Spatiotemporal population genomics of marine species : invasion, expansion, and connectivity

Submitted in partial fulfillment of the requirements for the degree of Doctor of Philosophy at the Massachusetts Institute of Technology and the Woods Hole Oceanographic Institution February 2017Every genome tells a story. This dissertation contains four such stories, focused on shared themes of marine population dynamics and rapid change, with an emphasis on invasive marine species. Biological invasions are often characterized by a range expansion, during which strong genetic drift is hypothesized to result in decreased genetic diversity with increased distance from the center of the historic range, or the point of invasion. In this dissertation, population genetic and genomic tools are used to approach complex and previously intractable fundamental questions pertaining to the non-equilibrium dynamics of species invasions and rapid range expansions in two invasive marine species: the lionfish, Pterois volitans; and the shrimp, Palaemon macrodactylus. Using thousands of loci sequenced with restriction enzyme associated DNA sequencing in these two systems, this research tests theoretical predictions of the genomic signatures of range expansions. Additionally, the first chapter elucidates patterns of population genetic connectivity for deep-sea invertebrates in the New Zealand region demonstrating intimate relationships between genetics, oceanographic currents, and life history traits. Invasive shrimp results extend our understanding of marine population connectivity to suggest that human-mediated dispersal may be as important— if not more important—than oceanographic and life history considerations in determining genetic connectivity during specific phases of marine invasions. In invasive populations of lionfish, measures of genomic diversity, including a difference between observed and expected heterozygosity, were found to correlate with distance from the point of introduction, even in the absence of spatial metapopulation genetic structure. These results indicate a signal of rapid range expansion. The final study in this dissertation uses an innovative temporal approach to explore observed genomic patterns in the lionfish. In all, this dissertation provides a broad perspective through the study of multiple species undergoing superficially parallel processes that, under more intense scrutiny, are found to be mechanistically unique. It is only through comparative approaches that predictable patterns of population dynamics will emerge.I was privileged to receive support through a National Science Foundation (NSF) Graduate Research Fellowship (Grant No. 1122374), a Woods Hole Oceanographic Institution (WHOI) Fellowship administered through the Academic Program Office, funding from NSF award OCE-1131620, and the National Oceanic and Atmospheric Administration (NOAA OER #NA08OAR4600757). Research funding for sample collection, laboratory materials, sequencing, and analysis was provided by the WHOI Coastal Ocean Institute, WHOI Ocean Ventures Fund, WHOI James Education Fund for Ocean Exploration, WHOI Biology Educational Fund, Woods Hole Sea Grant New Initiative Award, Massachusetts Office of Coastal Zone Management, Northeast Sea Grant Consortium, and the PADI Foundation (Grant No. 14904). Additional research support was provided by the NSF (OCE- 1131620) to Timothy M. Shank

Population genomics of rapidly invading lionfish in the Caribbean reveals signals of range expansion in the absence of spatial population structure.

