Testing for Convergent Evolution in Semi-Aquatic Anolis Lizards
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Testing for Convergent Evolution in Semi-aquatic Anolis Lizards by Christopher Kevin Boccia A thesis submitted in conformity with the requirements for the degree of Master of Science Department of Ecology and Evolutionary Biology University of Toronto © Copyright by Christopher Kevin Boccia 2018 ii Testing for Convergent Evolution in Semi-aquatic Anolis Lizards Christopher Kevin Boccia Master of Science Department of Ecology and Evolutionary Biology University of Toronto 2018 Abstract Twelve species from six different clades of Anolis lizard exhibit a semi-aquatic lifestyle. These unusual species are found only along neotropical streams, and are known to swim, capture aquatic prey, and dive to escape predators. Based on ecomorphology theory, and anoles’ famed predisposition for convergence, we would predict that these anole lineages should have undergone convergent evolution. However, previous morphometric research suggested that semi- aquatic anoles are not convergent. This thesis reinvestigates whether semi-aquatic anoles have convergently evolved using novel morphometric and experimental approaches. I assessed the morphology, swimming speed, and diving performance of semi-aquatic and non-aquatic anole species from throughout the neotropics. My results suggest that semi-aquatic anoles have converged upon similar morphologies, superior swimming performance, and a previously undiscovered potential adaptation for diving: underwater rebreathing. Semi-aquatic anoles show evidence of repeated multidimensional convergence, and, somewhat uniquely for Anolis, provide strong evidence for convergence between mainland and island forms. iii Acknowledgments I first became interested in semi-aquatic Anolis lizards while travelling through Panama and Costa Rica in the summer of 2015. No formal field guide exists for the reptiles and amphibians of Panama, so I constructed my own using checklists and online databases of herpetological images. Among the many anole species I researched, the ripple-patterned ‘semi-aquatics’ were particularly fascinating. I managed to find two of these species during my trip. The first sighting was spectacularly bizarre—while hiking through the mountains in Parque Nacional Omar Torrijos, I spotted an A. lionotus (highly stream associated) sitting in the middle of a heavily rutted dirt track, with no waterway in sight. Due in part to this curious observation, semi-aquatic anoles were first in line when I was deciding on an Anolis lizard-focused thesis. A project of this scope and complexity would not have been possible without the assistance of a small army of friends and lab-mates: Claire Manglicmot, Shree Senthivasan, Michael Foisy, James Boyko, Ken Toyama, Viviana Astudillo-Clavijo, Patrick Moldowan, Hollis Dahn, Sean Anderson, Meredith Swartwout, Alan Ward, Phil Honlë, Bryan Ospina, Elodie Morneau, Margarita Cantero Guerrero, field assistants: James Boccia, Isabela Borges, Camilo Estupiñan, Sebastian Ovalle, lab volunteers: Erica Fellin, Cole Brookson, Sophia Samuelsson, Perlina Lim, collaborators: Rosario Castañeda, Andrés García Aguayo, Ramón Martínez, museum loan coordinators: Amy Lathrop, Neftali Camacho, José Rosado, Jonathan Losos, and research station and permit staff: Organization for Tropical Studies, Bernal Matarrita Carranza, Minor Porras, Rebecca Cole. Special thanks to Luke Mahler for his endless hours of assistance with all aspects of the project, to Rosario Castañeda, Camilo Estupiñan, Sebastian Ovalle, Margarita Cantero Guerrero, and Ramón Martínez for helping me visit amazing sites in Colombia and Mexico, and to Shree Senthivasan, James Boccia, Ken Toyama, and Isabela Borges, who endured close encounters with lightning strikes, rat and ant invasions, and bites from all manner of tropical insects to help me complete all of my fieldwork. My research was supported by a National Geographic Young Explorer Grant, a Sigma Xi Grant- in-Aid of Research, and a Canada Graduate Scholarship-Master’s Program from the Natural Sciences and Engineering Research Council of Canada iv I obtained research permits to work with Costa Rican species from MINAE, the Costa Rican environmental agency (permit #: SINAC-SE-102-2017). All experimental methods were approved by the University of Toronto Local Animal Care Committee (LACC; protocol #: 20011469). v Table of Contents Acknowledgments.......................................................................................................................... iii Table of Contents .............................................................................................................................v List of Tables ............................................................................................................................... viii List of Figures ................................................................................................................................ ix List of Appendices ........................................................................................................................ xii 1 Morphological convergence in semi-aquatic anoles ....................................................................1 1.1 Introduction ..........................................................................................................................1 1.1.1 Convergent evolution ...............................................................................................1 1.1.2 Convergence in Anolis lizards .................................................................................1 1.1.3 Island/mainland disparity in convergence in anoles ................................................2 1.1.4 The expectation of convergence among semi-aquatic anoles ..................................3 1.1.5 Hypotheses and predictions .....................................................................................6 1.2 Methods................................................................................................................................6 1.2.1 Preamble ..................................................................................................................6 1.2.2 Linear morphometric data collection .......................................................................7 1.2.3 Phylogenetic principal component analysis of linear morphometric data .............10 1.2.4 Analysis of putative convergence in semi-aquatic anoles using linear discriminant analysis, nearest neighbour distances, and simulation ......................10 1.2.5 Testing for convergence using the “convevol” R package ....................................11 1.3 Linear morphometry results ...............................................................................................12 1.3.1 Male phylogenetic morphospace ...........................................................................12 1.3.2 Female phylogenetic morphospace ........................................................................19 1.3.3 “convevol” metric results .......................................................................................26 1.4 Discussion ..........................................................................................................................28 1.4.1 Evidence for convergence in semi-aquatic anoles .................................................28 vi 1.4.2 Conclusions and future directions ..........................................................................31 2 Aquatic performance of semi-aquatic anoles .............................................................................33 2.1 Introduction ........................................................................................................................33 2.1.1 Background ............................................................................................................33 2.1.2 Linking ecology, morphology, and performance in anoles ...................................34 2.1.3 Performance demands of semi-aquatic habitats .....................................................35 2.1.4 Hypotheses and predictions ...................................................................................35 2.2 Methods..............................................................................................................................36 2.2.1 Field work and lizard capture ................................................................................36 2.2.2 Swimming speed experiments ...............................................................................38 2.2.3 Quantification of swimming speed ........................................................................42 2.2.4 Analysis of aquatic and non-aquatic anole swimming speeds ...............................43 2.2.5 Observation and analysis of voluntary diving .......................................................45 2.3 Results ................................................................................................................................45 2.3.1 Swimming speed analysis ......................................................................................45 2.3.2 Voluntary diving results .........................................................................................49 2.4 Discussion ..........................................................................................................................53 2.4.1 Convergence in swimming and diving performance in aquatic anoles .................53 2.4.2 Conclusions and future directions ..........................................................................54