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  • 1. Alho, J. S.
    et al.
    Herczeg, G.
    Laugen, A. T.
    Raesaenen, K.
    Laurila, Anssi
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Population and Conservation Biology.
    Merila, J.
    Allen's rule revisited: quantitative genetics of extremity length in the common frog along a latitudinal gradient2011In: Journal of Evolutionary Biology, ISSN 1010-061X, E-ISSN 1420-9101, Vol. 24, no 1, p. 59-70Article in journal (Refereed)
    Abstract [en]

    Ecogeographical rules linking climate to morphology have gained renewed interest because of climate change. Yet few studies have evaluated to what extent geographical trends ascribed to these rules have a genetic, rather than environmentally determined, basis. This applies especially to Allen's rule, which states that the relative extremity length decreases with increasing latitude. We studied leg length in the common frog (Rana temporaria) along a 1500 km latitudinal gradient utilizing wild and common garden data. In the wild, the body size-corrected femur and tibia lengths did not conform to Allen's rule but peaked at mid-latitudes. However, the ratio of femur to tibia length increased in the north, and the common garden data revealed a genetic cline consistent with Allen's rule in some trait and treatment combinations. While selection may have shortened the leg length in the north, the genetic trend seems to be partially masked by environmental effects.

  • 2. Alho, Jussi S.
    et al.
    Herczeg, Gabor
    Söderman, Fredrik
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Evolution.
    Laurila, Anssi
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Evolution.
    Jönsson, K. Ingemar
    Merilä, Juha
    Increasing melanism along a latitudinal gradient in a widespread amphibian: local adaptation, ontogenic or environmental plasticity?2010In: BMC Evolutionary Biology, ISSN 1471-2148, E-ISSN 1471-2148, Vol. 10, no 1, p. 317-Article in journal (Refereed)
    Abstract [en]
    Background: The thermal benefits of melanism in ectothermic animals are widely recognized, but relatively little is known about population differentiation in the degree of melanism along thermal gradients, and the relative contributions of genetic vs. environmental components into the level of melanism expressed. We investigated variation in the degree of melanism in the common frog (Rana temporaria; an active heliotherm thermoregulator) by comparing the degree of melanism (i) among twelve populations spanning over 1500 km long latitudinal gradient across the Scandinavian Peninsula and (ii) between two populations from latitudinal extremes subjected to larval temperature treatments in a common garden experiment. Results: We found that the degree of melanism increased steeply in the wild as a function of latitude. Comparison of the degree of population differentiation in melanism (P-ST) and neutral marker loci (F-ST) revealed that the P-ST >F-ST, indicating that the differences cannot be explained by random genetic drift alone. However, the latitudinal trend observed in the wild was not present in the common garden data, suggesting that the cline in nature is not attributable to direct genetic differences. Conclusions: As straightforward local adaptation can be ruled out, the observed trend is likely to result from environment-driven phenotypic plasticity or ontogenetic plasticity coupled with population differences in age structure. In general, our results provide an example how phenotypic plasticity or even plain ontogeny can drive latitudinal clines and result in patterns perfectly matching the genetic differences expected under adaptive hypotheses.
  • 3. Cano, J. M.
    et al.
    Li, M-H
    Laurila, Anssi
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Population and Conservation Biology.
    Vilkki, J.
    Merila, J.
    First-generation linkage map for the common frog Rana temporaria reveals sex-linkage group2011In: Heredity, ISSN 0018-067X, E-ISSN 1365-2540, Vol. 107, no 6, p. 530-536Article in journal (Refereed)
    Abstract [en]

    The common frog (Rana temporaria) has become a model species in the fields of ecology and evolutionary biology. However, lack of genomic resources has been limiting utility of this species for detailed evolutionary genetic studies. Using a set of 107 informative microsatellite markers genotyped in a large full-sib family (800 F1 offspring), we created the first linkage map for this species. This partial map-distributed over 15 linkage groups-has a total length of 1698.8 cM. In line with the fact that males are the heterogametic sex in this species and a reduction of recombination is expected, we observed a lower recombination rate in the males (map length: 1371.5 cM) as compared with females (2089.8 cM). Furthermore, three loci previously documented to be sex-linked (that is, carrying male-specific alleles) in adults from the wild mapped to the same linkage group. The linkage map described in this study is one of the densest ones available for amphibians. The discovery of a sex linkage group in Rana temporaria, as well as other regions with strongly reduced male recombination rates, should help to uncover the genetic underpinnings of the sex-determination system in this species. As the number of linkage groups found (n = 15) is quite close to the actual number of chromosomes (n = 13), the map should provide a useful resource for further evolutionary, ecological and conservation genetic work in this and other closely related species.

  • 4. Cano, JM
    et al.
    Laurila, Anssi
    Uppsala University, Teknisk-naturvetenskapliga vetenskapsområdet, Faculty of Science and Technology, Biology, Department of Ecology and Evolution. Uppsala University, Teknisk-naturvetenskapliga vetenskapsområdet, Faculty of Science and Technology, Biology, Department of Ecology and Evolution, Population Biology. populationsbiologi.
    Palo, J
    Merilä, J
    Population differentiation in G matrix structure due to natural selection in Rana temporaria2004In: Evolution, Vol. 58, p. 2013-2020Article in journal (Refereed)
  • 5.
    Carreira, B. M.
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology. Univ Lisbon, cE3c Ctr Ecol Evolut & Environm Changes, Fac Ciencias, Bloco C2, P-1749016 Lisbon, Portugal.
    Segurado, P.
    Univ Lisbon, Inst Super Agron, Ctr Estudos Florestais, P-1349017 Lisbon, Portugal..
    Orizaola, German
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Goncalves, N.
    Univ Lisbon, cE3c Ctr Ecol Evolut & Environm Changes, Fac Ciencias, Bloco C2, P-1749016 Lisbon, Portugal..
    Pinto, V.
    Univ Lisbon, cE3c Ctr Ecol Evolut & Environm Changes, Fac Ciencias, Bloco C2, P-1749016 Lisbon, Portugal..
    Laurila, Anssi
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Rebelo, R.
    Univ Lisbon, cE3c Ctr Ecol Evolut & Environm Changes, Fac Ciencias, Bloco C2, P-1749016 Lisbon, Portugal..
    Warm vegetarians?: Heat waves and diet shifts in tadpoles2016In: Ecology, ISSN 0012-9658, E-ISSN 1939-9170, Vol. 97, no 11, p. 2964-2974Article in journal (Refereed)
    Abstract [en]

    Temperature can play an important role in determining the feeding preferences of ectotherms. In light of the warmer temperatures arising with the current climatic changes, omnivorous ectotherms may perform diet shifts toward higher herbivory to optimize energetic intake. Such diet shifts may also occur during heat waves, which are projected to become more frequent, intense, and longer lasting in the future. Here, we investigated how heat waves of different duration affect feeding preferences in omnivorous anuran tadpoles and how these choices affect larval life history. In laboratory experiments, we fed tadpoles of three species on animal, plant, or mixed diet and exposed them to short heat waves (similar to the heat waves these species experience currently) or long heat waves (predicted to increase under climate change). We estimated the dietary choices of tadpoles fed on the mixed diet using stable isotopes and recorded tadpole survival and growth, larval period, and mass at metamorphosis. Tadpole feeding preferences were associated with their thermal background, with herbivory increasing with breeding temperature in nature. Patterns in survival, growth, and development generally support decreased efficiency of carnivorous diets and increased efficiency or higher relative quality of herbivorous diets at higher temperatures. All three species increased herbivory in at least one of the heat wave treatments, but the responses varied among species. Diet shifts toward higher herbivory were maladaptive in one species, but beneficial in the other two. Higher herbivory in omnivorous ectotherms under warmer temperatures may impact species differently and further contribute to changes in the structure and function of freshwater environments.

  • 6.
    Carreira, Bruno M.
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology. Univ Lisbon, Fac Ciencias, Ctr Ecol Evolut & Environm Changes cE3c, Lisbon, Portugal.
    Segurado, Pedro
    Univ Lisbon, Inst Super Agron, Ctr Estudos Florestais, Lisbon, Portugal..
    Laurila, Anssi
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Rebelo, Rui
    Univ Lisbon, Fac Ciencias, Ctr Ecol Evolut & Environm Changes cE3c, Lisbon, Portugal..
    Can heat waves change the trophic role of the world's most invasive crayfish?: Diet shifts in Procambarus clarkii2017In: PLoS ONE, ISSN 1932-6203, E-ISSN 1932-6203, Vol. 12, no 9, article id e0183108Article in journal (Refereed)
    Abstract [en]

    In the Mediterranean basin, the globally increasing temperatures are expected to be accompanied by longer heat waves. Commonly assumed to benefit cold-limited invasive alien species, these climatic changes may also change their feeding preferences, especially in the case of omnivorous ectotherms. We investigated heat wave effects on diet choice, growth and energy reserves in the invasive red swamp crayfish, Procambarus clarkii. In laboratory experiments, we fed juvenile and adult crayfish on animal, plant or mixed diets and exposed them to a short or a long heat wave. We then measured crayfish survival, growth, body reserves and Fulton's condition index. Diet choices of the crayfish maintained on the mixed diet were estimated using stable isotopes (C-13 and N-15). The results suggest a decreased efficiency of carnivorous diets at higher temperatures, as juveniles fed on the animal diet were unable to maintain high growth rates in the long heat wave; and a decreased efficiency of herbivorous diets at lower temperatures, as juveniles in the cold accumulated less body reserves when fed on the plant diet. Heat wave treatments increased the assimilation of plant material, especially in juveniles, allowing them to sustain high growth rates in the long heat wave. Contrary to our expectations, crayfish performance decreased in the long heat wave, suggesting that Mediterranean summer heat waves may have negative effects on P. clarkii and that they are unlikely to boost its populations in this region. Although uncertain, it is possible that the greater assimilation of the plant diet resulted from changes in crayfish feeding preferences, raising the hypotheses that i) heat waves may change the predominant impacts of this keystone species and ii) that by altering species' trophic niches, climate change may alter the main impacts of invasive alien species.

