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Climate change drives microevolution in a wild bird

Climate change drives microevolution in a wild bird ARTICLE DOI: 10.1038/ncomms1213 Received 7 Jan 2011 | Accepted 26 Jan 2011 | Published 22 Feb 2011 1 2 3 4 1 Patrik Karell , Kari Ahola , Teuvo Karstinen , Jari Valkama & Jon E. Brommer To ensure long-term persistence, organisms must adapt to climate change, but an evolutionary response to a quantified selection pressure driven by climate change has not been empirically demonstrated in a wild population. Here, we show that pheomelanin-based plumage colouration in tawny owls is a highly heritable trait, consistent with a simple Mendelian pattern of brown (dark) dominance over grey (pale). We show that strong viability selection against the brown morph occurs, but only under snow-rich winters. As winter conditions became milder in the last decades, selection against the brown morph diminished. Concurrent with this reduced selection, the frequency of brown morphs increased rapidly in our study population during the last 28 years and nationwide during the last 48 years. Hence, we show the first evidence that recent climate change alters natural selection in a wild population leading to a microevolutionary response, which demonstrates the ability of wild populations to evolve in response to climate change. 1 2 Bird Ecology Unit, Department of Biosciences, University of Helsinki, PO Box 65 (Viikinkaari 1), Helsinki FI-00014, Finland. Tornihaukantie 8D 72, Espoo 3 4 FI-02620, Finland. Juusinkuja 1, Kauniainen FI-02700, Finland. Ringing Centre, Finnish Museum of Natural History, University of Helsinki, PO Box 17 (P. Rautatiekatu 13), Helsinki FI-00014, Finland. Correspondence and requests for materials should be addressed to P.K. ([email protected]). nATuRE CoMMunICATIons | 2:208 | DoI: 10.1038/ncomms1213 | www.nature.com/naturecommunications © 2011 Macmillan Publishers Limited. All rights reserved. ARTICLE n ATu RE Co MMun ICATIons | Do I: 10.1038/ncomms1213 lobal climate warming changes the environment of most organisms and is expected to lead to a change in selection Gpressures with microevolutionary consequences that allow the adaptation of organisms to this new environment and thereby long-term population persistence . Although such adaptation to new environmental conditions created by climate change is expected in wild-animal populations , solid evidence for a microevolutionary (that is, genetic) response to climate change is rare . Microevolution in response to climate change has been demonstrated in inverte- Grey Brown 4,5 brate populations , but these studies lack information on the mech- anisms and selective factors linking particular genotypes to climate. Other studies have found selection on heritable phenotypic traits correlated with climate change, but do not report any genetic change in the population or the role of environmental factors exceed those of selection and lead to unpredicted phenotypic changes . e Th rela - tive role of evolutionary versus ecological response in relation to 6–8 climate change is still largely unexplored . Furthermore, there is a 4 5 6 7 8 9 10 11 12 13 14 noticeable absence of empirical studies addressing whether climate Colour score change actually has the potential to drive changes in selection and thereby cause microevolution . Figure 1 | Frequency distribution of tawny owl colouration in the study Systems with genetically based colour polymorphism have been population. Colour scoring is based on scorings of brown pigmentation on 10,11 used in classic studies of microevolution in wild populations , four different parts of the plumage and ranges from 4 to 14 points in 491 because they allow assessment of genotypes by censusing the individuals scored in 1978–2008. The frequency of colouration is bimodal frequency of colour morphs. Colour polymorphism is thought to and the two morphs can be classified into a grey and a brown morph at the have evolved and to be maintained by morph-specific sensitivity to cut point between scores 9 and 10. The cut point (red line) was determined 12–14 environmental conditions , and colour polymorphism oen ft has visually as the lowest intermediate point between the two models . A grey 15,16 a relatively simple genetic basis . Hence, such systems should be (left) and a brown (right) tawny owl colour morph are shown above the highly suitable for studying the microevolutionary capacity of wild graph (photography courtesy of: Dick Forsman). populations to track environmental change. In this study, we explore the links between climate change and alteration of the selective regime on a highly heritable phenotypic trait, plumage colouration in the tawny owl (Strix aluco), a com- had at least one relative with a measured phenotype in the pedigree mon bird of prey throughout the temperate regions of Europe. In were included. Extra-pair paternity is low in this species , and tawny owls, plumage colouration is determined by the degree of we are thus confident in inferring relatedness on the basis of the reddish-brown pheomelanin pigmentation deposited in their plum- social pedigree. Sex, age (1, 2, ≥3 years) and year of first breeding age . This colouration is independent of age and sex, and is highly were tested as fixed effects, but were not significant, and were not heritable . e Th frequency distribution of colouration (scored on included in the final models. This basic animal model based on the an ordinal scale) shows a bimodal distribution (Fig. 1), suggesting colouration scoring method revealed that plumage colouration was there are two basic morphs (termed grey and brown). Earlier work 79.8 ± 13.8 (s.e.m.)% heritable, which is in accordance with previous revealed that the brown tawny owl morph has reduced survival high heritability estimates of colouration in tawny owls ranging compared with the grey morph, resulting in lower lifetime from 72% using parent–offspring regression and 93% in a cross- 18 17 reproductive success of the brown morph . fostering experiment . Such high heritability suggests that few In this study, we first use colour scores of parents and their genes have large effects on colouration of the phenotype. offspring near fledging to demonstrate that a simple genetic architecture may underlie the two morphs. Second, we model the Inferring Mendelian genetics on nestlings and their parents. survival using capture–mark–recapture methodology of individual- Because the estimated heritability of colouration is high and the based long-term data from 28 years in relation to climate conditions distribution of colour scores is bimodal (Fig. 1), allowing the to show that selection against the brown morph is related to climate. separation of two colour morphs, we tested whether a ‘major gene’ Climate change has made winters increasingly milder during the could be responsible for creating this pattern. We used data from last decades, and we show that selection against the brown morph 318 nestlings in 83 nests, which were colour scored as either brown disappeared accordingly. Last, we show that the proportion of the or grey morph in years 2006–2009. Tawny owls mate random brown morph has increased dramatically over time. u Th s, we have with respect to colour . We contrasted three different models shown that climate change can influence selection demonstrating (see Supplementary Information): two Mendelian models, in which that climate change may influence evolution in wild populations. plumage colour is assumed to be fully determined by one locus, where either the ‘brown’ allele is 100% dominant over the ‘grey’ Results allele or the other way around, and one additive genetic model Heritability of colouration in tawny owls. We colour scored all (many genes of small, additive effect). breeding tawny owls in our study population from 1978 onwards e Th model assuming