School of BioSciences - Theses
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ItemMove it or lose it: how and when to use targeted gene flow( 2023-04)A myriad of threats are currently assailing threatened and soon to be threatened populations. Habitat removal, climate change, wildlife disease and the invasion of non-native species are all placing increased pressure on the systems we undervalue for their role in providing clean air, water, carbon sequestration and natural beauty. Many populations, however, contain individuals expressing traits that enable them to survive and reproduce even in the presence of these existential threats. Unfortunately, many of these adaptive traits are rare in endangered populations. But useful variation in traits doesn't only occur within populations: geographic trait variation is ubiquitous and can arise from a number of different processes, including natural selection, spatial sorting, and drift. Natural selection allows populations to adapt to local environmental conditions and can lead to locally adapted variants. Spatial sorting, the spatial analogue to natural selection, can also lead to predictable geographic variation in traits across space, as invasion and recolonisation select for increased dispersal. Both of these forms of selection result in predictable trait variation that conservation biologists can harness to promote conservation benefits. Geographic variation might also arise through drift, but such variation is much less predictable. Once geographic variation exists, it is possible to harness such variation to affect conservation goals. This idea -- targeted gene flow -- has the objective of identifying and harnessing geographic trait variation to promote conservation benefit. Current work on targeted gene flow has focused on understanding how species respond to certain threats and on exploring the use of targeted gene flow to boost adaptive potential in threatened populations. In this thesis, I explore the utility of applying targeted gene flow to two different conservation problems: i) can targeted gene flow be deployed to facilitate evolutionary rescue in response to rapid (and flexible) environmental change? and ii) can targeted gene flow be deployed to directly mitigate a threatening process? To answer these questions, I use a blend of field studies and simulation models focused on the introduced pest, the Cane Toad (Rhinella marina). This thesis starts by providing the reader with background information and current applications of targeted gene flow, as well as identifying and framing the need for novel measures to reduce the impacts of cane toads in Australia. To explore this use case, we first need to understand how to apply targeted gene flow in an optimal fashion, as well as how to measure any benefits. In the opening data chapter of my thesis, I set out to understand how to optimally deploy targeted gene flow and build upon initial work in this area to examine how targeted gene flow should be deployed against differing threat profiles. I find that the optimal timing and size of a targeted gene flow action is highly sensitive to the maximum rate of change of the threat across time, and that if conducted correctly, targeted gene flow can provide enough adaptive potential to stave off extinction whilst retaining almost all of the genetic diversity of the population under threat. This measure, the expected benefit, is a novel metric to benchmark the effectiveness of targeted gene flow applications. In the subsequent chapters of this thesis, I extend the notion of targeted gene flow to a different context: reducing the dispersal ability of invasive species. Cane toads are one of the most harmful introduced species in Australia. Decades of sustained investment in cane toad control, research and management has unearthed a number of effective strategies for the local control of cane toad populations, but no landscape level solution currently exists. In chapter three, I quantify the financial benefit of keeping areas toad-free. I conduct field studies to generate estimates of toad density and detectability, before combining these with removal and cost models to provide an estimate of the value of cane toad quarantine across offshore islands as well as a potential toad-free haven on the mainland: the Pilbara region of Western Australia. My final chapter explores how targeted gene flow can be deployed to increase the effectiveness of a landscape barrier designed to contain the toad invasion and so create a toad-free haven over 265,000 km2 of the Australian mainland. This chapter provides the first case study of how targeted gene flow can be deployed to directly mitigate a threatening process. In doing so, I provide the first evidence that targeted gene flow can be used to directly reduce the negative impacts of an invasive species, through driving down their dispersal ability, and in doing so render landscape barriers substantially more effective. This thesis shares the process of exploring a new application of targeted gene flow, from theoretical conception to an applied trial. I provide the first evidence that targeted gene flow can be used to reduce the ability of an invasive species to move across the landscape, alongside extensions to the current framework surrounding how to optimally implement targeted gene flow to aid threatened populations. The resulting strategies are not limited to the impacts of cane toads but instead have application to a wide range of conservation scenarios. Generally, my thesis develops the under-appreciated idea that, by being creative with geographic trait variation, we have a powerful and cost-effective tool for conserving biodiversity.
