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Eric Garcia Phd Dissertation 1 Copy 2 UNIVERSITY OF CALIFORNIA SANTA CRUZ GENOMIC ANALYSIS OF DISJUNCT MARINE FISH POPULATIONS OF THE NORTHEASTERN PACIFIC AND SEA OF CORTEZ A dissertation submitted in partial satisfaction of the requirements for the degree of DOCTOR OF PHILOSOPHY in ECOLOGY AND EVOLUTIONARY BIOLOGY by Eric Garcia December 2018 The Dissertation of Eric Garcia is approved: _________________________________ Professor Giacomo Bernardi, Chair _________________________________ Professor Pete Raimondi _________________________________ Brian Simison, Ph.D. _________________________________ Professor Octavio Aburto ___________________________________ Lori Kletzer Vice Provost and Dean of Graduate Studies Copyright © by Eric Garcia December, 2018 Table of Contents General Introduction Studying evolution in the genomic era………………………..……………………..01 The Baja California disjunct fishes…………………………………………………..06 Chapter 1 Tempo and mode of divergence in Baja California disjunct fishes based on a genome- wide calibrated substitution rate……………………………..………………………13 Chapter 2 Patterns of genomic divergence and signals of selection in sympatric and allopatric northeastern Pacific and Sea of Cortez populations of the sargo (Anisotremus davidsonii) and longjaw mudsucker (Gillichthys mirabilis)……………..………..…42 Chapter 3 Genomic divergence and signals of convergent selection between northeastern Pacific and Sea of Cortez disjunct populations of four marine fishes…………………...…..81 General Conclusion..................................................................................................126 iii List of Tables General Introduction Table 1 - List and distribution of the 19 Baja California disjunct fishes……………07 Tempo and mode of divergence in Baja California disjunct fishes based on a genome-wide calibrated substitution rate. Table 1 - Number of samples collected per species and region...................................19 Table 2 - Divergence time estimates based on internally-calibrated Anisotremus RAD loci substitution rate.....................................................................................................24 Patterns of genomic divergence and signals of selection in sympatric and allopatric northeastern Pacific and Sea of Cortez populations of the sargo (Anisotremus davidsonii) and longjaw mudsucker (Gillichthys mirabilis) Table 1 - General characteristic and previously available genetic information of studied species.............................................................................................................49 Table 2 - Location and number of samples per species…...........................................51 Table 3 - Locus, polymorphism, and genetic diversity statistics of the Pacific and Sea of Cortez (Gulf) populations per species….................................................................58 Table 4 - Distance matrix reporting FST values and significance between sympatric populations of Anisotremus davidsonii and Gillichthys mirabilis...............................59 iv Genomic divergence and signals of convergent selection between northeastern Pacific and Sea of Cortez disjunct populations of four marine fishes Table 1 - Species characteristics and previously available genetic information….…86 Table 2 - Pacific and Sea of Cortez collecting sites and samples per species.............90 Table 3 - Locus, polymorphism, and genetic statistics of the Pacific and Sea of Cortez populations per species ……………….……………………………………………..95 Table 4 - List and function of genes presumed under selection and that are diverging between Pacific and Gulf populations of more than one species…………………...101 v List of Figures General Introduction Figure 1 - Visual representation of expected differentiation along the genome…..…04 Figure 2 - Typical Baja California disjunct distribution …………………….………06 Figure 3 - The studied species……………………………….………………………09 Tempo and mode of divergence in Baja California disjunct fishes based on a genome-wide calibrated substitution rate. Figure 1 - Time-calibrated phylogeny and distribution of studied Anisotremus species………………………………………………………………………………..25 Patterns of genomic divergence and signals of selection in sympatric and allopatric northeastern Pacific and Sea of Cortez populations of the sargo (Anisotremus davidsonii) and longjaw mudsucker (Gillichthys mirabilis) Figure 1 - Pacific and Sea of Cortez sampling localities and well-established phylogeographic breaks, Point Conception and Punta Eugenia..................................50 Figure 2 - DAPC cluster plots of Gillichthys mirabilis and Anisotremus davidsonii populations…………………………………….……………………………………..61 Figure 3 - STRUCTURE plots with Bayesian assignment of individual into distinct genetic clusters or populations……………..….