Theses - Zoology

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    Open Access
    Comparative ecology of the endemic Cyprus Warbler and the congeneric Sardinian Warbler: Implications of recent coexistence
    Jones, Victoria Ruth
    In 1992 the Sardinian Warbler was first recorded breeding in Cyprus. Since then, survey results from Paphos District suggest that the endemic Cyprus Warbler population has declined, while the Sardinian Warbler breeding population has increased and expanded in Paphos District. Colour-ringed Cyprus and Sardinian Warblers were observed during 2003 to 2005 breeding seasons on seven scrub study plots located across Paphos District. Both species appeared to establish home-ranges without reference to the other species, resulting in considerable interspecific home-range overlap. A playback experiment indicated that Cyprus Warblers reacted equally strongly to conspecific and congeneric song in areas where the two species coexist, but less strongly to congeneric than conspecific song in areas where Sardinian Warblers did not yet breed. The vegetation composition of Cyprus and Sardinian Warbler home-ranges was very similar. There was no indication that the species competed for nest sites. Cyprus and Sardinian Warbler have similar breeding biology; they laid similar sized first clutches and had similar chick output per pair for first nesting attempts. However Sardinian Warblers had a higher frequency of second nesting attempts and this resulted in a higher chick output per pair per year than was achieved by Cyprus Warblers. In both species total chick output per year was higher for pairs that nested early. Nest survival was similar for the two species. Cyprus and Sardinian Warbler diets were very similar. Body condition of both species’ chicks was higher earlier in the breeding season. Cyprus Warblers had higher productivity but lower chick body condition in the zone where their population has declined than in the zone with fewest breeding Sardinian Warblers. Productivity was positively related to arthropod biomass available on different plots for Sardinian Warbler, but not for Cyprus Warbler. There was no evidence of a negative impact of either species on the number or condition of nestlings produced by the congener.
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    Open Access
    A comparison of the costs of delivering conservation through land sharing and land sparing
    Collas, Lydia
    Globally, drastic biodiversity declines and the worsening climate crisis demand overhaul of existing land use policies which have failed to reconcile food production and environmental conservation. In Europe, most existing policies compensate farmers to voluntarily implement land-sharing measures, commonly referred to as wildlife-friendly farming, which seeks to deliver conservation benefits on the farmed land through agri-environment schemes (AES) offering a fixed price per hectare. Investment into sharing has continued despite the accumulation of evidence showing that, for the same amount of lost food production, substantially more would be delivered for conservation and climate change mitigation with the contrasting approach of land sparing, where high-yield farming allows large areas to be spared elsewhere in the landscape as (semi-)natural habitat. Following Brexit, the UK has the opportunity to rethink this approach; but until now policy decisions have had to be made without estimates of the relative taxpayer costs of using sharing and sparing to deliver target conservation outcomes. Addressing this critical research gap was the primary aim of this thesis, as follows. In this thesis, I sought to uncover the taxpayer and food production costs of delivering meaningful conservation outcomes with land sharing and sparing. First, I conducted a novel comparison of the costs of monitoring sharing and sparing schemes for compliance and effectiveness. Monitoring is a fundamental, though often overlooked, taxpayer cost. In terms of effectiveness monitoring, I found current monitoring levels to be insufficient to precisely determine the effects on wild species of sharing schemes; in contrast, the same effort could deliver relatively precise estimates of the much larger effects of sparing. Furthermore, turning to compliance monitoring, I found the cost-effectiveness of existing English AES could be vastly improved with more compliance monitoring; however, this may be politically unpopular with farmers. It is therefore notable that I also found relatively less money was wasted when monitoring sparing at a sub-optimal rate compared to sharing. Second, I used a discrete choice experiment involving 118 arable farmers to establish their willingness to accept (WTA) payment to participate in sharing and sparing schemes that delivered the same biodiversity and carbon outcomes. I found that all but the most farmland-tolerant outcomes were delivered at less taxpayer expense with sparing. Third, combining this assessment of farmer WTA with knowledge of how much schemes must be monitored, I compared the taxpayer costs of delivering the same environmental outcomes with fixed-price sharing and sparing schemes which paid all recruits at the WTA of the least-willing farmer required in the scheme to deliver the target outcome. I found that sparing delivered the same outcomes at less than half the taxpayer cost of sharing; and, importantly, sparing saw only 79% of the food production lost under sharing. Fourth, I examined the distribution of farmer stated WTA, finding that variation in responses was mostly driven by factors other than lost gross margin. Given marked inter-farmer variation in their stated WTA, variable-price schemes, which pay farmers their stated WTA rather than the rate required by the least-willing participant, offered savings to both sharing and sparing schemes. However, even under variable pricing, sharing was not cheaper than sparing in delivering our more farmland-sensitive outcomes. Finally, I examined whether a land-purchase strategy, where the government purchases land and then contracts organisations to manage and create habitat on it, would deliver sparing at less expense than a farm-subsidy approach. I found land purchase was more cost effective than the farm-subsidy approach if long timeframes, low discount rates and large budgets were considered; however the impacts on farming communities of largescale ownership changes warrant further consideration. To conclude, I found overwhelming evidence for UK arable farming that land sparing can deliver biodiversity and carbon outcomes at substantially lower cost than land sharing both in terms of taxpayer costs and lost food production. The relative costs of sharing would increase even more with consideration of species that do not tolerate farmland, in a country with a shorter history of agriculture where fewer habitat specialists have gone extinct compared the UK, and if the production required elsewhere to compensate greater volume of food production lost under sharing was taken into account. Furthermore, the effects of sharing may be near-impossible to precisely determine with current monitoring efforts and continued sub-optimal compliance monitoring would increase the costs of sharing-like options relatively more than the more sparing-like options of existing AES. Whilst variable pricing and land purchase may further reduce the costs of sparing, the costs of delivering meaningful environmental outcomes are most substantially reduced by pursuing a land-sparing, rather than land-sharing, approach. This work is of considerable significance to the UK government, given that prevailing land-sharing policy approaches can at best deliver less than half the environmental outcomes delivered by the same budget spent on land sparing.
