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Diversity of avian haemosporidian parasites : Host specificity, genetic structure and infection patterns

Huang, Xi LU (2018)
Abstract (Swedish)
Bland vilda djur finns närmast ett oräkneligt antal patogener. Dessa kan i vissa fall ge utbrott av zoonotiska sjukdomar vilket har hänt vid upprepade tillfällen under mänsklighetens historia. Men varför kan endast vissa av de patogener som normalt finns hos vilda djur infektera människor? Fågelinfluensa och West-Nile virus kan överföras från fåglar till människor medan rabies kan överföras från hundar. Däremot kan inte malaria som finns hos gorillor och schimpanser smitta människor, trots att dessa parasiter är mycket närbesläktade med människomalaria och att våra och apornas röda blodkroppar som parasiterna infekterar är mycket lika varandra. Man frågar sig därför varför vissa patogener kan göra väldigt ”långa hopp”, till exempel mellan... (More)
Bland vilda djur finns närmast ett oräkneligt antal patogener. Dessa kan i vissa fall ge utbrott av zoonotiska sjukdomar vilket har hänt vid upprepade tillfällen under mänsklighetens historia. Men varför kan endast vissa av de patogener som normalt finns hos vilda djur infektera människor? Fågelinfluensa och West-Nile virus kan överföras från fåglar till människor medan rabies kan överföras från hundar. Däremot kan inte malaria som finns hos gorillor och schimpanser smitta människor, trots att dessa parasiter är mycket närbesläktade med människomalaria och att våra och apornas röda blodkroppar som parasiterna infekterar är mycket lika varandra. Man frågar sig därför varför vissa patogener kan göra väldigt ”långa hopp”, till exempel mellan fåglar och däggdjur, medan andra ”sitter fast” hos en art trots att många andra liknande arter finns tillgängliga.
Detta leder in oss på ett centralt begrepp som kallas värdspecificitet. Grovt sett kan patogener delas in i två grupper; specialister som endast kan infektera en eller ett par närstående arter och generalister som kan infektera ett stort antal arter. Om vi skulle kunna förstå mekanismerna som styr variationen av patogeners värdspecificitet, skulle vi ha större möjligheter att förutsäga utbrott av nya sjukdomar och därför vara av stor betydelse för samhället i stort.
I min avhandling har jag studerat blodparasiter hos fåglar, och använt denna artrika grupp av släktingar till malaria för att undersöka förekomsten och infektionsgraden hos generalister som infekterar olika fågelarter. Dessa studier krävde först att jag med säkerhet kunde avgränsa dessas arttillhörighet. En stor utmaning vid studier av parasiter som lever inne i värdindividens celler är att det insamlade provet framförallt innehåller material från värdorganismen. Parasiter är också väldigt små och är fattiga på informativa strukturer vilket gör artbestämningen med hjälp av utseenden väldigt svårt. Det kan också vara svårt att ta fram parasiternas DNA sekvenser eftersom det mesta DNA’t i provet kommer från värden. Jag utvecklade därför en metod som använder konstgjorda DNA-strängar märkta med en molekyl som gör dem magnetiska, och när dessa binder till parasiternas DNA kan man tvätta bort det mesta av värdorganismens DNA.
Jag använde därefter resultaten från dessa framrenade sekvenser för att studera en parasit som påträffats både i Europa (siskor) och i Amerika (husfinkar). Trots att dessa är i det närmaste identiska i sitt mitokondrie-DNA fann jag att det fanns betydande skillnader i kärn-DNA’t i en omfattning att man kan misstänka att de utgör olika arter. I en annan studie undersökte jag tre generalist parasiter som är vanliga bland tättingar som häckar i skogarna kring Krankesjön. Jag fann att dessa är olika effektiva i att infektera de olika värdarterna. I arter som ofta är infekterade är infektionsnivåerna i genomsnitt högre än i arter som sällan blir infekterade. Jag fann också att närstående arter var mer lika i hur infekterade de blir. Så trots att dessa är generalister finns det ett antal arter som är deras ”huvudvärdar”. I analyser av den säsongsmässiga variation hos dessa huvudvärdar fann jag att årsungar var infekterade redan när vi började fånga de första friflygande individerna i början av sommaren, vilket betyder att de förmodligen blir infekterade redan i boet. Därefter minskar infektionsintensiteten gradvis, parallellt med att deras immunförsvar utvecklas.