  • 7.
    Cortazar-Chinarro, Maria
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Lattenkamp, Ella Z.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology. Max Planck Inst Psycholinguist, Dept Neurogenet Vocal Commun, Box 310, NL-6500 Nijmegen, Netherlands..
    Meyer-Lucht, Yvonne
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Luquet, Emilien
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology. Univ Claude Bernard Lyon I, CNRS, UMR 5023, LEHNA, 3-6 Rue Raphael Dubois,Batiments Darwin C & Forel, F-69622 Villeurbanne 43, France..
    Laurila, Anssi
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Höglund, Jacob
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Drift, selection, or migration?: Processes affecting genetic differentiation and variation along a latitudinal gradient in an amphibian2017In: BMC Evolutionary Biology, ISSN 1471-2148, E-ISSN 1471-2148, Vol. 17, article id 189Article in journal (Refereed)
    Abstract [en]

    Background: Past events like fluctuations in population size and post-glacial colonization processes may influence the relative importance of genetic drift, migration and selection when determining the present day patterns of genetic variation. We disentangle how drift, selection and migration shape neutral and adaptive genetic variation in 12 moor frog populations along a 1700 km latitudinal gradient. We studied genetic differentiation and variation at a MHC exon II locus and a set of 18 microsatellites. Results: Using outlier analyses, we identified the MHC II exon 2 (corresponding to the beta-2 domain) locus and one microsatellite locus (RCO8640) to be subject to diversifying selection, while five microsatellite loci showed signals of stabilizing selection among populations. STRUCTURE and DAPC analyses on the neutral microsatellites assigned populations to a northern and a southern cluster, reflecting two different post-glacial colonization routes found in previous studies. Genetic variation overall was lower in the northern cluster. The signature of selection on MHC exon II was weaker in the northern cluster, possibly as a consequence of smaller and more fragmented populations. Conclusion: Our results show that historical demographic processes combined with selection and drift have led to a complex pattern of differentiation along the gradient where some loci are more divergent among populations than predicted from drift expectations due to diversifying selection, while other loci are more uniform among populations due to stabilizing selection. Importantly, both overall and MHC genetic variation are lower at northern latitudes. Due to lower evolutionary potential, the low genetic variation in northern populations may increase the risk of extinction when confronted with emerging pathogens and climate change.

  • 8.
    Cortazar-Chinarro, Maria
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology. Uppsala University.
    Meyer-Lucht, Yvonne
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Laurila, Anssi
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Höglund, Jacob
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Signatures of historical selection on MHC reveal different selection patterns in the moor frog (Rana arvalis)2018In: Immunogenetics, ISSN 0093-7711, E-ISSN 1432-1211, Vol. 70, no 7, p. 477-484Article in journal (Refereed)
    Abstract [en]

    MHC genes are key components in disease resistance and an excellent system for studying selection acting on genetic variation in natural populations. Current patterns of variation in MHC genes are likely to be influenced by past and ongoing selection as well as demographic fluctuations in population size such as those imposed by post-glacial recolonization processes. Here, we investigated signatures of historical selection and demography on an MHC class II gene in 12 moor frog populations along a 1700-km latitudinal gradient. Sequences were obtained from 207 individuals and consecutively assigned into two different clusters (northern and southern clusters, respectively) in concordance with a previously described dual post-glacial colonization route. Selection analyses comparing the relative rates of non-synonymous to synonymous substitutions (dN/dS) suggested evidence of different selection patterns in the northern and the southern clusters, with divergent selection prevailing in the south but uniform positive selection predominating in the north. Also, models of codon evolution revealed considerable differences in the strength of selection: The southern cluster appeared to be under strong selection while the northern cluster showed moderate signs of selection. Our results indicate that the MHC alleles in the north diverged from southern MHC alleles as a result of differential selection patterns.

  • 9.
    Dahl, Emma
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Population and Conservation Biology.
    Orizaola, German
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Population and Conservation Biology.
    Nicieza, A. G.
    Laurila, Anssi
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Population and Conservation Biology.
    Time constraints and flexibility of growth strategies: Geographic variation in catch-up growth responses in amphibian larvae2012In: Journal of Animal Ecology, ISSN 0021-8790, E-ISSN 1365-2656, Vol. 81, no 6, p. 1233-1243Article in journal (Refereed)
    Abstract [en]

    1. As size is tightly associated with fitness, compensatory strategies for growth loss can be vital for restoring individual fitness. However, immediate and delayed costs of compensatory responses may prevent their generalization, and the optimal strategy may depend on environmental conditions. Compensatory responses may be particularly important in high-latitude habitats with short growing seasons, and thus, high-latitude organisms might be more efficient at compensating after periods of unfavourable growth conditions than low-latitude organisms. 2. We investigated geographical differences in catch-up growth strategies of populations of the common frog (Rana temporaria) from southern and northern Sweden in two factorial common garden experiments involving predation risk and two different causes of growth arrest (nutritional stress and low temperatures) to evaluate how the compensatory strategies can be affected by context-dependent costs of compensation. Larval and metamorphic traits, and post-metamorphic performance were used as response variables. 3. Only northern tadpoles exposed to low food completely caught up in terms of metamorphic size, mainly by extending the larval period. Low food decreased survival and post-metamorphic jumping performance in southern, but not in northern tadpoles, suggesting that northern tadpoles have a better ability to compensate after periods of restricted food. 4. Both northern and southern tadpoles were able to metamorphose at the same size as control tadpoles after being exposed to low temperatures, indicating that consequences of variation in temperature and food availability differed for tadpoles. However, the combination of low temperatures and predation risk reduced survival in both southern and northern tadpoles. Also, predation risk decreased energy storage in both experiments. 5. Our results highlight the influence of climatic variation and the type of stressor as selective factors shaping compensatory strategies.

  • 10.
    Dahl, Emma
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Population and Conservation Biology.
    Orizaola, German
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Population and Conservation Biology.
    Winberg, Svante
    Uppsala University, Disciplinary Domain of Medicine and Pharmacy, Faculty of Medicine, Department of Neuroscience, Physiology.
    Laurila, Anssi
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Population and Conservation Biology.
    Geographic variation in corticosterone response to chronic predator stress in tadpoles2012In: Journal of Evolutionary Biology, ISSN 1010-061X, E-ISSN 1420-9101, Vol. 25, no 6, p. 1066-1076Article in journal (Refereed)
    Abstract [en]

    Chronic stress often affects growth and development negatively, and these effects are often mediated via glucocorticoid hormones, which elevate during stress. We investigated latitudinal variation in corticosterone (CORT) response to chronic predator stress in Rana temporaria tadpoles along a 1500-km latitudinal cline in Sweden tadpoles, in a laboratory experiment. We hypothesized that more time-constrained high-latitude populations have evolved a lower CORT response to chronic stress to maintain higher growth under stressful conditions. Southern tadpoles had higher CORT content in response to predators after 1 day of exposure, whereas there was no increase in CORT in the northern populations. Two weeks later, there were no predator-induced CORT elevations. Artificially elevated CORT levels strongly decreased growth, development and survival in both northern and southern tadpoles. We suggest that the lower CORT response in high-latitude populations can be connected with avoidance of CORT-mediated reduction in growth and development, but also discuss other possible explanations.

  • 11.
    Dijk, Ben
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Laurila, Anssi
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Orizaola, German
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Johansson, Frank
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Is one defence enough?: Disentangling the relative importance of morphological and behavioural predator-induced defences2016In: Behavioral Ecology and Sociobiology, ISSN 0340-5443, E-ISSN 1432-0762, Vol. 70, no 2, p. 237-246Article in journal (Refereed)
    Abstract [en]

    Many organisms show predator-induced behavioural and morphological phenotypic plasticity. These defence mechanisms are often expressed simultaneously. To estimate the relative importance of these two defences, we conducted a laboratory experiment using tadpoles of the common frog (Rana temporaria) as prey and Aeshna dragonfly larvae as predators. We first raised tadpoles in the presence and absence of caged predators to induce differences in defensive morphology, and then conducted free ranging predator trials in environments that were either with or without the presence of predation cues to induce differences in defensive behaviour. This 2 x 2 design allowed us to separate the effects of inducible morphology from inducible behaviour. Caged predators induced deeper bodies and tailfins and reduced activity levels in tadpoles. The time to first capture was shortest in tadpoles without morphological or behavioural defences. Tadpoles with a behavioural defence had a significantly longer time to first capture. Tadpoles with only antipredator morphology tended to have a longer time to first capture as compared to those without any induced defences. This treatment also had a higher number of injured tadpoles as compared to other treatments, suggesting that inducible morphology facilitates predator escape due to the 'lure effect'. However, tadpoles with both behavioural and morphological defences did not have a longer time to first capture as compared to tadpoles with only morphological or behavioural induced defences. Our results suggest that both behavioural and morphological antipredator responses contribute to reduced capture efficiency by predators, but their simultaneous expression did not have any additive effect to the time of first capture and survival, and that the morphology response is most effective when tadpoles are active.

  • 12. Egea-Serrano, Andres
    et al.
    Hangartner, Sandra
    Laurila, Anssi
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Rasanen, Katja
    Multifarious selection through environmental change: acidity and predator-mediated adaptive divergence in the moor frog (Rana arvalis)2014In: Proceedings of the Royal Society of London. Biological Sciences, ISSN 0962-8452, E-ISSN 1471-2954, Vol. 281, no 1780Article in journal (Refereed)
    Abstract [en]

    Environmental change can simultaneously cause abiotic stress and alter biological communities, yet adaptation of natural populations to co-changing environmental factors is poorly understood. We studied adaptation to acid and predator stress in six moor frog (Rana arvalis) populations along an acidification gradient, where abundance of invertebrate predators increases with increasing acidity of R. arvalis breeding ponds. First, we quantified divergence among the populations in anti-predator traits (behaviour and morphology) at different rearing conditions in the laboratory (factorial combinations of acid or neutral pH and the presence or the absence of a caged predator). Second, we evaluated relative fitness (survival) of the populations by exposing tadpoles from the different rearing conditions to predation by free-ranging dragonfly larvae. We found that morphological defences (relative tail depth) as well as survival of tadpoles under predation increased with increasing pond acidity (under most experimental conditions). Tail depth and larval size mediated survival differences among populations, but the contribution of trait divergence to survival was strongly dependent on prior rearing conditions. Our results indicate that R. arvalis populations are adapted to the elevated predator pressure in acidified ponds and emphasize the importance of multifarious selection via both direct (here: pH) and indirect (here: predators) environmental changes.