brown dominance (Supplementary Table S1) using a semi-continuous scale, which is based on scoring the degree produces a ratio of brown/grey phenotypes that almost exactly of reddish-brown colouration in four different parts of the plumage. matches what is expected under this inheritance model in Hardy– An individual’s plumage colouration does not change throughout Weinberg equilibrium (52.8% of offsprings are observed and 55.2% life (repeatability >90% (ref. 18)). Because practically all male and are expected to be brown, G = 0.308, P = 0.58; Fig. 2, Supplementary female parents and their offspring have been individually marked Table S2). Repeating the above, but assuming that the allele for grey in the study population since 1978, we can estimate the heritability morph is dominant over the allele for brown produces a poorer t fi using quantitative genetic methods . We used a reduced pedigree, between observed and expected ratio of the offspring ( G = 12.98, in which 167 individuals whose phenotype was measured and who P = 0.0015; Fig. 2). er Th e are more brown offspring observed than n ATu RE Co MMun ICATIons | 2:208 | Do I: 10.1038/ncomms1213 | www.nature.com/naturecommunications © 2011 Macmillan Publishers Limited. All rights reserved. Frequency (%) n ATu RE Co MMun ICATIons | Do I: 10.1038/ncomms1213 ARTICLE Table 1 | Best five models explaining variation in survival of tawny owl colour morphs. NS Model QAICc QAICc Para­ Likeli­ weight meters hood (1) Φ p 1,771.51 0.454 32 1.00 (temp + col*snow) (t) (2) Φ p 1,772.52 0.274 33 0.60 (col*temp + col*snow) (t) (3) Φ p 1,773.64 0.156 33 0.35 (vole + temp + col*snow) (t) (4) Φ p 1,774.34 0.110 34 0.24 (col*vole + temp + col*snow) (t) (5) Φ p 1,780.18 0.006 52 0.01 (col + t) (t) Models are corrected for over-dispersion (c ˆ=1.19). Abbreviations: col, plumage colour; snow, snow depth (cm); temp, temperature (°C); t, time B×B B×G G×G B×B B×G G×G B×B B×G G×G B×B B×G G×G dependence; vole, vole abundance index and interaction ‘*’ between these.†The symbol Φ and p denote apparent survival and capture probability, respectively, with in subscript the covariates Observed Brown Grey Additive considered to affect each parameter. The interaction term is a shorthand notation for a model data dominance dominance model that also includes the effects separately (that is, ‘col*snow’ stand for ‘col + snow + col*snow’). Figure 2 | Genetic models of inheritance of colouration. n umber of brown (red bar) and grey (grey bar) offspring colour morphs produced by different combinations of parental colour morphs (B×B, B×G and G×G). that low winter temperature decreases survival probability. er Th e The first columns show the observations in the field, second, third and was also support for an interaction between colour morph and tem- fourth columns show the expected number of offspring colour morphs perature (col*temp) indicating lower survival for brown individuals according to models with brown dominance, grey dominance and an compared with grey ones in cold temperatures. Prey abundance in additive genetic model, respectively. The lines above the bars show late autumn also explained some variation in survival, as the third a G-test of association between models and their significance ranked model included the effect of prey abundance (vole) and (ns : P = 0.58, **P < 0.002, ***P < 0.0001). the fourth ranked model included an interaction between prey abundance and colour morph (col*vole). Recapture probability was not explained by variables prey abundance, temperature or snow expected when assuming full dominance of the grey allele over depth as none of the models where recapture was constrained by brown. e Th purely additive model also t fi ted the data poorly. these variables received any support. In this particular case, the colour scores of the adults were such that Model averaging of all candidate models (N = 175) revealed that the additive model predicted that all offspring from monomorphic variation in snow depth explained most of the variation in survival of crosses were the same morph as the parents; thus, these crosses the colour morphs. In our case, 99.4% of support stems from the four are not informative for testing. However, focusing on the hetero- best models (Table 1) and the averaging can therefore be considered morphic (BxG) cross, it is clear that there are more offspring of the to mainly describe the common features included in these models brown morph observed than expected also under the assumption (that is, colour morph–snow depth interaction). As snow depth of an additive genetic inheritance (G = 70.9, P < 0.0001; Fig. 2). increased, survival of the brown morph decreased more strongly Alternative approaches for statistically comparing the observed than for the grey morph (Fig. 3a). Simultaneously, snow depth has and expected frequencies of morphs all provided the same con- decreased over time (Fig. 3b; linear model, year: b = − 0.37 ± 0.13, clusion (Supplementary Information). We thus conclude from the F = 8.49, P = 0.007). As a consequence, there was a time trend in 1,25 above exercises on the basis of comparing fledglings’ morphs with survival of the colour morphs from 1981–2008, in which survival their parents’ morphs that we find evidence for genetic dominance of the grey morph was fairly stable across years, whereas survival of brown over grey, whereas dominance of grey and purely addi- of brown individuals improved dramatically towards the end of the tive genetic effects are not supported by this data. Although this time series (Fig. 3c). u Th s, we provide evidence that climate-driven modelling is not exhaustive, it does show that the tawny owl pheno- selection against the brown morph has decreased in recent years typic morph has a genetic architecture that relies on few genes with such that the survival propensity of the morphs have equalized in large effects, which is consistent with a Mendelian inheritance of recent, mild winters. colouration based on one locus with a ‘brown’ allele dominant over a ‘grey’ allele. Population-level response to climate-driven selection. When selection on a heritable trait changes, a response in the composi- Climate change and survival of tawny owl colour morphs. Several tion of the population is expected . We indeed found that the fre- aspects of the environment have changed for tawny owls. Climate quency of brown morphs increased markedly between 1981 and warming has led to milder winters, especially in subarctic regions . 2008. Compared with historical data, when on average one-third Furthermore, the cyclic dynamics of voles—the staple food of of the individuals were brown (Fig. 4a), we found that the brown tawny owls in Finland—has been fading and has become irregular morph rapidly increased in frequency especially during the last dec- 22,23 in recent years . We tested whether survival of tawny owl colour ade (Fig. 4b; binomial generalized linear model 1981–2008, year: morphs are differently ae ff cted by such changes by applying capture– b = 0.050 ± 0.009 s.e.m., z = 5.66, N = 28, P < 0.0001). This phenotypic recapture modelling to the data from 1981 to 2008 (N = 466 indi- change was present also on a larger nationwide scale. In a time viduals). We modelled survival probability of brown and grey adult series of tawny owls captured, marked and colour scored (grey or breeding tawny owls in relation to over-winter prey abundance and brown) by ornithologists all over Finland between 1961 and 2008 snow depth and temperature during a period in winter that was (N = 3,239 observations), we found a steadily increasing frequency critical for tawny owl survival (see Supplementary Information). of the brown morph (Fig. 4c, year: b = 0.025 ± 0.004 s.e.m., z = 6.94, e Th results of the modelling showed that all four best models, which N = 48, P < 0.0001). u Th s, the increase of the brown morph is a large