UCLA UCLA Electronic Theses and Dissertations Title Evolution and Population Genomics of Loliginid Squids Permalink https://escholarship.org/uc/item/0zw3h4ps Author Cheng, Samantha Hue Tone Publication Date 2015 Peer reviewed|Thesis/dissertation eScholarship.org Powered by the California Digital Library University of California UNIVERSITY OF CALIFORNIA Los Angeles Evolution and Population Genomics of Loliginid Squids A dissertation submitted in partial satisfaction of the requirements for the degree of Doctor of Philosophy in Biology by Samantha Hue Tone Cheng 2015 ABSTRACT OF THE DISSERTATION Evolution and Population Genomics of Loliginid Squids by Samantha Hue Tone Cheng Doctor of Philosophy in Biology University of California, Los Angeles, 2015 Professor Paul Henry Barber, Chair Globally, rampant harvesting practices have left vital marine resources in sharp decline precipitating a dramatic loss of the biodiversity and threatening the health and viability of natural populations. To protect these crucial resources and ecosystems, a comprehensive assessment of biodiversity, as well as a rigorous understanding of the mechanisms underlying it, is urgently needed. As global finfish fisheries decline, harvest of cephalopod fisheries, squid, in particular, has exponentially increased. However, while much is known about the evolution and population dynamics of teleost fishes, much less is understood about squids. This dissertation provides a robust, in-depth examination of these mechanisms in commercially important squids using a novel approach combining genetics and genomics methods. In the first chapter, a suite of genetic markers is used to thoroughly examine the distribution and evolution of a species complex of bigfin reef squid (Sepioteuthis cf. lessoniana) throughout the global center of marine biodiversity, the Coral Triangle, and adjacent areas. Phylogenetic analyses and species delimitation methods unequivocally demonstrate the presence of at least three cryptic lineages ii sympatrically distributed throughout the region. While these putative species are reciprocally monophyletic, they are difficult to distinguish morphologically and little is known about how they differ in life history and ecology. To this end, in chapter 2, patterns of population structure over the Coral Triangle and adjacent regions were examined using genetic and genomic methods to identify important processes shaping both genetic and demographic connectivity in two of these cryptic species. Using both mitochondrial DNA (cytochrome oxidase subunit 1) and genome-wide single nucleotide polymorphisms (generated from restriction site associated digest (RAD) sequencing), we find strong, but discordant, patterns of population structure between these sympatric sibling taxa suggesting contrasting dispersal life histories. Moreover, detection of putative outlier loci highlights the possible role of selective pressures from regional environmental differences in shaping ongoing divergence. Given the fine-scale resolution achieved in chapter 2 with using RAD sequencing, in chapter 3, we apply these methods to examine potential population structure in the highly valuable market squid fishery (Doryteuthis opalescens) in California. This fishery has long been hypothesized to be two separate stocks due to different spawning peaks and areas. Using genome-wide SNPs and a rigorous temporal sampling scheme, we determined that northern and southern regions do not represent two distinct spatial stocks. Rather, complex patterns of temporal population structure lend support to continual spawning of genetically distinct cohorts at both sites throughout the 2014 harvest season. Collectively, these results demonstrate that squid biodiversity and population structure is much more complex than previously thought. Through the use of genetic and genomic technologies, we can delineate populations and identify the mechanisms driving connectivity to provide key information for fisheries management and conservation. iii The dissertation of Samantha Hue Tone Cheng is approved. Frank E. Anderson Howard Bradley Shaffer Paul Henry Barber, Committee Chair University of California, Los Angeles 2015 iv TABLE OF CONTENTS Epigraph ……………………………………………………………………………… vi List of Tables ………………………………………………………………………… vii List of Figures ………………………………………………………………………... ix Acknowledgements …………………………………………………………………... xi Vita/Biographical Sketch …………………………………………………………….. xvi Introduction …………………………………………………………………………... 1 References ……………………………………………………………………. 6 Chapter 1. Molecular evidence for co-occuring cryptic lineages within the Sepioteuthis cf. lessoniana species complex in the Indian and Indo-West Pacific Oceans ………………………………………………………………... 