  • 13.
    Fisher, Matthew C.
    et al.
    Imperial Coll London, Sch Publ Hlth, Fac Med, Dept Infect Dis Epidemiol, St Marys Campus, London W2 1PG, England.
    Ghosh, Pria
    Imperial Coll London, Sch Publ Hlth, Fac Med, Dept Infect Dis Epidemiol, St Marys Campus, London W2 1PG, England;North West Univ, Unit Environm Sci & Management, Private Bag x6001, ZA-2520 Potchefstroom, South Africa.
    Shelton, Jennifer M. G.
    Imperial Coll London, Sch Publ Hlth, Fac Med, Dept Infect Dis Epidemiol, St Marys Campus, London W2 1PG, England.
    Bates, Kieran
    Imperial Coll London, Sch Publ Hlth, Fac Med, Dept Infect Dis Epidemiol, St Marys Campus, London W2 1PG, England.
    Brookes, Lola
    Inst Zool, Regents Pk, London NW1 4RY, England.
    Wierzbicki, Claudia
    Imperial Coll London, Sch Publ Hlth, Fac Med, Dept Infect Dis Epidemiol, St Marys Campus, London W2 1PG, England.
    Rosa, Goncalo M.
    Inst Zool, Regents Pk, London NW1 4RY, England;Univ Lisbon, Fac Ciencias, Ctr Ecol Evolut & Environm Changes CE3C, Lisbon, Portugal.
    Farrer, Rhys A.
    Imperial Coll London, Sch Publ Hlth, Fac Med, Dept Infect Dis Epidemiol, St Marys Campus, London W2 1PG, England.
    Aanensen, David M.
    Imperial Coll London, Sch Publ Hlth, Fac Med, Dept Infect Dis Epidemiol, St Marys Campus, London W2 1PG, England;Ctr Genom Pathogen Surveillance, Wellcome Genome Campus, Hinxton, Cambs, England.
    Alvarado-Rybak, Mario
    Univ Andres Bello, Fac Ecol & Recursos Nat, Ctr Invest Sustentabilidad, Republ 440, Santiago, Chile.
    Bataille, Arnaud
    Seoul Natl Univ, Sch Biol Sci, Lab Behav & Populat Ecol, Seoul 08826, South Korea;CIRAD, UMR ASTRE, F-34398 Montpellier, France;Univ Montpellier, ASTRE, CIRAD, INRA, Montpellier, France.
    Berger, Lee
    James Cook Univ, Coll Publ Hlth Med & Vet Sci, Hlth Res Grp 1, Townsville, Qld 4811, Australia.
    Böll, Susanne
    Agcy Populat Ecol & Nat Conservancy, Gerbrunn, Germany.
    Bosch, Jaime
    CSIC, Museo Nacl Ciencias Nat, C Jose Gutierrez Abascal 2, E-28006 Madrid, Spain.
    Clare, Frances C.
    Imperial Coll London, Sch Publ Hlth, Fac Med, Dept Infect Dis Epidemiol, St Marys Campus, London W2 1PG, England.
    Courtois, Elodie A.
    Univ Guyane, CNRS, IFREMER, LEEISA, Cayenne 97300, French Guiana.
    Crottini, Angelica
    Univ Porto, InBIO, CIBIO Ctr Invest Biodiversidade & Recursos Genet, P-4485661 Vairao, Portugal.
    Cunningham, Andrew A.
    Inst Zool, Regents Pk, London NW1 4RY, England.
    Doherty-Bone, Thomas M.
    Royal Zool Soc Scotland, Conservat Programmes, Edinburgh, Midlothian, Scotland.
    Gebresenbet, Fikirte
    Oklahoma State Univ, Dept Integrat Biol, Life Sci West 113, Stillwater, OK 74078 USA.
    Gower, David J.
    Nat Hist Museum, Life Sci, London SW7 5BD, England.
    Höglund, Jacob
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    James, Timothy Y.
    Univ Michigan, Dept Ecol & Evolutionary Biol, Ann Arbor, MI 48109 USA.
    Jenkinson, Thomas S.
    Univ Michigan, Dept Ecol & Evolutionary Biol, Ann Arbor, MI 48109 USA.
    Kosch, Tiffany A.
    Seoul Natl Univ, Sch Biol Sci, Lab Behav & Populat Ecol, Seoul 08826, South Korea;James Cook Univ, Coll Publ Hlth Med & Vet Sci, Hlth Res Grp 1, Townsville, Qld 4811, Australia.
    Lambertini, Carolina
    Univ Estadual Campinas, Inst Biol, Dept Biol Anim, Lab Hist Nat Anfibios Brasileiros, BR-13083862 Campinas, SP, Brazil.
    Laurila, Anssi
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Lin, Chun-Fu
    Endem Species Res Inst, Zool Div, 1 Ming Shen East Rd, Nantou 552, Taiwan.
    Loyau, Adeline
    UFZ Helmholtz Ctr Environm Res, Dept Conservat Biol, Permoserstr 15, D-04318 Leipzig, Germany;Univ Toulouse, CNRS, ECOLAB, INPT,UPS, Toulouse, France.
    Martel, An
    Univ Ghent, Dept Pathol Bacteriol & Avian Dis, Fac Vet Med, Salisburylaan 133, B-9820 Merelbeke, Belgium.
    Meurling, Sara
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Miaud, Claude
    Univ Paul Valery Montpellier, Univ Montpellier, PSL Res Univ, CEFE,UMR 5175,CNRS,EPHE,Biogeog & Ecol Vertebres, Montpellier, France.
    Minting, Pete
    Amphibian & Reptile Conservat ARC Trust, 655A Christchurch Rd, Bournemouth BH1 4AP, Dorset, England.
    Ndriantsoa, Serge
    Durrell Wildlife Conservat Trust, Madagascar Programme, Antananarivo, Madagascar.
    O'Hanlon, Simon J.
    Imperial Coll London, Sch Publ Hlth, Fac Med, Dept Infect Dis Epidemiol, St Marys Campus, London W2 1PG, England;Inst Zool, Regents Pk, London NW1 4RY, England.
    Pasmans, Frank
    Univ Ghent, Dept Pathol Bacteriol & Avian Dis, Fac Vet Med, Salisburylaan 133, B-9820 Merelbeke, Belgium.
    Rakotonanahary, Tsanta
    Durrell Wildlife Conservat Trust, Madagascar Programme, Antananarivo, Madagascar.
    Rabemananjara, Falitiana C. E.
    Durrell Wildlife Conservat Trust, Madagascar Programme, Antananarivo, Madagascar;IUCN SSC Amphibian Specialist Grp Madagascar, Antananarivo 101, Madagascar.
    Ribeiro, Luisa P.
    Univ Estadual Campinas, Inst Biol, Dept Biol Anim, Lab Hist Nat Anfibios Brasileiros, BR-13083862 Campinas, SP, Brazil.
    Schmeller, Dirk S.
    UFZ Helmholtz Ctr Environm Res, Dept Conservat Biol, Permoserstr 15, D-04318 Leipzig, Germany;Univ Toulouse, CNRS, ECOLAB, INPT,UPS, Toulouse, France.
    Schmidt, Benedikt R.
    Univ Zurich, Dept Evolutionary Biol & Environm Studies, Winterthurerstr 190, CH-8057 Zurich, Switzerland;Univ Neuchatel, Info Fauna Karch, Bellevaux 51,UniMail Batiment 6, CH-2000 Neuchatel, Switzerland.
    Skerratt, Lee
    James Cook Univ, Coll Publ Hlth Med & Vet Sci, Hlth Res Grp 1, Townsville, Qld 4811, Australia.
    Smith, Freya
    APHA, Natl Wildlife Management Ctr, Woodchester Pk GL10 3UJ, Glos, England.
    Soto-Azat, Claudio
    Univ Andres Bello, Fac Ecol & Recursos Nat, Ctr Invest Sustentabilidad, Republ 440, Santiago, Chile.
    Tessa, Giulia
    Nonprofit Assoc Zirichiltaggi Sardinia Wildlife C, Str Vicinale Filigheddu 62-C, I-07100 Sassari, Italy.
    Toledo, Luis Felipe
    Univ Estadual Campinas, Inst Biol, Dept Biol Anim, Lab Hist Nat Anfibios Brasileiros, BR-13083862 Campinas, SP, Brazil.
    Valenzuela-Sanchez, Andres
    Univ Andres Bello, Fac Ecol & Recursos Nat, Ctr Invest Sustentabilidad, Republ 440, Santiago, Chile;ONG Ranita Darwin, Nataniel Cox 152, Santiago, Chile.
    Verster, Ruhan
    North West Univ, Unit Environm Sci & Management, Private Bag x6001, ZA-2520 Potchefstroom, South Africa.
    Vörös, Judit
    Hungarian Nat Hist Museum, Dept Zool, Collect Amphibians & Reptiles, Baross U 13, H-1088 Budapest, Hungary.
    Waldman, Bruce
    Seoul Natl Univ, Sch Biol Sci, Lab Behav & Populat Ecol, Seoul 08826, South Korea.
    Webb, Rebecca J.
    James Cook Univ, Coll Publ Hlth Med & Vet Sci, Hlth Res Grp 1, Townsville, Qld 4811, Australia.
    Weldon, Che
    North West Univ, Unit Environm Sci & Management, Private Bag x6001, ZA-2520 Potchefstroom, South Africa.
    Wombwell, Emma
    Inst Zool, Regents Pk, London NW1 4RY, England.
    Zamudio, Kelly R.
    Cornell Univ, Dept Ecol & Evolutionary Biol, Ithaca, NY 14853 USA.
    Longcore, Joyce E.
    Univ Maine, Sch Biol & Ecol, Orono, ME 04469 USA.
    Garner, Trenton W. J.
    Inst Zool, Regents Pk, London NW1 4RY, England;Nonprofit Assoc Zirichiltaggi Sardinia Wildlife C, Str Vicinale Filigheddu 62-C, I-07100 Sassari, Italy;North West Univ, Unit Environm Sci & Management, Private Bag x6001, ZA-2520 Potchefstroom, South Africa.
    Development and worldwide use of non-lethal, and minimal population-level impact, protocols for the isolation of amphibian chytrid fungi2018In: Scientific Reports, ISSN 2045-2322, E-ISSN 2045-2322, Vol. 8, article id 7772Article in journal (Refereed)
    Abstract [en]

    Parasitic chytrid fungi have emerged as a significant threat to amphibian species worldwide, necessitating the development of techniques to isolate these pathogens into culture for research purposes. However, early methods of isolating chytrids from their hosts relied on killing amphibians. We modified a pre-existing protocol for isolating chytrids from infected animals to use toe clips and biopsies from toe webbing rather than euthanizing hosts, and distributed the protocol to researchers as part of the BiodivERsA project RACE; here called the RML protocol. In tandem, we developed a lethal procedure for isolating chytrids from tadpole mouthparts. Reviewing a database of use a decade after their inception, we find that these methods have been applied across 5 continents, 23 countries and in 62 amphibian species. Isolation of chytrids by the non-lethal RML protocol occured in 18% of attempts with 207 fungal isolates and three species of chytrid being recovered. Isolation of chytrids from tadpoles occured in 43% of attempts with 334 fungal isolates of one species (Batrachochytrium dendrobatidis) being recovered. Together, these methods have resulted in a significant reduction and refinement of our use of threatened amphibian species and have improved our ability to work with this group of emerging pathogens.

