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Speciation and Metabolic rate: Insights from an avian hybrid zone
Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.ORCID iD: 0000-0002-0706-458X
2017 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

The role of divergent climate adaptation in speciation has received surprisingly little scientific attention. My dissertation research focused on how resting metabolic rate (RMR) relates to the build up of prezygotic and postzygotic isolation in a natural Ficedula flycatcher hybrid zone. RMR is the amount of energy an organism needs to run its internal organs. Since RMR is related to life history traits and thermoregulation in other systems, it is likely to affect speciation processes at secondary contact. I found that adult collared flycatchers displace pied flycatchers into increasingly poor habitats (Paper I). Pied nestlings exhibit lower RMR in poor environments (Paper II), which may promote regional coexistence and habitat isolation by making it possible for pied flycatchers to escape competition from collared flycatchers and reduce the risk of hybridization by breeding in the poorer habitats. Further, I found that while collared flycatcher nestling RMR was not environmentally-dependent (Paper II, Paper III), those collared flycatcher nestlings that had a lower RMR in poor environments tended to have higher condition (Paper III). Further, RMR was genetically linked to a sexual ornament in collared males that has previously been shown to be beneficial in poor environments. Lastly, I found that by seven days old, nestlings increase their metabolic rate when listening to song, indicating that they are listening, and by 9 days they can discriminate between songs (Paper IV). Taken together, RMR could affect pre-zygotic isolation via correlations with life history strategies, song and sexual ornaments. RMR is also related to post zygotic isolation in Ficedula flycatchers. I found that flycatcher hybrids tended to have a higher RMR than the parental species (Paper V), and that there were many differentially expressed genes in energetically expensive organs in hybrids that were related to metabolic function (Paper VI). Thus, metabolic dysfunction, possibly caused by genetic incompatibilities, in Ficedula flycatcher hybrids could be a factor leading to infertility and postzygotic isolation between the parental species. Overall, I find that RMR could be a general physiological trait that affects both pre- and postzygotic isolation in hybridizing species at secondary contact, and ought to be more thoroughly considered in speciation research. 

Place, publisher, year, edition, pages
Uppsala: Acta Universitatis Upsaliensis, 2017. , 43 p.
Series
Digital Comprehensive Summaries of Uppsala Dissertations from the Faculty of Science and Technology, ISSN 1651-6214 ; 1462
Keyword [en]
resting metabolic rate, life history, hybridization, speciation, reproductive isolation, Ficedula flycatcher
National Category
Ecology Evolutionary Biology Genetics
Research subject
Biology with specialization in Animal Ecology
Identifiers
URN: urn:nbn:se:uu:diva-309969ISBN: 978-91-554-9776-7 (print)OAI: oai:DiVA.org:uu-309969DiVA: diva2:1054592
Public defence
2017-02-10, Zootissalen, Villavägen 9, Uppsala, 10:00 (English)
Opponent
Supervisors
Available from: 2017-01-19 Created: 2016-12-08 Last updated: 2017-01-25
List of papers
1. Competition-driven build-up of habitat isolation and selection favoring modified dispersal patterns in a young avian hybrid zone
Open this publication in new window or tab >>Competition-driven build-up of habitat isolation and selection favoring modified dispersal patterns in a young avian hybrid zone
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2016 (English)In: Evolution, ISSN 0014-3820, E-ISSN 1558-5646, Vol. 70, no 10, 2226-2238 p.Article in journal (Refereed) Published
Abstract [en]

Competition-driven evolution of habitat isolation is an important mechanism of ecological speciation but empirical support for this process is often indirect. We examined how an on-going displacement of pied flycatchers from their preferred breeding habitat by collared flycatchers in a young secondary contact zone is associated with (a) access to an important food resource (caterpillar larvae), (b) immigration of pied flycatchers in relation to habitat quality, and (c) the risk of hybridization in relation to habitat quality. Over the past 12 years, the estimated access to caterpillar larvae biomass in the habitat surrounding the nests of pied flycatchers has decreased by a fifth due to shifted establishment possibilities, especially for immigrants. However, breeding in the high quality habitat has become associated with such a high risk of hybridization for pied flycatchers that overall selection currently favors pied flycatchers that were forced to immigrate into the poorer habitats (despite lower access to preferred food items). Our results show that competition-driven habitat segregation can lead to fast habitat isolation, which per se caused an opportunity for selection to act in favor of future "voluntarily" altered immigration patterns and possibly strengthened habitat isolation through reinforcement.

