become model organisms for evolutionary models for phylogeographic studies; (iii) identify some studies due to the accumulated knowledge of long-term emerging themes and review available lizard phylogeo- demographics, life history strategies and adaptive eco- graphic studies to summarize trends and patterns; (iv) morphology and ecophysiology, which together provide describe case studies which have yielded important an ideal framework for phylogeographic and speciation insights into broader aspects of phylogeography; (v) studies. Lizards are easy to find, approach and capture emphasize some explicit linkages between phylogeogra- in the field for mark–release–recapture methods. They phy and patterns of speciation and alternative specia- tolerate experimental manipulation, such as in vivo abla- tion models; and (vi) synthesize the current state of tion of egg yolk mass (Sinervo & Huey 1990), alteration knowledge and suggest ways to capitalize on attributes of body mass (Olsson et al. 2009) and removal of of lizards to improve resolution of phylogeographic energy reserves by caudal autotomy (Naya et al. 2007). Ó 2010 Blackwell Publishing Ltd 3252 A. CAMARGO, B. SINERVO and J. W. SITES JR. Long-term demographic studies of several species Edwards 2009; Knowles 2009; Nielsen & Beaumont (Bull 2000; Sinervo & McAdam 2008; Vercken et al. 2009). The availability of nuclear genetic markers, 2008) have provided deep pedigrees leading to novel advances in coalescent theory and new GIS tools for insights into microevolutionary processes (Sinervo et al. generating ecological niche and paleoclimate models, are 2007, 2008), patterns of heritable variation and covaria- rapidly increasing the scope of phylogeographic studies tion (see Pemberton 2008, for general issues) and pat- (Swenson 2008; Buckley 2009; Hickerson et al. 2010; Si- terns of natural selection (Sinervo & McAdam 2008). As nervo et al. 2010). For example, some studies incorporate an example, Uta stansburiana has one of the deepest ver- external climatic and geologic data to generate a priori tebrate pedigrees in existence that covers both sexes; predictions that can then be tested with molecular the pedigree for long-term demographic studies at Los phylogographic approaches (e.g. Richards et al. 2007; Ban˜os, California, currently spans 21 generations and Knowles et al. 2007; Knowles & Carstens 2007a; 7464 individuals (1988–2008; 400 years in the human Moriarty-Lemmon et al. 2007; Carnaval & Moritz 2008; sense of time; Sinervo & McAdam 2008). Werneck et al. in review), but statistical methods can Some of the earliests tests of the theory of density- also estimate phylogeographic history without a priori dependent natural selection, based on r- vs. K-selected hypotheses (Templeton 2004, 2010a,b; Lemmon & life history strategies (MacArthur & Wilson 1967; Pianka Moriarty-Lemmon 2008). The application of multi-locus 1970), were carried out on lizards (Tinkle et al. 1970; coalescence methods to link phylogeography to species Pianka & Parker 1975). Thermal biology and biophysical delimitation issues is growing rapidly (Carstens & ecology models in lizards that emerged from early phys- Knowles 2007; Liu & Pearl 2007; Brumfield et al. 2008; iological studies (Huey 1982; Tracy 1982; Porter et al. Liu et al. 2008; Degnan & Rosenberg 2009; Yang & 2000) are now being applied to estimate geographic dis- Rannala 2010), as are multi-species assessments of the tributions based on thermal requirements and climate role of gene flow vs. natural selection across environ- (Kearney & Porter 2004, 2009; Buckley
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