together received 99.4% of the support (QAICc weight), included scale phenomenon occurring all over Finland, involving thousands an interaction where brown individuals had lower survival than of individuals. Hence, this phenotypic change is unlikely to be grey ones as snow cover became deeper (col*snow, Table 1). Tem- caused by genetic drift, because drift is only a major force for chang - perature (temp) was included in all four best models, which implies ing allele frequencies in small populations. Given the strong genetic n ATu RE Co MMun ICATIons | 2:208 | Do I: 10.1038/ncomms1213 | www.nature.com/naturecommunications © 2011 Macmillan Publishers Limited. All rights reserved. Number of offspring ARTICLE n ATu RE Co MMun ICATIons | Do I: 10.1038/ncomms1213 underpinning of tawny owl morphs (see above), we consider the selection on the proportional increase of the brown morph, we observed phenotypic trend in the proportion of the brown morph as categorized all breeding individuals into immigrants (r fi st breeder indicative for a shift in gene frequencies. Hence, we here document that is unmarked or marked outside the study area), local recruits microevolution of tawny owl plumage colour. (r fi st breeders marked as young) and old breeders (survivors from Apart from selection, immigration is an important population a previous breeding attempt). We then analysed the relative contri- dynamical feature in our study population . A proportional increase bution of grey and brown survivors, immigrants and local recruits in immigrating brown morphs could account for the observed over time to the observed increase in the frequency of the brown increase in their frequency in the population. To test the relative morph. We found that the increase in frequency of the brown morph importance of morph-specific immigration, local recruitment and in the population was explained only by an increase in the number of brown survivors over time, and not by any other numeral trend (binomial generalized linear model: b = 0.18 ± 0.09 s.e.m., z = 2.11, N = 28, P = 0.035, Fig. 5). We used our observed parent–os ff pring inheritance pattern to retrospectively infer the morphs of os ff pring produced during the last three decades. e Th re was no morph- 0.8 specic fi temporal trend in reproductive success or recruitment rate (Supplementary Information), which illustrates that the increase in the proportion of brown morphs in the population is not driven by a 0.6 change in productivity of the brown morph. Furthermore, we found no evidence for a phenotypically plastic within-individual coloura- tion change as winter climate gets milder (Supplementary Informa- 0.4 tion). We conclude that improved survival of brown adult tawny owls caused by warmer winters with less snow is the most likely candidate to drive the observed temporal increase in the brown morph. 0.2 Discussion Our study constitutes, to our knowledge, the first empirical evi - 0 5 10 15 20 25 dence of climate-driven change in selection on a heritable trait. Work on climate change induced evolution typically concerns the Snow depth (cm) documentation of temporal trends in traits that are assumed to be t fi ness-related (for example, phenology), possibly linked with an exploration of the genetic underpinning of such traits . Even if a focal trait is heritable and selectively important, surprisingly few studies have asked whether climate change has actually altered the selective regime. Selection can be environmentally dependent and yet not change as climate changes . Unless there is evidence that climate change drives an alteration in selection, it is potentially erroneous to attribute an observed temporal change in a trait (whether on the genetic or on the phenotypic level) to climate change, because a temporal trend can be caused also by other changes in the environment that occurred during the same time period. In this study, we show that a particularly powerful form of natu- ral selection (survival selection on reproducing adults) on tawny owl colour polymorphism is driven by climatic conditions in early winter. Differential performance of contrasting morphs under vari - able environmental conditions lies at the heart of theory behind the 1980 1985 1990 1995 2000 2005 2010 26 evolution of genetic polymorphism . There are three non-mutually Year exclusive explanations for why the brown tawny owl morph may be more sensitive to harsh winter conditions. First, colouration itself 1 may be the target of selection; for example, predation on brown individuals may be more severe under snow-rich conditions. e Th main tawny owl predator, however, is the eagle owl Bubo bubo , 0.8 Figure 3 | Survival of grey and brown tawny owls in relation to changes 0.6 in snow depth. s urvival estimates are based on averaging all candidate capture–mark–recapture models considering the effects of food supply (vole abundance), average snow depth and average temperature during 0.4 a critical period in winter (see s upplementary Information). Climatic data are derived from the database of the Finnish Meteorological Institute. (a) s urvival of brown and grey tawny owl colour morphs in relation to snow 0.2 depth. (b) s now depth during the critical period for tawny owl survival during 1981–2008 in s outhern Finland. (c) s urvival of grey and brown tawny owl colour morphs during 1981–2008. Grey tawny owls are denoted by grey circles and brown ones by red diamonds. Error bars are standard 1980 1985 1990 1995 2000 2005 2010 errors of the estimated survival and the lines are regression slopes based Year on the data. n ATu RE Co MMun ICATIons | 2:208 | Do I: 10.1038/ncomms1213 | www.nature.com/naturecommunications © 2011 Macmillan Publishers Limited. All rights reserved. Estimated survival (Phi) Snow depth (cm) Estimated survival (Phi) n ATu RE Co MMun ICATIons | Do I: 10.1038/ncomms1213 ARTICLE 0.5 0.5 0.5 0.4 0.4 0.4 0.3 0.3 0.3 0.2 0.2 0.2 0.1 0.1 0.1 29 97 198 157 219 174 205 114 24 82 170 179 347 393 625 468 558 348 0 0 0 1910 1940 1970 1980 1990 2000 2010 1960 1970 1980 1990 2000 2010 Year Year Year Figure 4 | Temporal changes in the frequency of the brown morph in Finland on different scales. (a) Historical data on colour morph frequencies in the early century (1911–1945) and mid-century (1946–1980) based on skins from the Zoological museum collection (u niversity of Helsinki). Each symbol represents the mean frequencies of seven 5-year periods ( ± s.e.m.). (b) Frequency of the brown morph in the study population based on captured breeding birds between 1981 and 2008. s hown are mean annual frequencies of the brown morph in 5-year periods ( ± s.e.m.). (c) n ationwide population frequency of brown individuals based on all breeding birds ringed or recaptured by amateur ringers in Finland and colour scored as either grey or brown. s ymbols are as in b. Total sample size is given along the x axis. The method of scoring colour morphs in a and b (filled diamonds) differs from the method used in c (filled dots), such that the averages and slope of the trend are not directly comparable, although the direction is. Our second main finding is a clear temporal shift towards a higher proportion of the brown morph in the population. In general, such a pattern is microevolution (change in allele frequen- 20 cies driven by selection), genetic drift (stochastic change in allele frequency) or phenotypic plasticity (environmentally induced change in expressed phenotype) . We show that the increase of the brown tawny owl morph occurs in a representative (nationwide) sample of the entire Finnish population of tawny owls (thousands of individuals), which makes it unlikely that random genetic drift drives this trend. e Th observed trend concerns phenotypes, but we 1980 1985 1990 1995 2000 2005 2010 1980 1985 1990 1995 2000 2005 2010 here demonstrate that tawny owl morphs are under tight genetic Year Year control