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    Embargo
    Ancient origins of the chordate forebrain: Conserved patterning of the anterior neuroectoderm in amphioxus
    Gattoni, Giacomo
    While the general organization of the chordate central nervous system (CNS) is highly conserved and consists of a dorsal neural tube with an anterior brain, the evolutionary origin of this key aspect of the chordate body plan remains obscure. In recent years, a conserved anterior gene regulatory network (aGRN) has been shown to pattern the larval anterior nervous system of several invertebrates, including the two non-chordate deuterostome phyla (echinoderms and hemichordates), in which the aGRN controls the development of the apical organ. Although clear homologs of the apical organ are not present in chordates, most aGRN genes are expressed in the vertebrate forebrain. In this PhD thesis I trace the evolution of the aGRN across deuterostomes using the cephalochordate amphioxus as the main model organism. I first show that during amphioxus development aGRN genes are expressed in a similar pattern to the one found in echinoderms and hemichordates, are regulated by Wnt/b-catenin signalling and are active in the anterior neuroectoderm that forms the larval brain. As a comparative system, I also characterize the development of the apical organ in an understudied group of echinoderms, the crinoids. To follow the fate of the amphioxus anterior neuroectoderm, I next investigate neurogenesis, proliferation and cell type differentiation in larval and adult brains. I demonstrate the presence of a hypothalamic-like region in the anterior cerebral vesicle, which derives from the region where the aGRN is active during development. Finally, I explore how changes in the specification of the body axes and in the expression of one of the upstream aGRN genes, FoxQ2, might have underlined the evolution of the complex vertebrate brain. Taken together, the results presented in this thesis support the conservation across deuterostome evolution of an aGRN that controls the development of the anterior neuroectoderm. In the chordate lineage, the network was integrated to the neurulation program to specify retinal and hypothalamic areas of the forebrain. Furthermore, this work provides a comprehensive characterization of neuroarchitecture and cell type composition across the amphioxus life cycle, facilitating the comparison with other chordate taxa to reconstruct the evolution of the chordate nervous system.
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    Open Access
    The genomics of adaptive colouration in Hypolimnas butterflies and the wood tiger moth, Arctia plantaginis
    Farré I Orteu, Anna; Farré I Orteu, Anna [0000-0002-3911-0747]
    Wing phenotypes in butterflies and moths are a striking example of adaptive evolution and are a tractable trait to dissect the genetic mechanisms underlying adaptations. Studies of Lepidoptera, mainly mimetic species from the tropics, have led to two general patterns. First, a limited set of genes have been re-used multiple times in controlling the evolution of wing phenotypes, and second, structural variation often underlies such traits. Clarifying the generality of these two patterns requires the dissection of the genetic architecture of wing phenotypes in a wider variety of species. In this thesis, I explore the genetic basis of wing mimicry in Hypolimnas butterflies and of aposematism in the wood tiger moth using a range of genomics and transcriptomics methods. First, I produce genome assemblies of two Hypolimnas species and investigate the evolution of W chromosomes in Lepidoptera. By comparing the H. misippus genome assembly to multiple Lepidoptera species, I provide evidence that suggests that the W chromosome has a shared origin across the Lepidoptera. Second, I identify the genetic basis of forewing mimicry in H. misippus using a dataset of 335 individuals sequenced using haplotagging, a linked read sequencing technique. To analyse these data, I develop a method called Wrath for the visualisation and exploration of candidate structural variants. I find that transposable element insertions are associated with forewing phenotype and present evidence for the usefulness of Wrath to explore haplotagging data. Third, I examine the evolution of mimicry in the Hypolimnas genus by identifying and comparing the genetic basis of wing phenotypes in H. misippus and H. bolina. Using a dataset of 214 whole genome sequences of H. bolina individuals together with my H. misippus data, I show that cortex, a gene involved in wing colour in many Lepidoptera, is the most likely candidate for the control of white colour elements in the two species. Furthermore, I present evidence that the regulatory elements controlling the presence of hindwing white are likely not homologous between the two species. Additionally, I show that a region close to optix, another well-known colour gene, is associated with orange elements in H. bolina. Finally, I explore the genetic basis of a complex phenotype involving aposematism and behavioural and physiological traits in the wood tiger moth, Arctia plantaginis, and show that this trait is associated with the duplication of a yellow family gene. This work contributes to our understanding of the evolution of wing phenotypes in the Lepidoptera. Overall, my results highlight the importance of structural variation in the evolution of wing colouration while also emphasising the repeatability of the genetic basis of adaptive traits.
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    Open Access
    Phylogenetic inference using ancient environmental DNA
    De Sanctis, Bianca
    Ancient environmental DNA (aeDNA) has revolutionized our ability to describe and analyze biological communities in space and time by allowing for joint sequencing of entire ecosystems across thousands of years. However, because samples contain damaged, short fragments from multiple individuals or taxa, the field has been so far limited in its scope, and aeDNA has only been applied to population and phylogenetic studies in the last few years. In this thesis, I first build a theoretical coalescent framework to analyze error in supervised binning algorithms, which assign reads from environmental samples to individual taxa in a reference database. Under this framework, I determine the expected error rate under a wide range of parameters and the degradation in assignment accuracy as samples diverge from their closest reference sequence, and with incompleteness of reference sequences. Second, I describe a phylogenetic placement algorithm for non-recombining sequences such as mitochondria or chloroplast DNA, and apply this method to Mammuthus or mammoth and Equus or horse samples from an Arctic-wide aeDNA dataset spanning the last 50,000 years. This analysis demonstrates the potential existence of a previously undiscovered clade of mammoths, and extends the survival of an existing clade. Next, I report one of the first whole genome ancient environmental DNA studies, using DNA extracted from 14-16,000 year old cave soil with material from two closely related species, Ursus arctos or the American black bear and Arctodus simus or the extinct giant short-faced bear. By comparing the ancient sequence against a modern reference panel of black bears and a high-quality fossil giant short-faced bear reference, I infer evolutionary relationships between the Late Pleistocene populations and their modern relatives. Lastly, I molecularly date an ancient environmental Betula or birch tree chloroplast sequence from Northern Greenland, confirming that it was approximately 2 million years old, the oldest DNA to be successfully sequenced so far. All together, this work demonstrates the ability to infer phylogenies and population histories of individual taxa from ancient environmental DNA.
