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Pathogens in Free-Ranging African Carnivores: Evolution, Diversity and Co-Infection

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Pathogens in Free-Ranging African Carnivores: Evolution, Diversity and Co-Infection Pathogens in free-ranging African carnivores: evolution, diversity and co-infection DISSERTATION zur Erlangung des akademischen Grades doctor rerum naturalium (Dr. rer. nat.) im Fach Biologie eingereicht an der Mathematisch-Naturwissenschaftlichen Fakultät I der Humboldt-Universität zu Berlin von Diplom Biologin Katja Verena Goller Präsident der Humboldt-Universität zu Berlin Prof. Dr. Jan-Hendrik Olbertz Dekan der Mathematisch-Naturwissenschaftlichen Fakultät I Prof. Dr. Andreas Herrmann Gutachter: 1. Prof. Dr. Richard Lucius 2. Prof. Dr. Heribert Hofer 3. Prof. Dr. Alex D. Greenwood Tag der mündlichen Prüfung: 04.04.2011 SUMMARY The ecological role of most wildlife pathogens is poorly understood because pathogens are rarely studied in relation to the long-term population dynamics of wildlife hosts. Instead, pathogen infections are reported on a case basis or studies are focused on periods when patho- gens cause noticeable mortality in their hosts. However, pathogens that appear to be of low virulence may also have an important effect if they operate in a synergistic fashion or affect life history parameters such as longevity or reproductive success. Furthermore, the effect of pathogens on population dynamics may be difficult to detect in wildlife, for example if they reduce the survival of young age classes that are rarely observed. Until now, research on the life history consequences of pathogen infection has mainly been confined to laboratory stud- ies where animals are raised and kept under strictly defined conditions, or to small, short lived species such as rodents, birds or insects, as well as to human populations. The aim of this thesis was to address these problems by assessing the impact of single infec- tions and co-infections by pathogens on key life history parameters and the influence of life history traits on infection status in a free-ranging social carnivore species, the spotted hyena Crocuta crocuta. The study was embedded in a long-term study on several clans of spotted hyenas from two subpopulations inhabiting the Serengeti National Park and the adjacent Ngorongoro Crater in Tanzania, East Africa. Data on key life history parameters were avail- able for several hundred individually known animals as was information on changing levels of prey availability. I established molecular biological methods (polymerase chain reactions (PCRs) and reverse transcription PCRs) to screen an extensive set of faecal, blood and tissue samples from individually known spotted hyenas and sympatric carnivores for the presence of coronavirus, calicivirus, canine distemper virus, canine parvovirus and the tick-borne blood parasite Hepatozoon sp. to determine the prevalence of the pathogens. Phylogenetic analyses revealed several new variants of pathogens in spotted hyenas and other sympatric carnivore species. I detected previously undescribed coronavirus variants and an unexpected high diversity and rapid temporal change of coronavirus variants circulating in one spotted hyena subpopulation across different years (Chapter 3.1); a result of considerable relevance to our understanding of coronaviral infections in wildlife populations. These results also highlight the importance of long-term monitoring of viral populations in wildlife. I identified previously undescribed calicivirus-like variants in spotted hyenas which were more closely related to human sapoviruses than to those typically infecting carnivore species i (Chapter 3.2). This result suggests a host species jump from humans to spotted hyenas fol- lowed by adaptation of the pathogen to the new host. I identified age-specific patterns of single infections with coronavirus or calicivirus whereby young Serengeti hyenas were significantly more likely to excrete virus than adults (Chapter 3.1, 3.2). To assess the possible effects of key life history parameters on the likelihood of in- fection with coronavirus, calicivirus, or both viruses, I applied a statistical model which in- cluded concurrent infection with helminths (Chapter 3.3). This model revealed that the most important factors influencing the likelihood of viral infection was (1) simultaneous helminth infection, suggesting that modulation of the immune response to helminth infection reduced the chance of virus infection, and (2) the synergistic effects of nutritional and physiological stress induced by low prey availability, thereby reducing maternal milk support which in turn is likely to lead to increased sibling rivalry in twin litters. Additionally, I investigated whether infection status as a juvenile reduced longevity and found that there was evidence of natural selection by non-virulent