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Toward a Tree-Of-Life for the Boas and Pythons: Multilocus Species-Level Phylogeny with Unprecedented Taxon Sampling ⇑ R

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Toward a Tree-Of-Life for the Boas and Pythons: Multilocus Species-Level Phylogeny with Unprecedented Taxon Sampling ⇑ R Molecular Phylogenetics and Evolution 71 (2014) 201–213 Contents lists available at ScienceDirect Molecular Phylogenetics and Evolution journal homepage: www.elsevier.com/locate/ympev Toward a Tree-of-Life for the boas and pythons: Multilocus species-level phylogeny with unprecedented taxon sampling ⇑ R. Graham Reynolds a, ,1, Matthew L. Niemiller b,2, Liam J. Revell a a Department of Biology, University of Massachusetts Boston, 100 Morrissey Blvd, Boston, MA 02125-3393, USA b Department of Ecology and Evolutionary Biology, Yale University, 21 Sachem St., New Haven, CT 06520, USA article info abstract Article history: Snakes in the families Boidae and Pythonidae constitute some of the most spectacular reptiles and com- Received 10 July 2013 prise an enormous diversity of morphology, behavior, and ecology. While many species of boas and Revised 10 November 2013 pythons are familiar, taxonomy and evolutionary relationships within these families remain contentious Accepted 20 November 2013 and fluid. A major effort in evolutionary and conservation biology is to assemble a comprehensive Tree- Available online 6 December 2013 of-Life, or a macro-scale phylogenetic hypothesis, for all known life on Earth. No previously published study has produced a species-level molecular phylogeny for more than 61% of boa species or 65% of Keywords: python species. Using both novel and previously published sequence data, we have produced a spe- Alethinophidia cies-level phylogeny for 84.5% of boid species and 82.5% of pythonid species, contextualized within a lar- Boidae Evolution ger phylogeny of henophidian snakes. We obtained new sequence data for three boid, one pythonid, and Phylogenetics two tropidophiid taxa which have never previously been included in a molecular study, in addition to Pythonidae generating novel sequences for seven genes across an additional 12 taxa. We compiled an 11-gene data- Snakes set for 127 taxa, consisting of the mitochondrial genes CYTB, 12S, and 16S, and the nuclear genes bdnf, bmp2, c-mos, gpr35, rag1, ntf3, odc, and slc30a1, totaling up to 7561 base pairs per taxon. We analyzed this dataset using both maximum likelihood and Bayesian inference and recovered a well-supported phylog- eny for these species. We found significant evidence of discordance between taxonomy and evolutionary relationships in the genera Tropidophis, Morelia, Liasis, and Leiopython, and we found support for elevating two previously suggested boid species. We suggest a revised taxonomy for the boas (13 genera, 58 spe- cies) and pythons (8 genera, 40 species), review relationships between our study and the many other molecular phylogenetic studies of henophidian snakes, and present a taxonomic database and alignment which may be easily used and built upon by other researchers. Ó 2013 Elsevier Inc. All rights reserved. 1. Introduction morphologies, behaviors, body sizes and ecologies. This group in- clude both the smallest (Tropidophis nigriventris, <250 mm total Alethinophidian squamates include most extant snakes (3030 length [TL]) and longest (Malayopython reticulatus, max. 10 m TL) of 3432 total sp.), though the majority of species (2838 sp.) are extant constricting snakes, as well as the largest snake to have ever included within the derived Caenophidia clade (i.e., Uetz and existed ( Titanoboa cerrejonensis, 13 m TL) [Head et al., 2009; Hošek, 2013). The earliest diverging lineages within the alethono- Uetz and Hošek, 2013]. They are also represented by enigmatic phidians are more frequently referred to as Henophidia (i.e., the and hyper-diverse families Tropidophiidae (the dwarf boas) and boas, pythons, and kin), or Alethinophidia sine Caenophidia (e.g., Uropeltidae (the shield-tailed snakes); as well as by the nearly-ex- Pyron et al., 2013a; Vidal et al., 2007). Henophidian snakes (includ- tinct insular Mascarene family Bolyeriidae. In particular, the boas ing the basal ‘‘Amerophidia;’’ Vidal et al., 2007) are one of the most (Boidae) and pythons (Pythonidae) represent highly diverse fami- spectacular groups of reptiles and constitute a vast diversity of lies with near-global tropical and subtropical distributions. Molec- ular phylogenetic and biogeographic studies of the boas and ⇑ Corresponding author. pythons have yielded important insights into evolutionary pro- E-mail addresses: [email protected] (R. Graham Reynolds), matthew. cesses (e.g., Colston et al., 2013; Noonan and Chippindale, [email protected] (M.L. Niemiller), [email protected] (L.J. Revell). 