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Avian malaria, life-history trade-offs and interspecific competition in Ficedula flycatchers
Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal Ecology.
2013 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

This thesis investigates the impact of avian malaria (Haemosporidia) parasites on the outcome of interspecific competition between two closely related bird species, pied (Ficedula hypoleuca) and collared (F. albicollis) flycatchers. I further investigated how variation in timing of breeding, life history strategies and immune competence genes (MHC genes) modulate the fitness effects of malaria parasites in one of the two species i.e. collared flycatchers. Collared flycatchers colonized the Baltic island Öland in the late 1950-ties and has since then been expanding their breeding range while competitively excluding pied flycatchers from the favourable habitats (deciduous forests). I investigated the underlying mechanisms behind this exclusion by combining detailed long-term breeding data with modern molecular genetic techniques identifying both the presence/absence and lineage specificity of haemosporidian blood parasites. I found that the rapid decline of pied flycatchers can be explained by the combined effects of competition over nestling sites, hybridization and haemosporidian infections. Haemosporidian infections have a negative impact on survival of pied flycatcher females but no detectable effect on collared flycatchers’ longevity or reproductive success. This may be due to the fact that collared flycatchers carry (and are potentially exposed to) a higher diversity of parasites than pied flycatchers, which in turn may select for a higher diversity of MHC genes and hence a better overall protection from the negative impact of parasites. Indeed, functional MHC diversity correlates negatively with malaria prevalence among collared flycatchers from Gotland. Moreover, I found that both, malaria infection intensity and immunoglobulin level influences how infected collared flycatchers respond to increased nestling food-demands. The latter results mean that there is variation in allocation strategies (i.e. in resource allocation between reproductive effort and immune competence) within the collared flycatcher population. Hence, this population has the ability to respond to novel selection pressures in terms of optimal allocation of resources into immune functions. In summary, my results show that local parasites may facilitate the expansion of a new colonizer. This is important in the context of global climate change that will probably increase the colonization rate of southern species and lead to novel host-parasite interactions.

Place, publisher, year, edition, pages
Uppsala: Acta Universitatis Upsaliensis, 2013. , 59 p.
Series
Digital Comprehensive Summaries of Uppsala Dissertations from the Faculty of Science and Technology, ISSN 1651-6214 ; 1056
Keyword [en]
Blood parasites, competitive asymmetry, immunocompetence, interspecific competition, life-history trade-offs, MHC, parasite-driven selection
National Category
Ecology
Identifiers
URN: urn:nbn:se:uu:diva-204349ISBN: 978-91-554-8708-9 (print)OAI: oai:DiVA.org:uu-204349DiVA: diva2:638550
Public defence
2013-09-13, Zootisalen, Evolution Museum Building, Uppsala, 10:00 (English)
Opponent
Supervisors
Available from: 2013-08-23 Created: 2013-07-31 Last updated: 2015-11-24Bibliographically approved
List of papers
1. Combined effects of interspecific competition and hybridization impede local coexistence of Ficedula flycatchers
Open this publication in new window or tab >>Combined effects of interspecific competition and hybridization impede local coexistence of Ficedula flycatchers
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2012 (English)In: Evolutionary Ecology, ISSN 0269-7653, E-ISSN 1573-8477, Vol. 26, no 4, 927-942 p.Article in journal (Refereed) Published
Abstract [en]

At secondary contact closely related species may both compete over similar resources and/or hybridize. Simulation models suggest that hybridization increases the risk of extinction beyond the risk resulting from interspecific competition alone, but such combined effects are rarely studied empirically. Here, we use detailed records on pairing patterns, breeding success, local recruitment and immigration collected during 8 years (2002-2009) to investigate the underlying mechanism of the rapid displacement of pied flycatchers by collared flycatchers on the Swedish island of A-land. We found no differences in average reproductive success or reproductive lifespan between the two species. However, we show that young male pied flycatchers failed to establish new territories as the density of male collared flycatchers increased. In addition, as the relative frequency of collared flycatchers increased, the risk of hybridization dramatically increased for female pied flycatchers, which speeds up the exclusion process since there is a high fitness cost associated with hybridization between the two species. In a nearby control area, within the same island, where pied flycatchers breed in the absence of collared flycatchers, no decline in the number of breeding pairs was observed during the same period of time. Our results demonstrate the crucial importance of studying the combined effects of various types of heterospecific interactions to understand and predict the ecological and evolutionary implications of secondary contact between congeneric species. These findings are particularly interesting in the light of recent climate change since the expected range shifts of many taxa will increase competitive and sexual interactions between previously separated species.

