Spiny Tails and Clades: A Fully Sampled Phylogeny of Hoplocercine Lizards (Iguanidae/ Hoplocercinae) and its Taxonomic and Nomenclatural Implications

Hoplocercine lizards (Enyalioides, Morunasaurus, and Hoplocercus) form a clade of ca. 20 currently recognized species. The phylogenetic relationships among hoplocercine lizards, whose members exhibit striking differences in morphology (e.g., spiny vs. non-spiny tails), have not been clearly resolved by previous molecular phylogenetic studies. We generated a considerably larger dataset including 130 new DNA sequences from one mitochondrial and four nuclear loci for all named and two unnamed species of Hoplocercinae. We analyzed the data under concatenated maximum likelihood (RAxML) and Bayesian (MrBayes) as well as summary coalescent (ASTRAL) approaches. While our phylogenetic hypotheses strongly supported the monophyly of Hoplocercinae, neither Enyalioides nor Morunasaurus was supported as monophyletic. Instead, M. groi was inferred with strong support to form a clade with E. heterolepis and E. laticeps. This clade was in turn the sister taxon to other species of Morunasaurus (M. annularis, M. peruvianus). The remaining species of Enyalioides formed a separate clade with a basal split between western (3 species) and eastern (13 species) subclades. Tree topology tests rejected the monophyly of Enyalioides but failed to reject monophyly of Morunasaurus, suggesting that further study is needed to resolve its taxonomic status. Based on our results, we establish the converted clade names Hoplocercinae, Hoplocercus, Enyalioides, and Morunasaurus, as well as the new clade name Zimiamviasaurus.  

[1]  M. Sabaj.  Codes for Natural History Collections in Ichthyology and Herpetology , 2020, Copeia.

[2]  K. Queiroz**,et al.  International Code of Phylogenetic Nomenclature (PhyloCode) , 2020 .

[3]  P. Cantino,et al.  Iguanidae T. Bell 1825 [O. Torres-Carvajal, K. de Queiroz and J. A. Schulte II], converted clade name , 2020 .

[4]  Johannes Müller,et al.  Convergent evolution of tail spines in squamate reptiles driven by microhabitat use , 2020, Biology Letters.

[5]  Maryam Rabiee,et al.  Multi-allele species reconstruction using ASTRAL , 2018, bioRxiv.

[6]  Lindsay E. Zanno,et al.  The evolution of tail weaponization in amniotes , 2018, Proceedings of the Royal Society B: Biological Sciences.

[7]  V. Reynoso,et al.  Never judge an iguana by its spines: Systematics of the Yucatan spiny tailed iguana, Ctenosaura defensor (Cope, 1866). , 2017, Molecular phylogenetics and evolution.

[8]  Robert Lanfear,et al.  PartitionFinder 2: New Methods for Selecting Partitioned Models of Evolution for Molecular and Morphological Phylogenetic Analyses. , 2016, Molecular biology and evolution.

[9]  Siavash Mirarab,et al.  Fast Coalescent-Based Computation of Local Branch Support from Quartet Frequencies , 2016, Molecular biology and evolution.

[10]  M. Ribeiro‐Júnior.  Catalogue of distribution of lizards (Reptilia: Squamata) from the Brazilian Amazonia. I. Dactyloidae, Hoplocercidae, Iguanidae, Leiosauridae, Polychrotidae, Tropiduridae. , 2015, Zootaxa.

[11]  K. de Queiroz,et al.  Three new species of woodlizards (Hoplocercinae, Enyalioides) from northwestern South America , 2015, ZooKeys.

[12]  Tandy J. Warnow,et al.  ASTRAL: genome-scale coalescent-based species tree estimation , 2014, Bioinform..

[13]  Alexandros Stamatakis,et al.  RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies , 2014, Bioinform..

[14]  K. de Queiroz,et al.  Phylogenetic relationships within the lizard clade Xantusiidae: using trees and divergence times to address evolutionary questions at multiple levels. , 2013, Molecular phylogenetics and evolution.

[15]  Reptiles , 2013, Current Biology.

[16]  K. de Queiroz,et al.  Two sympatric new species of woodlizards (Hoplocercinae, Enyalioides) from Cordillera Azul National Park in northeastern Peru , 2013, ZooKeys.

[17]  R. Lanfear,et al.  Partitionfinder: combined selection of partitioning schemes and substitution models for phylogenetic analyses. , 2012, Molecular biology and evolution.

[18]  Maxim Teslenko,et al.  MrBayes 3.2: Efficient Bayesian Phylogenetic Inference and Model Choice Across a Large Model Space , 2012, Systematic biology.

[19]  K. Queiroz**,et al.  A systematic revision of Neotropical lizards in the clade Hoplocercinae (Squamata: Iguania) , 2011 .

[20]  Mark A. Miller,et al.  Creating the CIPRES Science Gateway for inference of large phylogenetic trees , 2010, 2010 Gateway Computing Environments Workshop (GCE).

[21]  O. Gascuel,et al.  New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. , 2010, Systematic biology.

[22]  G. Boulenger.  Description of a new Species of Enyalius in the Brussels Museum. , 2009 .

[23]  J. Rougemont,et al.  A rapid bootstrap algorithm for the RAxML Web servers. , 2008, Systematic biology.

[24]  S. Kelley,et al.  Rapid development of multiple nuclear loci for phylogenetic analysis using genomic resources: an example from squamate reptiles. , 2008, Molecular phylogenetics and evolution.