……………………………………..62 vi Figure 4 - Outlier loci statistics in pairwise comparisons of populations of Anisotremus davidsonii and Gillichthys mirabilis..……………………………...…..65 Genomic divergence and signals of convergent selection between northeastern Pacific and Sea of Cortez disjunct populations of four marine fishes Figure 1 - Pacific and Sea of Cortez sampling localities…………..……......…...…..89 Figure 2 - DAPC cluster plots of Pacific and Sea of Cortez per species based on all loci……………………………………………..……………………………………..96 Figure 3 - STRUCTURE plots based on presumed neutral loci and outlier loci or loci suspected to be under selection…………..……......…...………………………….....97 Figure 4 - FST distribution and corresponding relative density of outlier loci per species…...………………...…………………..……………………………………..99 Figure 5 - Stacked barplot showing the percentages of outliers giving a GenBank match to a gene, a sequence or chromosome location without gene information, or not match found…...………………...…………………..……………………………...100 Figure 6 - KEGG assignments of outlier loci………………......…...……………...100 vii Abstract Genomic analysis of disjunct marine fish populations of the northeastern Pacific and Sea of Cortez Eric Garcia The formation of the Baja California peninsula separated the distributions of 19 marine fishes into disjunct Pacific and Sea of Cortez populations. Similarly, their Pacific distributions cross phylogeographic points that diminish the genetic connectivity of their populations. This resulted in multiple species experiencing a gradient of gene flow and an extraordinary framework to study mechanisms of divergence and signals of selection under different scenarios of isolation. Genetic isolation in these species has previously been studied using only a handful of markers. In this dissertation, Restriction Site-Associated DNA (RADseq) is used to genotype thousands of genome-wide makers to study the evolutionary history, characterized genomic patterns of divergence among populations, and search for signals of drift and selection, in four of these species: the sargo, Anisotremus davidsonii (ADA); the longjaw mudsucker, Gillichthys mirabilis (GMI), the California sheephead, Semicossyphus pulcher (SPU); and the zebraperch, Kyphosus azureus (KAZ). While, no evidence of isolation was found for SPU, estimated dates the disjunction of ADA, GMI, and KAZ, were 60, 284, and 23 thousand years, respectively. A dispersal episode where species migrated northwards and then became isolated by the warming of the seawater temperate in the south of the Baja California peninsula at the end of viii the last glaciation period, and a vicariant isolation resulting from the closure of a mid- peninsular seaway, are the plausible historical events that produced the current distributions of these species. Lower than expected levels of genomic gene flow (significant p-values) were seen across Point Conception in GMI (FST=0.15), Punta Eugenia in ADA (FST=0.02), and across the peninsula in KAZ, GMI and ADA (FST=0.03, 0.11, and 0.23, respectively). Furthermore, when comparing disjunct populations, 19 to 46 % of outlier loci matched coding genes in all species and analyses identified 15 genomic regions, potentially involved in processing environmental information, metabolism, immune response, and possibly reproduction, diverging in more than one of these species. Results are interpreted as supporting (1) the idea that ADA and GMI disjunct populations are in the initial phases of allopatric speciation and (2) the presence of convergent selection in these species. ix Dedication To my family, friends, and mentors. x Acknowledgements I would like to express my deep gratitude to my partner and family for supporting me throughout my Ph.D. adventure. Thank you for making my life so much better. I am forever in doubt to my committee members, Drs. Giacomo Bernardi, Pete Raimondi, Brian Simison, and Octavio Aburto, for the guidance and support at all times during this dissertation. Thank you to all EEB professors and fellow Ph.D. students for your lessons and discussions, which improved my understanding of evolution and academic life. Finally, I would like to thank all my friends for making Santa Cruz an incredible place to call home for all these years. This work was supported financially by the Consejo Nacional de Ciencia y Tecnología (CONACYT) in Mexico, UC Mexus, The Myers Trust, STARTS scholarship, Friends of the Long Marine Lab, and by the Graduate Student Association and the department of Ecology and Evolutionary Biology at UCSC. I would also like to thank Dr. Larry G. Allen for providing fish illustrations. xi GENERAL INTRODUCTION Studying Evolution in the Genomic Era Genetic differences are the building blocks of biodiversity. How this variation distinguishes populations and eventually creates new
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