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From rivers to ocean basins ‑ quantifying sex‑specific connectivity in sharks

Devloo‑Delva, F ORCID: 0000-0002-6757-2949 2021 , 'From rivers to ocean basins ‑ quantifying sex‑specific connectivity in sharks', PhD thesis, University of Tasmania.

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Abstract

Globally, elasmobranch populations (sharks and rays) are declining due to increasing anthropogenic and climate pressures. Genetic connectivity between elasmobranch populations is crucial to ensure their persistence and sustain the ecological integrity of ecosystems. Consequently, knowledge on connectivity is important to inform the conservation and management of threatened or commercially important species. Genetic connectivity implies gene flow among discrete populations occurring via the dispersal of individuals outside their population of origin, followed by reproduction — a process that can be biased between sexes (known as sex-biased dispersal or SBD). Male-biased dispersal (MBD) patterns have been observed for some elasmobranchs, yet the extent of SBD in this group is currently unknown.
Knowledge of SBD is often lacking due to technical limitations. Detecting SBD relies on knowledge of reproductive isolation (i.e. population structure) and the appropriate genetic and analytical tools. With improved genetic tools, SBD can be inferred directly with individual-based (e.g. population assignment testing) and population-based (e.g. spatial autocorrelation) approaches, or indirectly, with population-level metrics (e.g. comparing markers with sex-specific inheritance, termed ‘mixed-marker’). However, these methods contain many prerequisites and assumptions; for example, the need for discrete populations that have reached genetic drift – gene flow equilibrium. To overcome these caveats, two novel methods have been proposed that warrant testing in elasmobranchs. To evaluate historical SBD (>1,000 generations in the past), the first method contrasts the population diversity and/or structure from genetic markers located on sex chromosomes with that from mitochondrial DNA (mtDNA) or autosomal DNA (auDNA) markers. The second approach looks at the spatial distribution of closely related individuals (i.e. close-kin) to investigate reproductive dispersal over a contemporary timescale (i.e. a single generation).
To date, 90 studies on 50 elasmobranch species have allowed inference of SBD. Most studies tested SBD using a mixed-marker approach, and specifically by comparing mtDNA to auDNA markers. Male-biased dispersal was observed in 25 of the 50 studied species, yet no distinct patterns that explained the presence of MBD emerged. Regarding the remaining species, symmetric gene flow was found across both females and males. While this could suggest equal female and male dispersal, this observation may be obscured by several confounding factors: (i) the characteristics of dispersal (e.g. rate and distance), (ii) the analysis method (e.g. power of genetic markers), and (iii) the experimental design (e.g. sample size and spatial scope). These factors are discussed in detail throughout this thesis.
This thesis uses novel genomic approaches (such as nuclear single nucleotide polymorphisms, or SNPs, and mitochondrial genomes) to provide insights into the patterns of (i) population structure, (ii) sex-chromosome systems, and (iii) SBD in elasmobranchs. My thesis focuses on three shark species that allow me to identify dispersal patterns based on life history, local ecology, population size and different seascape features: the Northern River Shark, Glyphis garricki; the School Shark, Galeorhinus galeus; and the Bull Shark, Carcharhinus leucas.
Specifically, I first examine the current knowledge of population structure and SBD in elasmobranchs, and the tools that are commonly used (‘General Introduction’). Secondly, I investigate population structure in the three study species using genomic and close-kin methods. The School Shark and Bull Shark studies are considered separate data chapters (Chapters 1-2), while the Northern River Shark population study was published separately from my thesis, yet the results are be summarised. Thirdly, I further analyse the thousands of SNP markers to identify signals of sex-chromosome systems in my three study species and an additional 18 species with publicly available datasets (Chapters 3-4). To accomplish this, I develop a new analytical approach in the R environment to investigate the presence of sex-linked markers (SLMs). After I identify these SLMs and the spatial scale of population structure, I quantify the amount of sex-specific connectivity between populations (Chapters 5-6). Explicitly, I contrast the auDNA to mtDNA and SLMs to detect signals of long-term dispersal. Where adult sharks were available, I also look at signals of direct, contemporary (intra-generational) dispersal by assigning individuals back to their population of origin. A close-kin framework was expanded to quantify contemporary (inter-generational) philopatry and SBD.
Population structure was found at both broad (Bull Shark) and fine (Northern River Shark) spatial scales. Yet, no signals of population structure were detected for School Sharks between Tasmania and New Zealand. These results allowed me to discuss potential ecological drivers of population structure, such as biogeographical barriers, population sizes and philopatric behaviours. I also discussed how different confounding variables could obscure signals of structure (e.g. sampling bias with sex, life-stage, or family member, and inappropriate time and spatial scale of sampling).
I further demonstrated that 19 out of the 21 studied elasmobranch species contain X and Y chromosomes (overall 3,297 X-linked and 78 Y-linked markers), using the R function I developed for the ‘radiator’ package. The SLMs can be employed to contrast autosomal SNPs and mitochondrial genome data to investigate SBD. Given the broad taxonomic range in my results, I discussed how the XX/XY sex-chromosome system in elasmobranchs may have evolved from ancestral autosomes. This hypothesis is supported by the large number of highly conserved SLMs (n = 710) within the order of Carcharhiniformes. The Y-linked markers also allowed me to develop a rapid PCR-based test to identify the genetic sex of White Shark (Carcharodon carcharias) samples, which has direct management applications.
Lastly, I found supporting evidence of MBD in the Northern River Shark and the Bull Shark; whereas the lack of population structure for the School Shark did not allow further investigation of SBD. Specifically, for the Northern River Shark, the kinship approach showed a slight bias towards male dispersal (63 % of the dispersal was attributed to males), whereas SNPs and mtDNA demonstrated strong philopatric signals and no SBD. The Bull Shark kinship results revealed a stronger signal of MBD (100 %), yet only few kin pairs were found. Therefore, this result needs to be verified with larger sample sizes. However, at an intra-ocean-basin scale, the mixed-marker approach (including X-linked markers) suggested female philopatry for the Bull Shark.
My final discussion synthesised the dispersal patterns observed from my three study species and examines the potential ecological and evolutionary drivers for these patterns. I critically compared the genetic and analytical approaches for the detection of population structure and SBD. I concluded that genomic tools have improved the resolution of population connectivity analyses, although sampling biases can have a substantial effect, and that the close-kin approach will prove a valuable tool to assess dispersal at very fine spatial and temporal scales. Overall, the potential implications of these quantitative findings for management were highlighted and future work is proposed.

Item Type: Thesis - PhD
Authors/Creators:Devloo‑Delva, F
Keywords: sex-biased dispersal, elasmobranchs, genomics, SNPs, close-kin
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Copyright 2021 the author

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