[25]  B. Noonan,et al.  Dispersal and vicariance: the complex evolutionary history of boid snakes. , 2006, Molecular phylogenetics and evolution.

[26]  Robert C. Edgar,et al.  MUSCLE: multiple sequence alignment with high accuracy and high throughput. , 2004, Nucleic acids research.

[27]  J. Wiens,et al.  PHYLOGENETIC RELATIONSHIPS OF HOPLOCERCID LIZARDS: CODING AND COMBINING MERISTIC, MORPHOMETRIC, AND POLYMORPHIC DATA USING STEP MATRICES , 2003 .

[28]  J. Schulte,et al.  PHYLOGENETIC RELATIONSHIPS WITHIN IGUANIDAE INFERRED USING MOLECULAR AND MORPHOLOGICAL DATA AND A PHYLOGENETIC TAXONOMY OF IGUANIAN LIZARDS , 2003 .

[29]  Hidetoshi Shimodaira.  An approximately unbiased test of phylogenetic tree selection. , 2002, Systematic biology.

[30]  D. Janies,et al.  Total Evidence, Sequence Alignment, Evolution of Polychrotid Lizards, and a Reclassification of the Iguania (Squamata: Iguania) , 2001 .

[31]  Hidetoshi Shimodaira,et al.  Multiple Comparisons of Log-Likelihoods with Applications to Phylogenetic Inference , 1999, Molecular Biology and Evolution.

[32]  J. Macey,et al.  Molecular tests of phylogenetic taxonomies: a general procedure and example using four subfamilies of the lizard family Iguanidae. , 1998, Molecular phylogenetics and evolution.

[33]  J. Macey,et al.  Evolutionary Shifts in Three Major Structural Features of the Mitochondrial Genome Among Iguanian Lizards , 1997, Journal of Molecular Evolution.

[34]  V. Alifanov.  Lizard families Priscagamidae and Hoplocercidae (Sauria, Iguania): Phylogenetic position and new representatives from the Late Cretaceous of Mongolia , 1996 .

[35]  M. Nishida,et al.  Sequence evolution of mitochondrial tRNA genes and deep-branch animal phylogenetics , 1993, Journal of Molecular Evolution.

[36]  D. Frost,et al.  A Phylogenetic analysis and taxonomy of iguanian lizards (Reptilia, Squamata) / , 1989 .

[37]  Ronald Wilbur Brown,et al.  Composition of Scientific Words: A manual of methods and a lexicon of materials for the practice of logotechnics , 1978 .

[38]  G. Z. Wurst,et al.  The Occurrence of Parietal Eyes in Recent Lacertilia (Reptilia) , 1976 .

[39]  R. Estes,et al.  Iguanid Lizard from the Upper Cretaceous of Brazil , 1973, Science.

[40]  Richard E. Jones,et al.  A Survey of the Chronology of Ovulation in Anoline Lizard Genera , 1972 .

[41]  C. Burt,et al.  A preliminary check list of the lizards of South America , 1933 .

[42]  F. A. BATHER,et al.  International Code of Zoological Nomenclature , 1926, Nature.

[43]  Juan D. VÁSQUEZ-RESTREPO.  35 years behind the scenes: range extension of the rare Gro’s manticore, Morunasaurus groi (Squamata, Hoplocercidae), in Colombia , 2021 .

[44]  Omar Torres‐Carvajal,et al.  A new species of wood lizard (Hoplocercinae, Enyalioides) from the Río Huallaga Basin in Central Peru , 2021, Evolutionary Systematics.

[45]  D. Maddison,et al.  Mesquite: a modular system for evolutionary analysis. Version 2.6 , 2009 .

[46]  K. de Queiroz,et al.  Phylogeny of hoplocercine lizards (Squamata: Iguania) with estimates of relative divergence times. , 2009, Molecular phylogenetics and evolution.

[47]  K. de Queiroz,et al.  Species concepts and species delimitation. , 2007, Systematic biology.

[48]  M. P. Cummings,et al.  PAUP* Phylogenetic analysis using parsimony (*and other methods) Version 4 , 2000 .

[49]  S. Arabia,et al.  LIZARD ANTIPREDATORY BEHAVIORS PREVENTING EXTRACTION FROM CREVICES , 2000 .

[50]  K. Queiroz**,et al.  The General Lineage Concept of Species, Species Criteria, and the Process of Speciation , 1998 .

[51]  T. Papenfuss,et al.  Two novel gene orders and the role of light-strand replication in rearrangement of the vertebrate mitochondrial genome. , 1997, Molecular biology and evolution.

[52]  T. Ávila-Pires.  Lizards of Brazilian Amazonia (Reptilia:Squamata) , 1995 .

[53]  K. Queiroz**,et al.  A phylogeny of iguanidae , 1988 .

[54]  Teresa C. S. Avila-Pires,et al.  Répteis Squamata de Rondônia e Mato Grosso coletados através do programa Polonoroeste. , 1988 .

[55]  J. A. Peters,et al.  Catalogue of the neotropical Squamata: Part 2. Lizards and Amphisbaenians. , 1970 .

[56]  R. Etheridge.  A review of the Iguanid lizard genus Enyalius , 1969 .

[57]  G. Boulenger.  Description of a new Species of Lizard of the Genus Enyalius , 1883 .

[58]  Johann Georg Wagler,et al.  Natürliches System der Amphibien mit vorangehender Classification der Säugethiere und Vögel : ein Beitrag zur vergleichenden Zoologie / , 1830 .