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Population genetics and genomics of a marsupial species : analysis of native and invasive brushtail possum populations (Trichosurus vulpecula) : a dissertation presented in partial fulfilment of the requirements for the degree of Doctor of Philosophy in Conservation Biology, Massey University, Manawatū Campus, New Zealand
(Masey University, 2024-04-15) Pattabiraman, Nimeshika
One of the leading causes of global biodiversity decline is the introduction of invasive pest species that destroy native flora and compete with native fauna for food and other resources. Aotearoa New Zealand is one of the foremost countries in the world that has focussed on eradicating pest species and in particular exotic mammals from the archipelago, which lacks native, terrestrial mammals. The New Zealand Government recently set in train the ambitious task of removing all mustelids, rats, and possums from the terrestrial landscape by the year 2050. Brushtail possums (Trichosurus vulpecula) were introduced to Aotearoa New Zealand from Australia in the mid-1800s, after which they were translocated across the country and have become widespread, destroying indigenous habitat, eating native birds and invertebrates, and spreading bovine TB. Control efforts have seen possum numbers decline in the last two decades from close to 75 million in 2002 to 40 million in 2020. There is, however, a gap in the scientific understanding of possum populations with respect to their genetic composition and population structure across the country, and this knowledge could help us develop effective and dynamic management strategies to eradicate possums on a nationwide scale. In this thesis, I focus on three aspects of population structure and diversity of brushtail possums. First, I investigated a small geographical study area - The Kenepuru Peninsula - where I sought evidence of genetic correlations with geography, time and fur colour. I used two types of genetic markers that target the nuclear and mitochondrial regions of possum DNA with large population samples. In every case, it was determined that the possums comprised one freely interbreeding population at this scale. In particular I demonstrated that colour morphs associated with distinct subspecies in Australia, freely interbreed in New Zealand. I then increased the scale of sampling to include representation of populations across New Zealand and Australia, with the same genetic markers. This threw light on the heterogenous nature of possum diversity in New Zealand, and showed that even after ~110 generations, possums retained genetic separation among spatial groups. Additionally, the data showed evidence of multiple possum lineages across New Zealand that are derived from several Australian populations. High haplotype diversity in New Zealand suggests that the rapidly expanding population has retained novel haplotypes and the data thus far indicated a non-homogenous (metapopulation) distribution of possums without geographical concordance. As the project progressed, I was able to apply high-throughput genotyping-by-sequencing to generate a large genomic dataset. This dataset provided much more detail of the genotypic distribution of possums in Australia and among invasive metapopulations in New Zealand, as well as informing us of the relationship between them. This large, robust database of possum population structure and genetic diversity throughout Aotearoa New Zealand will support future studies in providing informed management decisions to eradicate brushtail possums.
Unrestricted gene flow between two subspecies of translocated brushtail possums (Trichosurus vulpecula) in Aotearoa New Zealand
(Springer Nature Switzerland AG, 2022-01) Pattabiraman N; Morgan-Richards M; Powlesland R; Trewick SA
Two lineages of brushtail possums (Trichosurus vulpecula) were historically introduced to Aotearoa New Zealand, and these two subspecies have different phenotypic forms. Despite over 100 years of potential interbreeding, they appear to retain morphological differences, which may indicate reproductive isolation. We examined this using population samples from a confined landscape and scored each specimen for phenotype using a number of fur colour traits. This resulted in a bimodal trait distribution expected for segregated grey and black lineages. We also sought evidence for genetic partitioning based on spatial and temporal effects. Genetic structure and rates of genetic mixing were determined using seven neutral, species-specific nuclear microsatellite markers and mitochondrial DNA control region sequence. Genotype analyses indicated high levels of variation and mtDNA sequences formed two major haplogroups. Pairwise tests for population differentiation of these markers found no evidence of subdivision, indicating that these brushtail possums behave as a single randomly mating unit. Despite maintenance of two main colour phenotypes with relatively few intermediates, previous inference of assortative mating and anecdotes of distinct races, our data indicate that New Zealand brushtail possums can freely interbreed, and that in some locations they have formed completely mixed populations where neutral genetic markers are unrelated to phenotype. This has implications for effective pest management towards eradication.