Resultaten i min avhandling har bidragit med nya metoder för att studera evolutionen av värd-parasit interaktioner och kommer att kunna ge vägledning för att på sikt förutsäga utbrott av nya sjukdomar.
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Abstract
Parasites live on or inside their hosts and usually cause fitness loss, sometimes even lead to outbreaks of emerging infectious disease. Understanding how a parasite can infect its hosts (i.e., host specificity of the parasite) is important to both basic studies on disease evolution and the whole ecosystem health.
In this thesis, I use avian haemosporidians, a group of species-rich protozoans as a model system to study host specificity of parasites, because of their high diversity in geographical distributions and host ranges.
Studying host specificity of avian haemosporidians is facing two main challenges. First, it is essential to have a method that accurately defines the species limits of the parasites, which cannot be done by... (More)
Parasites live on or inside their hosts and usually cause fitness loss, sometimes even lead to outbreaks of emerging infectious disease. Understanding how a parasite can infect its hosts (i.e., host specificity of the parasite) is important to both basic studies on disease evolution and the whole ecosystem health.
In this thesis, I use avian haemosporidians, a group of species-rich protozoans as a model system to study host specificity of parasites, because of their high diversity in geographical distributions and host ranges.
Studying host specificity of avian haemosporidians is facing two main challenges. First, it is essential to have a method that accurately defines the species limits of the parasites, which cannot be done by current identification methods. In some cases, a presumed generalist parasite that appears to infect multiple host species may have already adapted separately to different hosts, with the consequences that gene flow is restricted between them, and thus should be considered as reproductively isolated parasite species. In order to detect these cryptic species, reliable molecular markers are required. But genomic sequencing of avian haemosporidians is challenging since they coexist with hosts whose genome size is 50 times larger, causing an excessive amount of contamination in the yielded sequences. Second, the measurement of host specificity is in itself a complicated exercise. To assess host specificity of a parasite, one must consider the parasite’s ability to infect its host and reproduce in the host. The associations between a parasite and its hosts may vary with biotic and abiotic environmental factors, therefore the overall infection patterns of all potential hosts should be analysed, which was not reported in previous haemosporidian studies.
In this thesis, my aim is to answer these two open questions for better understanding host specificity with a set of case studies. In Paper I a cost-effective protocol was developed to obtain multiple nuclear gene sequences throughout the genome of avian haemosporidians from DNA extracted from wild-infected bird blood without any special treatment. Based on analyses of multiple nuclear genes, the phylogenetic structures were investigated respectively for a group of sympatric parasites that present similar morphological characters in Paper II, and allopatric parasites with identical mitochondrial gene sequences in Paper III, to clarify if they should be considered as the same species or several different but cryptic species. I then tested the infection patterns of three generalist parasites in a natural community in Paper IV and found that generalist parasites are not equally adapted to all species in their host ranges but better to a smaller subset of hosts. In Paper V I further investigated the seasonal dynamics of parasite infection patterns and found that infections peaked during the main nesting season in adults and a few weeks later in juveniles, as soon as they started to be captured. Juveniles must become infected already as nestlings, thereafter the infection intensities decrease along the development of their immune systems.
In summary, the findings in this study have provided new insights for further studies on host specificity of avian haemosporidians, with newly developed approaches to define the species limits and to investigate the infection patterns of parasites.
