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Thermal adaptation along a latitudinal gradient in damselflies
Umeå University, Faculty of Science and Technology, Department of Ecology and Environmental Sciences.
2012 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

Understanding how temperature affects biological systems is a central question in ecology and evolutionary biology. Anthropogenic climate change adds urgency to this topic, as the demise or success of species under climate change is expected to depend on how temperature affects important aspects of organismal performance, such as growth, development, survival and reproduction. Rates of biological processes generally increase with increasing temperature up to some maximal temperature. Variation in the slope of the initial, rising phase has attracted considerable interest and forms the focus of this thesis. I explore variation in growth rate-temperature relationships over several levels of biological organization, both between and within species, over individuals’ lifetime, depending on the ecological context and in relation to important life history characteristics such as generation length and winter dormancy.

      Specifically, I examine how a clade of temperate damselflies have adapted to their thermal environment along a 3,600 km long latitudinal transect spanning from Southern Spain to Northern Sweden. For each of six species, I sampled populations from close to the northern and southern range margin, as well from the center of the latitudinal range. I reared larvae in the laboratory at several temperatures in order to measure indiviudal growth rates. Very few studies of thermal adaptation have employed such an extensive sampling approach, and my finding reveal variation in temperature responses at several levels of organization.

      My main finding was that temperature responses became steeper with increasing latitude, both between species but also between latitudinal populations of the same species. Additional genetic studies revealed that this trend was maintained despite strong gene flow. I highlight the need to use more refined characterizations of latitudinal temperature clines in order to explain these findings. I also show that species differ in their ability to acclimate to novel conditions during ontogeny, and propose that this may reflect a cost-benefit trade-off driven by whether seasonal transitions occur rapidly or gradually during ontogeny.

      I also carried out a microcosm experiment, where two of the six species were reared either separately or together, to determine the interacting effects of temperature and competition on larval growth rates and population size structure. The results revealed that the effects of competition can be strong enough to completely overcome the rate-depressing effects of low temperatures. I also found that competition had stronger effects on the amount of variation in growth rates than on the average value.

      In summary, my thesis offers several novel insights into how temperature affects biological systems, from individuals to populations and across species’ ranges. I also show how it is possible to refine our hypotheses about thermal adaptation by considering the interacting effects of ecology, life history and environmental variation.

Place, publisher, year, edition, pages
Umeå: Umeå universitet , 2012. , 35 p.
Keyword [en]
Growth rate, metabolic theory of ecology, universal temperature dependence, environmental gradients, thermal performance, thermal sensitivity, environmental variability, optimality theory, life history, acclimation, size structure, competition, cannibalism, intraguild predation
National Category
Ecology
Identifiers
URN: urn:nbn:se:umu:diva-62276ISBN: 978-91-7459-529-1 (print)OAI: oai:DiVA.org:umu-62276DiVA: diva2:576965
Public defence
2013-01-18, N450, Umeå Universitet, Johan Bures väg 14, Umeå, 13:00 (English)
Opponent
Supervisors
Funder
Swedish Research Council Formas
Available from: 2012-12-21 Created: 2012-12-14 Last updated: 2017-02-01Bibliographically approved
List of papers
1. Generalists and specialists along a latitudinal transect: patterns of thermal adaptation in six species of damselflies
Open this publication in new window or tab >>Generalists and specialists along a latitudinal transect: patterns of thermal adaptation in six species of damselflies
2012 (English)In: Ecology, ISSN 0012-9658, E-ISSN 1939-9170, Vol. 93, no 6, 1340-1352 p.Article in journal (Refereed) Published
Abstract [en]

Tropical organisms colonizing temperate environments face reduced average temperatures and dramatic thermal fluctuations. Theoretical models postulate that thermal specialization should be favored either when little environmental variation is experienced within generations or when among-generation variation is small relative to within-generation variation. To test these predictions, we studied six temperate species of damselflies differing in latitudinal distribution. We developed a computer model simulating how organisms experience environmental variation (accounting for diapause and voltinism) and performed a laboratory experiment assaying thermal sensitivities of growth rates. The computer model showed opposing latitudinal trends in among-and within-generation thermal variability: within-generation thermal variability decreased toward higher latitudes, whereas relative levels of among-generation thermal variability peaked at midlatitudes (where a shift in voltinism occurred). The growth experiment showed that low-latitude species were more thermally generalized than mid- and high-latitude species, supporting the prediction that generalists are favored under high levels of within-generation variation. Northern species had steeper, near-exponential reaction norms suggestive of thermal specialization. However, they had strikingly high thermal optima and grew very slowly over most of the thermal range they are expected to experience in the field. This observation is at present difficult to explain. These results highlight the importance of considering interactions between life history and environmental variation when deriving expectations of thermal adaptation.