Genomic differentiation of brushtail possum (Trichosurus vulpecula) populations : a thesis presented in partial fulfilment of the requirements for the degree of Doctor of Philosophy in Zoology at Massey University, Manawatū, New Zealand
(Massey University, 2023-10-15) Carmelet-Rescan, David
Toxin resistance, an ecologically functional trait, has emerged as a result of the coevolutionary arms race between plants and herbivores. This adaptive response allows organisms to counteract the detrimental effects of toxins. Such adaptation occurs within three primary ecological contexts: predator resistance, prey resistance, and auto-resistance. In the context of plant-herbivore interactions, the production of toxic secondary metabolites by plants plays a pivotal role, triggering a dynamic arms race with herbivores. This ongoing battle leads to the development of diverse defensive strategies in plants and corresponding counter-adaptations in herbivores. Toxin resistance studies have not only shed light on coevolutionary dynamics but also provided insights into regional adaptations and population fragmentation. The case of sodium fluoroacetate, a potent toxin found in certain plant species, offers a specific example of toxin resistance in brushtail possums (Trichosurus vulpecula). Deepening our understanding of the underlying mechanisms driving toxin resistance becomes particularly interesting in this case because of the notable variation in sodium fluoroacetate resistance observed among subspecies. The brushtail possum (Trichosurus vulpecula) is protected in its natural range of Australia but as an invasive pest in New Zealand populations are controlled by the application of human made sodium fluoroacetate, providing a strong selective force for the potential parallel evolution of toxin resistance. I first focus on the population fragmentation and past connectivity of brushtail possum subspecies in their native range using ecological niche modelling and genetic analysis. My results suggest that Pliocene and Pleistocene climate oscillations played a significant role in shaping the distribution and structure of these widespread marsupials. The findings highlight the limited gene flow between subspecies that would have facilitated their adaptations to regional plant assemblages. I studied gene expression using RNA sequencing to reveal significant differences in transcription levels between adult and juvenile brushtail possums. These findings provide insights into the mechanisms associated with possum development, tissue development, cell cycle, and extracellular matrix. Furthermore, the downregulation of specific genes, such as Cytochrome P450, in juveniles may indicate their role in possums' dietary adaptations. Differential gene expression among subspecies of brushtail possum shed light on genomic differentiation and identified candidate genes involved in regional adaptations involving toxin tolerance. Further analyses comparing subspecies has identified genes under positive selection and enriched biological pathways that may be associated with sodium fluoroacetate resistance. These findings support the idea of genomic divergence in spatial populations and provide hypotheses on the metabolic pathways involved in toxin resistance. Collectively, these studies offer valuable insights into the coevolutionary dynamics, toxin resistance mechanisms, gene expression and selection patterns in brushtail possums (Trichosurus vulpecula) and formulated strong hypotheses related to sodium fluoroacetate resistance. This study presents a reliable method to use transcriptomics to investigate the expression and genomic differences behind observed phenotypic variation within a single species.
Landscape genetics for conservation management : brushtail possums (Trichosurus vulpecula) in New Zealand : a thesis presented in partial fulfilment of the requirements for the degree of Master of Science in Conservation Biology at Massey University, New Zealand
(Massey University, 2019) Pattabiraman, Nimeshika
The negative impact of brushtail possums (Trichosurus vulpecula) on New Zealand ecosystems became apparent soon after their introduction from Australia in 1858. Possums not only denude native vegetation but prey on native birds and invertebrates. They also carry bovine tuberculosis (TB) impacting the dairy industry and consequently the New Zealand economy. New Zealand possum populations have spread from several introduction sites and densities have increased. The resulting complex patterns of gene flow influences regional diversity, and potentially the effectiveness of control measures. Currently, ~100 million dollars are spent on 1080 management per year, mostly in response to Tb risk, but there is little information about the migration rates associated with resulting population density fluctuations. To determine whether the potential for intermixing between populations since their introductions could have caused a homogenizing effect on the genetic diversity across New Zealand, I began a detailed population genetic analysis by genotyping possums from 19 locations using nuclear microsatellites and mitochondrial DNA haplotyping from across the country to estimate population structure. Initial introductions of possums from multiple locations resulted in genetic and fur colour diversity but, in comparison to natural Australian populations, it appears that only a subset of genetic variants was brought to New Zealand from Australia. Mitochondrial sequence variation analyses showed overall high haplotype diversity with substantial differences among samples in haplotype frequencies, but with relatively low nucleotide diversity. Similarly, analysis of nuclear markers (microsatellite genotypes with Naïve Bayesian clustering) reveals that while there has been admixture between populations in various locations, indicated by shared genotypes, there are genetically distinct regional populations. Concordance of genetic and geographically distant sampling shows a well-developed population structure of possums across New Zealand. These results are also supported by pairwise Fst comparisons between all pairs of populations; although nearly all populations showed significant differences, there was no signature of isolation by distance as expected from their history of introductions. This study provides a foundation for further research into spatial structure of brushtail possums which will enable the effective targeting of management and is essential for modelling population recovery, disease spread, and potentially the emergence of toxin resistance. Predator-free 2050 is an ambitious objective considering current circumstances. In order to achieve its goals, even for the targeted species, we need to efficiently manage our resources and improve the accuracy of control measures to maintain long-term effects.