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    Embargo
    The Sea is the Limit: Foraging Ecology of Breeding Antarctic Procellariiformes
    Bentley, Lily
    In the dynamic marine environment, highly mobile predators are expected to select profitable foraging areas, especially when provisioning young in addition to meeting their own energy needs. Knowing how and where animals choose to forage is not only important to advance ecological theory, but also to assess and mitigate the impact of anthropogenic threats. In this thesis I examine the breeding-season foraging behaviour of several of the Procellariiformes, a wide-ranging, long-lived group of seabirds, many of which have experienced steep population declines since the mid-20th century. Advances in biologging technologies over the last four decades have made it possible not only to accurately track individual movements, but also to identify important behaviours at sea. In my first data chapter (Chapter 2), I combine data from multiple tag types to describe diving behaviour in three albatross species, and discuss the implications for both foraging ecology and bycatch susceptibility. Moving from foraging capability of the individual to foraging preferences at the level of genus, in Chapter 3 I analyse the divergent niches of a summer- and a winter- breeding species of Procellaria petrel. Here I compare the habitat preferences of Grey Petrels and White-chinned Petrels breeding at Gough Island and South Georgia, respectively. Using high-resolution remote sensing environmental data, I identify divergent foraging preferences in dynamic habitats. Finally, in Chapter 4, I compare habitat preferences and accessibility between the two species of Phoebetria albatrosses across six colonies. While most studies of habitat preference consider only a single species or site, here I investigate whether closely- related species inhabit the same ecological niche at sympatric and allopatric colonies throughout their range. I show that Light-mantled Albatrosses have a consistent foraging niche, whereas Sooty Albatrosses select different habitats in sympatry and allopatry. I then discuss the impact of interspecific competition on plasticity in habitat preferences in general. Overall, my thesis examines diverse aspects of seabird foraging ecology from the individual to community level, discusses habitat preferences (and their potential flexibility) in relation to species' evolutionary history and as drivers of community structure, and considers the implications for conservation planning.
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    Fossoriality In Snakes: Perspectives From Morphology And The Fossil Record
    Howard, Alexandra
    Snakes are a speciose clade of squamates that have diversified into almost all habitats, all with the same elongate limbless body plan. This thesis aims to improve scientific understanding of snake evolution by focusing on novel perspectives using both extant snakes and the fossil record. 1. Alternate phylogenetic positions of fossils affects body size estimates in snakes Body size is a readily available metric for both extant and extinct snakes. The competing hypothesis of ecological snake origins also predict different outcomes for the evolution of body size in snakes. I used a combination of ancestral state reconstructions, body size estimates of fossils from regression models, and evolutionary rate modelling to examine the evolution of body size in snakes, with a particular focus on early snake evolution. This project showed that snakes achieve a wide range of diversity of body size during the Cretaceous, trends that are not observed when using data from extant taxa. 2. Cranial osteology of Typhlopidae (Serpentes: Scolecophidia) Scolecophidia are a distinctive group of snakes that occupy the basal most diverging branches of the snake phylogeny. However, due to the small overall size of many taxa, they have been relatively understudied in regards to comparative anatomy. In this project I examined segmented CT scans of 10 different species of Typhlopoidea, the largest clade of Scolecophidia. Using these comparisons I identified variability in several morphological characters not previously thought to be variable in Scolecophidia, as well as the identification of features in large typhlopids such as the lateral wings of the basisphenoid, which were previously thought to be limited only to Alethinophidia. 3. Morphometrics provide evidence for the fossorial origin of snakes The problem of homoplasy, particularly in relation to adaptation to fossoriality, is potentially responsible for the incongruences between phylogenetic hypothesis of snakes that use either morphological or molecular data. In this project I used CT scans of 73 species of alethinophidian snake and geometric morphometrics to examine morphological correlates to fossoriality. I found that there is a clear morphological signal between the parietal of alethinophidian snakes and ecology. In general, the parietal of fossorial snakes is more elongate with a deep u or v shaped fronto-parietal suture, with an elongated posterior shelf that overlaps the braincase. These projects show how integrative research using both extant and palaeontological data can inform questions about the early evolution of clades, particularly the heavily debated ecological origin of snakes.
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    Open Access
    Tradeoffs and co-benefits among impacts of contrasting livestock systems
    Bartlett, Harriet; Bartlett, Harriet [0000-0002-7389-8785]
    Livestock farming generates some striking externalities; whilst it provides 30% of human dietary protein, it occupies 75% of agricultural land, emits 14-17% of anthropogenic greenhouse gas emissions, and uses more antimicrobials than human medicine. Demand for livestock products is high and rising, especially for pork which has quadrupled in the past 50 years. Livestock farming systems vary considerably in the scale of their externalities, but our understanding of how multiple externalities co-vary across contrasting production systems is limited. Research typically focuses on impacts in isolation, and the synergies or tradeoffs among them are assumed. To identify and promote the types of systems that best limit impacts or even carry co-benefits we need to explicitly consider multiple externalities and evaluate them across a wide range of alternative production systems. The main aim of my thesis was to do this for pig production. I recruited, visited, and evaluated over 100 pig farms in the UK and Brazil from those considered to be the most “intensive” through to those certified as Organic. My analyses treat a breed-to-finish system as a datapoint, which may consist of one or several farms (e.g. breeding, rearing and finishing farms). I developed metrics which advanced the quantitative characterisation of farm animal welfare to be compatible with life cycle assessments and to account for both quality of life and the quantity of life years required to produce a unit of product (Chapter 2). I systematically evaluated two externality costs that are commonly perceived to trade off against one another: land use and antimicrobial use (Chapter 3). I found weak evidence of a tradeoff between these externalities but importantly also found several systems characterised by low externality costs in both domains. These systems were spread across different label and husbandry types, and no type was an indicator of systems that performed well in both domains. I built upon these assessments of one or two costs by systematically contrasting the land use, greenhouse gas emissions, antimicrobial use and animal welfare of as many of my UK and Brazilian pig systems as possible (Chapter 4). I found evidence of positive associations between land use and greenhouse gas emissions, and antimicrobial use and poor animal welfare, but tradeoffs between these pairs of externalities - systems with low land use generally had low greenhouse gas emissions, but high antimicrobial use and poor welfare. Again however, I found systems that carried relatively low externality costs in all domains. I 6 conclude that contrary to prevailing wisdom, tradeoffs among these externalities are not inevitable. In parallel with this detailed work on pig production, I explored the viral zoonotic emerging infectious disease risks of contrasting ways of meeting livestock product demand (Chapter 5). Analyses to date typically ignore how land use affects emerging infectious disease risks. I created a framework that considered risk factors associated with livestock management and land use. I identified significant knowledge gaps and argued these shortfalls in understanding mean we cannot currently determine whether lower- or higher-yielding systems would better limit the risk of future pandemics. My findings challenge many commonly held perceptions about the externalities of farming systems and have important implications for mitigation strategies. My work illustrates the importance of using empirical evidence rather than relying on patchily supported assumptions. I believe that this warrants the systematic testing of other assumed relationships among externalities. I addressed some important knowledge gaps for the pork sector, and more broadly for emerging infectious disease risks, but the same must be done on a much larger scale, spanning other externalities and sectors.