  • 14. Givskov Sørensen, Jesper
    et al.
    Loeschcke, Volker
    Merilä, Juha
    Laurila, Anssi
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Population and Conservation Biology.
    Effects of predator exposure on Hsp70 expression and survival in tadpoles of the Common Frog (Rana temporaria)2011In: Canadian Journal of Zoology, ISSN 0008-4301, E-ISSN 1480-3283, Vol. 89, no 12, p. 1249-1255Article in journal (Refereed)
    Abstract [en]

    Predator-induced changes in prey behavior and morphology are widespread, but little is known about physiological and cellular-level responses in prey in response to predation risk. We investigated whether predator (larvae of the dragonfly Aeshna Fabricius, 1775) presence elevated the expression level of heat-shock protein 70 (Hsp70)-a commonly found response to stress-in tadpoles of the Common Frog (Rana temporaria L., 1758). In another experiment, we tested the survival of tadpoles in the presence of a free-ranging predator. Prior to this encounter, the tadpoles were exposed to either an Hsp-inducing environmental stress in the form of heat (31 degrees C) or to predator cues from a caged predator. We found no evidence for increased Hsp70 expression in tadpoles either in the presence of fed or starved predators. We did not find any effects of prior exposure to neither heat nor predator presence on survival at the end of experiment. Our results do not point to either Hsp70-mediated effect of predator-induced responses or to beneficial effects of the stress response on survival under predation risk.

  • 15. Gonda, A.
    et al.
    Trokovic, N.
    Herczeg, G.
    Laurila, Anssi
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Evolution, Population and Conservation Biology.
    Merilä, J.
    Predation- and competition-mediated brain plasticity in Rana temporaria tadpoles2010In: Journal of Evolutionary Biology, ISSN 1010-061X, E-ISSN 1420-9101, Vol. 23, no 11, p. 2300-2308Article in journal (Refereed)
    Abstract [en]

    An increasing number of studies have demonstrated phenotypic plasticity in brain size and architecture in response to environmental variation. However, our knowledge on how brain architecture is affected by commonplace ecological interactions is rudimentary. For example, while intraspecific competition and risk of predation are known to induce adaptive plastic modifications in morphology and behaviour in a wide variety of organisms, their effects on brain development have not been studied. We studied experimentally the influence of density and predation risk on brain development in common frog (Rana temporaria) tadpoles. Tadpoles grown at low density and under predation risk developed smaller brains than tadpoles at the other treatment combinations. Further, at high densities, tadpoles developed larger optic tecta and smaller medulla oblongata than those grown at low densities. These results demonstrate that ecological interactions - like intraspecific competition and predation risk - can have strong effects on brain development in lower vertebrates.

  • 16.
    Griesser, Michael
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology. Univ Zurich, Dept Anthropol;Univ Bern, Inst Ecol & Evolut.
    Mourocq, Emeline
    Univ Zurich, Dept Anthropol;Univ Bern, Inst Ecol & Evolut.
    Barnaby, Jonathan
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Bowgen, Katharine M.
    Bournemouth Univ, Fac Sci & Technol, Dept Life & Environm Sci.
    Eggers, Sonke
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology. Swedish Univ Agr Sci, Dept Ecol.
    Fletcher, Kevin
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Kozma, Radoslav
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Kurz, Franziska
    Laurila, Anssi
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Nystrand, Magdalena
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Sorato, Enrico
    Linkoping Univ, IFM Biol..
    Ekman, Jan
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Experience buffers extrinsic mortality in a group-living bird species2017In: Oikos, ISSN 0030-1299, E-ISSN 1600-0706, Vol. 126, no 9, p. 1258-1268Article in journal (Refereed)
    Abstract [en]

    Extrinsic mortality has a strong impact on the evolution of life-histories, prey morphology and behavioural adaptations, but for many animals the causes of mortality are poorly understood. Predation is an important driver of extrinsic mortality and mobile animals form groups in response to increased predation risk. Furthermore, in many species juveniles suffer higher mortality than older individuals, which may reflect a lower phenotypic quality, lower competitiveness, or a lack of antipredator or foraging skills. Here we assessed the causes of mortality for 371 radio tagged Siberian jays. This sedentary bird species lives in family groups that contain a breeding pair as well as related and unrelated non-breeders. Ninety-five percent of death were due to predation (n = 59 out of 62 individuals) and most individuals were killed by Accipiter hawks. Multivariate Cox proportional hazards models showed that non-breeders had a lower survival than breeders, but only in territories in managed forest with little visual cover. Examining breeders, only sex influenced survival with males having a lower survival than females. For non-breeders, juveniles had lower survival than older non-breeders, and those on managed territories had lower survival than those on unmanaged territories. Additionally, a low feather quality reduced the survival probability of non-breeders only. Thus, living on managed territories and having a low feature quality affected only non-breeders, particularly juveniles. These findings add to previous research demonstrating that juvenile Siberian jays acquire critical antipredator skills from experienced group members. Thus, experience can buffer extrinsic mortality, highlighting that group living not only provides safety in numbers, but also provide social opportunities to learn critical life-skills.

  • 17. Hangartner, S.
    et al.
    Laurila, Anssi
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Population and Conservation Biology.
    Raesaenen, K.
    The quantitative genetic basis of adaptive divergence in the moor frog (Rana arvalis) and its implications for gene flow2012In: Journal of Evolutionary Biology, ISSN 1010-061X, E-ISSN 1420-9101, Vol. 25, no 8, p. 1587-1599Article in journal (Refereed)
    Abstract [en]

    Knowledge on the relative contribution of direct genetic, maternal and environmental effects to adaptive divergence is important for understanding the drivers of biological diversification. The moor frog (Rana arvalis) shows adaptive divergence in embryonic and larval fitness traits along an acidification gradient in south-western Sweden. To understand the quantitative genetic basis of this divergence, we performed reciprocal crosses between three divergent population pairs and reared embryos and larvae at acid and neutral pH in the laboratory. Divergence in embryonic acid tolerance (survival) was mainly determined by maternal effects, whereas the relative contributions of maternal, additive and nonadditive genetic effects in larval life-history traits differed between traits, population pairs and rearing environments. These results emphasize the need to investigate the quantitative genetic basis of adaptive divergence in multiple populations and traits, as well as different environments. We discuss the implications of our findings for maintenance of local adaptation in the context of migrant and hybrid fitness.

  • 18. Hangartner, Sandra
    et al.
    Laurila, Anssi
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Population and Conservation Biology.
    Effects of the disinfectant Virkon S on early life-stages of the moor frog (Rana arvalis)2012In: Amphibia-Reptilia, ISSN 0173-5373, E-ISSN 1568-5381, Vol. 33, no 3-4, p. 349-353Article in journal (Refereed)
    Abstract [en]

    Emerging diseases, such as the chytrid fungus Batrachochytrium dendrobatidis, contribute to global population declines of amphibians. Virkon S is one of the most commonly used disinfectants to reduce risk of spreading such pathogens. Virkon S is classified as harmful to aquatic organisms, but until today no negative effects on tadpoles have been reported. We studied the effects of three concentrations of Virkon S on early life-stages (embryos and hatchlings) of the moor frog Rana anvils. Overall, Virkon S had no significant effects. However, hatching success was highest in the control treatment, suggesting that Virkon S may have weak negative effects on amphibian embryos. We suggest that further studies are needed to assess the negative effect of Virkon S on amphibians, and recommend that Virkon S is used with care and a minimized run-off into natural wetlands.

  • 19. Hangartner, Sandra
    et al.
    Laurila, Anssi
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Population and Conservation Biology.
    Räsänen, Katja
    Adaptive Divergence in Moor Frog (Rana Arvalis) Populations Along an Acidification Gradient: Inferences from QST-FST Correlations2012In: Evolution, ISSN 0014-3820, E-ISSN 1558-5646, Vol. 66, no 3, p. 867-881Article in journal (Refereed)
    Abstract [en]

    Microevolutionary responses to spatial variation in the environment seem ubiquitous, but the relative role of selection and neutral processes in driving phenotypic diversification remain often unknown. The moor frog (Rana arvalis) shows strong phenotypic divergence along an acidification gradient in Sweden. We here used correlations among population pairwise estimates of quantitative trait (PST or QST from common garden estimates of embryonic acid tolerance and larval life-history traits) and neutral genetic divergence (FST from neutral microsatellite markers), as well as environmental differences (pond pH, predator density, and latitude), to test whether this phenotypic divergence is more likely due to divergent selection or neutral processes. We found that trait divergence was more strongly correlated with environmental differences than the neutral marker divergence, suggesting that divergent natural selection has driven phenotypic divergence along the acidification gradient. Moreover, pairwise PSTs of embryonic acid tolerance and QSTs of metamorphic size were strongly correlated with breeding pond pH, whereas pairwise QSTs of larval period and growth rate were more strongly correlated with geographic distance/latitude and predator density, respectively. We suggest that incorporating measurements of environmental variation into QSTFST studies can improve our inferential power about the agents of natural selection in natural populations.

  • 20. Hangartner, Sandra
    et al.
    Laurila, Anssi
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Population and Conservation Biology.
    Räsänen, Katja
    Adaptive divergence of the moor frog (Rana arvalis) along an acidification gradient2011In: BMC Evolutionary Biology, ISSN 1471-2148, E-ISSN 1471-2148, Vol. 11, p. 366-Article in journal (Refereed)
    Abstract [en]

    Background: Environmental stress can result in strong ecological and evolutionary effects on natural populations, but to what extent it drives adaptive divergence of natural populations is little explored. We used common garden experiments to study adaptive divergence in embryonic and larval fitness traits (embryonic survival, larval growth, and age and size at metamorphosis) in eight moor frog, Rana arvalis, populations inhabiting an acidification gradient (breeding pond pH 4.0 to 7.5) in southwestern Sweden. Embryos were raised until hatching at three (pH 4.0, 4.3 and 7.5) and larvae until metamorphosis at two (pH 4.3 and 7.5) pH treatments. To get insight into the putative selective agents along this environmental gradient, we measured relevant abiotic and biotic environmental variables from each breeding pond, and used linear models to test for phenotype-environment correlations.

    Results: We found that acid origin populations had higher embryonic and larval acid tolerance (survival and larval period were less negatively affected by low pH), higher larval growth but slower larval development rates, and metamorphosed at a larger size. The phenotype-environment correlations revealed that divergence in embryonic acid tolerance and metamorphic size correlated most strongly with breeding pond pH, whereas divergence in larval period and larval growth correlated most strongly with latitude and predator density, respectively.

    Conclusion: Our results suggest that R. arvalis has diverged in response to pH mediated selection along this acidification gradient. However, as latitude and pH were closely spatially correlated in this study, further studies are needed to disentangle the specific agents of natural selection along acidification gradients. Our study highlights the need to consider the multiple interacting selective forces that drive adaptive divergence of natural populations along environmental stress gradients.