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ItemLight manipulation by Christmas beetles: quantification, mechanisms and ecological relevance( 2022)The brilliant and colourful appearances of Christmas beetles (Scarabeidae - Rutelinae) are famous for decorating eucalyptus trees during the Australian summer. Millions of years of evolution perfected the design of their hardened fore wings (elytra) to manipulate light and create striking optical effects. However, little is known about the exact underlying nanostructures or the ecological variables driving their evolution. Despite the recent increase in biophotonics studies, this remains the case for many organisms with striking colourful appearances. By studying light manipulation in Christmas beetles, I aim to develop methods and concepts generalisable to other organisms. Christmas beetles produce a wide variety of optical effects including saturated colours, black, and pearlescent white. Some species look mirror-like and metallic gold or brass. Moreover, these colours change with the viewing or illumination angle. Christmas beetles can also interact with long wavelengths outside of the human-visible spectrum, in the near-infrared (NIR), and reflect circularly polarised light, which makes them appear as different colours through the right and left lenses of 3D cinema glasses. To better understand this diversity, I proposed a method for its quantification, studied some of its underlying mechanisms and tested if it can be explained by ecological differences. To characterise the beetles’ optical effects, I proposed a generalization of existing spectroscopy methods and parameters to describe reflection profiles across the visible and NIR spectrum, regardless of their underlying mechanism. Ultimately these methods break down complex optical effects into simpler traits and can facilitate comparison between studies. The proposed terminology attempts to conceptually unify disparate fields (biology and optics) and allows a clear distinction with terms used to describe colour perception. To study the optical mechanisms in Christmas beetles, I analysed the architecture of their elytra. I discovered that unlike scarab beetles studied to date, three different Christmas beetle species use multicomponent photonic systems, with an upper layer acting as a green pigment-based filter and an underlaying broadband reflector, that particularly enhances NIR reflectance. For beetles with spiral nanostructures, I found a trade-off between polarisation and NIR reflectance. This diversity of photonic structures shows that beetles are a promising model for understanding complex optical properties of natural materials. To investigate ecological correlates of the optical effects in Christmas beetles, I used a biophysical essay and a phylogenetic comparative analysis. High reflectance reduced heating of the beetle elytra under controlled conditions, but I did not find any evidence that highly reflective species occur in hotter environments. Christmas beetles do not follow a simple eco-geographical pattern, possibly because their optical effects respond to species-specific combinations of environmental challenges. I demonstrated that diversity in optical effects and photonic mechanisms is more than meets the eye, even for a small group such as Christmas beetles. My thesis highlights the value of a cross-disciplinary approach where optical methods can spark stimulating biological questions and the comparative study of phylogenetically related species can inform species selection for photonics studies. The resulting conversation between the two disciplines accelerates progress in the search for the biological function of striking optical effects.
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ItemThe evolution of salmon lice (Lepeophtheirus salmonis) in response to parasite management strategies in salmon aquaculture( 2022)Parasites, pathogens and other pests have a major impact on global agriculture. Pest populations are able to adapt to novel selection pressures on farms, making long-term pest management a challenge. This is exemplified by the repeated evolution of pesticide resistance over the last century. Resistance can be slowed or avoided by applying evolutionary principles to pest management. This first requires understanding the evolutionary dynamics of the pest under contemporary farming conditions. Such knowledge is especially needed in rapidly emerging and changing farm systems, such as aquaculture. Salmon farming – among the biggest aquaculture industries – is significantly affected by parasitic sea lice (especially the salmon louse Lepeophtheirus salmonis). Efforts to control this parasite have been undermined by salmon lice evolving resistance to most chemical pesticides. An abundance of non-chemical technologies have been introduced as alternatives, but there has been little research into whether they may also drive louse evolution. This thesis explores the potential for L. salmonis to adapt to the pressures faced in salmon aquaculture today; in particular, possible resistance to non-chemical management strategies. Chapter 1 outlines the need for evolutionary perspectives in pest management, and provides an overview of the thesis. In Chapter 2, I review the literature and conclude that salmon lice could, theoretically, adapt to non-chemical methods. This chapter explores how non-chemical resistance might arise, how it might have ripple effects on wild salmon, and how it could be prevented using evolutionarily-enlightened pest management. Chapters 3 and 4 focus on one non-chemical strategy: using physical barriers to prevent lice from entering salmon cages. In Chapter 3 I describe an empirical study that identified significant inter-family variation in louse swimming behaviour, with some families preferring deeper water than others. Chapter 4 addresses whether preventative cage barriers could impose selection on this behaviour, by inadvertently allowing deeper-swimming lice to pass underneath barriers to infest salmon. This was tested using a particle-tracking model, which predicted strong directional selection on swimming behaviour. Taken together, Chapters 3 and 4 offer the first evidence that lice could adapt to physical barriers. Chapter 5 describes a metapopulation model designed to predict evolutionary dynamics of lice across the larger, interconnected farm network. This model will be a versatile tool for future research exploring how various management regimes could limit the spread of resistance through the population. Finally, Chapter 6 ties the threads of this thesis together into a research framework that can be applied to the wider aquaculture sector to assist with managing resistance. This thesis combines theoretical, empirical and modelling techniques to predict the trajectory of L. salmonis evolution in response to different pest management strategies. Key areas for future study are highlighted – more research is crucial if the salmon industry wishes to find ways to stymie louse resistance. More broadly, this thesis illustrates that pests can adapt to management strategies – especially non-chemical methods – in surprising ways. By looking at the world from the parasite’s point of view, we can discover new techniques for safeguarding farms against undesirable evolutionary processes.