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    Maximising Return on Investment for Species Conservation
    Correa, Roberto Johannes
    Determining how best to allocate scarce funds is crucial to the action plans that governments and conservation organizations are developing to prevent species from going extinct. A Return on Investment (ROI) approach that explicitly incorporates the costs, benefits and risks of investment has been shown to improve the effectiveness and efficiency of prioritization schemes, yet has not, to date, been applied to single species. This PhD thesis examines how an ROI approach can be applied at species level, using African elephants as a case study. In order to model the effects of investment, an important first step is being able to estimate current levels of spend accurately. I used annual spend data, collected for 192 protected areas across sub-Saharan Africa, to assess how the level of spend varies in relation to contextual factors. I found spend per unit area was significantly higher in smaller protected areas that had more range-restricted species, contained rhinos, were managed or received support from non-profit organizations, and were located in more effectively governed countries. I used the model, which explains 78% of the variation in annual spend per unit area, to predict spend across protected areas without data. From this I estimated that a total of US\$367 million is spent annually on the management of protected areas in sub-Saharan Africa, with a median spend of US\$185 km$^{-2}$yr$^{-1}$. Secondly, identifying the level of spend needed to conserve wildlife populations, together with the enabling conditions and barriers, is vital in helping decision-makers improve the allocation of limited financial resources. I collected elephant census data for 90 protected areas (>40% African elephant population) and assessed how population trends vary in relation to level of spend and other contextual factors. I found a strong positive relationship between elephant population growth rate and level of spend (km$^{-2}$yr$^{-1}$) and a smaller positive effect of government effectiveness. Using the best fit model, which explains 53% of the variation in population trends, I estimated that a median spend of US\$1,085 km$^{-2}$yr$^{-1}$ is necessary to stabilize elephant populations within my sample of 90 protected areas. I compared this to current levels of spend and found that 78% of protected areas experienced spend deficits; and overall funding must be increased by an estimated US\$1.5 billion yr$^{-1}$ if elephant numbers are to be stabilized across all sampled sites. Finally, I developed an ROI framework for single species-based priority setting and tested it by evaluating the optimal allocation of funds across protected areas in sub-Saharan Africa under different objectives centred around maximizing (i) the number of elephants and (ii) the number of stable populations at the end of five years of differing levels of external investment (on top of current government spending). I found that the ROI framework substantially increased the number of elephants (n >18,000) or stable populations (n =28) compared to the current external investment. However, there was a considerable trade-off between the number of additional elephants and additional stable populations, particularly at lower levels of external investment. This was driven by the interplay of several factors: (i) the shape of the species response curve to investment, (ii) population sizes in each protected area, (iii) the sizes of the protected areas, (iv) the existing levels of investment, and (v) the available budget. These factors are often not considered in conventional priority-setting approaches, to the detriment of efficient resource allocation. This thesis demonstrates how an ROI framework could be used by governments and conservation organizations that finance species conservation to evaluate the impact that increasing or decreasing their overall investments would have on species recovery. Based on the findings of this thesis, I provide several recommendations and possible solutions to improve the allocation of conservation resources, and thus support more informed and better justified investment in the conservation of species
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    The demography of Red Sea reef fishes since the Last Glacial Maximum
    Emms, Madeleine
    Coral reefs are at increasing risk of climate-induced mass bleaching events and mass mortality, yet we do not know how coral reef fish species respond to habitat loss on temporal and spatial scales relevant to climate change. The Red Sea represents an ideal model system to address this given that many reef fish populations persisted during the Last Glacial Maximum despite a significant loss of coral reefs. I studied their demogaphic history to determine the impact of environmentally-induced habitat loss. High-throughput sequencing data combined with an Approximate Bayesian Computation framework (including machine learning techniques) provided sufficient power to estimate population parameters for five reef fish species, Dascyllus abudafur, Dascyllus trimaculatus, Dascyllus marginatus, Pomacanthus maculosus, and Carcharhinus melanopterus. The genetic bottleneck experienced during the Last Glacial Maximum (LGM) was not as small as was expected, highlighting the importance of coral reef habitat and refugia. Studying the impact of the LGM on Dascyllus marginatus, a species with a restricted range in the Indian Ocean, enabled me to use this study design to determine that the refugia was unlikely to have been outside the Red Sea, but rather in-situ. The extensiveness of an external population did not appear to affect the response to habitat loss. Lastly, studying the impact of the LGM on Carcharhinus melanopterus, a larger, more motile shark species, showed a similar pattern of response to habitat loss. I then compared the Red Sea barrier with other biogeographic barriers across the Indo-Pacific; in this case it was stronger than some but not as strong as the Indo-Pacific barrier. Overall, the demographic histories showed a similar and mild response to environmentally-induced habitat loss in the Red Sea across species, albeit with some ecological differences. Two case studies allowed me to uncover more about the unique history of the Red Sea, and provided opportunities to discuss other important questions around coral reef refugia and the biogeography of the Indo-Pacific.