  • 21. Hettyey, A.
    et al.
    Vincze, K.
    Zsarnoczai, S.
    Hoi, H.
    Laurila, Anssi
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Population and Conservation Biology.
    Costs and benefits of defences induced by predators differing in dangerousness2011In: Journal of Evolutionary Biology, ISSN 1010-061X, E-ISSN 1420-9101, Vol. 24, no 5, p. 1007-1019Article in journal (Refereed)
    Abstract [en]

    While theoretical studies predict that inducible defences should be fine-tuned according to the qualities of the predator, very few studies have investigated how dangerousness of predators, i.e. the rate at which predators kill prey individuals, affects the strength of phenotypic responses and resulting benefits and costs of induced defences. We performed a comprehensive study on fitness consequences of predator-induced responses by involving four predators (leech, water scorpion, dragonfly larva and newt), evaluating costs and benefits of responses, testing differences in dangerousness between predators and measuring responses in several life history traits of prey. We raised Rana dalmatina tadpoles in the presence of free-ranging predators, in the presence of caged predators, and exposed naive and experienced tadpoles to free-ranging predators. Tadpoles adjusted the intensities of their behavioural and morphological defences to predator dangerousness. Survival was lower in the nonlethal presence of the most dangerous predator, while we could not detect costs of induced defences at or after metamorphosis. When exposed to free-ranging predators, small, but not large, tadpoles benefited from exhibiting an induced phenotype in terms of elevated survival when compared to naive tadpoles, but we did not observe higher survival either in tadpoles exhibiting more extreme phenotypes or in tadpoles exposed to the type of predator they were raised with. These results indicate that while predator-induced defences can mirror dangerousness of predators, costs and benefits do not necessarily scale to the magnitude of plastic responses.

  • 22. Hettyey, Attila
    et al.
    Herczeg, Gabor
    Laurila, Anssi
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Evolution, Population Biology.
    Crochet, Pierre-Andre
    Merila, Juha
    Body temperature, size, nuptial colouration and mating success in male Moor Frogs (Rana arvalis)2009In: Amphibia-Reptilia, ISSN 0173-5373, E-ISSN 1568-5381, Vol. 30, no 1, p. 37-43Article in journal (Refereed)
    Abstract [en]

    Variation in colouration has rarely been related to sexual Selection ill anuran amphibians, even though such a relationship has been proven for many other vertebrate taxa. Male and female Moor Frogs (Rana arvalis) have a cryptic brown colour pattern, but males develop a conspicuous blue nuptial colouration during the reproductive season. To investigate: the possibility that colouration plays a role in sexual selection in this species, we Studied the temporal variation in blue colouration. determined if body size or body temperature affected blueness and investigated if blueness of males could be related to their mating, success. Results confirmed previous observation,,, that males develop and maintain blue colouration for only a very few nights during peak reproductive activity. Colouration of males was unrelated to body size, but males exhibiting higher body temperatures were somewhat bluer (hall males with lower body temperatures. Further, males in amplexus had higher body temperatures than non-mated males. Finally, Mating Success Was positively related to blueness in small males, whereas in large males no such relationship was detected. While our results align with the hypothesis that the bright blue colouration of males may be a target of sexual selection. alternative explanations are also discussed.

  • 23. Hettyey, Attila
    et al.
    Laurila, Anssi
    Uppsala University, Teknisk-naturvetenskapliga vetenskapsområdet, Faculty of Science and Technology, Biology, Department of Ecology and Evolution. Uppsala University, Teknisk-naturvetenskapliga vetenskapsområdet, Faculty of Science and Technology, Biology, Department of Ecology and Evolution, Population Biology. populationsbiologi.
    Herczeg, G
    Jönsson, KI
    Kovacs, T
    Merilä, Juha
    Does testis weight decline towards the Subarctic? A case study on the common frog, Rana temporaria2005In: Naturwissenschaften, Vol. 92, p. 188-192Article in journal (Refereed)
  • 24. Hettyey, Attila
    et al.
    Zsarnoczai, Szilvia
    Vincze, Krisztina
    Hoi, Herbert
    Laurila, Anssi
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Population and Conservation Biology.
    Interactions between the information content of different chemical cues affect induced defences in tadpoles2010In: Oikos, ISSN 0030-1299, E-ISSN 1600-0706, Vol. 119, no 11, p. 1814-1822Article in journal (Refereed)
    Abstract [en]

    Animals often alter their behaviour, morphology and physiology in the presence of predators. These induced defences can be fine-tuned by a variety of environmental factors such as predator species, acute predation risk or food availability. It has, however, remained unclear what cues influence the extent and quality of induced defences and how the information content of these cues interact to determine the development of antipredator defences. We performed an experiment to study the significance of direct chemical cues, originating from the predators themselves, and indirect cues, released by attacked or consumed prey, for phenotypic responses in Rana dalmatina tadpoles. We reared tadpoles in the presence of caged predators (Triturus vulgaris, Aeshna cyanea) fed either one or three tadpoles every other day outside the tadpole-rearing tanks. Fifteen hours after food provisioning, predators were put back into the tanks containing focal tadpoles either after washing (direct + digestion-released cues) or with the water containing remnants of the prey (direct + all types of indirect cues). Our results suggest that direct cues together with digestion-released cues can be sufficient to induce strong antipredator responses. Induced defences depended on both direct cues, affecting predator-specific responses, and the quantity of indirect cues, resulting in graded responses to differences in predation threat. Moreover, direct and indirect cues interacted in behaviour, resulting in predator-specific graded responses. We also observed a decrease in the extent of predator-induced responses in large tadpoles as compared to small ones. Our results, thus, suggest that prey integrate multiple cues about predators to optimize induced defences and that this process changes during ontogeny.

  • 25.
    Hjernquist, Mårten B.
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Population and Conservation Biology.
    Söderman, Fredrik
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Population and Conservation Biology.
    Jonsson, K. Ingemar
    Herczeg, Gabor
    Laurila, Anssi
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Population and Conservation Biology.
    Merila, Juha
    Seasonality determines patterns of growth and age structure over a geographic gradient in an ectothermic vertebrate2012In: Oecologia, ISSN 0029-8549, E-ISSN 1432-1939, Vol. 170, no 3, p. 641-649Article in journal (Refereed)
    Abstract [en]

    Environmental variation connected with seasonality is likely to affect the evolution of life-history strategies in ectotherms, but there is no consensus as to how important life-history traits like body size are influenced by environmental variation along seasonal gradients. We compared adult body size, skeletal growth, mean age, age at first reproduction and longevity among 11 common frog (Rana temporaria) populations sampled along a 1,600-km-long latitudinal gradient across Scandinavia. Mean age, age at first reproduction and longevity increased linearly with decreasing growth season length. Lifetime activity (i.e. the estimated number of active days during life-time) was highest at mid-latitudes and females had on average more active days throughout their lives than males. Variation in body size was due to differences in lifetime activity among populations-individuals (especially females) were largest where they had the longest cumulative activity period-as well as to differences between populations in skeletal growth rate as determined by skeletochronological analyses. Especially, males grew faster at intermediate latitudes. While life-history trait variation was strongly associated with latitude, the direction and shape of these relationships were sex- and trait-specific. These context-dependent relationships may be the result of life-history trade-offs enforced by differences in future reproductive opportunities and time constraints among the populations. Thus, seasonality appears to be an important environmental factor shaping life-history trait variation in common frogs.

  • 26.
    Johansson, Magnus P.
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Ermold, Friederike
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Kristjansson, B. K.
    Holar Univ Coll, Aquaculture & Fish Biol, Sauoarkrokur, Iceland..
    Laurila, Anssi
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Divergence of gastropod life history in contrasting thermal environments in a geothermal lake2016In: Journal of Evolutionary Biology, ISSN 1010-061X, E-ISSN 1420-9101, Vol. 29, no 10, p. 2043-2053Article in journal (Refereed)
    Abstract [en]

    Experiments using natural populations have provided mixed support for thermal adaptation models, probably because the conditions are often confounded with additional environmental factors like seasonality. The contrasting geothermal environments within Lake Myvatn, northern Iceland, provide a unique opportunity to evaluate thermal adaptation models using closely located natural populations. We conducted laboratory common garden and field reciprocal transplant experiments to investigate how thermal origin influences the life history of Radix balthica snails originating from stable cold (6 degrees C), stable warm (23 degrees C) thermal environments or from areas with seasonal temperature variation. Supporting thermal optimality models, warm-origin snails survived poorly at 6 degrees C in the common garden experiment and better than cold-origin and seasonal-origin snails in the warm habitat in the reciprocal transplant experiment. Contrary to thermal adaptation models, growth rate in both experiments was highest in the warm populations irrespective of temperature, indicating cogradient variation. The optimal temperatures for growth and reproduction were similar irrespective of origin, but cold-origin snails always had the lowest performance, and seasonal- origin snails often performed at an intermediate level compared to snails originating in either stable environment. Our results indicate that central life-history traits can differ in their mode of evolution, with survival following the predictions of thermal optimality models, whereas ecological constraints have shaped the evolution of growth rates in local populations.

  • 27.
    Johansson, Magnus P.
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Laurila, Anssi
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Maximum thermal tolerance trades off with chronic tolerance of high temperature in contrasting thermal populations of Radix balthica2017In: Ecology and Evolution, ISSN 2045-7758, E-ISSN 2045-7758, Vol. 7, no 9, p. 3149-3156Article in journal (Refereed)
    Abstract [en]

    Thermal adaptation theory predicts that thermal specialists evolve in environments with low temporal and high spatial thermal variation, whereas thermal generalists are favored in environments with high temporal and low spatial variation. The thermal environment of many organisms is predicted to change with globally increasing temperatures and thermal specialists are presumably at higher risk than thermal generalists. Here we investigated critical thermal maximum (CTmax) and preferred temperature (T-p) in populations of the common pond snail (Radix balthica) originating from a small-scale system of geothermal springs in northern Iceland, where stable cold (ca. 7 degrees C) and warm (ca. 23 degrees C) habitats are connected with habitats following the seasonal thermal variation. Irrespective of thermal origin, we found a common T-p for all populations, corresponding to the common temperature optimum (T-opt) for fitness-related traits in these populations. Warm-origin snails had lowest CTmax. As our previous studies have found higher chronic temperature tolerance in the warm populations, we suggest that there is a trade-off between high temperature tolerance and performance in other fitness components, including tolerance to chronic thermal stress. T-p and CTmax were positively correlated in warm-origin snails, suggesting a need to maintain a minimum "warming tolerance" (difference in CTmax and habitat temperature) in warm environments. Our results highlight the importance of high mean temperature in shaping thermal performance curves.