Keyword
Competition, Coexistence, Extinction, Hybridization, Reproductive interference
National Category
Biological Sciences
Identifiers
urn:nbn:se:uu:diva-157138 (URN)10.1007/s10682-011-9536-0 (DOI)000305218900011 ()
Available from: 2011-08-17 Created: 2011-08-17 Last updated: 2017-12-08Bibliographically approved
2. Malaria infections reinforce competitive asymmetry between two Ficedula flycatchers in a recent contact zone
Open this publication in new window or tab >>Malaria infections reinforce competitive asymmetry between two Ficedula flycatchers in a recent contact zone
2013 (English)In: Molecular Ecology, ISSN 0962-1083, E-ISSN 1365-294X, Vol. 22, no 17, 4591-4601 p.Article in journal (Refereed) Published
Abstract [en]

Parasites may influence the outcome of interspecific competition between closely-related host species through lower parasite virulence in the host with which they share the longer evolutionary history. We tested this idea by comparing the prevalence of avian malaria (Haemosporidia) lineages and their association with survival in pied and collared flycatchers (Ficedula hypoleuca & F. albicollis) breeding in a recent contact zone on the Swedish island of Öland. A nested PCR protocol amplifying haemosporidian fragments of mtDNA was used to screen the presence of malaria lineages in 1048 blood samples collected during 6 years. Competitively inferior pied flycatchers had a higher prevalence of blood parasites, including the lineages that were shared between the two flycatcher species. Multistate mark-recapture models revealed a lower survival of infected versus uninfected female pied flycatchers, while no such effects were detected in male pied flycatchers or in collared flycatchers of either sex. Our results show that a comparatively new host, the collared flycatcher, appears to be less susceptible to a local northern European malarial lineage where the collared flycatchers have recently expanded their distribution. Pied flycatchers experience strong reproductive interference from collared flycatchers, and the additional impact of species-specific blood parasite effects adds to this competitive exclusion. These results support the idea that parasites can strongly influence the outcome of interspecific competition between closely-related host species, but that the invading species need not necessarily be more susceptible to local parasites.

Keyword
annual survival, apparent competition, Haemoproteus, Plasmodium
National Category
Ecology
Identifiers
urn:nbn:se:uu:diva-204308 (URN)10.1111/mec.12409 (DOI)000323506400018 ()23980765 (PubMedID)
Available from: 2013-07-29 Created: 2013-07-29 Last updated: 2017-12-06Bibliographically approved
3. Malaria-infected female collared flycatchers (Ficedula albicollis) do not pay the cost of late breeding
Open this publication in new window or tab >>Malaria-infected female collared flycatchers (Ficedula albicollis) do not pay the cost of late breeding
2014 (English)In: PLoS ONE, ISSN 1932-6203, E-ISSN 1932-6203, Vol. 9, no 1, e85822- p.Article in journal (Refereed) Published
Abstract [en]

Life-history theory predicts that the trade-off between parasite defense and other costly traits such as reproduction may be most evident when resources are scarce. The strength of selection that parasites inflict on their host may therefore vary across environmental conditions. Collared flycatchers (Ficedula albicollis) breeding on the Swedish island Oland experience a seasonal decline in their preferred food resource, which opens the possibility to test the strength of life-history trade-offs across environmental conditions. We used nested-PCR and quantitative-PCR protocols to investigate the association of Haemosporidia infection with reproductive performance of collared flycatcher females in relation to a seasonal change in the external environment. We show that despite no difference in mean onset of breeding, infected females produced relatively more of their fledglings late in the season. This pattern was also upheld when considering only the most common malaria lineage (hPHSIB1), however there was no apparent link between the reproductive output and the intensity of infection. Infected females produced heavier-than-average fledglings with higher-than-expected recruitment success late in the season. This reversal of the typical seasonal trend in reproductive output compensated them for lower fledging and recruitment rates compared to uninfected birds earlier in the season. Thus, despite different seasonal patterns of reproductive performance the overall number of recruits was the same for infected versus uninfected birds. A possible explanation for our results is that infected females breed in a different microhabitat where food availability is higher late in the season but also is the risk of infection. Thus, our results suggest that another trade-off than the one we aimed to test is more important for explaining variation in reproductive performance in this natural population: female flycatchers appear to face a trade-off between the risk of infection and reproductive success late in the season.

