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The Effects of Species Biology, Riverine Architecture and Flow Regime upon Patterns of Genetic Diversity and Gene Flow in Three Species of Northern Australian Freshwater Fish Author Huey, Joel Anthony Published 2008 Thesis Type Thesis (PhD Doctorate) School School of Environment DOI https://doi.org/10.25904/1912/2398 Copyright Statement The author owns the copyright in this thesis, unless stated otherwise. Downloaded from http://hdl.handle.net/10072/366611 Griffith Research Online https://research-repository.griffith.edu.au The effects of species biology, riverine architecture and flow regime upon patterns of genetic diversity and gene flow in three species of northern Australian freshwater fish. Joel Anthony Huey, B Env Sci (Hons) Griffith School of Environment Australian Rivers Institute Griffith University Submitted in fulfilment of the requirements of the degree of Doctor of Philosophy December, 2007 “Well, if I was a catfish, mama, I said, swimmin’ deep down in deep blue sea. Have these gals now, sweet mama, Sittin’ out, sittin’ out, folks, for poor me; Sittin’ out, folks, for poor me; Sittin’ out, folks, for poor me; Sittin’ out, folks, for me; Sittin’ out, folks, for me; Sittin’ out, folks, for me.” Catfish Blues - Robert Petway (1941) Synopsis Understanding patterns of dispersal, the movement of individuals or propagules, among populations of riverine species is imperative to their management and conservation. However, directly estimating dispersal can often be difficult. Therefore, estimates of gene flow, the movement of genes, are often used to infer dispersal among natural populations. In riverine species, gene flow is determined by species biology, riverine architecture and flow regime. While many studies investigate the role of species dispersive strategies by comparing patterns of genetic structure in different species across the same geographic range, few also attempt to investigate the role of the non-biotic influences on gene flow in a comparative manner. Instead, studies regarding landscape processes (river architecture and hydrology) are based upon observations in a single riverine environment and not compared to other catchments that may differ in riverine architecture or hydrology. This study attempts to investigate all three factors influencing gene flow and genetic diversity using a comparative approach. This is done by contrasting two species of freshwater fish in two riverine systems that differ in their hydrological and structural makeup. By comparing patterns of genetic structure for each fish species, the role of species biology (behavioural and physical adaptations) can be explored. Then, by comparing patterns of genetic structure for each species, between riverine systems that differ in their landscape processes, the role of hydrology and riverine architecture in determining genetic structure can be explored. This study employed three different genetic markers to elucidate patterns of genetic structure and genetic diversity. These were, direct sequencing and screening of the control region of the mitochondrial DNA genome, microsatellite loci and allozymes. The two systems used in this study were the Lake Eyre Basin of central Australia and the Gulf of Carpentaria Basin of northern Australia. The catchments of the Lake Eyre Basin are typical dryland systems, exhibiting low catchment relief, refugial waterholes, and highly variable hydrological inputs causing infrequent and widespread flooding. This contrasts with catchments in the Gulf of Carpentaria Basin, which are architecturally diverse and experience large monsoonal inputs that are seasonally predictable. It was hypothesised that the differing landscape processes (riverine architecture and flow regimes) in these two systems would differentially influence i patterns of genetic structure in freshwater fish, generating different patterns in each system. Three freshwater fish species were used as model taxa in this study. Neosilurus hyrtlii is an abundant and widespread freshwater catfish species, found across northern Australia, some central Australian catchments, and parts of eastern Queensland. Believed to be a strong disperser, N. hyrtlii was expected to exhibit low levels of genetic structure among populations within catchments. Alternatively, members of the genus Ambassisdae are geographically more restricted, and believed to be weaker dispersers. Two species were used in this study, Ambassis sp. and Ambassis macleayi. Ambassis sp. was used to represent the arid-zone rivers of the Lake Eyre Basin, while A. macleayi represented the Gulf of Carpentaria Basin. Both of these species were expected to exhibit higher levels of genetic structure than N. hyrtlii, based upon breeding and behavioural strategies. Within