in a manner that is consistent with a one locus–two allele genetic architecture. In addition, we demonstrate that phenotypic Figure 5 | Factors explaining the increase in the proportion of the plasticity does not explain the trend. We therefore believe that brown morph in the study population. n umber of brown (a) and grey the increase in the proportion of brown tawny owls during the last (b) survivors (denoted by diamonds, solid line), immigrants (circles, two decades constitutes a microevolutionary change. dashed line) and recruits (triangles, dashed-dotted line) in the breeding A recent review concluded that three study systems provide population during the study period. evidence for microevolutionary changes over time with a puta- tive link to climate change. es Th e are: a shift in the critical photo - period that ae ff cts diapause in pitcher-plant mosquitoes , shifts in which is not a visual predator. Furthermore, the brown morph is the distribution of chromosomal arrangements and Adh alleles in 28 4,5 in fact considered to be more cryptic , although this need not hold Drosophila , and quantitative genetic evidence that timing of breed- under snow-rich conditions. Second, colouration may, through ing in red squirrels Tamiasciurus hudsonicus advanced in concert pleiotropic effect be associated with another property that is the with climate warming . For the first two examples, climate change real target of selection. Increasing evidence, both on molecular could not be firmly established as the causal agent of the temporal 3 34 and individual level, suggests that the differential performance of change . Recent developments in quantitative genetics suggest that morphs across environments can be caused by genetic covariation the last example is not as rigorous a demonstration of microevolu- between colouration (melanization) and a physiological property, tion as initially suggested. We show that warming of winter climate 14,18,29–32 such as metabolism or immune function . Third, pleiotropic leads to reduced selection against the brown morph, and we demon- effects between energy homoeostasis and melanin pigmentation strate that at the same time the frequency of the brown morph in can lead to differential predation pressure if the melanistic (brown) the Finnish population increases to a level that is above the historic morph has higher energetic requirements and needs to forage record of the species. Intuitively, a release of selection on a highly more and thus becomes more susceptible to predation under harsh heritable trait should lead to a microevolutionary response, and we winter conditions. Additional research is needed in establishing the provide statistical evidence that selection (rather than immigra- possible pleiotropic link between genes expressing colouration and tion or local recruitment) indeed drives the observed increase in physiological properties. Nevertheless, the observed pattern with the frequency of the brown morph. On the other hand, our survival an interaction between winter harshness and morph suggests that analysis does not show a selective advantage of the brown morph: intrinsic differences between the morphs drive their propensity for survival during the last (warm) winters was approximately equal for survival. the grey and brown morphs. Furthermore, the brown morph has n ATu RE Co MMun ICATIons | 2:208 | Do I: 10.1038/ncomms1213 | www.nature.com/naturecommunications © 2011 Macmillan Publishers Limited. All rights reserved. N individuals Frequency of brown ARTICLE nATuRE CoMMunICATIons | DoI: 10.1038/ncomms1213 no reproductive advantage. How can the frequency of the brown Capture–mark–recapture modelling and model selection. Survival of adult grey and brown tawny owls was estimated using capture–mark–recapture methodol- increase despite an absence of selective advantages? We believe that ogy on live encounters data (Cormack–Jolly–Seber model) of 1,065 observations as yet unknown details of the genetics provide the link between the of 466 tawny owls Supplementary Table S3, using the programme MARK . We climate-driven change in selection and the observed increase in used a sliding-window approach (all possible time windows between 5 and 44 days the frequency of the brown morph. In particular, we currently lack were considered) to find the relevant time period during which survival (full-time detailed quantitative understanding of how the selective mechanism dependent CMR model, Φ p ) correlated best with climate (average temperature (t) (t) and snow depth). Annual survival of tawny owls was highly correlated with operates on the genotypes. This is because if one accepts that morph temperature and snow depth (Supplementary Table S4). Measures of temperature inheritance patterns are caused by a one locus–two allele model and snow depth from the time window that correlated best with annual tawny with brown dominance over grey (as our findings suggest), there owl survival were selected as covariates for further modelling (Supplementary are two genotypes that produce a brown morph (heterozygous Bg Table S4). We tested for the effects of real covariates by replacing the dummy variable ‘time dependence (t)’ with interactions of colour morph and prey and homozygous BB), but we necessarily measure selection on these abundance (col*vole), temperature (col*temp) and snow depth (col*snow) in two combined (that is, morph-based). One possibility is that winter both survival (Φ) estimation as well as recapture (p). We applied model climate-driven selection against the heterozygote is less than selec- averaging on the candidate models to get a more conservative estimate of Φ tion against the homozygote. Indeed, if pleiotropic effects of the and p. Although averaging is performed over all candidate models, the weighting putative grey and brown colour genes indeed cause the differential by QAIC model weights ensures that the information in the best fitting models contributes most. survival of tawny owl morphs then a heterozygote brown individual Further methodological details are provided in the Supplementary Methods. may well perform differently than a homozygous brown individual. In the buzzard Buteo buteo, Mendelian inheritance of colour genes has been suggested to underlie the plumage colour polymorphism References observed in that species with a selective advantage for the hetero- 1. Davis, M. B. & Shaw, R. G. Range shifts and adaptive responses to quaternary zygous morph . From a population-genetic perspective, such a ‘hid- climate. Science 292, 763–679 (2001). 2. Parmesan, C. Ecological and evolutionary responses to recent climate change. den’ heterozygote advantage in combination with a temporal release Annu. Rev. Ecol. Evol. Syst. 37, 637–669 (2006). of selection has the potential to explain both the maintenance of 3. Gienapp, P., Teplitsky, C., Alho, S., Mills, J. A. & Merilä, J. Climate change and the brown morph in the population and the increase in frequency evolution: disentangling environmental and genetic responses. Mol. Ecol. 17, of the brown morph, despite the fact that selection continuously 167–178 (2008). acts against the brown morph (model developed in Supplementary 4. Umina, P. A., Weeks, A. R., Kearney, M. R., McKechnie, S. W. & Hoffmann, A. A rapid shift in a classical clinal pattern in Drosophila reflecting climate change. Information). This hypothesis is testable once the molecular genetic Science 308, 691–693 (2005). basis of tawny owl plumage colour polymorphism has been clarified 5. Balanya, J., Oller, J. M., Huey, R. B., Gilchrist, G. W. & Serra, L. Global genetic and selection on the genotypic level can be estimated. change tracks global climate warming in Drosophila subobscura. Science 313, Our study demonstrates a climate change driven alteration of 1773–1775 (2006). selection on a heritable trait coupled with a population-level evo- 