Genetic structure and biogeography of three commercially important African freshwater fishes: Lates niloticus, Bagrus docmak and Bagrus bayad

Basiita, Rose Komugisha (2016) Genetic structure and biogeography of three commercially important African freshwater fishes: Lates niloticus, Bagrus docmak and Bagrus bayad. PhD thesis, James Cook University.

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Abstract

The complex geology and hydrological evolution of Africa has resulted in a landscape characterised by some of the world's largest freshwater lakes and rivers. These freshwater habitats contain diverse fish fauna from which commercial inland fisheries support millions of people in Africa and other parts of the world through fish exports. Despite the extreme importance of African fisheries, versus increased threats that have led to their stagnation and decline, fisheries conservation and management based on genetic knowledge of stock structure has remained poorly studied and understood in Africa. It is clear though, that biogeography of fish fauna will often follow patterns of stock structure along gradients of interconnected, or fragmented habitats. Understanding the genetic structure and diversity of commercial fish species along these gradients in Africa is vital in identifying management units (MUs) for sustainable management and potential aquaculture development of aquatic species.

The widely distributed bagrid catfishes (Bagrus docmak and B. bayad) and the Nile perch, Lates niloticus, have been identified as model species that could be used to not only understand the biogeography of the African aquatic fauna, but are also important commercial fisheries and candidate species for aquaculture development. These fish species are indigenous to Africa and valued for food, as well as important components of recreational-based fisheries. These three species have been overexploited in their natural environments, with the Nile perch also in decline within environments where it has been translocated.

The overarching objective of this thesis was to develop and utilise new genetic resources to understand the genetic structure and biogeography of these three important African freshwater fishes and further understanding on how genetic population structure has been shaped by both the geology and anthropological (i.e., translocations), especially in the Great Lakes Region of Africa. The knowledge acquired will be useful for the management and conservation of existing fisheries and aquaculture development programmes.

Firstly, to address the lack of genetic resources for important commercial fish species in Africa, high throughput Next Generation Sequencing (NGS) was used to generate novel genomic resources for two commercially important fish species, L. niloticus and B. docmak. Roche 454 GS-FLX shotgun sequencing was used to generate over 160,000 sequence fragments for B. docmak, from which hundreds of microsatellites markers with primers were in silico mined. Of these a subset of 20 novel microsatellite loci were tested in the laboratory from which 15 markers successfully amplified and were characterized in B docmak individuals from Lake Albert in East Africa (mean allelic richness (N(A)) of 4.5, mean Hₒ, and Hₑ, of 0.535 ± 0.37 and 0.605 ± 0.028, respectively). These 15 loci also were found to cross-amplify in a sister species, Bagrus bayad. For the Nile perch, next generation sequencing on Roche 454 GS-FLX instrumentation yielded ~122,000 sequences, which have been deposited at in NCBI (accession# SRP051308), and allowed the design of primers for 285 in silico perfect microsatellite loci. Thirty-one microsatellite loci were tested for polymorphism. Additionally, 16 microsatellites previously characterized for Lates calcarifer (a sister species) were tested in L. niloticus. The successful development of the microsatellite markers de novo in these species were used to resolve the stock structure of these species in the ensuing data chapters of the thesis. Furthermore, although not evaluated herein, these markers will also have utility in parentage analysis in future breeding programs for aquaculture development.

Whilst there is some understanding of how macroevolutionary drivers have shaped teleost speciation in East Africa, there is a paucity of research into how the same biogeographical factors have affected microevolution (ie evolution of populations within a species). To address this deficiency, population genetic diversity, demography and structure were investigated in the widely distributed and migratory (potamodromous) African teleost species, Bagrus docmak. Samples were acquired from five geographical locations in East Africa, within two major drainage basins; the Albertine Rift and Lake Victoria Basin. Individuals (N = 175) were genotyped at 12 microsatellite loci and 93 individuals sequenced at the mitochondrial DNA control region. Results suggested populations from Lakes Edward and Victoria had undergone a severe historic bottleneck resulting in very low nucleotide diversity (π = 0.004 and 0.006 respectively) and negatively significant Fu values (-3.769 and-5.049, at P < 0.05). High genetic structuring between drainages was detected at both historical (mtDNA ɸST = 0.62, P = 0.000) and contemporary (microsatellite FST = 0.46, P = 0.000) levels. Patterns of low genetic diversity and strong population structure revealed are consistent with speciation patterns that have been linked to the complex biogeography of East Africa, suggesting that these biogeographical features have operated as both macro- and micro-evolutionary forces in the formation of the East African teleost fauna.