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Please use this url to cite or link to this publication:
author
supervisor
opponent
  • Dr. Santiago-Alarcón, Diego, Institute of Ecology INECOL, Veracruz, Mexico
organization
publishing date
type
Thesis
publication status
published
subject
keywords
Haemoproteus, Sequence capture, host specificity, quantitative PCR, phylogeny
pages
158 pages
publisher
Lund University, Faculty of Science, Department of Biology
defense location
The Blue Hall, Ecology Building, Sölvegatan 37, Lund
defense date
2018-09-28 09:30
external identifiers
  • scopus:85056353651
ISBN
978-91-7753-779-3
978-91-7753-778-6
language
English
LU publication?
yes
id
4da684b3-15ab-4569-81ae-d60c5857689d
date added to LUP
2018-08-30 13:28:25
date last changed
2019-02-20 11:25:14
@phdthesis{4da684b3-15ab-4569-81ae-d60c5857689d,
  abstract     = {Parasites live on or inside their hosts and usually cause fitness loss, sometimes even lead to outbreaks of emerging infectious disease. Understanding how a parasite can infect its hosts (i.e., host specificity of the parasite) is important to both basic studies on disease evolution and the whole ecosystem health.<br/>In this thesis, I use avian haemosporidians, a group of species-rich protozoans as a model system to study host specificity of parasites, because of their high diversity in geographical distributions and host ranges.<br/>Studying host specificity of avian haemosporidians is facing two main challenges. First, it is essential to have a method that accurately defines the species limits of the parasites, which cannot be done by current identification methods. In some cases, a presumed generalist parasite that appears to infect multiple host species may have already adapted separately to different hosts, with the consequences that gene flow is restricted between them, and thus should be considered as reproductively isolated parasite species. In order to detect these cryptic species, reliable molecular markers are required. But genomic sequencing of avian haemosporidians is challenging since they coexist with hosts whose genome size is 50 times larger, causing an excessive amount of contamination in the yielded sequences. Second, the measurement of host specificity is in itself a complicated exercise. To assess host specificity of a parasite, one must consider the parasite’s ability to infect its host and reproduce in the host. The associations between a parasite and its hosts may vary with biotic and abiotic environmental factors, therefore the overall infection patterns of all potential hosts should be analysed, which was not reported in previous haemosporidian studies.<br/>In this thesis, my aim is to answer these two open questions for better understanding host specificity with a set of case studies. In Paper I a cost-effective protocol was developed to obtain multiple nuclear gene sequences throughout the genome of avian haemosporidians from DNA extracted from wild-infected bird blood without any special treatment. Based on analyses of multiple nuclear genes, the phylogenetic structures were investigated respectively for a group of sympatric parasites that present similar morphological characters in Paper II, and allopatric parasites with identical mitochondrial gene sequences in Paper III, to clarify if they should be considered as the same species or several different but cryptic species. I then tested the infection patterns of three generalist parasites in a natural community in Paper IV and found that generalist parasites are not equally adapted to all species in their host ranges but better to a smaller subset of hosts. In Paper V I further investigated the seasonal dynamics of parasite infection patterns and found that infections peaked during the main nesting season in adults and a few weeks later in juveniles, as soon as they started to be captured. Juveniles must become infected already as nestlings, thereafter the infection intensities decrease along the development of their immune systems.<br/>In summary, the findings in this study have provided new insights for further studies on host specificity of avian haemosporidians, with newly developed approaches to define the species limits and to investigate the infection patterns of parasites.<br/>},
  author       = {Huang, Xi},
  isbn         = {978-91-7753-779-3},
  keyword      = {Haemoproteus,Sequence capture,host specificity,quantitative PCR,phylogeny},
  language     = {eng},
  pages        = {158},
  publisher    = {Lund University, Faculty of Science, Department of Biology},
  school       = {Lund University},
  title        = {Diversity of avian haemosporidian parasites : Host specificity, genetic structure and infection patterns},
  year         = {2018},
}