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The Role of Habitat Gaps and Oceanography on the Biogeography and Population Genetics of Rocky Intertidal Gastropods in the Bay of Biscay

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The Role of Habitat Gaps and Oceanography on the Biogeography and Population Genetics of Rocky Intertidal Gastropods in the Bay of Biscay UNIVERSITY OF SOUTHAMPTON FACULTY OF NATURAL AND ENVIRONMENTAL SCIENCES Ocean and Earth Science, National Oceanography Centre Southampton The role of habitat gaps and oceanography on the biogeography and population genetics of rocky intertidal gastropods in the Bay of Biscay by Edward Wort A thesis submitted in partial fulfilment for the degree of Doctor of Philosophy August 2018 Abstract In biogeography, patterns of species abundance, distribution, size, population genetics and morphology often do not follow simple latitudinal gradients – which are classically assumed in such “rules” as the abundant centre hypothesis and Bergmann’s rule. Rather, the biogeography of a species or groups of species are more likely to be associated with abiotic and biotic variables such as availability of suitable habitat, temperature, dispersal potential, and habitat specificity. However, previous biogeographic studies rarely go beyond simple pattern description, particularly for marine species. In this thesis, I find that regional patterns of abundance, distribution, size, morphology, and population genetics are often associated with regional and local differences in environmental and biotic variables, such as upwelling intensity, habitat availability, and intrinsic attributes of species ecology, such as their level of habitat specificity. For example, a lower availability of suitable habitat can result in a fragmented distribution and subsequently lower genetic connectivity for species dependent upon that habitat. Differing abundances and recruitment among localities may also affect intraspecific competition, so density-dependent interactions occur, resulting in smaller/larger individuals. This would not necessarily follow the classically assumed temperature-size rule of smaller individuals usually being found at higher temperatures. Within a species, differing growth rates and adaptations to environmental variables can result in local morphological variation. These biogeographic concepts are explored in depth using rocky intertidal species of the Bay of Biscay as a model system, which contains a 230 km habitat gap and regional variation in temperature unrelated to a latitudinal gradient. In Chapter 2, the almost complete mitochondrial genome of Steromphala umbilicalis is described in relation to other Vetigastropoda. By removing different genes, and using amino acid or nucleotide sequences, different phylogenies are generated. From this, it is proposed that selection mechanisms may be occurring. In Chapter 3, the population genetics of the congeners S. umbilicalis (habitat generalist) and S. pennanti (habitat specialist), are described over the sympatric portion of their range, using both a newly developed mitochondrial marker and microsatellites. By combining this information with abundance estimates, S. umbilicalis is shown to have a more continuous distribution and is more abundant, and therefore shows greater genetic connectivity than S. pennanti which has a more fragmented distribution and lower abundance. In Chapter 4, the abundances, size structures and distributions of S. umbilicalis, S. pennanti, Phorcus lineatus, Patella vulgata and Patella depressa are explored using multiple linear regression for environmental variables including sea surface temperature, air temperature, wave exposure, distance to the habitat gap, and adjacent rocky substrate. Sea temperature showed a positive relationship with P. depressa abundance and the opposite for P. vulgata. Subsequent density-dependent interactions in P. depressa resulted in smaller individuals being associated with higher abundance between localities, and between quadrats within localities for both Patella species. The habitat gap amplified the differences in abundance between the cool water region in northern France dominated by P. vulgata and the warm water Basque region dominated by P. depressa. In Chapter 5, the aspect ratio of S. umbilicalis is explored at the macroscale in relation to multiple environmental variables. Sea temperature shows the best relationship with aspect ratio, both with initial European data and an expanded dataset including museum specimens from the British Isles. Whilst the underlying mechanism is unclear, it may be linked to a decreased growth rate at higher temperature, resulting in a more pointed shell. This work throws new light on biogeographic patterns and processes, particularly regarding temperature around range centres. It has implications when considering the impacts of global warming, particularly in relation to rocky intertidal biogeography. i ii Table of Contents Abstract ............................................................................................................................... i Table of Contents ............................................................................................................. iii Table of Tables ................................................................................................................. vii Table of Figures ................................................................................................................. ix List of Accompanying Materials ................................................................................. xi Academic Thesis: Declaration Of Authorship .................................................. xiii Acknowledgements .........................................................................................................xv Chapter 1: Introduction ................................................................................................... 1 1.1 Project outline ................................................................................ 1 1.2 Marine Biogeography ...................................................................... 1 1.3 Biogeography of Rocky Shores ........................................................ 1 1.4 Intertidal biogeography of the Bay of Biscay ................................... 4 1.5 Thesis aims and objectives ............................................................. 6 Chapter 2: Testing the contribution of individual genes in mitochondrial genomes for assessing phylogenetic relationships in Vetigastropoda .......................................................... 9 2.1 Introduction ................................................................................... 9 2.3 Methods and results ..................................................................... 10 2.3 Discussion .................................................................................... 15 Chapter 3: Contrasting genetic structure of two sympatric congeneric gastropods: do differences in habitat preference, abundance, and distribution matter? ............................................. 17 3.1 Introduction ................................................................................. 17 3.2 Materials and Methods ................................................................. 19 3.2.1 Sampling ............................................................................... 19 3.2.2 Mitochondrial DNA locus selection and primer design ........... 21 3.2.3 Obtaining S. umbilicalis transcriptome ................................... 21 3.2.4 DNA extraction ...................................................................... 22 3.2.5 Microsatellite identification and primer development ............. 23 3.2.6 PCR, sequencing and peak scoring ......................................... 24 3.2.7 Microsatellite peak scoring and analysis ................................ 25 iii 3.2.8 Mitochondrial DNA analyses .................................................. 27 3.3 Results ......................................................................................... 27 3.3.1 Mitochondrial DNA results ..................................................... 27 3.3.2 Abundance distributions ....................................................... 28 3.3.3 Microsatellite population genetics ......................................... 29 3.4 Discussion ................................................................................... 34 3.4.1 Differences between species .................................................. 35 3.4.2 Patterns associated with both species .................................... 36 3.5 Conclusions ................................................................................. 38 Chapter 4: Explaining biogeographic patterns of abundance and body size of rocky intertidal gastropods in the Bay of Biscay ...... 39 4.1 Introduction ................................................................................. 39 4.1.1 Background and hypotheses .................................................. 39 4.1.2 Study species and focal region .............................................. 43 4.2 Methods ....................................................................................... 46 4.2.1 Surveys .................................................................................. 46 4.3.2 Environmental data ................................................................ 48 4.2.3 Statistical analyses ................................................................ 49 4.3 Results ......................................................................................... 51 4.3.1 Linear model statistics ........................................................... 51 4.3.2 Patellids ................................................................................ 52 4.3.3 Trochids ...............................................................................
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