Keyword
avian malaria, blood parasites, Haemoproteus, Haemosporidia, reproductive cost, reproductive success, trade-off
National Category
Ecology
Identifiers
urn:nbn:se:uu:diva-204310 (URN)10.1371/journal.pone.0085822 (DOI)000330288000027 ()
Available from: 2013-07-29 Created: 2013-07-29 Last updated: 2017-12-06Bibliographically approved
4. Immunoglobulin level and infection intensity influence how malaria-infected collared flycatchers respond to brood size manipulation
Open this publication in new window or tab >>Immunoglobulin level and infection intensity influence how malaria-infected collared flycatchers respond to brood size manipulation
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(English)Article in journal (Refereed) Submitted
Abstract [en]

1.The existence of a trade-off between investment in reproduction and immune function is well-established in many species. However, variation in the underlying physiological allocation strategies, which is what selection operates on, remains largely unexplored.

2.We investigated how haemosporidian infection influenced stress hormone level and ability to increase parental effort in female collared flycatchers (Ficedula albicollis). We especially focused on how estimates of investment in humoral immune response and level of parasitemia influenced subsequent parental investment (i.e. offspring provisioning and offspring mass).

3.To achieve these goals, we combined a brood size manipulation experiment with nested- and quantitative PCR methods to establish infection status and intensity. In addition, we quantified immunoglobulin Y (IgY) and stress protein levels.

4. Malaria-infected females reared enlarged broods with lower mass but there was large variation in their response to the experiment. Only infected females with low IgY levels decreased their relative provisioning rate and there was a positive relationship between the intensity of infection and total brood mass.

5. Our study implies that malaria-infected flycatchers experience a trade-off between keeping their infection at bay (i.e. low level of parasitemia) and responding to increased offspring demands (i.e. high offspring mass in enlarged broods). However, relatively immunocompetent individuals (i.e. individuals with high IgY levels) did not compromise their parental care suggesting that the main cost of raising the immune response does not lay in antibody production.

Keyword
Avian malaria, Haemoproteus, life-history strategy, parental effort, Plasmodium
National Category
Ecology
Identifiers
urn:nbn:se:uu:diva-204309 (URN)
Available from: 2013-07-29 Created: 2013-07-29 Last updated: 2015-11-24Bibliographically approved
5. MHC diversity, malaria and lifetime reproductive success in collared flycatchers
Open this publication in new window or tab >>MHC diversity, malaria and lifetime reproductive success in collared flycatchers
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2012 (English)In: Molecular Ecology, ISSN 0962-1083, E-ISSN 1365-294X, Vol. 21, no 10, 2469-2479 p.Article in journal (Refereed) Published
Abstract [en]

Major histocompatibility complex (MHC) genes encode proteins involved in the recognition of parasite-derived antigens. Their extreme polymorphism is presumed to be driven by co-evolution with parasites. Hostparasite co-evolution was also hypothesized to optimize within-individual MHC diversity at the intermediate level. Here, we use unique data on lifetime reproductive success (LRS) of female collared flycatchers to test whether LRS is associated with within-individual MHC class II diversity. We also examined the association between MHC and infection with avian malaria. Using 454 sequencing, we found that individual flycatchers carry between 3 and 23 functional MHC class II B alleles. Predictions of the optimality hypothesis were not confirmed by our data as the prevalence of blood parasites decreased with functional MHC diversity. Furthermore, we did not find evidence for an association between MHC diversity and LRS.

Keyword
fitness, genetic variation, immune response, major histocompatibility complex, optimality hypothesis, parasites, selection
National Category
Biological Sciences
Identifiers
urn:nbn:se:uu:diva-174920 (URN)10.1111/j.1365-294X.2012.05547.x (DOI)000303388300014 ()
Available from: 2012-05-30 Created: 2012-05-30 Last updated: 2017-12-07Bibliographically approved

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