  • 28.
    Johansson, Magnus P.
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Quintela, M.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology. Univ A Coruna, Grp Invest BIOCOST, La Coruna, Spain.;Inst Marine Res, Populat Genet, Box 1870 Nordnes, N-5817 Bergen, Norway..
    Laurila, Anssi
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Genetic divergence and isolation by thermal environment in geothermal populations of an aquatic invertebrate2016In: Journal of Evolutionary Biology, ISSN 1010-061X, E-ISSN 1420-9101, Vol. 29, no 9, p. 1701-1712Article in journal (Refereed)
    Abstract [en]

    Temperature is one of the most influential forces of natural selection impacting all biological levels. In the face of increasing global temperatures, studies over small geographic scales allowing investigations on the effects of gene flow are of great value for understanding thermal adaptation. Here, we investigated genetic population structure in the freshwater gastropod Radix balthica originating from contrasting thermal habitats in three areas of geothermal activity in Iceland. Snails from 32 sites were genotyped at 208 AFLP loci. Five AFLPs were identified as putatively under divergent selection in Lake Myvatn, a geothermal lake with an almost 20 degrees C difference in mean temperature across a distance of a few kilometres. In four of these loci, variation across all study populations was correlated with temperature. We found significant population structure in neutral markers both within and between the areas. Cluster analysis using neutral markers classified the sites mainly by geography, whereas analyses using markers under selection differentiated the sites based on temperature. Isolation by distance was stronger in the neutral than in the outlier loci. Pairwise differences based on outlier F-ST were significantly correlated with temperature at different spatial scales, even after correcting for geographic distance or neutral pairwise F-ST differences. In general, genetic variation decreased with increasing environmental temperature, possibly suggesting that natural selection had reduced the genetic diversity in the warm origin sites. Our results emphasize the influence of environmental temperature on the genetic structure of populations and suggest local thermal adaptation in these geothermal habitats.

  • 29.
    Jones, M
    et al.
    Uppsala University, Teknisk-naturvetenskapliga vetenskapsområdet, Faculty of Science and Technology, Biology, Department of Evolutionary Biology. Department of Ecology and Evolution, Population Biology.
    Laurila, A
    Uppsala University, Teknisk-naturvetenskapliga vetenskapsområdet, Faculty of Science and Technology, Biology, Department of Evolutionary Biology. Department of Ecology and Evolution, Population Biology. populationsbiologi.
    Peuhkuri, N
    Piironen, J
    Seppä, T
    Timing an ontogenetic niche shift: responses of emerging salmon alevins to chemical cues from predators and competitors2003In: Oikos, Vol. 102, p. 155-163Article in journal (Refereed)
  • 30. Kuparinen, Anna
    et al.
    Laugen, Ane T.
    Laurila, Anssi
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Population and Conservation Biology.
    Merilä, Juha
    Developmental threshold model challenged by temperature2010In: Evolutionary Ecology Research, ISSN 1522-0613, E-ISSN 1937-3791, Vol. 12, no 7, p. 821-829Article in journal (Refereed)
    Abstract [en]

    Question: Does the L-shape of the reaction norm for age and size at ontogenetic transitions arise irrespective of temperature? The developmental threshold model suggests that this shape arises due to a threshold in body size to undertake the transition. Data studied: Ages and sizes at metamorphosis measured in a common garden experiment in Rana temporaria originating from six populations along a latitudinal gradient. Individuals were exposed to three temperature treatments and two levels of food. Search method: Population-specific age and size at metamorphosis were plotted against each other, and the shape of the reaction norm across populations was further illustrated by an exponential decay function. The observed patterns were further explored via linear mixed-effect models. Conclusion: The L-shape of the reaction norm depends on temperature, suggesting that at low temperature a developmental threshold in age rather than in size regulates the process of metamorphosis.

  • 31.
    Laugen, Ane T
    et al.
    Uppsala University, Teknisk-naturvetenskapliga vetenskapsområdet, Faculty of Science and Technology, Biology, Department of Ecology and Evolution. Uppsala University, Teknisk-naturvetenskapliga vetenskapsområdet, Faculty of Science and Technology, Biology, Department of Ecology and Evolution, Population Biology. populationsbiologi.
    Kruuk, LEB
    Laurila, Anssi
    Uppsala University, Teknisk-naturvetenskapliga vetenskapsområdet, Faculty of Science and Technology, Biology, Department of Ecology and Evolution. Uppsala University, Teknisk-naturvetenskapliga vetenskapsområdet, Faculty of Science and Technology, Biology, Department of Ecology and Evolution, Population Biology. populationsbiologi.
    Räsänen, Katja
    Uppsala University, Teknisk-naturvetenskapliga vetenskapsområdet, Faculty of Science and Technology, Biology, Department of Ecology and Evolution. Uppsala University, Teknisk-naturvetenskapliga vetenskapsområdet, Faculty of Science and Technology, Biology, Department of Ecology and Evolution, Population Biology. populationsbiologi.
    Stone, J
    Merilä, Juha
    Quantitative genetics of larval life-history traits in Rana temporaria in different environmental conditions2005In: Genetical research, Vol. 86, p. 161-170Article in journal (Refereed)
  • 32.
    Laugen, Ane T.
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Evolutionary Biology, Population Biology.
    Laurila, Anssi
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Evolutionary Biology, Population Biology.
    Jönsson, J. Ingemar
    Söderman, Fredrik
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Evolutionary Biology, Population Biology.
    Merilä, Juha
    Do common frogs (Rana temporaria) follow Bergmann’s rule?2005In: Evolutionary Ecology Research, ISSN 1522-0613, E-ISSN 1937-3791, Vol. 7, no 5, p. 717-731Article in journal (Refereed)
    Abstract [en]

    Questions: Does intraspecific extension of Bergmanns rule – larger size within a species incooler areas – hold true for ectotherms in general, and for the common frog (Rana temporaria)in particular? What is the relative importance of genetic and environmental factors (i.e. directenvironmental induction) in determining latitudinal patterns of body size variation in commonfrogs?Methods: We tested for a positive association between mean body size and latitude incommon frogs (Rana temporaria) across a 1600 km long latitudinal gradient in Scandinaviaboth for wild-collected adults and laboratory-reared metamorphs.Results: In adults, the mean body size increased from south to mid-latitudes, and declinedthereafter. This occurred despite the fact that the mean age of adult frogs increased withincreasing latitude, and age and body size were positively correlated. The latitudinal pattern ofbody size variation in metamorphs reared in a common garden experiment was similar to thatobserved among wild-caught adults.Conclusions: The results suggest that the concave pattern of body size variation across thelatitudinal cline may be at least partly genetically determined, and that although there isconsiderable geographic variation in mean body size of R. temporaria, this variation does notconform with Bergmann’s rule.

  • 33.
    Laugen, Ane T.
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Evolutionary Biology, Population Biology.
    Laurila, Anssi
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Evolutionary Biology, Population Biology.
    Merilä, Juha
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Evolutionary Biology, Population Biology.
    Latitudinal and temperature-dependent variation in embryonic development and growth in Rana temporaria2003In: Oecologia, ISSN 0029-8549, E-ISSN 1432-1939, Vol. 135, no 4, p. 548-554Article in journal (Refereed)
    Abstract [en]

    Variation in seasonal time constraints and temperature along latitudinal gradients are expected to select for life history trait differentiation, but information about the relative importance of these factors in shaping patterns of divergence in embryonic traits remains sparse. We studied embryonic survival, growth and development rates in the common frog (Rana temporaria) along a 1,400-km latitudinal gradient across Sweden by raising embryos from four populations in the laboratory at seven temperatures (9 degrees C, 12 degrees C, 15 degrees C, 18 degrees C, 21 degrees C, 24 degrees C, 27 degrees C). We found significant differences in mean values of all traits between the populations and temperature treatments, but this variation was not latitudinally ordered. In general, embryonic survival decreased at the two highest temperatures in all populations, but less so in the southernmost as compared to the other populations. The northernmost population developed slowest at the lowest temperature, while the two mid-latitude populations were slowest at the other temperatures. Hatchling size increased with increasing temperature especially in the two northern populations, whereas the two southern populations showed peak hatchling size at 15 degrees C. Analyses of within-population genetic variation with a half-sib design revealed that there was significant additive genetic variation in all traits, and egg size-related maternal effects were important in the case of hatchling size. Overall, our results indicate that unlike larval growth and development, variation in embryonic development and growth in R. temporaria cannot be explained in terms of a latitudinal gradient in season length. While adaptation to a latitudinal variation in temperature might have contributed to the observed differentiation in embryonic performance, the effects of other, perhaps more local environmental factors, seem to have overridden them in importance.

  • 34.
    Laugen, Ane T.
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Evolutionary Biology, Population Biology.
    Laurila, Anssi
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Evolutionary Biology, Population Biology.
    Merilä, Juha
    Maternal and genetic contributions to geographical variation in Rana temporaria larval life-history traits2002In: Biological Journal of the Linnean Society, ISSN 0024-4066, E-ISSN 1095-8312, Vol. 76, no 1, p. 61-70Article in journal (Refereed)
    Abstract [en]

    The relative importance of genetic, environmental, and maternal effects as determinants of geographical variation in vertebrate life-histories has not often been explored. We examined the role of genetic and maternal effects as determinants of population divergence in survival and three important larval life-history traits (growth rate, age, and size at metamorphosis) using reciprocal crosses between two latitudinally separated populations of the common frog (Rana temporaria Linnaeus). Genetic effects were important in all three traits as indicated by the significant effect of male origin, but there was also evidence for nonadditive genetic contributions on metamorphic size and growth rate. Likewise, maternal effect contributions to population divergence were large, partially environment dependent, and apparently acting primarily through egg size in two of three traits. These results suggest that both genetic and maternal effects are important determinants of geographical variation in amphibian life-histories, and that much of the differentiation resulting from maternal effects is mediated through variation in egg size.

  • 35.
    Laugen, Ane T.
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Evolutionary Biology, Population Biology.
    Laurila, Anssi
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Evolutionary Biology, Population Biology.
    Räsänen, Katja
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Evolutionary Biology, Population Biology.
    Merilä, Juha
    Latitudinal countergradient variation in the common frog (Rana temporaria) developmental rates: evidence for local adaptation2003In: Journal of Evolutionary Biology, ISSN 1010-061X, E-ISSN 1420-9101, Vol. 16, no 5, p. 996-1005Article in journal (Refereed)
    Abstract [en]

    Adaptive genetic differentiation along a climatic gradient as a response to natural selection is not necessarily expressed at phenotypic level if environmental effects on population mean phenotypes oppose the genotypic effects. This form of cryptic evolution--called countergradient variation--has seldom been explicitly demonstrated for terrestrial vertebrates. We investigated the patterns of phenotypic and genotypic differentiation in developmental rates of common frogs (Rana temporaria) along a ca. 1600 km latitudinal gradient across Scandinavia. Developmental rates in the field were not latitudinally ordered, but displayed large variation even among different ponds within a given latitudinal area. In contrast, development rates assessed in the laboratory increased strongly and linearly with increasing latitude, suggesting a genetic capacity for faster development in the northern than the southern larvae. Experiments further revealed that environmental effects (temperature and food) could easily override the genetic effects on developmental rates, providing a possible mechanistic explanation as to why the genetic differentiation was not seen in the samples collected from the wild. Our results suggest that the higher developmental rates of the northern larvae are likely to be related to selection stemming from seasonal time constrains, rather than from selection dictated by low ambient temperatures per se. All in all, the results provide a demonstration of environmental effects concealing substantial latitudinally ordered genetic differentiation understandable in terms of adaptation to clinal variation in time constrains.