pathogens on a host population (Chapter 3.3). The longevity differed between individuals with either a single coronavirus- or calicivirus infection or individuals co-infected with both viruses. A single infection with coronavirus had the worst impact whereas co-infection with both viruses had more benign consequences. These results showed that key ecological parameters may influence infection status of juvenile spotted hyenas and that infection status in turn may significantly influence longevity. Furthermore, my research revealed evidence of coronavirus infection in the Serengeti hyena population and a lack of current infection in the Ngorongoro Crater population (Chapter 3.4). This difference in viral presence between the two subpopulations was probably caused by a significantly higher persistence of susceptible individuals in clans in the Serengeti subpopula- tion than in the Crater subpopulation, even though both subpopulations were part of the same metapopulation and shared the same social structure. This result illustrates that pathogen dy- namics within apparently similar and closely adjacent subpopulations may significantly differ as a consequence of variation in demographic stochasticity. My phylogenetic analysis on Hepatozoon sp. revealed variants that infect sympatric carnivore hosts (Chapter 3.5). Monitoring of young spotted hyenas less than two months of age showed that Hepatozoon infections, previously thought to be benign in this species, cause mortality in young animals. I identified canine distemper virus (CDV) infection as cause of mortality in an African wild dog Lycaon pictus pack close to the Serengeti National Park boundary that was not associated ii with increased CDV mortality among wild carnivores inside the Park (Chapter 3.6). The phy- logenetic analysis of this variant provided further information on the diversity of CDV vari- ants infecting wild carnivores, and evidence of different CDV variants adapted to canids in comparison to variants in lions and spotted hyenas. Thus the variant I identified in wild dogs will be of key importance to future research on CDV in the wild carnivore guild in this world biodiversity site. This is the first study that combines ecological and epidemiological data from a long-term study on a host with extensive molecular genetic and phylogenetic studies on a variety of pathogens to investigate the impact of single infections and co-infections by pathogens on key life history parameters and the influence of life history parameters on infection status in a free-ranging social mammal species, the spotted hyena. Keywords: African carnivores, pathogens, co-infection, spotted hyena, life histories iii ZUSAMMENFASSUNG Die ökologische Rolle der meisten Wildtier-Pathogene in Bezug zur langfristigen Populati- onsdynamik ihrer Wirte ist nur ansatzweise erforscht und wird deshalb nur unzureichend ver- standen. Stattdessen ist die Erforschung von Infektionen mit Pathogenen oft beschränkt auf einzelne Fallstudien oder auf Perioden mit deutlich erhöhten Mortalitätsraten innerhalb der Wirtspopulation. Pathogene mit geringer Virulenz können jedoch durch synergistisches Auf- treten verheerende Auswirkungen auf die Fitness ihrer Wirte haben oder sich auf wichtige individuelle lebensgeschichtliche Merkmale, wie zum Beispiel Lebensdauer oder Reprodukti- onserfolg, auswirken. Des Weiteren sind die Auswirkungen von Krankheitserregern auf die Populationsdynamik der Wildtiere schwer abzuschätzen, zum Beispiel wenn sie die Überle- benschancen von selten zu beobachtenden Jungtieren beeinträchtigen. Bis heute sind Untersu- chungen von Infektionen mit Pathogenen und deren Auswirkungen auf Lebensgeschichten meist auf Laborstudien beschränkt, in denen Tiere unter streng definierten Bedingungen ge- züchtet und gehalten werden, bzw. auf Studien an kleinen, kurzlebigen Arten wie Nagern, Vögeln und Insekten oder auf Studien an der Humanpopulation. Ziel dieser Arbeit war, die Auswirkungen von Einzel- oder Koinfektionen auf individuelle lebensgeschichtliche Schlüsselparameter sowie die Einflüsse bestimmter lebensgeschichtli- cher Merkmale auf den Infektionsstatus anhand einer frei lebenden sozialen Karnivorenart, der Tüpfelhyäne Crocuta crocuta, zu untersuchen. Diese Arbeit war in eine Langzeitstudie integriert und wurde an mehreren Gruppen von Tüpfelhyänen zweier Subpopulationen durch- geführt, die im Serengeti Nationalpark sowie in dem angrenzenden Ngorongoro Krater in Tansania in Ostafrika lebten. Daten über wichtige lebensgeschichtliche Merkmale von mehre- ren hundert individuell bekannten Tieren in Kombination mit Daten über die wechselhafte Beuteverfügbarkeit in den Territorien der Gruppen standen hierfür zur Verfügung. Ich etab- lierte molekularbiologische Methoden (Polymerase Kettenreaktionen (PCRs) und Reverse Transkriptions PCRs), um eine Vielzahl an Kot-, Blut- und Gewebeproben individueller
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