ECOLOGY, THE AMAZON BARRIER, AND SPECIATION IN WESTERN ATLANTIC Halichoeres (LABRIDAE) By LUIZ A. ROCHA A DISSERTATION PRESENTED TO THE GRADUATE SCHOOL OF THE UNIVERSITY OF FLORIDA IN PARTIAL FULFILLMENT OF THE REQUIREMENTS FOR THE DEGREE OF DOCTOR OF PHILOSOPHY UNIVERSITY OF FLORIDA 2003 Copyright 2003 by Luiz A. Rocha To my wife, Claudia, for her unconditional support and patience. ACKNOWLEDGMENTS I would like to thank Brian Bowen for introducing me to the study of phylogeography, for letting me work in his lab, and for sharing his extensive knowledge and excitement with me. After Brian left to work on other seas, Debra Murie and Gustav Paulay kindly accepted me as their student. I extend special thanks to Debra Murie, who has been very supportive and ensured that the genetics lab was an excellent place to work. Gustav Paulay provided me with constructive criticism, professional guidance and friendship. I would like to thank the members of my committee (Carter Gilbert, Stephen Karl, William Smith-Vaniz, and Colette St. Mary), all of whom contributed to the success of my research. Carter Gilbert’s deep knowledge of ichthyology has been a constant inspiration. Stephen Karl was always interested in my work, has supported me from the beginning, and financed two trips to the Bahamas. William Smith-Vaniz gave me full access to his extensive library, and financed a trip to St. Croix, USVI. Colette St. Mary always lent a hand when I needed it; and thoughtfully helped me clarify many portions of my research. I thank D. Ross Robertson (the best fish collector I’ve ever met) for participating in most of the field trips, and critically reading most of my work. Anna Bass, Howard Choat, Bruce Collette, Marcia Coura, Bertran Feitoza, Carlos Ferreira, Sergio Floeter, Joao Luiz Gasparini, Zandy Hillis-Star, Daryl Parkyn, Brenda-Lee Philips, Jo Pitt, Claudia Rocha, Ierece Rosa, Ricardo Rosa, David Snyder, Su Sponaugle, Benjamin Victor and Doug Weaver obtained samples and helped in laboratory and field work. IV Gerald Allen, Bertran Feitoza and Paul Humann allowed me to use their excellent underwater photographs. Discussions with Sergio Floeter, Craig Moritz, Ivan Sazima, Geerat Vermeij and Mark Westneat greatly improved this work. Logistical support and/or collecting permits were provided by the Bermuda Biological Station for Research; the Bermuda Fisheries Department; the National Park Service at St. Croix; the Smithsonian Research Laboratory at Carrie Bow Cay, Belize; and the Brazilian Navy Station at St. Paul’s Rocks. Financial support for laboratory and field work was provided by the National Science Foundation (through a grant to Brian Bowen); the Smithsonian Tropical Research Institute; and PADI (Professional Association of Diving Instructors), Project Aware. A doctorate scholarship was provided by CAPES (Fundacao Coordenacao de Aperfeicoamento de Pessoal de Nivel Superior), Brazilian Ministry of Education. v 1 TABLE OF CONTENTS Page ACKNOWLEDGMENTS iv LIST OF TABLES viii LIST OF FIGURES ix ABSTRACT x CHAPTER 1 INTRODUCTION AND BACKGROUND 1 Wrasses of the Genus Halichoeres in the Atlantic 2 This Study 3 2 PATTERNS OF DISTRIBUTION AND PROCESSES OF SPECIATION IN BRAZILIAN REEF FISHES 5 Introduction 5 Methods 6 Discussion 8 Endemism in Brazilian Coastal Reefs: the Numbers 8 The Amazon Barrier 9 Speciation and the Amazon Barrier 1 The Caribbean region: A center of origin or accumulation? 15 Speciation in the Western Atlantic: Dispersal or Vicariance? 16 Environmental Differences Driving Species Distributions and Speciation on Brazilian Oceanic Islands 18 The Southern Oceanic Islands 21 Disjunct Distributions 22 Conclusions 24 3 ECOLOGICAL SPECIATION IN A CLOSELY RELATED REEF FISH SPECIES PAIR (.Halichoeres : LABRIDAE) 26 Introduction 26 Materials and Methods 27 Results 30 Discussion 33 vi 4 5 CRYPTIC SPECIATION DRIVEN BY ENVIRONMENTAL CONDITIONS IN Halichoeres bivittatus (LABRIDAE) 38 Introduction 38 Methods and Materials 40 Results 40 Discussion 42 COLOR PATTERN VARIATION, AND THE PHYLOGEOGRAPHY OF FOUR SPECIES OF Halichoeres (LABRIDAE) IN THE WESTERN ATLANTIC 46 Introduction 46 Methods and Materials 49 Results 49 Halichoeres cyanocephalus 49 Halichoeres garnoti 50 Halichoeres maculipinna 52 Halichoeres poeyi 54 Discussion 56 Halichoeres cyanocephalus 56 Halichoeres garnoti 56 Halichoeres maculipinna 58 Halichoeres poeyi 59 Conclusion 60 6 GENERAL CONCLUSIONS 61 Reconciling Local Adaptation with the Pelagic Larval Stage 62 Conclusions 63 LIST OF REFERENCES 66 BIOGRAPHICAL SKETCH 77 1 3- LIST OF TABLES 4- Table page 4- 3-1. Sample size, number of haplotypes, haplotype diversity and nucleotide diversity of 5- the populations surveyed 31 2. Population pairwise Ost for Halichoeres brasiliensis and H. radiatus 3 1. Sample size, number