Genetic structure, population connectivity and taxonomic identity of the black-lip pearl oyster Pinctada margaritifera (Bivalvia: Pteriidae), across its Indo-Pacific distribution

Lal, Monal M. (2016) Genetic structure, population connectivity and taxonomic identity of the black-lip pearl oyster Pinctada margaritifera (Bivalvia: Pteriidae), across its Indo-Pacific distribution. PhD thesis, James Cook University.

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The black-lip pearl oyster Pinctada margaritifera (L.) is a bivalve mollusc highly valued for cultured pearl and pearlshell production throughout its extensive Indo-Pacific natural distribution, where it makes substantial contributions to local economies and supports coastal community livelihoods. Despite its commercial importance, substantial knowledge gaps exist for this species, particularly regarding genetic structure and population connectivity at both local and regional scales, as well as its taxonomic identity. This information is required for the development of sustainable fishery management strategies, as well as responsible aquaculture practices, to ensure the persistence of healthy wild populations, and continued commercial production.

The overarching goal of the research undertaken for this thesis was to investigate the stock structure, connectivity and taxonomy of P. margaritifera, to inform fishery management and aquaculture practices across the extent of its Indo-Pacific distribution, with a particular focus on the Fiji Islands. Specifically, over four separate investigations, I develop novel genomewide single nucleotide polymorphism (SNP) markers for this species, and use them to investigate population genetic structure, diversity, connectivity and local adaptation of Fijian oysters, as well as for populations sampled from across the broader ~18,000 km species distribution. I also compare estimates of population connectivity derived from genomic analyses with an independent hydrodynamic particle dispersal model, to corroborate patterns of larval transport between study sites. Finally, I utilise phylogenomic analyses to assess the evolutionary relationships of the black-lip pearl oyster across its natural distribution, and also to ascertain its taxonomic identity among other members of the family Pteriidae.

The first investigation developed 5,243 novel genome-wide SNP markers for P. margaritifera, and tested their utility by assessing population structure, genetic diversity, as well as detecting regions of the genome underlying functional differences among populations. It involved 156 Fijian oysters sampled from three wild, and one hatchery produced population. Shallow but significant genetic structure was revealed among all wild populations (average pairwise Fₛₜ = 0.046), with clear evidence of a genetic bottleneck in the hatchery population (Nₑ(LD) = 6.1), compared to wild populations (Nₑ(LD) >192.5). Fₛₜ outlier detection to differentiate individuals between the orange and black tissue colour morphotypes characteristic of this species, revealed 42-62 highly differentiated SNPs (p<0.02), while casecontrol association discovered up to 152 SNPs (p<0.001). Database searches revealed that five of these SNPs were associated with a melanin biosynthesis pathway, demonstrating their biological relevance. This investigation demonstrated the utility of genome-wide SNP data for assessment of genetic structure and diversity in P. margaritifera, with transferability to other highly-dispersive marine taxa for their conservation and management.

The second investigation utilised 4,123 genome-wide SNPs, together with an independent hydrodynamic particle dispersal model to assess genetic structure, diversity, local adaptation and population connectivity at 6 farm and 5 wild Fijian sites. Weak fine-scale patterns of population structure indicative of broad-scale admixture were observed among wild oysters, while a hatchery-sourced farmed population exhibited a higher degree of genetic divergence (hatchery oysters cf. all other populations Fₛₜ=0.085–0.102). This hatchery-produced population had also experienced a bottleneck (Nₑ(LD)=5.1; 95% C.I.=[5.1-5.3]); compared to infinite Nₑ(LD) estimates for all wild oysters. Simulation of larval transport pathways confirmed the existence of broad-scale admixture by surface ocean currents, correlating well with finescale patterns of population structure discovered. Fₛₜ outlier tests failed to detect genetic signatures supportive of selection, with only 2-5 directional outlier SNPs identified (average Fₛₜ=0.116). The lack of biologically significant population genetic structure, absence of evidence for local adaptation and larval dispersal simulation, all indicated the existence of a single genetic stock of P. margaritifera in the Fiji Islands for management purposes. The combined use of independent high resolution genomic and oceanographic data as demonstrated here is a novel approach that can be applied to other broadcast spawning taxa.

The third investigation examined the microevolutionary forces influencing genetic structure, connectivity and adaptive variation across the ~18,000 km Indo-Pacific distribution of P. margaritifera. Concordance with a theoretical population model known as the Core- Periphery Hypothesis (CPH), was used as a framework for this assessment. The CPH predicts that genetic diversity is expected to be highest at the centre of a species' distribution, progressively decreasing with increased differentiation towards outer range limits, as populations become increasingly isolated, fragmented and locally adapted. Analyses utilising 9,624 genome-wide SNPs and 580 oysters sampled from 14 sites, discovered differing patterns of significant and substantial broad-scale genetic structure between the Indian and Pacific Ocean basins. Indian Ocean populations were markedly divergent (Fₛₜ=0.253-0.418, p<0.001), compared to Pacific Ocean oysters, where basin-wide gene flow was much higher (Fₛₜ=0.001-0.109, p<0.001). Visualisation of population structure at selectively neutral loci resolved three and five discrete genetic clusters for the Indian and Pacific Oceans respectively, while evaluation of genetic structure at adaptive loci for Pacific populations (89 SNPs under directional selection; Fₛₜ=0.101-0.437, FDR=0.05), revealed five clusters identical to those detected at neutral SNPs, suggesting environmental heterogeneity within the Pacific. Patterns of structure and connectivity were supported by Mantel tests of isolation by distance (IBD) and independent hydrodynamic particle dispersal simulations. These findings have revealed that population organisation in this species is highly complex and far more elaborate than generalised CPH predictions, with structuring being produced by the interaction of ocean currents, IBD and seascape features at a broad scale, together with habitat geomorphology and local adaptation at regional levels.

