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Avian Malaria and Interspecific Interactions in Ficedula Flycatchers
Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.ORCID iD: 0000-0002-3058-0072
2019 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

Parasitism is a core theme in ecological and evolutionary studies. Despite this, there are still gaps in our knowledge regarding host-parasite interactions in nature. Furthermore, in an era of human-induced, global climatic and environmental change revealing the roles that parasites play in host life-histories, interspecific interactions and host distributions is of the utmost importance. In this thesis, I explore avian malaria parasites (haemosporidians) in two species of passerine birds: the collared flycatcher Ficedula albicollis and the pied flycatcher F. hypoleuca. In Paper I, I show that an increase in spring temperature has led to rapid divergence in breeding times for the two flycatcher species, with collared flycatchers breeding significantly earlier than pied flycatchers. This has facilitated regional coexistence through the build up of temporal isolation. In Paper II, I explore how malaria assemblages across the breeding ranges of collared and pied flycatchers vary. I find that pied flycatcher populations have significantly higher infection prevalence than collared flycatchers, but collared flycatchers have a higher diversity of parasites. Additionally, I find that recently colonised flycatchers have kept their original parasite assemblages while gaining further parasites from native pied flycatchers. In Paper III, I explore age-related patterns of malaria infections in collared flycatchers. I find that female collared flycatchers have higher overall infection rates than males and that infected female collared flycatchers have significantly higher mortality rates than uninfected females while males pay no survival cost. Despite this, female collared flycatchers do not pay a fitness cost, despite their shorter lifespans. In Paper IV, I explore nest defence behaviours of infected and uninfected collared flycatchers. I find that malaria infection significantly interacts with age and that young, infected collared flycatchers have a lower intensity of defence behaviours than uninfected individuals, while the opposite pattern is present in older collared flycatchers, with infected birds having higher defence behaviours. Therefore, I argue that Papers III and VI suggest patterns of terminal investment are present in collared flycatchers. Finally, in Paper V, I investigate parasite transmission in pied and collared flycatchers. I find that infected individuals of both species produce higher quantities of volatile organic compounds (VOCs) than uninfected individuals. Additionally, there is a significant increase in VOCs produced when the number of malaria gametocytes is higher. This suggests that malaria parasites are able to manipulate their hosts into producing insect-vector attracting compounds and that this is further increased at peak infectivity. These findings help to fill in some of the gaps in the literature regarding host-parasite relationships and the role of environmental change on hosts.

Place, publisher, year, edition, pages
Uppsala: Acta Universitatis Upsaliensis, 2019. , p. 44
Series
Digital Comprehensive Summaries of Uppsala Dissertations from the Faculty of Science and Technology, ISSN 1651-6214 ; 1781
Keywords [en]
ficedula, flycatcher, avian malaria
National Category
Ecology
Research subject
Biology with specialization in Animal Ecology
Identifiers
URN: urn:nbn:se:uu:diva-377921ISBN: 978-91-513-0589-9 (print)OAI: oai:DiVA.org:uu-377921DiVA, id: diva2:1295138
Public defence
2019-04-26, Zootissalen, EBC, Villavägen 9, Uppsala, 10:00 (English)
Opponent
Supervisors
Available from: 2019-04-02 Created: 2019-03-10 Last updated: 2019-05-07
List of papers
1. Climate-driven build-up of temporal isolation within a recently formed avian hybrid zone.
Open this publication in new window or tab >>Climate-driven build-up of temporal isolation within a recently formed avian hybrid zone.
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2018 (English)In: Evolution, ISSN 0014-3820, E-ISSN 1558-5646, Vol. 72, no 2, p. 363-374Article in journal (Refereed) Published
Abstract [en]

Divergence in the onset of reproduction can act as an important source of reproductive isolation (i.e., allochronic isolation) between co-occurring young species, but evidence for the evolutionary processes leading to such divergence is often indirect. While advancing spring seasons strongly affect the onset of reproduction in many taxa, it remains largely unexplored whether contemporary spring advancement directly affects allochronic isolation between young species. We examined how increasing spring temperatures affected onset of reproduction and thereby hybridization between pied and collared flycatchers (Ficedula spp.) across habitat types in a young secondary contact zone. We found that both species have advanced their timing of breeding in 14 years. However, selection on pied flycatchers to breed earlier was weaker, resulting in a slower response to advancing springs compared to collared flycatchers and thereby build-up of allochronic isolation between the species. We argue that a preadaptation to a broader niche use (diet) of pied flycatchers explains the slower response to raising spring temperature, but that reduced risk to hybridize may contribute to further divergence in the onset of breeding in the future. Our results show that minor differences in the response to environmental change of co-occurring closely related species can quickly cause allochronic isolation.