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    Evolution of Axial Skeleton Diversity across Reptilia
    Roberts, Lucy; Roberts, Lucy [0000-0002-1293-8667]
    The axial skeleton is a key diagnostic character of vertebrate animals. Comprising the vertebral column and ribs, the axial skeleton is a support structure from which all appendages of the vertebrate body are suspended. Reptilia is a hugely diverse clade of vertebrates, with regards to body form, body size, function, and behaviour. However, despite this established diversity, we know little about the diversity of the axial skeleton across Reptilia, or how axial skeleton evolution is related to development, body form, or function. In this thesis I investigate the diversity and evolution of the axial skeleton across Reptilia, divided into the following chapters: Chapter 1: Introduction; Chapter 2: Axial skeleton morphology; Chapter 3: Combining geometric morphometrics and maximum likelihood modelling to quantify regionalization: Methodology and sensitivity analyses; Chapter 4: Multiple independent trajectories to highly regionalized axial skeleton morphologies across Reptilia: Implications for development and function; Chapter 5: Axial skeletal segmentation across Reptilia: Phylogenetic, ecological, and developmental correlates; and Chapter 6, conclusion: Mammals are not a uniquely regionalized clade: A complex evolutionary history of axial skeleton morphology, function, and development across Reptilia. My results show multiple independent evolutionary trajectories to high degrees of regionalization across Reptilia, demonstrating a greater complexity in axial skeleton evolution, and a greater diversity in axial skeleton morphology across Reptilia, than previously expected. Further to this, I model the evolution of segment counts across Reptilia, comparing segment evolution with body mass and ecological traits. I establish that segmentation played an integral role in the evolution of body form and ecology across Reptilia. High segment counts are associated with aquatic and fossorial ecologies regardless of phylogeny, whereas high relative cervical counts are strongly associated with the acquisition of powered flight in birds, but not in pterosaurs. Overall, I uncover a complex history of axial skeleton evolution across Reptilia. Each extant clade has its own evolutionary trajectory toward highly regionalized forms, and variable trajectories to high and low segment counts. Previous interpretations of axial skeleton diversity across Vertebrata have focused on the origin of mammals, inferring uniquely complex axial skeleton morphologies across Mammalia. However, morphometric analysis here reveals multiple independent gains and losses of regionalization across Reptilia, associated with adaptations to specialised body forms. Amongst sampled taxa, extant crocodilians, most extant squamates, and many extant birds are just as regionalized as sampled mammals. This implies greater degrees of axial skeleton diversity across vertebrates than previously thought and presents the potential for uncovering similar complexity in axial skeleton macroevolution across other vertebrate clades, and Vertebrata as a whole.
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    Mushroom body expansion and the cognitive ecology of Heliconius butterflies
    Young, Fletcher
    Heliconius butterflies, a Neotropical genus of approximately 50 species, exhibit a marked expansion of an insect brain structure called the mushroom bodies (MBs), which are 3-4 times larger than in other Lepidoptera, including closely related Heliconiini genera. MBs are known to play a role in learning and memory, particularly in olfactory contexts, however the relative cognitive capabilities of Heliconius remain unknown. The central objective of my PhD is to investigate the behavioural consequences of, and selective pressures that drove, expansion of Heliconius MBs. I have explored these questions by collecting comparative behavioural and neuroanatomical data across Heliconius and closely related Heliconiini. To explore patterns of MB evolution in the Heliconiini, I conducted phylogenetic comparative analyses across a neuroanatomical dataset of 41 species, including 30 Heliconius and representatives of all Heliconiini genera. Phylogenetic generalised linear mixed modelling shows that within the Heliconiini, increased MB size is associated with the Heliconius genus, even when controlling for the size of the central brain, the antennal lobe and the medulla. Moreover, variable rates analyses indicate that the branch leading to Heliconius experienced a significant increase in the rate of evolution of MB size. But what drove this expansion? There are two main adaptive hypotheses to explain this MB expansion. One is that it facilitates an improved shape learning and recognition of Passiflora host plants. To test this, I conducted shape learning assays across six Heliconiini species. However, Heliconius did not, a as group, out-perform the outgroup species. In addition, I conducted geometric morphometric analyses on Passiflora leaf shape to determine the morphospace of host plants Heliconiini species exploit. There was no correlation between host plant morphospace and MB size. Together these findings suggest MB expansion in Heliconius is not associated with an improved ability for the visual identification of host plants. The second relates to Heliconius’ unique foraging strategy. Heliconius are the only Lepidoptera known to actively feed on pollen, which they collect from a limited number of relatively rare plants. In visiting these plants, Heliconius establish “traplines” – routes through the forest that they follow with a high degree of spatial and temporal fidelity, and which seemingly relies on an advanced spatial memory ability. Through a series of behavioural experiments, I show that Heliconius can learn the location of a food resource in a T-maze, in addition to outperforming non-Heliconius Heliconiini in long-term memory and non-elemental learning tasks – cognitive abilities assumed to be crucial for traplining. There was no difference, however, between Heliconius and non-Heliconius in a reversal learning task. Nonetheless, these results are consistent with the elaboration of the Heliconius MB being driven by the cognitive demands of trapline foraging for pollen. Finally, I investigate the possible neural correlates associated with long-term memory performance by comparing the mushroom bodies of Heliconius erato and Dryas iulia individuals involved in the long-term memory assay with control individuals reared in non-learning environments, in addition to a group of freshly-eclosed butterflies. Overall, the mushroom bodies of Heliconius erato exhibited significantly more age- and experience-related plasticity than Dryas iulia. Importantly, an increase in synapse count was associated directly with visual learning in Heliconius erato. At an individual level, within Heliconius erato, but not Dryas iulia, increases in synapse density and count were correlated with improved recall accuracy.