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ItemTrawling for the unknown: An investigation of the impacts of harvest and oceanic warming on the life-histories of fish( 2021)Fishing is globally important as humans rely on fish for 17% of their total protein intake and millions of people are directly or indirectly dependent on fisheries as a source of income. Fisheries harvests do, however, impose a number of impacts on fish populations. Harvest can cause demographic truncation (loss of large and old individuals), as well as reducing the reproductive capacity of populations and modify ecological interactions. Furthermore, fishing is inherently size-selective, where the preferential catch of certain phenotypes using different gears can combine with relatively high rates of fishing mortality to drive potentially rapid evolutionary responses in populations (called fisheries induced evolution or ‘FIE’). As a result of fishing, many harvested stocks are expressing a faster ‘pace-of-life’, characterised by faster growth, earlier maturation, and increased relative reproductive investment. Concurrent to fishing activity, the world’s oceans are warming at unprecedented rates which is having significant impact on the physical environment experienced by fish. Importantly, warming is thought to drive a similar increase in the pace-of-life expressed by fish via direct physiological and indirect temperature-dependent processes. This can be seen in almost ubiquitous shifts to faster growth, earlier maturity and smaller adult size, a phenomenon called the temperature size rule (TSR). Warming is also impacting fish populations through factors such as increased mortality, range shifts and increased incidence of hypoxic conditions. Our understanding of how the effects of harvest and warming may combine to impact on fishes, and influence their subsequent recovery after initial impact, is poor. An improved understanding of the combined impacts of fishing and warming oceans and the mechanisms underpinning these, as well as heuristic, cost effective ‘monitoring’ tools are needed if we are to properly manage fish stocks into the future. In this thesis, I tested a recently published biphasic growth model that attempts to estimate age at maturity from commonly collected size-at-age data (Chapter 2). Statistical techniques such as these could be utilised as cost and time-effective fishery monitoring tools. I used data from multiple North Sea stocks to parameterise the biphasic model and found that the method performed poorly given the data. This poor performance was primarily due to the lack of temporal continuity and representation of older individuals which decreased the ability of the technique to model growth and thus estimate maturity. I suggest that future fisheries monitoring should include improved data collection across all age and size classes so that we can adequately utilise potentially cost-effective statistical techniques to estimate key life-history parameters. I then ran a multi-generational selection experiment that applied interactive treatments of warming (26 C ‘control’ and 30 C ‘warmed’) and realistic fisheries selection (random harvest ‘control’, ‘sigmoidal’ and ‘Gaussian’ selection) to 18 populations of the tropical freshwater zebrafish (Danio rerio). My sigmoidal treatment was designed to mimic trawl fisheries, where the largest individuals are harvested, and my Gaussian selection treatment simulated gillnet or slot limited fishing, where the midrange of sizes were affected by fishing. Selection was applied to six generations, where I followed responses across these ‘F’ generations as well as two common garden generations where selection was relaxed. Studying responses under common garden conditions reveals information as to the nature of responses, where plastic, maternal and evolutionary processes can be teased apart. In Chapter 3, I tracked the expression of early life-history traits in populations exposed to fishing and warming and found that recruitment collapsed after four generations of warming treatment. Moreover, temperature interacted with fishing such that sigmoidal harvested populations had the lowest recruitment rate. This interaction indicates that the removal of large fish individuals through harvesting can exacerbate warming-induced recruitment collapse. Preserving size diversity in fish populations is important to help increase the resilience of fisheries to the impacts of warming. In Chapter 4, I tested two alternative explanations of the temperature size rule (TSR), which describes the phenomena of increased juvenile growth, early maturity and smaller adult sizes at higher temperatures in ectotherms. Debate centres around whether TSR is the result of warming-induced physiological constraints on growing to larger sizes, or an adaptive outcome stemming from temperature-induced energy allocations. I found evidence that the metabolic rates of fish held at elevated temperatures acclimated after three generations. This result indicates that the commonly proposed physiological limitation mechanism could not solely explain TSR. Instead, I found evidence that populations adjusted reproductive investment via earlier maturation and higher early investment in reproduction, suggesting that TSR could be explained by shifts in resource allocation. These results have implications for models used to predict warming impacts in our oceans. Finally, I analysed trends in the expression of multiple juvenile and adult life-history traits through generations (Chapter 5). Here I found that warming and sigmoidal fishing treatments led to the largest reductions in adult body sizes. In contrast, fisheries selectivity that preserved large individuals allowed warmed population to maintain body sizes similar to those in the control temperatures. Temperature impacts on life-history traits recovered rapidly in common garden generations, whereas the legacy of fisheries selection remained. These findings suggest that even five generations of realistic fishing pressure can have long term impacts on populations, affecting their response to management interventions. Together, my work advances our understanding of how harvested populations respond to significant contemporary and future stressors and provides valuable insights into the future sustainable management of fisheries resources.