National Category
Evolutionary Biology
Identifiers
urn:nbn:se:umu:diva-57156 (URN)10.1890/11-1910.1 (DOI)000305296600012 ()
Available from: 2012-07-09 Created: 2012-07-09 Last updated: 2017-12-07Bibliographically approved
2. Latitudinally structured variation in the temperature dependence of damselfly growth rates
Open this publication in new window or tab >>Latitudinally structured variation in the temperature dependence of damselfly growth rates
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2013 (English)In: Ecology Letters, ISSN 1461-023X, E-ISSN 1461-0248, Vol. 16, no 1, 64-71 p.Article in journal (Refereed) Published
Abstract [en]

The Metabolic Theory of Ecology predicts that the slope of the rate–temperature relationship, E, remains consistent across traits and organisms, acting as a major determinant of large-scale ecological patterns. Although E has recently been shown to vary systematically, we have a poor understanding of its ecological significance. To address this question, we conducted a common-garden experiment involving six damselfly species differing in distribution, estimating E at the level of full-sib families. Each species was sampled throughout its latitudinal range, allowing us to characterise variation in E along a latitudinal gradient spanning 3600 km. We show that E differs among populations and increases with latitude. E was right-skewness across species, but this was largely an artefact of the latitudinal trend. Increased seasonality towards higher latitude may contribute to the latitudinal trend in E. We conclude that E should be seen as a trait involved in local adaptation.

Keyword
Environmental variation; growth rate; metabolic theory of ecology; thermal dependence; universal temperature dependence
National Category
Environmental Sciences
Identifiers
urn:nbn:se:umu:diva-62267 (URN)10.1111/ele.12013 (DOI)
Funder
Formas
Available from: 2012-12-14 Created: 2012-12-14 Last updated: 2017-12-06Bibliographically approved
3. Large-scale patterns in genetic variation, gene flow and differentiation in five species of European Coenagrionid damselfly provide mixed support for the central-marginal hypothesis
Open this publication in new window or tab >>Large-scale patterns in genetic variation, gene flow and differentiation in five species of European Coenagrionid damselfly provide mixed support for the central-marginal hypothesis
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2013 (English)In: Ecography, ISSN 0906-7590, E-ISSN 1600-0587, Vol. 36, no 6, 744-755 p.Article in journal (Refereed) Published
Abstract [en]

Recently, an increased effort has been directed towards understanding the distribution of genetic variation within and between populations, particularly at central and marginal areas of a species' distribution. Much of this research is centred on the central-marginal hypothesis, which posits that populations at range margins are sparse, small and genetically diminished compared to those at the centre of a species' distribution range. We tested predictions derived from the central-marginal hypothesis for the distribution of genetic variation and population differentiation in five European Coenagrionid damselfly species. We screened genetic variation (microsatellites) in populations sampled in the centre and margins of the species' latitudinal ranges, assessed genetic diversity (HS) in the populations and the distribution of this genetic diversity between populations (FST). We further assessed genetic substructure and migration with Bayesian assignment methods, and tested for significant associations between genetic substructure and bioclimatic and spatial (altitude and latitude) variables, using general linearized models. We found no general adherence to the central-marginal hypothesis; instead we found that other factors such as historical or current ecological factors often better explain the patterns uncovered. This was illustrated in Coenagrion mercuriale whose colonisation history and behaviour most likely led to the observation of a high genetic diversity in the south and lower genetic diversity with increasing latitude, and in C. armatum and C. pulchellum whose patterns of low genetic diversity coupled with the weakest genetic differentiation at one of their range margins suggested, respectively, possible range shifts and recent, strong selection pressure.