Keyword
Competitive exclusion, ecological speciation, habitat segregation, prezygotic isolation, speciation
National Category
Evolutionary Biology
Identifiers
urn:nbn:se:uu:diva-307727 (URN)10.1111/evo.13019 (DOI)000385550700005 ()27464950 (PubMedID)
Funder
Swedish Research Council
Available from: 2016-11-21 Created: 2016-11-21 Last updated: 2016-12-08Bibliographically approved
2. Adjustment of resting metabolic rate by pied flycatchers to the environment promotes regional coexistence with sister species
Open this publication in new window or tab >>Adjustment of resting metabolic rate by pied flycatchers to the environment promotes regional coexistence with sister species
(English)Article in journal (Refereed) Submitted
Abstract [en]

Differences in life history strategies of closely related species can result in variation in relative fitness across heterogeneous environments and promote coexistence. However, physiological mechanisms mediating such variation in relative fitness have not been identified. Resting metabolic rate (RMR) is tightly associated with life-history strategies and could therefore moderate differences in fitness responses to fluctuations in local environments, particularly when species have evolved to different climatic niches in allopatry. We explore whether differences in RMR match changes in relative fitness between collared (Ficedula albicollis) and pied flycatchers (Ficedula hypoleuca) across environmental conditions experienced in a recent hybrid zone. We found a negative correlation between nestling RMR and temperatures experienced during growth in pied flycatchers, which was absent in collared flycatchers. This implies that pied flycatchers are better adapted to the typical seasonal changes in temperature and food availability experienced at these northern breeding sites. There was sufficient additive genetic variance in RMR to respond to selection in both species that may either facilitate ecological character displacement or lead to a breakdown of coexistence. Generally, subtle differences in climate adaptation may play an important role to patterns of competition, coexistence or displacements between closely related species at recent secondary contact.

National Category
Natural Sciences Ecology
Identifiers
urn:nbn:se:uu:diva-309966 (URN)
Available from: 2016-12-08 Created: 2016-12-08 Last updated: 2017-01-10Bibliographically approved
3. Sexual selection affects climate adaptation in collared flycatchers
Open this publication in new window or tab >>Sexual selection affects climate adaptation in collared flycatchers
(English)Article in journal (Refereed) Submitted
Abstract [en]

The role of sexual selection in climate adaptation is debated. We tested whether sexual selection has the potential to speed up adaptation to new thermal environments in a natural population of collared flycatchers. Based on a three-year cross-fostering experiment, we found that the size of a sexually selected trait predicted offspring metabolic rate: male collared flycatchers with large forehead patches sired offspring with low metabolic rate regardless of the ambient temperature. Thus, there was a stable significant relationship between forehead patch size of genetic fathers and offspring metabolic rate. Nestlings with low metabolic rate experienced a survival advantage when growing under high temperatures, which is consistent with the prediction that a low metabolic rate confers a fitness advantage in warm climates. Our study shows that sexual selection can affect climate adaptation. 

Keyword
sexual selection, climate adaptation, resting metabolic rate, Ficedula flycatcher
National Category
Evolutionary Biology
Identifiers
urn:nbn:se:uu:diva-309967 (URN)
Available from: 2016-12-08 Created: 2016-12-08 Last updated: 2016-12-08
4. Song discrimination by nestling collared flycatchers during early development
Open this publication in new window or tab >>Song discrimination by nestling collared flycatchers during early development
2016 (English)In: Biology Letters, ISSN 1744-9561, E-ISSN 1744-957X, Vol. 12, no 7, 20160234Article in journal (Refereed) Published
Abstract [en]

Pre-zygotic isolation is often maintained by species-specific signals and preferences. However, in species where signals are learnt, as in songbirds, learning errors can lead to costly hybridization. Song discrimination expressed during early developmental stages may ensure selective learning later in life but can be difficult to demonstrate before behavioural responses are obvious. Here, we use a novel method, measuring changes in metabolic rate, to detect song perception and discrimination in collared flycatcher embryos and nestlings. We found that nestlings as early as 7 days old respond to song with increased metabolic rate, and, by 9 days old, have increased metabolic rate when listening to conspecific when compared with heterospecific song. This early discrimination between songs probably leads to fewer heterospecific matings, and thus higher fitness of collared flycatchers living in sympatty with closely related species.