The population dynamics of bovine tuberculosis in possums : a thesis presented in partial fulfilment of the requirements for the degree of Master of Science in Mathematics at Massey University
(Massey University, 1991) Sleeman, Maree
With the recent outcry concerning the spread of Bovine Tuberculosis throughout the New Zealand Possum population, there is an increasing need to study some of the diverse modelling approaches to this problem. This thesis centres on modelling the epidemics of this disease using two and three-dimensional dynamical systems, which describe the change in the possum population and change in the number of individuals that are diseased. Introductory material is covered in Chapter One, which reports on the first, through to some of the most recent research completed in the area of disease epidemics. A review of the previous model of possum tuberculosis is also introduced. Chapter Two looks at the effects on the dynamics of the model of changing the recovery curve parameter, which measures the degree of recovery of possums following a control operation. Detailed steady-state analysis is carried out on the system and local stability determined. In Chapter Three, a three-dimensional model is investigated that allows for a latent period following infection of disease. Instead of a possum being able to spread the disease immediately after becoming infected itself, there is a latent time until the disease becomes contagious. An in-depth description is given as to how this model originates, then steady-state analysis is explored, and finally local stability of the steady-states is examined. Restricting the contact rate of an individual possum with the rest of the population is the model studied in Chapter Four. Rather than a possum being able to come in contact with the whole population in a set time, as was the situation in the previous models, the number of contacts is fixed at some realistic value for the given time period. Steady-state analysis is carried out for this new model, along with the local stability analysis. Chapter Five looks at the various models and how they relate to the model in Chapter Two. as this model is the base for the subsequent ones. Computer generated plots are examined in order to display the numerical differences between the models. A brief comparison is given between these and some other models in the literature, and concludes by discussing some of the advantages and disadvantages of the various models. Finally, Chapter Six discusses the need for implementing spatially distributed models in the future, to allow for patchiness within the population.
Bleaching of possum fur : a thesis presented in fulfilment of the requirements for the degree of Master of Technology in Chemical Technology at Massey University, Palmerston North, New Zealand
(Massey University, 2002) Dick, Robert Graeme
The goal of this project was to develop a process for the industrial scale bleaching of possum fur. Research was undertaken into the bleaching of possum with regard to whiteness of final fur, damage occurring to fur and prevention of matting to fur. A process was supplied consisting of kill, mordant, oxidative bleach, strip and reductive bleach steps. This process produced fur with a loss of around 9.5% and alkali solubility of around 70%. Improvements made to this process gave a loss of around 5% and alkali solubility of around 50%. The main alterations made to the process were (i) Changing the reducing agent and pH of the mordant and lengthening this stage. (ii) Altering the temperature, time and pH of the oxidative bleach. (iii) Shortening the strip stage (iv) Altering the reagent system of the reductive bleach The displacement bleaching system used was found to be successful in preventing matting of the fibre provided care is taken in transferring the wet fur for drying. The main difficulty encountered in scaling up the laboratory process was a compression of the fur during oxidative bleaching resulting in a build up of pressure and flow problems through the fur. This is due in part to the hollow nature of possum fibre which gives it a large degree of buoyancy and the swelling of the fibres during oxidative bleaching. Changes in the surface chemistry of the fibres occurring during oxidative bleaching are also thought to play some part since these problems are not encountered with fibre which has undergone a successful oxidative bleach. These problems were countered by using a shallower bed of fur for bleaching, reducing the flowrate through the fur and reducing the temperature of the oxidative bleach to give a more gradual bleach. These modifications allowed the successful bleaching of a 3.5 kg batch of fur. A larger scale pilot plant for the bleaching of 15 kg batches was constructed. An attempted run on this plant using the conditions developed in the smaller plant was unsuccessful. It was specified that the lid on the top of the plant be clamped in place however this was not undertaken as a cost and time saving measure. This then came unstuck during bleaching leading to the overflow of the vessel. Further work is required to optimise the lower temperature oxidative bleach. With this undertaken it is recommended that the lid be clamped into place on the larger plant and the design parameters determined on the smaller plant verified before further scale-up is attempted. A full scale plant could not be constructed within the time frame of the project.