9 Chapter 2. (Not) going the distance: contrasting patterns of geographical subdivision in sibling taxa of reef squid (Loliginidae: Sepioteuthis cf. lessoniana) in the Coral Triangle …………………………………………….. 34 Figures and Tables …………………………………………………………… 67 References ……………………………………………………………………. 83 Chapter 3. Genome-wide SNPs reveal complex fine-scale population structure in the California market squid fishery (Doryteuthis opalescens) …………………... 95 Figures and Tables …………………………………………………………… 124 References ……………………………………………………………………. 138 v EPIGRAPH We need the tonic of wilderness…At the same time that we are earnest to explore and learn all things, we require all things be mysterious and unexplorable, that land and sea be infinitely wild, unsurveyed and unfathomed by us because unfathomable. We can never have enough of Nature. – Walden; or, Life in the Woods, Henry David Thoreau My soul is full of longing for the secrets of the sea, and the heart of the great ocean sends a thrilling pulse through me. – The Secret of the Sea, Henry Wadsworth Longfellow vi LIST OF TABLES Table 2.1 Sampling localities and sample sizes for mitochondrial and SNP datasets. Note, sample sizes for SNP data reflect how many individuals were retained following stringent filtering for quality and coverage (denoted by *) ……… 67 Table 2.2 Summary statistics for mitochondrial and genome-wide single nucleotide polymorphisms employed in this study ……………………………………... 68 Table 2.3 Genetic differentiation over hypothesized barriers to dispersal for Lineage B using SNP and mtDNA CO1 datasets. Significance indicated by + = p < 0.1,* = p < 0.05, ** = p < 0.01…………………………………………......... 69 Table 2.4 Genetic differentiation over hypothesized barriers to dispersal for Lineage C using SNP and mtDNA CO1 datasets. Significance indicated by + = p < 0.1,* = p < 0.05, ** = p < 0.01………………………………………………. 69 Table 2.5 Back-assignment proportions of individuals to original sampling locations using discriminant analysis of principal components……………………….. 70 Table 2.6 Pairwise FST between sampling locations for Lineage B. Values above the diagonals represent analysis with neutral loci and values below represent outlier loci. Values in bold are statistically significant (p<0.0001)…………. 70 Table 2.7 Pairwise FST between sampling locations for Lineage C. Values above the diagonals represent analysis with neutral loci and values below represent outlier loci. Values in bold are statistically significant (p<0.0001)…………. 70 Table 3.1 Sample collection of D. opalescens from northern and southern California landings during the 2014 harvest season…………………………………….. 124 Table 3.2a List of morphometric measurements made for each individual squid ……… 125 Table 3.2b Description of maturity scale employed for D. opalescens (after Evans 1976) ………………………………………………………………………… 125 Table 3.3 Average differences in morphometric measurements between individuals grouped by sex by region (A) and location by time (B). Bold values indicate average measurements between comparisons that are significantly different as indicated by Tukey HSD tests (p>0.05). Groups for sex by region (A) are north males (NM), north females (NF), south males (SM) and south females (SF). Groups for location by time (B) are as follows: North - May (N5), June (N6), July (N7), August (N8); South – June (S6), July (S7), August (S8), September (S9). Morphometric measurements abbreviated as DML (dorsal mantle length), FW (fin width), and FL (fin length). Negative differences signify that the second group is larger than the first group…… 126 Table 3.4 Summary statistics: Number of successfully sequenced individuals (n) per sampling location, expected heterozygocity (He), observed heterozygocity (Ho), percent polymorphic loci (%)………………………………………….. 127 Table 3.5A Pairwise FST between temporal replicates in northern California. FST with p>0.05 indicated in bold……………………………………………………... 128 Table 3.5B Pairwise FST between temporal replicates in southern California. FST with p>0.05 indicated in bold……………………………………………………... 128 Table 3.5C Pairwise FST between temporal replicates from northern vs. southern vii California. FST with p>0.05 indicated in bold……………………………….. 128 Table 3.6 Estimated migration rates between temporal replicates in northern and southern California fishing regions for D. opalescens. Columns indicate sampling locations where migrants are coming from and rows indicate where they are migrating to. Values in italics indicate level of self- recruitment…………………………………………………………………… 129 viii LIST OF FIGURES Figure 2.1 Sampling locations through the Coral Triangle and adjacent regions. Gray shading indicates exposed continental shelf during low sea level stands during the Pleistocene (after Voris 2000). Primary oceanographic features are illustrated as well (after Wykrti 1971): NEC