6. Ozgul, A. et al. The dynamics of phenotypic change and the shrinking sheep of St. Kilda. Science 325, 464–467 (2009). lutionary response; all of which are required for long-term survival 7. Réale, D., McAdam, A. G., Boutin, S. & Berteaux, D. Genetic and plastic of species. Because colour polymorphism is highly heritable, studies responses of a northern mammal to climate change. Proc. R. Soc. Lond. B 270, on these systems are likely to provide important benchmark insights 591–596 (2003). in the effects of environmental change on population level changes, 8. Teplitsky, C., Mills, J. A., Alho, J. S., Yarrall, J. W. & Merilä, J. Bergmann’s not only in terms of phenotypic changes , but also in terms of rule and climate change revisited: disentangling environmental and genetic responses in a wild bird population. Proc. Natl Acad. Sci. USA 105, changes in genetic diversity and the evolvability of organisms 13492–13496 (2008). (see also Supplementary Information) and changes in latitudinal 9. Sheldon, B. C. Genetic perspectives on the evolutionary consequences of distributions of morphs in colour polymorphic species . climate change in birds. in Ee ff ct of Climate Change on Birds (eds Møller, A. P, Fiedler, W. & Berthold, P.) 149–168 (Oxford University Press, 2010). 10. Sumner, F. B. Genetic and distributional studies of three subspecies of Methods Data sets. Tawny owls were studied from 1981 to 2008 in a study area of Peromyscus. J. Genet. 23, 275–376 (1930). 11. Fisher, R. A. & Ford, E. B. e Th spread of a gene in natural conditions in a colony about 250 km in Southern Finland (60°15N′, 24°15E′). The study area is of the moth Panaxia dominula L. Heredity 1, 143–174 (1947). dominated by mixed forests, agricultural areas and small freshwater courses and was established in 1977–78. From 1980 onwards ~125 nest boxes in suitable 12. Majerus, M. E. N. Melanism, Evolution in Action. (Oxford University Press, habitats were available for tawny owls to breed in. Considerable effort was put 1998). 13. Galeotti, P., Rubolini, D., Dunn, P. O. & Fasola, M. Colour polymorphism in into finding the nests of all tawny owls in the study population by searching for birds: causes and functions. J. Evol. Biol. 16, 635–646 (2003). natural nest sites and new boxes set up by private individuals in the approximate area where hooting individuals had been recorded earlier in spring and where 14. Roulin, A. The evolution, maintenance and adaptive function of genetic colour polymorphism in birds. Biol. Rev. 79, 1–34 (2004). a breeding thus was expected. The same monitoring scheme was used by K.A. and 15. Mundy, N. I. A window on the genetics of evolution: MC1R and plumage T.K. during all years and the effort remained similar in all years. The majority of all breeding male and female owls in the study population were caught, ringed colouration in birds. Proc. R. Soc. Lond. B. 272, 1633–1640 (2005). 16. Hoekstra, H. E. Genetics, development and evolution of adaptive pigmentation and their reproductive output was measured. Plumage colouration was scored in vertebrates. Heredity 97, 222–234 (2006). using a semi-continuous ordinal scale (range from 4 (grey) to 14 (reddish-brown)) on all breeding individuals on each encounter (N = 1116 records of 491 individuals) 17. Gasparini, J. et al. Strength and cost of an induced immune response are using a standardized and repeatable scoring that shows colouration is independ- associated with a heritable melanin-based colour trait in female tawny owls. J. Anim. Ecol. 78, 608–616 (2009). ent of age and sex . Museum skin specimens collected by the public between 18. Brommer, J. E., Ahola, K. & Karstinen, T. The colour of fitness: plumage 1915 and 1980 and stored by the Natural History Museum, University of Helsinki, (N = 126) were colour scored in the same way as in the study population. National coloration and lifetime reproductive success in the tawny owl. Proc. R. Soc. Lond. B. 272, 935–940 (2005). level tawny owl colour morph data collected by ornithologists in Finland were 19. Lynch, M. & Walsh, B. Genetics and Analysis of Quantitative Traits (Sinauer, obtained from the Finnish Ringing Centre. We extracted the data on all records of adult ringed and recaptured tawny owls in Finland to which colour morph (grey 1998). 20. Saladin, V., Ritschard, M., Roulin, A., Bize, P. & Richner, H. Analysis of genetic or brown) had been assigned during 1961–2008 (30% of all data, 3,194/10,601 parentage in the tawny owls (Strix aluco) reveals extra-pair paternity is low. records). Genetics. We used a REML linear mixed model (‘animal model’) to estimate J. Ornithol. 148, 113–116 (2007). heritability of plumage colouration. The additive genetic effects were estimated 21. Intergovernmental Panel on Climate Change (IPCC). Climate change 2007: Synthesis report. Fourth assessment report, http://www.ipcc.ch/ (2007). using pedigree-derived estimates of relatedness across all individuals . We tested 22. Ims, R. A., Henden, J.- A. & Killengreen, S. T. Collapsing population cycles. whether parent–offspring resemblance (83 nests with 318 offspring, data from 2006 to 2009) followed a purely additive genetic model, or a one locus–two allele Trends Ecol. Evol. 23, 79–86 (2008). 23. Brommer, J. E., Pietiäinen, H., Ahola, K., Karell, P., Karstinen, T. & Kolunen, H. model under Hardy–Weinberg equilibrium, in which either ‘brown’ or ‘grey’ e r Th eturn of the vole cycle in southern Finland refutes the generality of were dominant over the other allele. nATuRE CoMMunICATIons | 2:208 | DoI: 10.1038/ncomms1213 | www.nature.com/naturecommunications © 2011 Macmillan Publishers Limited. All rights reserved. nATuRE CoMMunICATIons | DoI: 10.1038/ncomms1213 ARTICLE the loss of cycles through ‘climatic forcing’. Global Change Biol. 16, 577–586 38. White, G. C. & Burnham, K. P. Program MARK: survival estimation from (2010). populations of marked animals. Bird Study 46, S120–S138 (1999). 24. Karell, P., Ahola, K., Karstinen, T., Zolei, A. & Brommer, J. E. Population 39. Burnham, K. P. & Anderson, D. R. Model Selection and Inference—A Practical dynamics in a cyclic environment: Consequences of cyclic food abundance Information Theoretical Approach (Springer, 1998). on tawny owl reproduction and survival. J. Anim. Ecol. 78, 150–162 (2009). 25. Charmantier, A., McCleery, R. H., Cole, L. R., Perrins, C., Kruuk, L. E. B. & Acknowledgments Sheldon, B. C. Adaptive phenotypic plasticity in response to climate change in This is report number 9 of Kimpari Bird Projects (KBP). We thank the other members of a wild bird population. Science 320, 800–803 (2008). KBP—Juhani Ahola, Pentti Ahola, Bo Ekstam, Arto Laesvuori and Martti Virolainen— 26. Fisher, R. A. e G Th enetical Theory of Natural Selection (Clarendon Press, 1930). for the many hours spent conducting fieldwork. We thank all bird ringers in Finland who 27. Mikkola, H. Owls of Europe. (T & A. D. Poyser, 1983). have provided data on tawny owl colour morphs, Martti Hildén for help with Museum 28. Gehlbach, F. R. e Eas Th tern Screech owl: Life History, Ecology, and Behaviour skins and Hannu Pietiäinen for insightful comments on the manuscript. P.K. was in the Suburbs and Countryside. (Texas A&M, 1994). supported by the Academy of Finland (projects 1118484 and 1131390 to J.E.B.) and 29. Ducrest, A.- L., Keller, L. & Roulin, A. Pleiotropy in the melanocortin system, J.E.B. was employed as an Academy Researcher. coloration and behavioural syndromes. Trends Ecol. Evol. 23, 502–510 (2008). 