Development and evaluation of molecular tests for investigation of tissue tropism of adenovirus in tissues of brushtail possum (Trichosurus vulpecula) : a thesis presented in partial fulfilment of the requirements for the degree of Master of Veterinary Studies at Massey University
(Massey University, 2006) Lu, Guangjin
(Trichosurus vulpecula) is considered to be a vertebrate pest, which causes severe damage to the native ecosystem. Biological control, such as immunocontraception, is considered to be the only foreseeable long-term solution to the control of the possum population. Possum adenovirus has been investigated as a possible candidate for use in the biological control of this pest in New Zealand. Attempts to isolate the virus by cell culture have been unsuccessful and could be due to inappropriate culture systems. The localization of adenovirus in possums may be indicative of the tissue tropism of the virus and be helpful in finding the appropriate tissue samples for cell culture. However, this information is not available to date. In this study, the main aim was to establish a sensitive detection method to detect the presence of adenovirus in possum tissues and allow an investigation of tissue tropism. Direct and indirect in situ polymerase chain reaction (in situ PCR) and in situ hybridization (ISH) were established using canine adenovirus type 1 (CAdV-1) as a parallel model for optimizing the experimental conditions. The result showed that both in situ PCR and ISH detection systems were able to detect canine adenoviruses in cultured MDCK cells at a low level of infection. In situ PCR methods were able to detect CAdV-1 in MDCK cells at 8 hours after infection with strong staining in the nuclei, while ISH was able to detect CAdV-1 at 14 hours after infection. The same approaches were applied to detect possum adenovirus in formalin-fixed, paraffin-embedded sections of possum intestinal tissues using a probe from possum adenovirus hexon gene. However, no possum adenovirus was detected in these tissues. This result indicates that further investigation using the same approach should be applied to other possum tissues. In order to investigate the presence of antibody to possum adenovirus, an agar gel immunodiffusion (AGID) test was established using canine adenovirus type 1 (CAdV-1) as antigen. Possum sera from various regions of New Zealand were obtained from the possum serum bank of this laboratory. Of the 268 sera tested, none of them were antibody positive to CAV-1. This result could be due to the insensitivity of AGID test per se and the absence of the shared cross-reaction antigen between these two viruses, suggesting that further investigation using viruses from the group of atadenovirus as antigen is needed.
An Australian abroad : the secret life of the brushtail possum (Trichosurus vulpecula) : a thesis presented in partial fulfilment of the requirements for the degree of Doctor of Philosophy in Veterinary Science at Massey University, Manawatu, New Zealand
(Massey University, 2016) Richardson, Kyle Stephen
The “superspreader” hypothesis relates disease transmission to social contacts and assumes transmission is driven by the frequency, type and distribution of contacts among infected and susceptible individuals. I investigated characteristics of brushtail possum (Trichosurus vulpecula) home ranges for six wild free-living subpopulations, (four grids were studied; all of them before possum depopulation and two of them after possum depopulation) constructing social networks relevant to bovine tuberculosis (TB) transmission before and after depopulation. I also experimentally infected possums with a novel strain of TB to monitor secondary case infections in relation to these contact and other factors, including population density and sex ratio. Before depopulation home range estimates showed adult males had larger home ranges than female and younger possums. Home range overlap and area of overlap differed between subpopulations, and possum sex and age; with adult males having more and larger overlaps with other possums. Possums were fitted with proximity-logging collars and contacts registered between April and October, 2012. The number of connections an individual has with others and the probability of the distribution of contacts it has within the population, or node degree and betweenness, also known as the shortest distance between individuals, were associated with sex, with males having higher values for each. Males also contacted more possums than females. Post-depopulation results showed an influx of male possums, higher population density, and smaller home range sizes than before depopulation. Possums post-depopulation also lacked an apparent ‘routine’ in contact networks, interacting with other possums haphazardly. The greater level of contact among adult males, than before depopulation, and their effects on recovering populations post-depopulation, was likely the cause of more TB infection in adults and males. This thesis provides empirical evidence that adult male possums have home range and contact network characteristics that are likely to enhance their involvement in the transmission and persistence of TB, relative to female and younger possums. Observations of experimentally infected individuals showed that infected males survived longer than females and that, as a consequence, those males potentially acted as a “supershedding” subgroup. I therefore provide evidence that adult male possums are the most important drivers of TB transmission and persistence of infection in populations, and could be targeted for control measures.