2006a,b; Noonan and Sites, 2010; Rawlings et al., 2008; Reynolds URL: http://www.rgrahamreynolds.info (R. Graham Reynolds). et al., 2013a), and an understanding of taxonomy, divergence, 1 Present address: Department of Organismic and Evolutionary Biology, Harvard and diversification is becoming especially relevant given that many University, 26 Oxford St., Cambridge, MA 02138, USA. 2 Present address: Department of Biology, University of Kentucky, 200 Thomas boa and python species are of significant conservation concern Hunt Morgan Building, Lexington, KY 40506, USA. (Bohm et al., 2013; IUCN, 2012). 1055-7903/$ - see front matter Ó 2013 Elsevier Inc. All rights reserved. http://dx.doi.org/10.1016/j.ympev.2013.11.011 202 R. Graham Reynolds et al. / Molecular Phylogenetics and Evolution 71 (2014) 201–213 A number of studies have investigated higher-level relation- There have been fewer molecular phylogenetic studies among ships among the henophidian snakes, largely recovering concor- the pythons, though several genera are well-characterized. Keogh dant topologies among families and subfamilies (Gower et al., et al. (2008) examined relationships among the Southeast Asian 2005; Heise et al., 1995; Lawson et al., 2004; Pyron and Burbrink, blood pythons (Python curtus, P. brongersmai, P. breitensteini), find- 2012; Pyron et al., 2013a,b; Slowinski and Lawson, 2002; Vidal ing support for the specific distinction of these lineages. Rawlings and Hedges, 2002, 2004; Vidal et al., 2007, 2009; Wiens et al., et al. (2004) examined molecular divergence in the mitochondrial 2008, 2012). However, the placement of some families, such as control region among the Liasis pythons of the Lesser Sundan archi- Bolyeriidae and Calabariidae, remains contentious (Greene, 1997; pelago, Australia, and New Guinea, finding support for the eleva- Lawson et al., 2004, 2005; Lynch and Wagner, 2009; Noonan and tion of three species (L. fuscus, L. mackloti, and L. olivaceus) and a Chippindale, 2006b; Vidal and Hedges, 2002, 2004; Wiens et al., sister relationship to Apodora (but see Rawlings et al., 2008; this 2008; Zaher, 1994; but see Pyron and Burbrink, 2012; Pyron study). Using partial coding sequence (cds) from the mitochondrial et al., 2013a). A recent study (Pyron et al., 2013b), produced the cytochrome B (CYTB) gene paired with morphological data, Harvey most comprehensive species-level phylogeny for the squamate et al. (2000) resolved a phylogeny for the scrub pythons (Morelia reptiles heretofore published. This project included the henophi- amethistina complex) of eastern Indonesia, PNG, and Australia, dian snakes, though these authors only achieved 56% and 65% spe- recognizing five species (M. amethistina, M. clastolepis, M. kinghorni, cies sampling for the boas and pythons, respectively, with M. nauta, and M. tracyae). Though only two species were included significant missing data (Pyron et al., 2013b). in the molecular dataset, Schleip (2008) identified at least six Other studies have attempted to infer interspecific relationships new species within the white-lipped python complex (Leiopython specifically within the boas and the pythons. For the Boidae, initial albertisii) using a combined molecular and morphometric molecular phylogenies used a single mitochondrial (mtDNA) mar- approach. ker (CYTB) and excellent taxon representation to infer relationships Finally, a number of explicitly intraspecific molecular (single lo- among extant boids (Burbrink, 2004; Campbell, 1997). For Python- cus and multilocus) studies of the boas (Hynková et al., 2009; idae, mtDNA studies built upon the morphological phylogeny in- McCartney-Melstad et al., 2012; Puente-Rolón et al., 2013; Rey- ferred by Kluge (1993) and assisted greatly in clarifying nolds et al., 2011, 2013b; Rodríguez-Robles et al., 2001; Tzika relationships and taxonomy among these species, though often et al., 2008; Wood et al., 2008) and pythons (Auliya et al., 2002; with limited taxon sampling (e.g., Rawlings et al., 2008). Multilocus Austin et al., 2010; Carmichael, 2007; Rawlings and Donnellan, approaches to higher level relationships among boas and pythons 2003) have been conducted, with some discovery of cryptic spe- have generally included limited taxon sampling (e.g., Lee, 2005; cies. North American rubber boas (Charina) were found to comprise Noonan and Chippindale, 2006a; Noonan and Sites, 2010; Pyron two species (Rodríguez-Robles et al., 2001). Hynková et al. (2009) and Burbrink, 2012; Pyron et al., 2013a; Vidal and Hedges, 2004; suggested that Central American Boa constrictor might constitute Vidal et al., 2007), though Lynch and Wagner (2009) provided a ro- a separate species (B. imperator), a finding that is supported bust phylogenetic hypothesis for 39 boid taxa (33 species and 6 (though not explicitly tested) by the CYTB gene tree in Reynolds subspecies), representing 61% of boid species. While most rela- et al. (2013a). This taxonomic arrangement has not been widely ac- tionships have remained remarkably stable even with increased cepted
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