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    Open Access
    Motor control and directional accuracy of phonotaxis in female field crickets
    Ntelezos, Athanasios
    This thesis addresses two aspects of the phonotactic behavior of female field crickets (Gryllus bimaculatus) as they orient towards singing males: the first one is how the auditory input is integrated into the motor activity underlying their walking responses, and the second one is how accurately they can localize a singing male in a dynamic stimulus situation. Although it has been established that the conspecific calling song is recognized via a circuit in the brain, it is not clear how pattern recognition is linked to descending motor control of phonotaxis. To analyze the auditory-induced motor responses, I recorded high-speed videos of crickets performing phonotaxis and tracked the movement of their bodies and appendages. The video analysis showed that when crickets commence phonotaxis, their body parts and appendages are activated and moved from anterior to posterior in the following order: antennae, head, prothorax, front legs, middle legs. During phonotaxis the antennae move continuously side-to-side in a rhythmic pattern, and on top of this rhythmic movement is superimposed a shift to the side the calling song is presented from. Moreover, the prothorax makes small rhythmic movements that are coupled to the stepping cycle, and on top of these rhythmic movements also steers towards the side the calling song is presented from. Following up on the results of the video analysis, I recorded the activity of the antennal muscles of the scape in crickets that performed phonotaxis. The scape contains two muscles: the adductor muscle that adducts the antenna towards the median line, and the abductor muscle that abducts it laterally. The activity of the adductor muscle is coupled to the adduction movement of the antenna during the contralateral presentation of the calling song, while the activity of the abductor muscle is coupled to the abduction movement during the ipsilateral presentation of the calling song. The antennal movement and muscular activity – especially the abduction movement and the activity of the abductor muscle – are coupled to the calling song on a chirp-to-chirp basis. The neurites of the motoneurons of the antennal muscles are located in the deutocerebrum, while the ascending auditory pathway projects into the protocerebrum. I discuss that additional auditory brain interneurons must be involved for the transfer and processing of the auditory-to-motor signal from the protocerebrum to the deutocerebrum. I also investigated the function of several thoracic muscles for potential contribution to the prothoracic movements contributing to phonotaxis. Of all the muscles tested, only the activity of pronotal muscle 56 was coupled to the prothoracic movements in crickets performing phonotaxis. Specifically, the activity of muscle 56 was coupled both to the rhythmic prothoracic movements that are coupled to the stepping cycle and to the auditory-induced steering of the prothorax. Like the antennae, the prothorax turns to the active speaker and also responds to the calling song on a chirp-to-chirp basis. I discuss that auditory input to the motoneurons of muscle 56 in the prothoracic ganglion is likely indirect via a pathway descending from the brain. Finally, I tested the accuracy of female crickets walking on a trackball as they performed phonotaxis towards a speaker oscillating constantly between 45° left and 45° right relative to their long axis. In a group of crickets, I used a drop of wax to fix the prothorax against the mesothorax and test the effect of the immobilization of the prothorax has on auditory steering. The performance of the crickets with the fixed prothorax was not statistically different from the performance of the crickets that could freely move the prothorax, however, the crickets with the fixed prothorax generally understeered towards the more lateral angles of stimulus. Overall, in this dynamic situation the angular resolution of the crickets was 6-11° in their frontal range, which is less accurate than the previously reported 1-2° for phonotaxis towards a static sound source. The results show that crickets find orientation towards a moving sound source more challenging than towards a static one. This was further corroborated with tests where the crickets steered to the correct side when two speakers positioned 5° to the left and 5° to the right alternated in the presentation of the calling song, meaning their angular resolution for static sound sources was at least 5°.
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    Freshwater Mussels as Biofilters
    (2004-03) McIvor, Anna Louise
    Freshwater mussels (Bivalvia: Unionidae) are filter feeders, removing phytoplankton and other suspended particulate matter from the water. The removal of suspended matter from water is often considered desirable, in order to reduce algal blooms and in the treatment of drinking water. This thesis investigates the potential role of freshwater mussels as living filters, or “biofilters”, in a variety of settings. Initial measurements of the filtration rates of British freshwater mussels showed that individual mussels can filter up to half a litre of water per hour. Calculations of the filtration rates of mussel populations in four British rivers indicate that mussel filtering removes between 7% and 30% of the particulate matter in a parcel of water travelling 10km downstream. This implies that mussels play an important role in the removal of suspended particulate matter in river ecosystems. In a large-scale experiment on the Ouse Washes RSPB reserve, mussels were placed in three eutrophic ditches to assess their potential use in the biomanipulation of these ditches. Although mussels suffered high mortality in two ditches, in the third ditch 70% of mussels survived, and the section of ditch containing mussels remained clear of floating macrophytes throughout the summer. However, mussels had little effect on the water quality in ditches, and further work is needed before they are used in future biomanipulations. The novel use of mussels in drinking water treatment was investigated by placing mussels in large flow-through tanks at Coppermills drinking water treatment plant (operated by Thames Water). Mussels reduced the concentration of chlorophyll a and suspended solids in the water flowing through tanks, and increased sedimentation through the production of faeces and pseudofaeces. Therefore mussels behaved as flocculators, and could be used in the early stages of drinking water treatment. In order to assess the feasibility of producing the large numbers of mussels needed for their use as biofilters, freshwater mussels were cultured in the laboratory. Juveniles of $\textit{Anodonta anatina}$ and $\textit{A. cygnea}$ were successfully reared for over a year, and reached 14mm in length (mean = 11.3mm, n = 17) with 20% survival. $\textit{Unio pictorum}$ and $\textit{Pseudanodonta complanata}$ were also reared for 274 and 100 days respectively, although they had lower survival and growth. The apparatus used in these rearing attempts was small and inexpensive, and could be scaled up to produce the required number of mussels for their use as biofilters. Additionally, the rearing of $\textit{P. complanata}$ is vital for the conservation of this rare mussel species, and offers the first opportunity to study its juvenile morphology and habitat requirements.