Place, publisher, year, edition, pages
Hoboken: Wiley-Blackwell, 2013
Keyword
environmental factors, microsatellite loci, range expansion, populations, odonata, evolutionary, dispersal, abundance, G(ST), perspectives
National Category
Ecology
Identifiers
urn:nbn:se:umu:diva-74502 (URN)10.1111/j.1600-0587.2012.00064.x (DOI)000319290600011 ()
Available from: 2013-07-02 Created: 2013-07-01 Last updated: 2017-12-06Bibliographically approved
4. Latitudinal patterns of phenology and age-specific thermal performance across six Coenagrion damselfly species (Odonata)
Open this publication in new window or tab >>Latitudinal patterns of phenology and age-specific thermal performance across six Coenagrion damselfly species (Odonata)
(English)Manuscript (preprint) (Other academic)
Abstract [en]

Using a combination of computer simulations and laboratory experiments we test if the thermal sensitivity of growth rates change during ontogeny and if variation in age-specific growth rates can be predicted based on the natural progression of average temperature or thermal variability in the field. Although annual fluctuations in temperature represent a key characteristic of temperate environments, very few studies of thermal performance have considered the ecological importance of the studied traits within a seasonal context. Instead, thermal performance is assumed to remain constant throughout ontogeny and reflect selection acting over the whole life cycle. Our laboratory experiment revealed that the slope of reaction norms of growth rates changed during ontogeny in five out of six species. In four species from Southern and Central Europe, reaction norms were steepest during early ontogeny, becoming less steep later in life (low-temperature acclimation). In one species from Northern Europe, no change in the slope of reaction norms occurred. In the other North European species, reaction norms became steeper during ontogeny (high-temperature acclimation). Because high-latitude species have a short flight season and inhabit a strongly seasonal environment, we had expected high-latitude species to show strong low-temperature acclimation responses. Instead, we found the reversed pattern: low-latitude species displayed strong low-temperature acclimation responses and high-latitude species displayed weak, or even reversed, acclimation responses to low temperatures. Therefore, we suggest that acclimation to low temperatures may be less beneficial and possibly more costly in habitats with rapid seasonal transitions in average temperature. We conclude that thermal performance traits are more dynamic than typically assumed and caution against using results from single ontogenetic stages to predict species’ responses to changing environmental conditions.

National Category
Ecology
Identifiers
urn:nbn:se:umu:diva-62272 (URN)
Funder
Swedish Research Council Formas
Available from: 2012-12-14 Created: 2012-12-14 Last updated: 2017-02-01Bibliographically approved
5. Competitive interactions modify the temperature dependence of damselfly growth rates
Open this publication in new window or tab >>Competitive interactions modify the temperature dependence of damselfly growth rates
2014 (English)In: Ecology, ISSN 0012-9658, E-ISSN 1939-9170, Vol. 95, no 5, 1394-1406 p.Article in journal (Refereed) Published
Abstract [en]

Individual growth rates and survival are major determinants of individual fitness, population size structure, and community dynamics. The relationships between growth rate, survival, and temperature may thus be important for predicting biological responses to climate change. Although it is well known that growth rates and survival are affected by competition and predation in addition to temperature, the combined effect of these factors on growth rates, survival, and size structure has rarely been investigated simultaneously in the same ecological system. To address this question, we conducted experiments on the larvae of two species of damselflies and determined the temperature dependence of growth rate, survival, and cohort size structure under three scenarios of increasing ecological complexity: no competition, intraspecific competition, and interspecific competition. In one species, the relationship between growth rate and temperature became steeper in the presence of competitors, whereas that of survival remained unchanged. In the other species, the relationship between growth rate and temperature was unaffected by competitive interactions, but survival was greatly reduced at high temperatures in the presence of interspecific competitors. The combined effect of competitive interactions and temperature on cohort size structure differed from the effects of these factors in isolation. Together, these findings suggest that it will be challenging to scale up information from single-species laboratory studies to the population and community level.

Keyword
activation energy, Arrhenius equation, cannibalism, Coenagrion, damselflies, exploitation competition, interference competition, intraguild predation, microcosm experiment, size structure, thermal performance
National Category
Ecology
Identifiers
urn:nbn:se:umu:diva-90858 (URN)10.1890/13-0875.1 (DOI)000336740500028 ()
Note

Originally included in thesis in manuscript form, with the title "Competition modifies the temperature dependence of damselfly growth rates".

Available from: 2014-07-17 Created: 2014-07-01 Last updated: 2017-12-05Bibliographically approved

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