© The Author(s), 2019. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Bors, E. K., Herrera, S., Morris, J. A., Jr., & Shank, T. M. Population genomics of rapidly invading lionfish in the Caribbean reveals signals of range expansion in the absence of spatial population structure. Ecology and Evolution, 9(6), (2019):3306-3320, doi:10.1002/ece3.4952.Range expansions driven by global change and species invasions may have significant genomic, evolutionary, and ecological implications. During range expansions, strong genetic drift characterized by repeated founder events can result in decreased genetic diversity with increased distance from the center of the historic range, or the point of invasion. The invasion of the Indo‐Pacific lionfish, Pterois volitans, into waters off the US East Coast, Gulf of Mexico, and Caribbean Sea provides a natural system to study rapid range expansion in an invasive marine fish with high dispersal capabilities. We report results from 12,759 single nucleotide polymorphism loci sequenced by restriction enzyme‐associated DNA sequencing for nine P. volitans sampling areas in the invaded range, including Florida and other sites throughout the Caribbean, as well as mitochondrial control region D‐loop data. Analyses revealed low to no spatially explicit metapopulation genetic structure, which is partly consistent with previous finding of little structure within ocean basins, but partly divergent from initial reports of between‐basin structure. Genetic diversity, however, was not homogeneous across all sampled sites. Patterns of genetic diversity correlate with invasion pathway. Observed heterozygosity, averaged across all loci within a population, decreases with distance from Florida while expected heterozygosity is mostly constant in sampled populations, indicating population genetic disequilibrium correlated with distance from the point of invasion. Using an FST outlier analysis and a Bayesian environmental correlation analysis, we identified 256 and 616 loci, respectively, that could be experiencing selection or genetic drift. Of these, 24 loci were shared between the two methods.We thank the many participants of the Gulf and Caribbean Fisheries Institute for providing lionfish samples from around the Caribbean region, as well as Dr. Bernard Castillo at the University of the Virgin Islands and Kristian Rogers at the Biscayne Bay National Park. We would like to acknowledge Alex Bogdanoff at NOAA, Beaufort NC, for assistance with sample acquisition; Camrin Braun at WHOI, for assistance with the calculation of oceanic distances between sites; Dr. Tom Schultz at Duke Marine Lab and Dr. Margaret Hunter at USGS for discussions concerning ongoing population genetic projects; and Jack Cook at the WHOI Graphics department for his assistance in generating maps of the study area. We would like to extend a special thank you to Dr. John Wakeley of Harvard University for assistance in the interpretation of data. This material is based upon work supported by the National Science Foundation Graduate Research Fellowship under Grant No. 1122374. Sequencing funding was provided in part by the PADI Foundation Grant No. 14904. Additional research support was provided by the Woods Hole Oceanographic Institution (WHOI) Ocean Ventures Fund, the Coastal Ocean Institute at WHOI, the National Science Foundation (OCE‐1131620 to TMS), and the James Education Fund for Ocean Exploration within the Ocean Exploration Institute at WHOI. Publication of this paper was supported, in part, by the Henry Mastin Graduate Student Fund administered by the Oregon State University Department of Fisheries and Wildlife. Finally, we sincerely thank the reviewers and editors who helped to strengthen this manuscript

Mass spectral characterization of peptide transmitters/hormones in the nervous system and neuroendocrine organs of the American lobster Homarus americanus

The American lobster Homarus americanus is a decapod crustacean with both high economic and scientific importance. To facilitate physiological investigations of peptide transmitter/hormone function in this species, we have used matrix-assisted laser desorption/ionization Fourier transform mass spectrometry (MALDI-FTMS), matrix-assisted laser desorption/ionization time-of-flight mass spectrometry (MALDI-TOFMS) and nanoscale liquid chromatography coupled to electrospray ionization quadrupole time-of-flight tandem mass spectrometry (nanoLC-ESI-Q-TOF-MS/MS) to elucidate the peptidome present in its nervous system and neuroendocrine organs. In total, 84 peptides were identified, including 27 previously known H. americanus peptides (e.g. VYRKPPFNGSIFamide [Val1-SIFamide]), 23 peptides characterized previously from other decapods, but new to the American lobster (e.g. pQTFQYSRGWTNamide [Arg7-corazonin]), and 34 new peptides de novo sequenced/detected for the first time in this study. Of particular note are a novel B-type allatostatin (TNWNKFQGSWamide) and several novel FMRFamide-related peptides, including an unsulfated analog of sulfakinin (GGGEYDDYGHLRFamide), two myosuppressins (QDLDHVFLRFamide and pQDLDHVFLRFamide), and a collection of short neuropeptide F isoforms (e.g. DTSTPALRLRFamide, and FEPSLRLRFamide). Our data also include the first detection of multiple tachykinin-related peptides in a non-brachyuran decapod, as well as the identification of potential individual-specific variants of orcokinin and orcomyotropin-related peptide. Taken collectively, our results not only expand greatly the number of known H. americanus neuropeptides, but also provide a framework for future studies on the physiological roles played by these molecules in this commercially and scientifically important species

Patterns of deep-sea genetic connectivity in the New Zealand region : implications for management of benthic ecosystems