Thirdly, in order to understand the population genetic structure of Nile perch, an iconic species of high commercial importance, both in the species' native range and where it has been translocated, Nile perch tissue samples were acquired from two West (Senegal River and Lake Kainji on the Niger River) and four East African (Lakes Albert, Kyoga, Victoria and Turkana) locations. Nineteen polymorphic microsatellite loci were used to study the genetic variation among populations across regions (West and East Africa), as well as between native and introduced populations within East Africa. Results revealed strong and significant genetic structuring among populations across the sampled distribution (divergence across regions, FCT = 0.26, P =.0.000). STRUCTURE analysis at a broad scale revealed K.=.2 clusters, whereby Nile perch from West Africa were assigned to one genetic cluster, while all individuals from East Africa regardless of whether native or introduced populations were assigned to another genetic cluster. Analyses at a regional scale revealed further structuring of up to K = 3 genetic clusters in East African Nile perch. Lower genetic diversity based on analysis of allelic richness (AR) was observed for the two translocated populations of Lake Kyoga (AR = 3.61) and Lake Victoria (AR = 3.52), compared to Nile perch populations from their putative parental populations of Lakes Albert (AR = 4.12,) and Turkana (AR = 4.43). The lower genetic diversity in the translocated populations may be an indication of previous bottlenecks and may also indicate a difficulty for these populations to persist and adapt to climatic changes and anthropogenic pressures that are currently present in the East African region. On the contrary, except for Nile perch from Lake Turkana, the Nile perch populations examined indicated signs of homozygote excess with positive and significant FIS values (P < 0.05), a critical finding useful in identifying genetically diverse aquaculture foundational stocks. Finally, the distinct genetic clusters identified in the current study between the West and East African Nile perch have been maintained by presence of biogeographic barriers and restricted gene flow between the two regions and, as such, the two genetic groupings should be possibly managed separately as two fishery stocks.

Lastly, the biogeographic relationships of a congener catfish, B. bayad, among drainages of Lake Albert in East Africa, Lake Kainji on the Niger River and the Senegal River in West Africa were also explored in the current study. Present and historical connectivity of B. bayad from these three drainages were investigated using 223 bp of the mitochondrial DNA d-loop region and nine polymorphic microsatellites in order to define management and conservation units for the species. Mitochondrial DNA via haplotype networks and phylogenetic tree analysis revealed two haplotypic clades, whereby the West African populations were divergent from the East African population. Overall, haplotype diversity (Hd ± SD = 0.87 ± 0.03) was high across all sampled B. bayad individuals. Comparably higher genetic diversity was observed in the B. bayad individuals from Lakes Albert and Kainji, whilst the lowest diversity was from those individuals sampled from the Senegal River (Hd ± SD = 0.27 ± 0.11). Bayesian analyses using nine microsatellites identified three genetic clusters (K = 3), grouping B .bayad by drainage. Thus, whereas the mitochondrial results highlight the existence of two evolutionary significant units, the microsatellite data seems to resolve the stock structure of the species into three contemporary genetic groupings. Therefore, based on these findings, three fishery management units are recommended to take into account the three genetic populations that appear to correspond to the drainages under study. Separate management units for identified genetic groupings will be important in drawing strategies specific to each drainage system, as varying levels of genetic diversity were also identified.

Overall this thesis provides the first comprehensive set of species-specific genomic resources developed for the freshwater African bagrids (B. docmak and B. bayad) and the Nile Perch, L. niloticus. Using the genomic resources developed, the three freshwater species examined, showed strong phylogeographic and genetic structure patterns that enabled the successful identification of management units (MUs). The identification of these management units will be useful in the formulation of future conservation strategies and identification of stocks suitable for aquaculture development for these species. The molecular data generated herein is central to the management of freshwater fisheries in Africa, especially West and East Africa (that have been identified each as a unique genetic group) and contributes to the understanding of microevolutionary forces in shaping the evolution of the African freshwater fish fauna.

Item ID: 49871
Item Type: Thesis (PhD)
Keywords: aquaculture, Bagrus bayad, Bagrus docmak, Bagrus, biogeography, catfish, commercial fish species, fisheries management, freshwater fisheries, freshwater fishes, genetic clusters, genetic structure, genetics, geographical distribution, Great Lakes Region, microevolution, Nile perch, Semutundu
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Publications arising from this thesis are available from the Related URLs field. The publications are:

Chapter 2: Basiita, Rose K., Zenger, Kyall R., Mwanja, Matthew T., and Jerry, Dean R. (2015) Development of genome-wide microsatellite genetic resources in a commercially important African freshwater fish species – the Nile perch, Lates niloticus. Animal Genetics, 46 (3). p. 340.

Chapter 3: Basiita, Rose Komugisha, Zenger, Kyall Richard, and Jerry, Dean Robert (2017) Populations genetically rifting within a complex geological system: the case of strong structure and low genetic diversity in the migratory freshwater catfish, Bagrus docmak, in East Africa. Ecology and Evolution. pp. 1-16. (In Press)

Date Deposited: 15 Aug 2017 02:39
FoR Codes: 07 AGRICULTURAL AND VETERINARY SCIENCES > 0704 Fisheries Sciences > 070401 Aquaculture @ 60%
07 AGRICULTURAL AND VETERINARY SCIENCES > 0704 Fisheries Sciences > 070403 Fisheries Management @ 40%
SEO Codes: 83 ANIMAL PRODUCTION AND ANIMAL PRIMARY PRODUCTS > 8301 Fisheries - Aquaculture > 830102 Aquaculture Fin Fish (excl. Tuna) @ 100%
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