  • 36.
    Laurila, Anssi
    et al.
    Uppsala University, Teknisk-naturvetenskapliga vetenskapsområdet, Faculty of Science and Technology, Biology, Department of Ecology and Evolution. Uppsala University, Teknisk-naturvetenskapliga vetenskapsområdet, Faculty of Science and Technology, Biology, Department of Ecology and Evolution, Population Biology. Populationsbiologi.
    Järvi-Laturi, Maria
    Pakkasmaa, Susanna
    Uppsala University, Teknisk-naturvetenskapliga vetenskapsområdet, Faculty of Science and Technology, Biology, Department of Ecology and Evolution, Population Biology.
    Merilä, Juha
    Temporal variation in predation risk: stage-dependency, graded responses and fitness costs in tadpole antipredator defences2004In: Oikos, Vol. 107, p. 90-99Article in journal (Refereed)
  • 37.
    Laurila, Anssi
    et al.
    Uppsala University, Teknisk-naturvetenskapliga vetenskapsområdet, Faculty of Science and Technology, Biology, Department of Ecology and Evolution. Uppsala University, Teknisk-naturvetenskapliga vetenskapsområdet, Faculty of Science and Technology, Biology, Department of Ecology and Evolution, Population Biology. populationsbiologi.
    Pakkasmaa, Susanna
    Merilä, Juha
    Population divergence in growth rate and antipredator defences in Rana arvalis.2006In: Oecologia, Vol. 147, no 4, p. 585-595Article in journal (Refereed)
    Abstract [en]

    Growth and development rates often differ among populations of the same species, yet the factors maintaining this differentiation are not well understood. We investigated the antipredator defences and their efficiency in two moor frog Rana arvalis populations differing in growth and development rates by raising tadpoles in outdoor containers in the nonlethal presence and absence of three different predators (newt, fish, dragonfly larva), and by estimating tadpole survival in the presence of free-ranging predators in a laboratory experiment. Young tadpoles in both populations reduced activity in the presence of predators and increased hiding behaviour in the presence of newt and fish. Older tadpoles from the slow-growing Gotland population (G) had stronger hiding behaviour and lower activity in all treatments than tadpoles from the fast-growing Uppland population (U). However, both populations showed a plastic behavioural response in terms of reduced activity. The populations differed in induced morphological defences especially in response to fish. G tadpoles responded with relatively long and deep body, short tail and shallow tail muscle, whereas the responses in U tadpoles were often the opposite and closer to the responses induced by the other predators. U tadpoles metamorphosed earlier, but at a similar size to G tadpoles. There was no evidence that growth rate was affected by predator treatments, but tadpoles metamorphosed later and at larger size in the predator treatments. G tadpoles survived better in the presence of free-ranging predators than U tadpoles. These results suggest that in these two populations, low growth rate was linked with low activity and increased hiding, whereas high growth rate was linked with high activity and less hiding. The differences in behaviour may explain the difference in survival between the populations, but other mechanisms (i.e. differences in swimming speed) may also be involved. There appears to be considerable differentiation in antipredator responses between these two R. arvalis populations, as well as with respect to different predators.

  • 38. Lesbarreres, D
    et al.
    Primmer, Craig
    Laurila, Anssi
    Uppsala University, Teknisk-naturvetenskapliga vetenskapsområdet, Faculty of Science and Technology, Biology, Department of Ecology and Evolution. Uppsala University, Teknisk-naturvetenskapliga vetenskapsområdet, Faculty of Science and Technology, Biology, Department of Ecology and Evolution, Population Biology. populationsbiologi.
    Merilä, Juha
    Environmental and population dependency of genetic variability-fitness correlations in Rana temporaria.2005In: Molecular ecology, Vol. 14, p. 311-323Article in journal (Refereed)
  • 39.
    Lindgren, Beatrice
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Population and Conservation Biology.
    Laurila, Anssi
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Population and Conservation Biology.
    Are high-latitude individuals superior competitors?: A test with Rana temporaria tadpoles2010In: Evolutionary Ecology, ISSN 0269-7653, E-ISSN 1573-8477, Vol. 24, no 1, p. 115-131Article in journal (Refereed)
    Abstract [en]

    Species with a wide distribution over latitudinal gradients often exhibit increasing growth and development rates towards higher latitudes. Ecological theory predicts that these fast-growing genotypes are, in the absence of trade-offs with fast growth, better competitors than low-latitude conspecifics. While knowledge on key ecological traits along latitudinal clines is important for understanding how these clines are maintained, the relative competitive ability of high latitude individuals against low latitude conspecifics has not been tested. Growth and development rates of the common frog Rana temporaria increase along the latitudinal gradient across Scandinavia. Here we investigated larval competition over food resources within and between two R. temporaria populations originating from southern and northern Sweden in an outdoor common garden experiment. We used a factorial design, where southern and northern tadpoles were reared either as single populations or as mixes of the two populations at two densities and predator treatments (absence and non-lethal presence of Aeshna dragonfly larvae). Tadpoles from the high latitude population grew and developed faster and in the beginning of the experiment they hid less and were more active than tadpoles from the low latitude population. When raised together with high latitude tadpoles the southern tadpoles had a longer larval period, however, the response of high latitude tadpoles to the competition by low latitude tadpoles did not differ from their response to intra-population competition. This result was not significantly affected by density or predator treatments. Our results support the hypothesis that high latitude populations are better competitors than their low latitude conspecifics, and suggest that in R. temporaria fast growth and development trade off with other fitness components along the latitudinal gradient across Scandinavia.

  • 40.
    Lindgren, Beatrice
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Evolution.
    Laurila, Anssi
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Evolution.
    Physiological variation along a geographical gradient: is growth rate correlated with routine metabolic rate in Rana temporaria tadpoles?2009In: Biological Journal of the Linnean Society, ISSN 0024-4066, E-ISSN 1095-8312, Vol. 98, no 1, p. 217-224Article in journal (Refereed)
    Abstract [en]

    Shorter season length and lower temperature towards higher latitudes and altitudes often select for intraspecific clines in development and growth rates. However, the physiological mechanisms enabling these clines are not well understood. We studied the relationship between routine metabolic rate (RMR) and larval life-history traits along a 1500-km latitudinal gradient across Sweden. In a laboratory common garden experiment, we exposed eight common frog Rana temporaria populations to two experimental temperatures (15 and 18 degrees C) and measured RMR using flow-through respirometry. We found significant differences among populations in RMR, but there was no evidence for a linear relationship between latitude and RMR in either temperature treatment. However, we found a concave relationship between latitude and RMR at the lower experimental temperature. RMR was not correlated with growth rate at population or at individual levels. The results obtained suggest that, unlike in growth and development rates, there is no latitudinal cline in RMR in R. temporaria tadpoles. (C) 2009 The Linnean Society of London, Biological Journal of the Linnean Society, 2009, 98, 217-224.

  • 41.
    Lindgren, Beatrice
    et al.
    Uppsala University, Teknisk-naturvetenskapliga vetenskapsområdet, Faculty of Science and Technology, Biology, Department of Ecology and Evolution. Uppsala University, Teknisk-naturvetenskapliga vetenskapsområdet, Faculty of Science and Technology, Biology, Department of Ecology and Evolution, Population Biology. populationsbiologi.
    Laurila, Anssi
    Uppsala University, Teknisk-naturvetenskapliga vetenskapsområdet, Faculty of Science and Technology, Biology, Department of Ecology and Evolution. Uppsala University, Teknisk-naturvetenskapliga vetenskapsområdet, Faculty of Science and Technology, Biology, Department of Ecology and Evolution, Population Biology. populationsbiologi.
    Proximate causes of adaptive growth rates: growth efficiency variation among latitudinal populations of Rana temporaria.2005In: Journal of Evolutionary Biology, Vol. 18, no 820-828Article in journal (Refereed)
  • 42.
    Magnus, Johansson
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Friederike, Ermold
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Kristjánsson, Bjarni
    Hólar University Collage, Iceland.
    Anssi, Laurila
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Local adaptation of gastropod life history to contrasting thermal environments in a geothermal lakeArticle in journal (Refereed)
  • 43. Merilä, Juha
    et al.
    Laurila, Anssi
    Uppsala University, Teknisk-naturvetenskapliga vetenskapsområdet, Faculty of Science and Technology, Biology, Department of Ecology and Evolution. Uppsala University, Teknisk-naturvetenskapliga vetenskapsområdet, Faculty of Science and Technology, Biology, Department of Ecology and Evolution, Population Biology. populationsbiologi.
    Laugen, Ane T
    Uppsala University, Teknisk-naturvetenskapliga vetenskapsområdet, Faculty of Science and Technology, Biology, Department of Ecology and Evolution. Uppsala University, Teknisk-naturvetenskapliga vetenskapsområdet, Faculty of Science and Technology, Biology, Department of Ecology and Evolution, Population Biology. populationsbiologi.
    Räsänen, Katja
    Uppsala University, Teknisk-naturvetenskapliga vetenskapsområdet, Faculty of Science and Technology, Biology, Department of Ecology and Evolution, Population Biology.
    Heads or tails? Variation in tadpole body proportions in response to temperature and food stress.2004In: Evolutionaru Ecology Research, Vol. 6, p. 727-738Article in journal (Refereed)
  • 44. Merilä, Juha
    et al.
    Laurila, Anssi
    Uppsala University, Teknisk-naturvetenskapliga vetenskapsområdet, Faculty of Science and Technology, Biology, Department of Ecology and Evolution. Uppsala University, Teknisk-naturvetenskapliga vetenskapsområdet, Faculty of Science and Technology, Biology, Department of Ecology and Evolution, Population Biology. populationsbiologi.
    Lindgren, Beatrice
    Uppsala University, Teknisk-naturvetenskapliga vetenskapsområdet, Faculty of Science and Technology, Biology, Department of Ecology and Evolution. Uppsala University, Teknisk-naturvetenskapliga vetenskapsområdet, Faculty of Science and Technology, Biology, Department of Ecology and Evolution, Population Biology. populationsbiologi.
    Variation in the degree and costs of adaptive phenotypic plasticity among Rana temporaria populations2004In: Journal of Evolutionary Biology, Vol. 17, p. 1132-1140Article in journal (Refereed)
  • 45. Merilä, Juha
    et al.
    Söderman, Fredrik
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Evolution, Population Biology.
    O'Hara, Robert
    Räsänen, Katja
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Evolution, Population Biology.
    Laurila, Anssi
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Evolution, Population Biology.
    Local adaptation and genetics of acid-stress tolerance in the moor frog, Rana arvalis2004In: Conservation Genetics, ISSN 1566-0621, E-ISSN 1572-9737, Vol. 5, no 4, p. 513-527Article in journal (Refereed)
    Abstract [en]