30. Piault, R., Gasparini, J., Bize, P., Jenni-Eiermann, S. & Roulin, A. Pheomelanin- based coloration and the ability to cope with variation in food supply and Author contributions parasitism. Am. Nat. 174, 548–556 (2009). Data from the study population were collected by K.A., T.K. and data on skin specimen 31. Stütz, A. M., Morrison, C. D. & Argyropoulos, G. The Agouti-related protein by P.K. J.V. provided national data on tawny owl ringing data. Analyses and writing was and its role in energy homeostasis. Peptides 26, 1771–1781 (2005). done by P.K. and J.E.B. 32. Boswell, T. & Takeuchi, S. Recent developments in our understanding of the avian melanocortin system: its involvement in the regulation of pigmentation Additional information and energy homeostasis. Peptides 26, 1733–1743 (2005). Supplementary Information accompanies this paper at http://www.nature.com/ 33. Bradshaw, W. E. & Holzapfel, C. M. Genetic shi ft in photoperiodic response naturecommunications correlated with global warming. Proc. Natl Acad. Sci. USA 98, 14509–14511 (2001). 34. Hadfield, J. D., Wilson, A. J., Garant, D., Sheldon, B. C. & Kruuk, L. E. B. The Competing financial interests: The authors declare no competing financial interests. misuse of BLUP in ecology and evolution. Am. Nat. 175, 116–125 (2010). Reprints and permission information is available online at http://npg.nature.com/ 35. Krüger, O., Lindström, J. & Amos, W. Maladaptive mate choice maintained by reprintsandpermissions/ heterozygote advantage. Evolution 55, 1207–1214 (2001). 36. Galeotti, P., Rubolini, D., Sacchi, R. & Fasola, M. Global changes and animal How to cite this article: Karell, P. et al. Climate change drives microevolution in a wild phenotypic responses: melanin-based plumage redness of scops owls increased bird. Nat. Commun. 2:208 doi: 10.1038/ncomms1213 (2011). with temperature and rainfall during the last century. Biol. Lett. 5, 532–534 (2009). License: This work is licensed under a Creative Commons Attribution-NonCommercial- 37. Roulin, A., Burri, R. & Antoniazza, S. Owl melanin-based plumage redness is more frequent near than away from the equator: implications on the effect of Share Alike 3.0 Unported License. To view a copy of this license, visit http:// climate change on biodiversity. Biol. J. Linn. Soc. (in the press). creativecommons.org/licenses/by-nc-sa/3.0/ nATuRE CoMMunICATIons | 2:208 | DoI: 10.1038/ncomms1213 | www.nature.com/naturecommunications © 2011 Macmillan Publishers Limited. 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Climate change drives microevolution in a wild bird

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Science, Humanities and Social Sciences, multidisciplinary; Science, Humanities and Social Sciences, multidisciplinary; Science, multidisciplinary
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ARTICLE DOI: 10.1038/ncomms1213 Received 7 Jan 2011 | Accepted 26 Jan 2011 | Published 22 Feb 2011 1 2 3 4 1 Patrik Karell , Kari Ahola , Teuvo Karstinen , Jari Valkama & Jon E. Brommer To ensure long-term persistence, organisms must adapt to climate change, but an evolutionary response to a quantified selection pressure driven by climate change has not been empirically demonstrated in a wild population. Here, we show that pheomelanin-based plumage colouration in tawny owls is a highly heritable trait, consistent with a simple Mendelian pattern of brown (dark) dominance over grey (pale). We show that strong viability selection against the brown morph occurs, but only under snow-rich winters. As winter conditions became milder in the last decades, selection against the brown morph diminished. Concurrent with this reduced selection, the frequency of brown morphs increased rapidly in our study population during the last 28 years and nationwide during the last 48 years. Hence, we show the first evidence that recent climate change alters natural selection in a wild population leading to a microevolutionary response, which demonstrates the ability of wild populations to evolve in response to climate change. 1 2 Bird Ecology Unit, Department of Biosciences, University of Helsinki, PO Box 65 (Viikinkaari 1), Helsinki FI-00014, Finland. Tornihaukantie 8D 72, Espoo 3 4 FI-02620, Finland. Juusinkuja 1, Kauniainen FI-02700, Finland. Ringing Centre, Finnish Museum of Natural History, University of Helsinki, PO Box 17 (P. Rautatiekatu 13), Helsinki FI-00014, Finland. Correspondence and requests for materials should be addressed to P.K. ([email protected]). nATuRE CoMMunICATIons | 2:208 | DoI: 10.1038/ncomms1213 | www.nature.com/naturecommunications © 2011 Macmillan Publishers Limited. All rights reserved. ARTICLE n ATu RE Co MMun ICATIons | Do I: 10.1038/ncomms1213 lobal climate warming changes the environment of most organisms and is expected to lead to a change in selection Gpressures with microevolutionary consequences that allow the adaptation of organisms to this new environment and thereby long-term population persistence . Although such adaptation to new environmental conditions created by climate change is expected in wild-animal populations , solid evidence for a microevolutionary (that is, genetic) response to climate change is rare . Microevolution in response to climate change has been demonstrated in inverte- Grey Brown 4,5 brate populations , but these studies lack information on the mech- anisms and selective factors linking particular genotypes to climate. Other studies have found selection on heritable phenotypic traits correlated with climate change, but do not report any genetic change in the population or the role of environmental factors exceed those of selection and lead to unpredicted phenotypic changes . e Th rela - tive role of evolutionary versus ecological response in relation to 6–8 climate change is still largely unexplored . Furthermore, there is a 4 5 6 7 8 9 10 11 12 13 14 noticeable absence of empirical studies addressing whether climate Colour score change actually has the potential to drive changes in selection and thereby cause microevolution . Figure 1 | Frequency distribution of tawny owl colouration in the study Systems with genetically based colour polymorphism have been population. Colour scoring is based on scorings of brown pigmentation on 10,11 used in classic studies of microevolution in wild populations , four different parts of the plumage and ranges from 4 to 14 points in 491 because they allow assessment of genotypes by censusing the individuals scored in 1978–2008. The frequency of colouration is bimodal frequency of colour morphs. Colour polymorphism is thought to and the two morphs can be classified into a grey and a brown morph at the have evolved and to be maintained by morph-specific sensitivity to cut point between scores 9 and 10. The cut point (red line) was determined 12–14 environmental conditions , and colour polymorphism oen ft has visually as the lowest intermediate point between the two models . A grey 15,16 a relatively simple genetic basis . Hence, such systems should be (left) and a brown (right) tawny owl colour morph are shown above the highly suitable for studying the microevolutionary capacity of wild graph (photography courtesy of: Dick Forsman). populations to track environmental change. In this study, we explore the links between climate change and alteration of the selective regime on a highly heritable phenotypic trait, plumage colouration in the tawny owl (Strix aluco), a com- had at least one relative with a measured phenotype in the pedigree mon bird of prey throughout the temperate regions of Europe. In were included. Extra-pair paternity is low in this species , and tawny owls, plumage colouration is determined by the degree of we are thus confident in inferring relatedness on the basis of the reddish-brown pheomelanin pigmentation deposited in their plum- social pedigree. Sex, age (1, 2, ≥3 years) and year of first breeding age . This colouration is independent of age and sex, and is highly were tested as fixed effects, but were not significant, and were not heritable . e Th frequency distribution of colouration (scored on included in the final models. This basic animal model based on the an ordinal scale) shows a bimodal distribution (Fig. 1), suggesting colouration scoring method revealed that plumage colouration was there are two basic morphs (termed grey and brown). Earlier work 79.8 ± 13.8 (s.e.m.)