Keywords
Competitive exclusion, ecological speciation, prezygotic isolation, reinforcement, speciation, temporal segregation
National Category
Evolutionary Biology Ecology
Identifiers
urn:nbn:se:uu:diva-341102 (URN)10.1111/evo.13404 (DOI)000424131100011 ()29214649 (PubMedID)
Funder
Swedish Research CouncilAcademy of Finland
Available from: 2018-02-06 Created: 2018-02-06 Last updated: 2019-03-10Bibliographically approved
2. Interspecific transfer of parasites following a range‐shift in Ficedula flycatcher
Open this publication in new window or tab >>Interspecific transfer of parasites following a range‐shift in Ficedula flycatcher
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2018 (English)In: Ecology and Evolution, ISSN 2045-7758, E-ISSN 2045-7758, Vol. 8, no 23, p. 12183-12192Article in journal (Refereed) Published
Abstract [en]

Human‐induced climate change is expected to cause major biotic changes in species distributions and thereby including escalation of novel host‐parasite associations. Closely related host species that come into secondary contact are especially likely to exchange parasites and pathogens. Both the Enemy Release Hypothesis (where invading hosts escape their original parasites) and the Novel Weapon Hypothesis (where invading hosts bring new parasites that have detrimental effects on native hosts) predict that the local host will be most likely to experience a disadvantage. However, few studies evaluate the occurrence of interspecific parasite transfer by performing wide‐scale geographic sampling of pathogen lineages, both within and far from host contact zones. In this study, we investigate how haemosporidian (avian malaria) prevalence and lineage diversity vary in two, closely related species of passerine birds; the pied flycatcher Ficedula hypoleuca and the collared flycatcher F. albicollis in both allopatry and sympatry. We find that host species is generally a better predictor of parasite diversity than location, but both prevalence and diversity of parasites vary widely among populations of the same bird species. We also find a limited and unidirectional transfer of parasites from pied flycatchers to collared flycatchers in a recent contact zone. This study therefore rejects both the Enemy Release Hypothesis and the Novel Weapon Hypothesis and highlights the complexity and importance of studying host‐parasite relationships in an era of global climate change and species range shifts.

National Category
Ecology
Identifiers
urn:nbn:se:uu:diva-366254 (URN)10.1002/ece3.4677 (DOI)000454107200069 ()30598810 (PubMedID)
Funder
Swedish Research Council
Available from: 2018-11-19 Created: 2018-11-19 Last updated: 2019-03-10Bibliographically approved
3. Sex-specific decrease in longevity following malaria infection in a natural bird population
Open this publication in new window or tab >>Sex-specific decrease in longevity following malaria infection in a natural bird population
(English)Manuscript (preprint) (Other academic)
Keywords
Avian malaria, BaSTA, collared flycatcher, sex bias, survival, terminal investment
National Category
Ecology
Research subject
Biology with specialization in Animal Ecology
Identifiers
urn:nbn:se:uu:diva-378637 (URN)
Available from: 2019-03-07 Created: 2019-03-07 Last updated: 2019-03-10
4. Age and malaria infection affect nest defence behaviours in collared flycatchers
Open this publication in new window or tab >>Age and malaria infection affect nest defence behaviours in collared flycatchers
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(English)Manuscript (preprint) (Other academic)
Keywords
Avian malaria, Collared flycatcher, Ficedula albicollis, nest-defence, terminal investment
National Category
Ecology
Research subject
Biology with specialization in Animal Ecology
Identifiers
urn:nbn:se:uu:diva-378638 (URN)
Available from: 2019-03-07 Created: 2019-03-07 Last updated: 2019-03-10
5. Malaria infected birds produce higher levels of vector-attracting compounds
Open this publication in new window or tab >>Malaria infected birds produce higher levels of vector-attracting compounds
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(English)Manuscript (preprint) (Other academic)
Keywords
Avian malaria, Ficedula, gametocytaemia, host manipulation, malaria vector, volatile organic compounds
National Category
Ecology
Research subject
Biology with specialization in Animal Ecology
Identifiers
urn:nbn:se:uu:diva-378936 (URN)
Available from: 2019-03-10 Created: 2019-03-10 Last updated: 2019-03-10

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