The age-structured population models : a thesis presented in partial fulfilment of the requirements for the degree of Master of Science in Mathematics at Massey University
(Massey University, 1995) Hamzah, Norhayati
Mathematical theories of population dynamics have been derived and have been effectively used in the last two hundred years. These theories have appeared both implicitly and explicitly in many important studies of populations: human populations, as well as populations of animals, cells and viruses. The aim of this thesis is to understand how these models have developed with a view to an improved formulation. Nowadays, the structured model can be considered to be of great importance and use. Mathematicians have realised that in real biological and ecological situations, a model should be developed which is at least structured on age especially with higher order animals, for example human and possum populations, so in this thesis we pay much attention to these type of population models. We shall also be discussing the qualitative nature of the solutions to the model: such as the long-term behaviour, steady-age distribution and the stability of the solution in great details. In chapter 1, we begin with the historical background of the unstructured population in which the properties of individuals are ignored and only the total population is considered. The Malthusian and Verhulst model are set as examples. We then proceed in chapter 2 with the simplest McKendrick's age- structured population model. In chapter 3, we shall show how Laplace transform can be used to solved the problem. We have also chosen some arbitrary functions for either one or both the birth and/or death rate, so that we can make deductions from the assumption of these special cases. Chapter 4, discusses the long-term behaviour: steady age distribution (s.a.d.) and the stability of the solution being analysed. We then generalise the linear age- dependent population model in chapter 5 to a non-linear age-dependent model where the limiting effects (overcrowding and limitation of resources) has an effect, on the specific age class only. Chapter 6 discusses the more realistic non-linear model similar to that described in chapter 5 but here the limiting effects have an effect on the whole population. Finally, we realise that since these models need to be tested, we shall, in chapter 7 test our model with possum populations on data collected from the Orongorongo Valley in Wellington. And then make suggestions for future work in Chapter 8.
Habitat and seasonal effects on blowfly ecology in possum carcasses in the Manawatu : a thesis presented in partial fulfilment for the requirements for the degree of Master of Science in Ecology at Massey University
(Massey University, 1993) Appleton, Clive
Flies were trapped on Keeble farm and in Keeble forest reserve between May 1992 to February 1993. Fewer Calliphoridae were trapped in pasture during summer than in autumn or winter and different fly species showed differing preferences for bush or pasture at different times of the year. More flies were trapped around the bush margin than in either bush or pasture during spring and summer. In pasture the most numerous calliphorid trapped was Calliphora stygia (Fabricius, 1781), whereas in bush during summer Calliphora hilli Patton, 1925 was the predominant species. Lucilia sericata (Meigen, 1826) was never trapped in bush. Decaying possum carcases were examined in bush and pasture between February 1992 and February 1993. The number of maggots that left these carcases was affected by the time of the year and whether the carcases were in bush or pasture. More maggots left bush located possum carcases during spring and summer while more maggots left possum carcases in pasture during autumn and winter. Decay rates were most rapid during spring and summer. Temperatures were warm enough for adult fly activity during winter but the possum carcases decayed much slower, especially in bush. C, stygia and Calliphora vicina Robineau-Desvoidy, 1830 were generally the first species of maggot to leave possum carcases and they were the only species present throughout the year in both habitats. L. sericata and Chrysomya ruficacies (Macquart, 1843) maggots were restricted to possum carcases in pasture during spring and summer while Calliphoroides antennaris (Hutton, 1881) was restricted to possum carcases in bush. Hydrotaea rostrata Robineau-Desvoidy, 1830 was the only species restricted to summer. In spring 1992, 3400 flies emerged from a 2.5 kg possum carcase placed in pasture and 4200 flies emerged from a 3.1 kg possum carcase placed in bush. Estimated emergence success of adult flies was 22.0% in pasture and 20.2% in bush. This was l5% lower on average than the emergence level of comparable maggots raised in the laboratory. Flies began emerging in the bush l0 days after those in pasture. L. sericata was restricted to pasture and C. antennatis was restricted to bush. Overall the major flystrike species to emerge were C. stygia and L. sericata. C. stygia made stygia made up 46% of the total number of flies that emerged in pasture and 78% of those in bush, while L. sericata comprised l5.5% of the total number of flies that emerged in pasture. The emergence success of field-collected maggots in the laboratory was significantly correlated with the estimated average total number of maggots that left the carcases in the field. Maggots showed the highest emergence success in winter when larval competition in the carcase was lowest. The temperature of a possum carcase containing fly maggots in bush reached 19.7° C during spring 1992 whereas the temperature exceeded 35°C on occasions in another carcase in pasture at the same time. Proportionally fewer maggots emerged from the possum carcase in pasture possibly because the high temperatures killed many maggots, especially those of C. stygia. Maggots and bacterial decay both elevated carcase temperatures above ambient. Bacteria raised the temperature by about 2°C whereas maggots raised the temperature by 18.3°C to 26°C above ambient. The carcase temperature significantly affected the number of maggots that left the possum carcases, and the number of maggots that left was directly related to the total maggot biomass that left the carcase. A minimum of 24% to 26% of. the fresh weight of the possum carcases was converted to maggot weight.

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