The fourth and final investigation examined evolutionary relationships and the taxonomic identity of P. margaritifera. This study was required as the current species classification is not supported by molecular data, and includes a total of six subspecies that are described exclusively using morphological characters. Here, 69 oysters were sampled from 14 populations in both the Indian and Pacific Oceans. Samples were also collected from the congeneric taxa P. maxima and P. mazatlanica (n=29 and n=10, respectively), and phylogenetic reconstruction carried out using both 8,308 genome-wide SNPs and 10,000 dominant loci. Reconstructions using neighbour-joining (Nei's 1972 unbiased distances), maximum likelihood and Bayesian approaches all indicate that the taxonomy of P. margaritifera is more complex than previously indicated, with distinct evolutionary significant units (ESUs) identified within Tanzanian and Iranian populations, correlating with type localities for two Indian Ocean morphological subspecies descriptions. Contrastingly, phylogenies generated for Pacific Ocean P. margaritifera resolved a large monophyletic clade, suggesting little support for two of three morphological subspecies classifications reported from this ocean basin. Furthermore, P. mazatlanica specimens all formed a basal clade closest to French Polynesian P. margaritifera, suggesting it may not constitute a separate species. Collectively, these findings provide evidence to support a suggestion by previous studies that P. margaritifera comprises a species complex; however, further investigation involving finer-scale sampling with higher sample densities is required to resolve regional ESU boundaries.

Collectively, this thesis presents the most comprehensive evaluation of genetic structure, population connectivity and evolutionary relationships for P. margaritifera to date. The data generated have permitted fundamental insights into the stock and taxonomic structure of this species, which are invaluable for its sustainable fishery management and aquaculture, with extension to other taxa possessing similar biological attributes.

Item ID: 49812
Item Type: Thesis (PhD)
Keywords: aquaculture, black-lip pearl oyster, colour morphotype, core-periphery hypothesis, Fiji Islands, fine-scale differentiation, genetics, hydrodynamic dispersal, Pacific pearl oysters, phylogeny, Pinctada margaritifera, population genomics, SNP, species distribution, taxonomic identity
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Publications arising from this thesis are available from the Related URLs field. The publications are:

Chapter 1: Lal, Monal M., Southgate, Paul C., Jerry, Dean R., and Zenger, Kyall R. (2016) Fishing for divergence in a sea of connectivity: the utility of ddRADseq genotyping in a marine invertebrate, the black-lip pearl oyster Pinctada margaritifera. Marine Genomics, 25. pp. 57-68.

Chapter 2: Lal, Monal M., Southgate, Paul C., Jerry, Dean R., Bosserelle, Cyprien, and Zenger, Kyall R. (2016) A parallel population genomic and hydrodynamic approach to fishery management of highly-dispersive marine invertebrates: the case of the Fijian Black-Lip Pearl Oyster Pinctada margaritifera. PLoS One, 11 (8). pp. 1-26.

Chapter 3: Lal, Monal M., Southgate, Paul C., Jerry, Dean R., Bosserelle, Cyprien, and Zenger, Kyall R. (2017) Swept away: ocean currents and seascape features influence genetic structure across the 18,000 Km Indo-Pacific distribution of a marine invertebrate, the black-lip pearl oyster Pinctada margaritifera. BMC Genomics, 18. pp. 1-21.

Date Deposited: 09 Aug 2017 03:57
FoR Codes: 06 BIOLOGICAL SCIENCES > 0604 Genetics > 060411 Population, Ecological and Evolutionary Genetics @ 40%
07 AGRICULTURAL AND VETERINARY SCIENCES > 0704 Fisheries Sciences > 070401 Aquaculture @ 20%
07 AGRICULTURAL AND VETERINARY SCIENCES > 0704 Fisheries Sciences > 070403 Fisheries Management @ 40%
SEO Codes: 83 ANIMAL PRODUCTION AND ANIMAL PRIMARY PRODUCTS > 8301 Fisheries - Aquaculture > 830104 Aquaculture Oysters @ 50%
83 ANIMAL PRODUCTION AND ANIMAL PRIMARY PRODUCTS > 8302 Fisheries - Wild Caught > 830299 Fisheries- Wild Caught not elsewhere classified @ 30%
83 ANIMAL PRODUCTION AND ANIMAL PRIMARY PRODUCTS > 8305 Primary Animal Products > 830504 Pearls @ 20%
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