Keyword
species recognition, song, metabolic rate, Ficedula flycatcher
National Category
Evolutionary Biology
Identifiers
urn:nbn:se:uu:diva-303751 (URN)10.1098/rsbl.2016.0234 (DOI)000382423700005 ()
Funder
Swedish Research Council
Available from: 2016-09-23 Created: 2016-09-23 Last updated: 2016-12-08Bibliographically approved
5. Hybrid Dysfunction Expressed as Elevated Metabolic Rate in Male Ficedula Flycatchers
Open this publication in new window or tab >>Hybrid Dysfunction Expressed as Elevated Metabolic Rate in Male Ficedula Flycatchers
2016 (English)In: PLoS ONE, ISSN 1932-6203, E-ISSN 1932-6203, Vol. 11, no 9, e0161547Article in journal (Refereed) Published
Abstract [en]

Studies of ecological speciation are often biased towards extrinsic sources of selection against hybrids, resulting from intermediate hybrid morphology, but the knowledge of how genetic incompatibilities accumulate over time under natural conditions is limited. Here we focus on a physiological trait, metabolic rate, which is central to life history strategies and thermoregulation but is also likely to be sensitive to mismatched mitonuclear interactions. We measured the resting metabolic rate of male collared, and pied flycatchers as well as of naturally occurring F1 hybrid males, in a recent hybrid zone. We found that hybrid males had a higher rather than intermediate metabolic rate, which is indicative of hybrid physiological dysfunction. Fitness costs associated with elevated metabolic rate are typically environmentally dependent and exaggerated under harsh conditions. By focusing on male hybrid dysfunction in an eco-physiological trait, our results contribute to the general understanding of how combined extrinsic and intrinsic sources of hybrid dysfunction build up under natural conditions.

National Category
Zoology
Identifiers
urn:nbn:se:uu:diva-307010 (URN)10.1371/journal.pone.0161547 (DOI)000382855600038 ()
Funder
Swedish Research Council, 621-2012-3722
Available from: 2016-12-08 Created: 2016-11-08 Last updated: 2016-12-08Bibliographically approved
6. RNA sequencing provides insight into metabolic dysfunction of hybrids between a recently diverged songbird species pair
Open this publication in new window or tab >>RNA sequencing provides insight into metabolic dysfunction of hybrids between a recently diverged songbird species pair
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(English)Manuscript (preprint) (Other academic)
Abstract [en]

Hybrid dysfunction is thought to gradually build up through the accumulation of clashes between genes as they diverge between the parental species. However, analyses of genetic incompatibilities are generally biased towards long diverged species that are kept under laboratory conditions. Here, we used RNAseq to evaluate 1) whether there was differential gene expression between naturally occurring Ficedula flycatcher hybrids and parental species in energetically expensive alimentary organs, and 2) if such differential gene expression was, based on Gene Ontology (GO) terms, functionally related to Resting Metabolic Rate (RMR) and energy production. We found substantial differential gene expression in all pairwise contrasts, but fewer functional differences between the parental species than between hybrids and either parental species. Some of the differentially expressed genes underlay the OXPHOS pathway, and significantly more than expected GO terms associated with metabolic function were differentially expressed between hybrids and either parental species in the liver. Our results corroborate the idea that tightly co-evolved mitochondrial and nuclear genes underlying the Oxidative Phosphorylation (OXPHOS) pathway can become miss-matched in hybrids and cause malfunctioning phenotypes. Mitonuclear interactions affecting OXPHOS have the potential to both quickly diverge in allopatry as populations adapt to different climate regimes and to cause hybrid genetic dysfunction at secondary contact 

Keyword
Dobzhansky Muller interactions, RNA seq, mitonuclear incompatibility, genetic incompatibility, Resting metabolic rate, hybrid, Ficedula flycatcher
National Category
Evolutionary Biology Genetics
Identifiers
urn:nbn:se:uu:diva-309968 (URN)
Available from: 2016-12-08 Created: 2016-12-08 Last updated: 2016-12-08

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