    As potential to adapt to environmental stress can be essential for population persistence, knowledge on the genetic architecture of local adaptation is important for conservation genetics. We investigated the relative importance of additive genetic, dominance and maternal effects contributions to acid stress tolerance in two moor frog (Rana arvalis) populations originating from low and neutral pH habitats. Experiments with crosses obtained from artificial matings revealed that embryos from the acid origin population were more tolerant to low pH than embryos from the neutral origin population in embryonic survival rates, but not in terms of developmental stability, developmental and growth rates. Strong maternal effect and small additive genetic contributions to variation were detected in all traits in both populations. In general, dominance contributions to variance in different traits were of similar magnitude to the additive genetic effects, but dominance effects outweighed the additive genetic and maternal effects contributions to early growth in both populations. Furthermore, the expression of additive genetic variance was independent of pH treatment, suggesting little additive genetic variation in acid stress tolerance. The results suggest that although local genetic adaptation to acid stress has taken place, the current variation in acid stress tolerance in acidified populations may owe largely to non-genetic effects. However, low but significant heritabilities ( h(2) approximate to 0.07 - 0.22) in all traits - including viability itself - under a wide range of pH conditions suggests that environmental stress created by low pH is unlikely to lower moor frog populations' ability to respond to selection in the traits studied. Nevertheless, acid conditions could lower populations' ability to respond to selection in the long run through reduction in effective population size.

  • 46.
    Murillo-Rincon, Andrea P.
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology. Christian Albrechts Univ Kiel, Inst Zool, D-24118 Kiel, Germany..
    Kolter, Nora A.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Laurila, Anssi
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Orizaola, German
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Intraspecific priority effects modify compensatory responses to changes in hatching phenology in an amphibian2017In: Journal of Animal Ecology, ISSN 0021-8790, E-ISSN 1365-2656, Vol. 86, no 1, p. 128-135Article in journal (Refereed)
    Abstract [en]

    1. In seasonal environments, modifications in the phenology of life-history events can alter the strength of time constraints experienced by organisms. Offspring can compensate for a change in timing of hatching by modifying their growth and development trajectories. However, intra-and interspecific interactions may affect these compensatory responses, in particular if differences in phenology between cohorts lead to significant priority effects (i.e. the competitive advantage that early-hatching individuals have over late-hatching ones). 2. Here, we conducted a factorial experiment to determine whether intraspecific priority effects can alter compensatory phenotypic responses to hatching delay in a synchronic breeder by rearing moor frog (Rana arvalis) tadpoles in different combinations of phenological delay and food abundance. 3. Tadpoles compensated for the hatching delay by speeding up their development, but only when reared in groups of individuals with identical hatching phenology. In mixed phenology groups, strong competitive effects by non-delayed tadpoles prevented the compensatory responses and delayed larvae metamorphosed later than in single phenology treatments. Non-delayed individuals gained advantage from developing with delayed larvae by increasing their developmental and growth rates as compared to single phenology groups. 4. Food shortage prolonged larval period and reduced mass at metamorphosis in all treatments, but it did not prevent compensatory developmental responses in larvae reared in single phenology groups. 5. This study demonstrates that strong intraspecific priority effects can constrain the compensatory growth and developmental responses to phenological change, and that priority effects can be an important factor explaining the maintenance of synchronic life histories (i.e. explosive breeding) in seasonal environments.

  • 47.
    Murillo-Rincon, Andrea P.
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology. Christian Albrechts Univ Kiel, Inst Zool, Kiel, Germany..
    Laurila, Anssi
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Orizaola, Germán
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Compensating for delayed hatching reduces offspring immune response and increases life-history costs2017In: Oikos, ISSN 0030-1299, E-ISSN 1600-0706, Vol. 126, no 4, p. 565-571Article in journal (Refereed)
    Abstract [en]

    Organisms are exposed to multiple sources of stress in nature. When confronted with a stressful period affecting growth and development, compensatory responses allow the restoration of individual fitness, providing an important buffering mechanism against climatic and other environmental variability. However, tradeoffs between increased growth/development and other physiological traits are predicted to prevent these high growth and development rates from becoming constitutive. Here, we investigated how compensatory responses in growth and development affect immune responses. By using low temperature to stop embryonic development, we exposed moor frog Rana arvalis tadpoles to two levels of time-constraints: non-delayed hatching and 12-day delayed hatching. In a common garden experiment, we recorded larval growth and development, as well as their immune response, measured as the inflammatory reaction after the injection of phytohaemagglutinin (PHA). Tadpoles originating from delayed hatching treatments had a lower immune response to PHA challenge than those from the non-delayed hatching treatment. In general, tadpoles from the delayed hatching treatment reached metamorphosis faster and at a smaller size than control tadpoles. However, immune-challenged tadpoles were not able to accelerate their development in response to delayed hatching. Our results indicate that 1) the innate immune response can be reduced in organisms undergoing compensatory developmental responses in growth and development and 2) compensatory capacity can be reduced when organisms are immunologically challenged. These dual findings reveal the complexity of handling multiple stressors and highlight the importance of examining the costs and limits of mounting an immune response in the context of increasing phenological instability ascribed to climate change.

  • 48. Nikinmaa, Mikko
    et al.
    Leveelahti, Lotta
    Dahl, Emma
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Evolution, Population and Conservation Biology.
    Rissanen, Eeva
    Rytkonen, Kalle T.
    Laurila, Anssi
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Evolution, Population and Conservation Biology.
    Population origin, development and temperature of development affect the amounts of HSP70, HSP90 and the putative hypoxia-inducible factor in the tadpoles of the common frog Rana temporaria2008In: Journal of Experimental Biology, ISSN 0022-0949, E-ISSN 1477-9145, Vol. 211, no 12, p. 1999-2004Article in journal (Refereed)
    Abstract [en]

    We raised Rana temporaria tadpoles from three different populations from southern, mid and northern Sweden (the total north-to-south distance between populations is approximately 1500 km) at two temperatures, and measured the differences in HSP70, HSP90 and putative HIF-1 alpha levels (Rana temporaria HIF-1 alpha was sequenced in the present study) with immunoblotting. The levels of the studied proteins increased with developmental stage. Also, the levels increased with latitude at the lower but not at the higher developmental temperature. This shows that there is a clear difference between the populations at the molecular level but that this difference can be modified by the environmental conditions experienced during development. The proteins analyzed may be involved in the regulation of developmental processes. If this is the case, the tadpoles from the northernmost population have the most advanced complement of regulatory proteins at developmental stages approaching metamorphosis.

  • 49.
    Nunes, Ana L.
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Population and Conservation Biology.
    Cruz, Maria J.
    Tejedo, Miguel
    Laurila, Anssi
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Population and Conservation Biology.
    Rebelo, Rui
    Nonlethal injury caused by an invasive alien predator and its consequences for an anuran tadpole2010In: Basic and Applied Ecology, ISSN 1439-1791, E-ISSN 1618-0089, Vol. 11, no 7, p. 645-654Article in journal (Refereed)
    Abstract [en]

    Nonlethal tail injury resulting from unsuccessful predation attempts is common in anuran larvae and can potentially induce significant fitness costs in terms of survival and growth. We tested the hypotheses that the alien red swamp crayfish, Procambarus clarkii, is an important inducer of tail injury in tadpoles of the Iberian spadefoot toad, Pelobates cultripes, and that tail damage can have important consequences for the tadpoles' life history and morphology. This was investigated by first estimating frequencies of caudal injury in P. cult ripes tadpoles in temporary ponds, with and without crayfish. Secondly, we performed a laboratory experiment in which four levels of tail injury frequency were combined with two levels of food availability. The frequency of tadpoles with damaged tails was higher in ponds with crayfish and the presence of this predator was the strongest predictor of tail injury frequency in a pond. Induced tail loss decreased larval survivorship and affected tail morphology, with injured tadpoles developing deeper tail muscles and shallower tail fins. The magnitude of these effects depended on injury frequency, as well as on food availability. The results suggest that P. clarkii is inflicting tail injuries at much higher levels than those occurring before its introduction; these injuries affect tadpole morphology and may induce delayed fitness costs.

  • 50.
    Nunes, Ana L.
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Orizaola, German
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Laurila, Anssi
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Rebelo, Rui
    Morphological and life-history responses of anurans to predation by an invasive crayfish: an integrative approach2014In: Ecology and Evolution, ISSN 2045-7758, E-ISSN 2045-7758, Vol. 4, no 8, p. 1491-1503Article in journal (Refereed)
    Abstract [en]

    Predator-induced phenotypic plasticity has been widely documented in response to native predators, but studies examining the extent to which prey can respond to exotic invasive predators are scarce. As native prey often do not share a long evolutionary history with invasive predators, they may lack defenses against them. This can lead to population declines and even extinctions, making exotic predators a serious threat to biodiversity. Here, in a community-wide study, we examined the morphological and life-history responses of anuran larvae reared with the invasive red swamp crayfish, Procambarus clarkii, feeding on conspecific tadpoles. We reared tadpoles of nine species until metamorphosis and examined responses in terms of larval morphology, growth, and development, as well as their degree of phenotypic integration. These responses were compared with the ones developed in the presence of a native predator, the larval dragonfly Aeshna sp., also feeding on tadpoles. Eight of the nine species altered their morphology or life history when reared with the fed dragonfly, but only four when reared with the fed crayfish, suggesting among-species variation in the ability to respond to a novel predator. While morphological defenses were generally similar across species (deeper tails) and almost exclusively elicited in the presence of the fed dragonfly, life-history responses were very variable and commonly elicited in the presence of the invasive crayfish. Phenotypes induced in the presence of dragonfly were more integrated than in crayfish presence. The lack of response to the presence of the fed crayfish in five of the study species suggests higher risk of local extinction and ultimately reduced diversity of the invaded amphibian communities. Understanding how native prey species vary in their responses to invasive predators is important in predicting the impacts caused by newly established predator-prey interactions following biological invasions.

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