the Lake Eyre Basin, N. hyrtlii exhibited weak genetic structure within catchments, indicative of high levels of gene flow and strong dispersal ability. This contrasted with Ambassis sp., which revealed moderate genetic structure within catchments, suggesting that this species does not exploit flood events to the same extent as N. hyrtlii. Similarly, patterns of genetic structure among catchments revealed very different evolutionary histories. While both species exhibited restricted contemporary gene flow among catchments, N. hyrtlii revealed recent divergence among catchments, with estimates overlapping with the proposed drying of Lake Eyre, approximately 60,000 years ago. In contrast, Ambassis sp. exhibited a complicated evolutionary history, with two divergent clades detected in different catchments. These clades (4.2% divergent at mtDNA) were assumed to represent separate colonisation events from the Gulf of Carpentaria. Sampling of N. hyrtlii across the Gulf of Carpentaria Basin was poor, making estimates of genetic structure within catchments unfeasible. However, for A. macleayi, strong genetic structure was detected among populations within catchments, indicative of poor dispersal ability. Both species displayed restricted gene flow among catchments. However, again they displayed very different evolutionary histories. For N. hyrtlii, divergence among catchments was older than predictions based upon the ii presence of a large freshwater lake in the Gulf of Carpentaria during lower sea levels. This lake is believed to have been fresh until approximately 10,000 years ago. For A. macleayi, estimates of divergence between catchments were even older than that predicted for N. hyrtlii. Also, a catchment in the Gulf or Carpentaria displayed some evidence for a drainage rearrangement, with two divergent clades existing in different rivers of the same catchment. When results were compared for N. hyrtlii and Ambassis spp., between the Lake Eyre and Gulf of Carpentaria catchments, two striking results were uncovered. Firstly, using mtDNA and microsatellites, genetic diversity negatively correlated with the coefficient of variation of the mean annual flow. This suggested that in catchments that experienced extreme flow variability, populations of N. hyrtlii were experiencing frequent population bottlenecks and local extinctions and recolonisations. This would act to reduce the effective population size (Ne), and generate much reduced genetic diversity. The same pattern was not observed in Ambassis spp., possibly due to their habit of remaining in refugial waterholes during floods, or basic differences in biology for each species in each catchment. Also, for Ambassis spp., much stronger genetic structure was detected among populations within catchments in the Gulf of Carpentaria compared to the Lake Eyre Basin. Again, this was suggested to have been due to differing landscape processes in each basin, or basic differences in biology for each species. These results and inferences highlights the complex interaction between species biology, riverine architecture and flow regime in determining population processes in freshwater fish taxa. From a management perspective, these results also emphasize the need for comprehensive genetic surveys of riverine species and regions before developing conservation strategies for species and catchments. If the management strategy for a species is based upon research on a different species, or from the same species in a different region, erroneous assumptions may be made about species dispersal ability or effective population size, possibly having serious consequences. iii Acknowledgements Professor Jane Hughes was a source of considerable assistance, motivation, assurance and critical assessment. Jane always managed to be available when needed for a quick chat or major disaster. Ultimately, this project would have required much more time and involved many more catastrophes without Jane’s experienced involvement. My secondary supervisor, Dr. Andrew Baker engaged me in many awareness raising philosophical and scientific conversations. Andrew provided many comments on the multitude of drafts that I sent him, generating a final product that was better than if he hadn’t been involved. Ultimately, Andrew made me think about science, and why we do it. My wife and best friend Simone was my unflinching support. Despite many late nights, weekends and field trips, she still gave me reassurance and encouragement. This made it possible to keep motivated when times where tough. In the process of collecting samples, I had many people lend a helping hand. Most importantly, James Fawcett, with whom I shared my field trips, provided help, guidance, distraction, and many a laugh. He never left me behind in a waterhole, despite