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    The evolution and function of pharyngeal arch signalling centres in jawed vertebrates
    Rees, Jenaid
    Pharyngeal arches are paired columns of tissue that form when pouches of foregut endoderm contact surface ectoderm on either side of the embryonic vertebrate head. In fishes, endodermal pouches fuse with surface ectoderm to form gill slits. Once delineated, pharyngeal arches undergo morphogenesis and differentiation, giving rise to skeletal elements of the jaw and gills (in fishes), or the jaw, ear and throat (in amniotes). In my first data chapter, I demonstrate a requirement for Fgf signalling in endoderm–ectoderm fusion and gill slit formation in a cartilaginous fish, the little skate (Leucoraja erinacea). Once formed, skate gill arches expand laterally, and give rise to cartilaginous appendages called branchial rays, which develop under the influence of a Shh-expressing signalling centre called the gill arch epithelial ridge (GAER), and arise exclusively within the posterior region of the gill arches. In my second data chapter, I demonstrate that the skate GAER is of endodermal origin, forming at the endoderm–ectoderm interface, and I discover that Wnt signalling from GAER-adjacent ectoderm contributes to the maintenance of gill arch anteroposterior skeletal polarity, by restricting GAER Shh signal transduction and chondrogenesis to the posterior arch environment. Chick (Gallus gallus) embryos also have a SHH-expressing signalling centre (the posterior ectodermal margin, or PEM) in their second (hyoid) pharyngeal arch, which is associated with posterior expansion of the hyoid arch and neck closure. In my final data chapter, I show that an initially broad domain of SHH expression in the posterior hyoid arch epithelium splits into two discrete domains – the PEM and a domain in the proximal hyoid epithelium (PHE) – with distinct functions in promoting hyoid arch expansion and middle ear skeletogenesis, respectively. Taken together, my work reveals molecular mechanisms important for the formation and patterning of pharyngeal arches and the pharyngeal skeleton across jawed vertebrates.
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    Eviction Behaviour in the Kalahari Meerkats
    Perez, Monika
    Evictions are common in a substantial number of social species, yet they have seldom been studied in detail, and we know relatively little about the causes and consequences of eviction. While previous research has largely focused on the profiles of subordinate females (evictees) that make them most likely to be evicted, in this dissertation I examine eviction behaviour in detail from the dominant females’ perspective (evictor) using the Kalahari meerkats (Suricata suricatta). I focus on how eviction behaviour varies with current environmental, social, and individual conditions and determine whether eviction behaviour is personality-driven or context-dependent (Chapter Three). I find no evidence of eviction behaviour being personality-driven as eviction behaviour is not consistent within individuals over time. However, it appears that evictions are strongly associated with the social environment, especially with the profiles of subordinate females. The dominants evict more and higher proportion of females when there are more subordinate females present and when the age difference between the subordinate and the dominant is small. The dominant females also start evicting earlier in their pregnancy if pregnant subordinates are present in the group. In Chapter Four, I demonstrate a correlation between faecal androgen metabolites and eviction behaviour. I find that androgens increase significantly during pregnancy in dominant females and the androgens levels are consistent within individuals over multiple pregnancies. Androgens levels appear to be associated with the offset of eviction however not the number of evictions. This suggests a threshold relationship between androgens and evictions. I also find no relationship between androgen levels experienced in utero and offspring weight, or survival. However, all individuals that have successfully become dominant later in life, have all experienced relatively low levels of androgens in utero. Though this relationship is interesting, the reason for this is still unknown. Finally, I examine the fitness consequences of eviction on the dominant female. Litters born to dominant females that have evicted more subordinates during their pregnancies have higher chance of survival to 1 week as well as to emergence from their natal burrow. This result supports the hypothesis that the dominants evict subordinates in order to lower the risk of infanticide by the subordinates. Lastly, using a structural equation model, I show the relationship between the profile of dominant females, eviction behaviour, and litter emergence supporting my hypothesis of evictions indirectly increasing litter survival through the eviction of pregnant subordinate females.
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    Body Size Histories in Cenozoic Reptiles From Global to Community Scales
    Parker, Abigail
    Body size is a key ecological trait influencing trophic relationships, geographic distributions, and many other aspects of animal interactions with the environment. For poikilotherms, body size has a strong functional relationship to thermoregulation. This relationship means that body size evolution in reptiles may be related to climatic change over time. In this thesis, I describe histories of maximum body size change in reptiles across the Cenozoic and examine which factors drive reptile size evolution at different scales. I characterize maximum body size trends of crocodylians, turtles, lizards, snakes, and birds across all terrestrial continents through the Cenozoic. My results show coordinated trends across groups, most notably with size peaking in the Late Miocene in all groups except for squamates. This finding refutes the claim that, following the extinction of the dinosaurs, terrestrial mammals were unique in experiencing an ecological release allowing them to fill large-bodied niches. Trends also show association between size increase and global cooling. To test whether this pattern observed over geologic time holds across space in the modern world, I model the relationship between climate and body size distributions in modern turtle communities. There are significant relationships between temperature and turtle body size, with larger size associated with higher temperatures, which support predictions from metabolic theory. Conflicting relationships between size and temperature observed in the past and present suggest that, across the Cenozoic, the influence of temperature was superseded by other factors facilitating size increase. Such factors potentially include interactions between animal groups, as supported by correlated size histories, and changes in habitat availability as Cenozoic cooling increased environmental heterogeneity. As a case study tracing the effects of changes in habitats on reptile size at smaller scales, I examine reptile body sizes at sites from the Plio-Pleistocene of East Africa. Reptile body size reconstructions from the Shungura Formation (3.6-1 Ma) of southern Ethiopia indicate that size evolution is linked to local-scale changes in the environment, such as vegetation structure and lake level. These findings inform understanding of what factors limit or enable the evolution of giant reptiles and, more broadly, how local and short-term environmental influences shape trait change in a way that scales up to deep-time trends.