of haplotypes, haplotype diversity and nucleotide diversity of the populations surveyed 41 2. Population pairwise Ost for Halichoeres bivittatus 42 1. Sample size, number of haplotypes, haplotype diversity and nucleotide diversity of the populations surveyed 51 5-2. Population pairwise Ost for Halichoeres garnoti 51 5-3. Population pairwise Ost for Halichoeres maculipinna 53 5-4. Population pairwise Ost for Halichoeres poeyi 55 viii LIST OF FIGURES Figure PaSe 2- 2-1. Tropical western Atlantic 7 3- 2-2. Schematic view of the Amazon sediment deposition and freshwater discharge, 3- during stands of high and low sea level 10 2-3.4- Contours of species diversity of the families Labridae, Pomacentridae and Scaridae western Atlantic 16 4- in the tropical 5- 4. Operation of the Amazon barrier 18 1. Tropical western Atlantic 29 3-2. Phylogenetic tree of Halichoeres radiatus and H. brasiliensis haplotypes 32 3. Halichoeres brasiliensis at the Brazilian coast and Halichoeres radiatus at Fernando de Noronha 35 rubble bottom off eastern Florida and at the Bahamas. 39 1 . Halichoeres bivittatus over 2. Phylogenetic tree of Halichoeres bivittatus haplotypes 43 1. Halichoeres cyanocephalus at northeastern Brazil and Dry Tortugas, Florida 47 5-2. Halichoeres garnoti at Bermuda and St. Lucia 48 5-3. Halichoeres maculipinna at northeastern Brazil and the Bahamas 48 5-4. Halichoeres poeyi in a turbid coralline algae reef off northeastern Brazil 48 5-5. Phylogenetic tree of Halichoeres cyanocephalus haplotypes 50 5-6. Phylogenetic tree of Halichoeres garnoti haplotypes 52 5-7. Phylogenetic tree of Halichoeres maculipinna haplotypes 54 poeyi haplotypes 55 5-8. Phylogenetic tree of all (3 1 ) Halichoeres IX Abstract of Dissertation Presented to the Graduate School of the University of Florida in Partial Fulfillment of the Requirements for the Degree of Doctor of Philosophy ECOLOGY, THE AMAZON BARRIER, AND SPECIATION IN WESTERN ATLANTIC Halichoeres (LABRIDAE) By Luiz A. Rocha August 2003 Chair: Debra Murie Major Department: Fisheries and Aquatic Sciences Recent estimates indicate that about 12% of the Brazilian reef fish species are endemic. Most ichthyologists agree that this endemism is generated by the barrier formed by the freshwater and sediment discharge of large rivers in northeastern South America (mainly the Amazon, Orinoco and their tributaries). However, little is known about the dynamics of this barrier. Recent studies have shown that the barrier can be crossed through deep sponge bottoms on the outer continental shelf off northeastern South America. Moreover, the recent discovery of species regarded as Brazilian endemics in the extreme southern Caribbean is showing that the Amazon barrier is weaker than previously thought. Two hypotheses were generated to explain the effects of the Amazon barrier on western Atlantic reef fish: • The Amazon is a strong barrier to dispersal; but sea-level fluctuations influence the effectiveness of the barrier; and may greatly affect fish species diversity in the western tropical Atlantic. x • Larval exchange between Brazil and the Caribbean is small but constant; contrasting selection pressures in divergent environments (continental Brazil versus insular Caribbean) may be the central force driving speciation. To test these hypotheses, a total of 632 samples of seven species of Halichoeres were obtained from 13 locations across the western Atlantic. Although congruent population structure was expected in these species because of their similar dispersal potential and exposure to the Amazon barrier, varying degrees of genetic separation were observed. The observed distribution of genetic partitions indicates that gene flow exists between environmentally similar, but geographically distant locations. Deep genetic divergences coincided with environmental differences between locations, regardless of distance or dispersal barriers. The pattern drawn from our study indicates that divergent environmental conditions can be as important as (or sometimes more important than) vast distances of unsuitable habitat (either open ocean waters or the area influenced by the Amazon) in producing genetic partitions; and that benthic-stage habitat preferences may be strongly influencing the biogeography of western Atlantic reef fishes. xi CHAPTER 1 INTRODUCTION AND BACKGROUND The northeastern coast of South America (between the mouths of the Orinoco and Amazon rivers) is characterized by soft bottoms, turbid waters, and the world’s largest freshwater runoff (Curtin 1986). This area, known as the Amazon barrier, is recognized as a barrier to the dispersal of reef-building corals (Cox and Moore 2000), rocky-shore gastropods (Vermeij 1978), and shallow-water reef fishes (Gilbert 1972). The presence of this barrier