© The Author(s), 2012. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in PLoS One 7 (2012): e49474, doi:10.1371/journal.pone.0049474.Patterns of genetic connectivity are increasingly considered in the design of marine protected areas (MPAs) in both shallow and deep water. In the New Zealand Exclusive Economic Zone (EEZ), deep-sea communities at upper bathyal depths (<2000 m) are vulnerable to anthropogenic disturbance from fishing and potential mining operations. Currently, patterns of genetic connectivity among deep-sea populations throughout New Zealand’s EEZ are not well understood. Using the mitochondrial Cytochrome Oxidase I and 16S rRNA genes as genetic markers, this study aimed to elucidate patterns of genetic connectivity among populations of two common benthic invertebrates with contrasting life history strategies. Populations of the squat lobster Munida gracilis and the polychaete Hyalinoecia longibranchiata were sampled from continental slope, seamount, and offshore rise habitats on the Chatham Rise, Hikurangi Margin, and Challenger Plateau. For the polychaete, significant population structure was detected among distinct populations on the Chatham Rise, the Hikurangi Margin, and the Challenger Plateau. Significant genetic differences existed between slope and seamount populations on the Hikurangi Margin, as did evidence of population differentiation between the northeast and southwest parts of the Chatham Rise. In contrast, no significant population structure was detected across the study area for the squat lobster. Patterns of genetic connectivity in Hyalinoecia longibranchiata are likely influenced by a number of factors including current regimes that operate on varying spatial and temporal scales to produce potential barriers to dispersal. The striking difference in population structure between species can be attributed to differences in life history strategies. The results of this study are discussed in the context of existing conservation areas that are intended to manage anthropogenic threats to deep-sea benthic communities in the New Zealand region.This work was funded in part by a Fulbright Fellowship administered by Fulbright New Zealand and the U.S. Department of State, awarded in 2011 to EKB. Funding and support for research expedition was provided by Land Information New Zealand, New Zealand Ministry of Fisheries, NIWA, Census of Marine Life on Seamounts (CenSeam), and the Foundation for Research, Science and Technology. Other research funding was provided by the New Zealand Ministry of Science and Innovation project “Impacts of resource use on vulnerable deep-sea communities” (FRST contract CO1X0906), the National Science Foundation (OCE-0647612), and the Deep Ocean Exploration Institute (Fellowship support to TMS)

Sites and collected samples included in this study.

<p>Sites and collected samples included in this study.</p

Pairiwse Fst values between populations of the quill worm, <i>Hyalinoecia longibranchiata,</i> using a fragment of the <i>COI</i> gene.

<p>Above the diagonal indicates ranges of p-values. The “−” denotes a p>0.05. The “*” denotes a p<0.05. The “**” denotes a p<0.01. The “***” denotes a p<0.001.</p

Intra-population mt<i>COI</i> diversity statistics for the squat lobster, <i>Munida gracilis</i>.

<p>Regions are designated as CP for Challenger Plateau and CR for Chatham Rise. <i>n</i> is the total number of individuals sampled for a site, S is the number of polymorphic nucleotide sites in the sequence, h is the number of haplotypes represented at the site, Hd is haplotype diversity, and pi is nucleotide diversity.</p

TCS haplotype networks for <i>Hyalinoecia longibranchiata</i>.

<p>Part (A) shows results for <i>COI</i> sequences and part (B) shows results for <i>16S</i> sequences. Each circle represents an observed haplotype and the circles are proportional to the number of individuals sampled with that haplotype. Each color indicates a sampling site and when a haplotype was present at multiple sites, a pie chart indicates the proportions with absolute numbers appearing in text in the pie chart. Each line connecting colored circles represents a single nucleotide sequence change. Lines with small black circles indicate interior haplotypes not found in the dataset (multiple nucleotide changes between sampled haplotypes).</p

<i>16S</i> AMOVA results for <i>Hyalinoecia longibranchiata</i>.

<p><i>16S</i> AMOVA results for <i>Hyalinoecia longibranchiata</i>.</p