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    The acquisition and maintenance of dominance in male and female cooperatively breeding meerkats, Suricata suricatta
    Duncan, Christopher
    In group-living species with strong reproductive skew, acquiring a position of dominance is often essential for maximising fitness, and where the frequency of lifetime dominance acquisition is low, substantial variation in fitness among individuals can arise. However, even among dominant individuals there is still substantial variance in fitness attainment, driven by processes such as the maintenance of status, fecundity, and fertility. In this thesis, to understand better the variation in fitness among individuals, I use 26 years of long-term data to investigate the acquisition of dominance and the subsequent maintenance of status and group persistence in a population of cooperatively breeding meerkats, Suricata suricatta, located in the Southern Kalahari. In Chapters 3 and 4, I characterise the distinct routes that subordinates of both sexes pursue to acquire dominance. While there is variation in the frequency that certain dominance routes are used, I find no substantial differences between routes in the traits that determine the acquisition of dominance, the length of tenures or the reproductive success of dominants. In Chapter 5, I distinguish between the reproductive consequences of intrasexual competition from within and outside the group for dominant males. This reveals that while resident immigrant subordinate males compete with the dominant male for reproduction, they also buffer against reproductive competition from outside the group, thereby offsetting their reproductive costs. In Chapter 6, I investigate the factors that influence the maintenance of both sexes’ dominance tenures, while accounting for the distinct causes of tenure loss. I show that heavier dominants are more likely to maintain their position and that dominants of both sexes experience similar levels of within-group intrasexual competition, with increasing numbers of resident competitors increasing the risk of displacement. In addition, dominant males are uniquely vulnerable to extra-group takeovers and resident subordinate males appear to aid in the defence of the group, with higher numbers of subordinate males reducing takeover risk. Furthermore, males are also distinct from female dominants in that a substantial number abandon their dominance, a process that I find is associated with the availability of reproductive opportunities within the group. Finally in Chapter 7, I characterise the processes influencing group persistence, which is important for both the maintenance of a dominant’s tenure and ensuring the persistence of their lineage. I show that groups iii can persist for over a decade and that maintaining a large group size is essential for maximising group longevity. I also find that an endemic form of tuberculosis, Mycobacterium suricattae, plays a considerable role in the failure of groups, being associated with the failure of most long lived groups in the population.
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    Behavioural principles underlying navigational decision-making in Drosophila melanogaster larvae
    Croteau-Chonka, Elise; Croteau-Chonka, Elise [0000-0001-5116-3772]
    An animal’s survival depends on timely decisions informed by sensory information. Studies in humans and large model organisms have elucidated auxiliary roles of large brain regions in the evolution of such perceptual decisions. What remains challenging is acquiring a detailed understanding of the underlying neural mechanisms at a synaptic level and across entire brain circuits. The Drosophila melanogaster larva is an apt model system for probing the mechanisms of decision-making given its rich behavioural repertoire, small nervous system, genetic tractability, and available neuronal wiring diagrams. Taking inspiration from the application of two-alternative forced choice (TAFC) tasks to study perceptual decision-making in other model systems, I employed a closed-loop system to optogenetically activate larval nociceptive neurons based on the direction of precisely detected lateral head sweeps (i.e. casts). I sought to uncover the behavioural computations driving the stereotyped larval navigation sequence comprising repeated head casts followed by crawling in a new direction. I found that in control conditions where stimulus intensity is identical between left and right casts, the percentage of larvae that stop exploration and crawl in the direction favourable for survival (i.e. toward the first stimulated direction) significantly increases with number of casts. However, in experimental conditions where the aversive stimulus differs between sides, the percentage that accept the correct side (i.e. lower intensity) increases more significantly with cast number. When controlling for integrated intensity across casts, I observe a higher fraction of larvae accepting the lower intensity stimulus in experimental conditions compared to controls. These results suggest a mechanism of side-to-side comparison and possible sensory evidence accumulation that facilitates improved decision-making. In this thesis, I introduce the construction and implementation of two computational models for comparison to the larval behaviour trajectories. Both models reflect features of the experiment paradigm, though they differ in their assumptions about how the larva uses information from its environment to guide the acceptance or rejection of a given cast. The resulting predictions I generated about larval behaviour capture some, but not all, qualitative signatures within both the experimental and control datasets. I explore avenues for future model investigation and collection of additional behavioural data in order to draw more definitive mechanistic conclusions. While powerful, the closed-loop system I employed tracks only a single larva at a time. Transitioning my sensory discrimination task to a high-throughput system would be advantageous not only to expand the investigation of other stimulus levels but also to screen stimuli of different valences or from other sensory modalities. In this thesis, I detail my contributions to the development, validation, testing, and experimental application of a new tracking system that is capable of behaviour detection and closed-loop optogenetic and thermogenetic stimulation of 16 larvae simultaneously. This facilitated the first observations of operant conditioning in the Drosophila larva in which the animal successfully adapted its casting behaviour following repeated coupling with reward presentation. Although operant learning occurs over a longer time scale than perhaps what is required for perceptual decision-making, the two tasks are related in creating an association between the animal’s body posture and available sensory information. Together, my work on the sensory discrimination task, behavioural modeling, tool development, and analysis of the operant learning results lays a foundation for future investigation of decision-making behaviour in Drosophila larvae, with implications for further understanding the circuit mechanisms underlying larval taxis, learning, and memory.
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    British mycology: a historical perspective and genetic analysis of Boletus edulis Bull.
    (2022-04-30) Smith, Nathan
    The thesis presented is organised into two sections. The first is a scientific account of the population genetics of Boletus edulis Bull. and the second utilises the methods of history to explore the impact of legacy on British mycology. In this section, which represents the first year of my postgraduate study, I developed an array of six microsatellite markers. These were used to assess population structure of Boletus edulis Bull. on a continental, national, and regional level, with the finding that, in contrast to previous studies, detectable population structure exists within the species in Europe. The markers were then used to explore population differences in heterozygosity and to examine whether heterozygosity-fitness correlations were present in populations, a first for ectomycorrhizal fungi. Some HFCs were detectable but were not consistent across populations studied. The second section of the thesis uses the methodological tools of the history of science to explore the origins of British mycology, presenting the first comprehensive critical study of the discipline. It examines the origins of British mycology in in popular microscopy. Focusing on the Yorkshire “Grand Period”, it explores questions of mycological identity and legacy and how these led to conflicts between different two different mycological groups: the Yorkshire Mycological Committee and the British Mycological Society. In closing, it seeks to draw comparisons between the state of mycology at the turn of the twentieth century and the state of mycology today.