% heritable, which is in accordance with previous revealed that the brown tawny owl morph has reduced survival high heritability estimates of colouration in tawny owls ranging compared with the grey morph, resulting in lower lifetime from 72% using parent–offspring regression and 93% in a cross- 18 17 reproductive success of the brown morph . fostering experiment . Such high heritability suggests that few In this study, we first use colour scores of parents and their genes have large effects on colouration of the phenotype. offspring near fledging to demonstrate that a simple genetic architecture may underlie the two morphs. Second, we model the Inferring Mendelian genetics on nestlings and their parents. survival using capture–mark–recapture methodology of individual- Because the estimated heritability of colouration is high and the based long-term data from 28 years in relation to climate conditions distribution of colour scores is bimodal (Fig. 1), allowing the to show that selection against the brown morph is related to climate. separation of two colour morphs, we tested whether a ‘major gene’ Climate change has made winters increasingly milder during the could be responsible for creating this pattern. We used data from last decades, and we show that selection against the brown morph 318 nestlings in 83 nests, which were colour scored as either brown disappeared accordingly. Last, we show that the proportion of the or grey morph in years 2006–2009. Tawny owls mate random brown morph has increased dramatically over time. u Th s, we have with respect to colour . We contrasted three different models shown that climate change can influence selection demonstrating (see Supplementary Information): two Mendelian models, in which that climate change may influence evolution in wild populations. plumage colour is assumed to be fully determined by one locus, where either the ‘brown’ allele is 100% dominant over the ‘grey’ Results allele or the other way around, and one additive genetic model Heritability of colouration in tawny owls. We colour scored all (many genes of small, additive effect). breeding tawny owls in our study population from 1978 onwards e Th model assuming brown dominance (Supplementary Table S1) using a semi-continuous scale, which is based on scoring the degree produces a ratio of brown/grey phenotypes that almost exactly of reddish-brown colouration in four different parts of the plumage. matches what is expected under this inheritance model in Hardy– An individual’s plumage colouration does not change throughout Weinberg equilibrium (52.8% of offsprings are observed and 55.2% life (repeatability >90% (ref. 18)). Because practically all male and are expected to be brown, G = 0.308, P = 0.58; Fig. 2, Supplementary female parents and their offspring have been individually marked Table S2). Repeating the above, but assuming that the allele for grey in the study population since 1978, we can estimate the heritability morph is dominant over the allele for brown produces a poorer t fi using quantitative genetic methods . We used a reduced pedigree, between observed and expected ratio of the offspring ( G = 12.98, in which 167 individuals whose phenotype was measured and who P = 0.0015; Fig. 2). er Th e are more brown offspring observed than n ATu RE Co MMun ICATIons | 2:208 | Do I: 10.1038/ncomms1213 | www.nature.com/naturecommunications © 2011 Macmillan Publishers Limited. All rights reserved. Frequency (%) n ATu RE Co MMun ICATIons | Do I: 10.1038/ncomms1213 ARTICLE Table 1 | Best five models explaining variation in survival of tawny owl colour morphs. NS Model QAICc QAICc Para­ Likeli­ weight meters hood (1) Φ p 1,771.51 0.454 32 1.00 (temp + col*snow) (t) (2) Φ p 1,772.52 0.274 33 0.60 (col*temp + col*snow) (t) (3) Φ p 1,773.64 0.156 33 0.35 (vole + temp + col*snow) (t) (4) Φ p 1,774.34 0.110 34 0.24 (col*vole + temp + col*snow) (t) (5) Φ p 1,780.18 0.006 52 0.01 (col + t) (t) Models are corrected for over-dispersion (c ˆ=1.19). Abbreviations: col, plumage colour; snow, snow depth (cm); temp, temperature (°C); t, time B×B B×G G×G B×B B×G G×G B×B B×G G×G B×B B×G G×G dependence; vole, vole abundance index and interaction ‘*’ between these.†The symbol Φ and p denote apparent survival and capture probability, respectively, with in subscript the covariates Observed Brown Grey Additive considered to affect each parameter. The interaction term is a shorthand notation for a model data dominance dominance model that also includes the effects separately (that is, ‘col*snow’ stand for ‘col + snow + col*snow’). Figure 2 | Genetic models of inheritance of colouration. n umber of brown (red bar) and grey (grey bar) offspring colour morphs produced by different combinations of parental colour morphs (B×B, B×G and G×G). that low winter temperature decreases survival probability. er Th e The first columns show the observations in the field, second, third and was also support for an interaction between colour morph and tem- fourth columns show the expected number of offspring colour morphs perature (col*temp) indicating lower survival for brown individuals according to models with brown dominance, grey dominance and an compared with grey ones in cold temperatures. Prey abundance in additive genetic model, respectively. The lines above the bars show late autumn also explained some variation in survival, as the third a G-test of association between models and their significance ranked model included the effect of prey abundance (vole) and (ns : P = 0.58, **P < 0.002, ***P < 0.0001). the fourth ranked model included an interaction between prey abundance and colour morph (col*vole). Recapture probability was not explained by variables prey abundance, temperature or snow expected when assuming full dominance of the grey allele over depth as none of the models where recapture was constrained by brown. e Th purely additive model also t fi ted the data poorly. these variables received any support. In this particular case, the colour scores of the adults were such that Model averaging of all candidate models (N = 175) revealed that the additive model predicted that all offspring from monomorphic variation in snow depth explained most of the variation in survival of crosses were the same morph as the parents; thus, these crosses the colour morphs. In our case, 99.4% of support stems from the four are not informative for testing. However, focusing on the hetero- best models (Table 1) and the averaging can therefore be considered morphic (BxG) cross, it is clear that there are more offspring of the to mainly describe the common features included in these models brown morph observed than expected also under the assumption (that is, colour morph–snow depth interaction). As snow depth of an additive genetic inheritance (G = 70.9, P < 0.0001; Fig. 2). increased, survival of the brown morph decreased more strongly Alternative approaches for statistically comparing the observed than for the grey morph (Fig. 3a). Simultaneously, snow depth has and expected frequencies of morphs all provided the same con- decreased over time (Fig. 3b; linear model, year: b = − 0.37 ± 0.13, clusion (Supplementary Information). We thus conclude from the F = 8.49, P = 0.007). As a consequence, there was a time trend in 1,25 above exercises on the basis of comparing fledglings’ morphs with survival of the colour morphs from 1981–2008, in which survival their parents’ morphs that we find evidence for genetic dominance of the grey morph was fairly stable across years, whereas survival of brown over grey, whereas dominance of grey and purely addi- of brown individuals improved dramatically towards the end of the tive genetic effects are not supported by this data. Although this time series (Fig. 3c). u Th s, we provide evidence that climate-driven modelling is not exhaustive, it does show that the tawny owl pheno- selection against the brown morph has decreased in recent years typic morph has a genetic architecture that relies on few genes with such that the survival propensity of the morphs have equalized in large effects, which is consistent with a Mendelian inheritance of recent, mild winters. colouration based on one locus with a ‘brown’ allele dominant over a ‘grey’ allele. Population-level response to climate-driven selection. When selection on a heritable trait changes, a response in the composi- Climate change and survival of tawny owl colour morphs. Several tion of the population is expected . We indeed found that the fre- aspects of the environment have changed for tawny owls. Climate quency of brown morphs increased markedly between 1981 and warming has led to milder winters, especially in subarctic regions . 2008. Compared with historical data, when on average one-third Furthermore, the cyclic dynamics of voles—the staple food of of the individuals were brown (Fig. 4a), we found that the brown tawny owls in Finland—has been fading and has become irregular morph rapidly increased in frequency especially during the last dec- 22,23 in recent years . We tested whether survival of tawny owl colour ade (Fig. 4b; binomial generalized linear model 1981–2008, year: morphs are differently ae ff cted by such changes by applying capture– b = 0.050 ± 0.009 s.e.m., z = 5.66, N = 28, P < 0.0001). This phenotypic recapture modelling to the data from 1981 to 2008 (N = 466 indi- change was present also on a larger nationwide scale. In a time viduals). We modelled survival probability of brown and grey adult series of tawny owls captured, marked and colour scored (grey or breeding tawny owls in relation to over-winter prey abundance and brown) by ornithologists all over Finland between 1961 and 2008 snow depth and temperature during a period in winter that was (N = 3,239 observations), we found a steadily increasing frequency critical for tawny owl survival (see Supplementary Information). of the brown morph (Fig. 4c, year: b = 0.025 ± 0.004 s.e.m., z = 6.94, e Th results of the modelling showed that all four best models, which N = 48, P < 0.0001). u Th s, the increase of the brown morph is a large together received 99.4% of the support (QAICc weight), included scale phenomenon occurring all over Finland, involving thousands an interaction where brown individuals had lower survival than of individuals. Hence, this phenotypic change is unlikely to be grey ones as snow cover became deeper (col*snow, Table 1). Tem- caused by genetic drift, because drift is only a major force for chang - perature (temp) was included in all four best models, which implies ing allele frequencies in small populations. Given the strong genetic n ATu RE Co MMun ICATIons | 2:208 | Do I: 10.1038/ncomms1213 | www.nature.com/naturecommunications © 2011 Macmillan Publishers Limited. All rights reserved. Number of offspring ARTICLE n ATu RE Co MMun ICATIons | Do I: 10.1038/ncomms1213 underpinning of tawny owl morphs (see above), we consider the selection on the proportional increase of the brown morph, we observed phenotypic trend in the proportion of the brown morph as categorized all breeding individuals into immigrants (r fi st breeder indicative for a shift in gene frequencies. Hence, we here document that is unmarked or marked outside the study area), local recruits microevolution of tawny owl plumage colour. (r fi st breeders marked as young) and old breeders (survivors from Apart from selection, immigration is an important population a previous breeding attempt). We then analysed the relative contri- dynamical feature in our study population . A proportional increase bution of grey and brown survivors, immigrants and local recruits in immigrating brown morphs could account for the observed over time to the observed increase in the frequency of the brown increase in their frequency in the population. To test the relative morph. We found that the increase in frequency of the brown morph importance of morph-specific immigration, local recruitment and in the population was explained only by an increase in the number of brown survivors over time, and not by any other numeral trend (binomial generalized linear model: b = 0.18 ± 0.09 s.e.m., z = 2.11, N = 28, P = 0.035, Fig. 5). We used our observed parent–os ff pring inheritance pattern to retrospectively infer the morphs of os ff pring produced during the last three decades. e Th re was no morph- 0.8 specic fi temporal trend in reproductive success or recruitment rate (Supplementary Information), which illustrates that the increase in the proportion of brown morphs in the population is not driven by a 0.6 change in productivity of the brown morph. Furthermore, we found no evidence for a phenotypically plastic within-individual coloura- tion change as winter climate gets milder (Supplementary Informa- 0.4 tion). We conclude that improved survival of brown adult tawny owls caused by warmer winters with less snow is the most likely candidate to drive the observed temporal increase in the brown morph. 0.2 Discussion Our study constitutes, to our knowledge, the first empirical evi - 0 5 10 15 20 25 dence of climate-driven change in selection on a heritable trait. Work on climate change induced evolution typically concerns the Snow depth (cm) documentation of temporal trends in traits that are assumed to be t fi ness-related (for example, phenology), possibly linked with an exploration of the genetic underpinning of such traits . Even if a focal trait is heritable and selectively important, surprisingly few studies have asked whether climate change has actually altered the selective regime. Selection can be environmentally dependent and yet not change as climate changes . Unless there is evidence that climate change drives an alteration in selection, it is potentially erroneous to attribute an observed temporal change in a trait (whether on the genetic or on the phenotypic level) to climate change, because a temporal trend can be caused also by other changes in the environment that occurred during the same time period. In this study, we show that a particularly powerful form of natu- ral selection (survival selection on reproducing adults) on tawny owl colour polymorphism is driven by climatic conditions in early winter. Differential performance of contrasting morphs under vari - able environmental conditions lies at the heart of theory behind the 1980 1985 1990 1995 2000 2005 2010 26 evolution of genetic polymorphism . There are three non-mutually Year exclusive explanations for why the brown tawny owl morph may be more sensitive to harsh winter conditions. First, colouration itself 1 may be the target of selection; for example, predation on brown individuals may be more severe under snow-rich conditions. e Th main tawny owl predator, however, is the eagle owl Bubo bubo , 0.8 Figure 3 | Survival of grey and brown tawny owls in relation to changes 0.6 in snow depth. s urvival estimates are based on averaging all candidate capture–mark–recapture models considering the effects of food supply (vole abundance), average snow depth and average temperature during 0.4 a critical period in winter (see s upplementary Information). Climatic data are derived from the database of the Finnish Meteorological Institute. (a) s urvival of brown and grey tawny owl colour morphs in relation to snow 0.2 depth. (b) s now depth during the critical period for tawny owl survival during 1981–2008 in s outhern Finland. (c) s urvival of grey and brown tawny owl colour morphs during 1981–2008. Grey tawny owls are denoted by grey circles and brown ones by red diamonds. Error bars are standard 1980 1985 1990 1995 2000 2005 2010 errors of the estimated survival and the lines are regression slopes based Year on the data. n ATu RE Co MMun ICATIons | 2:208 | Do I: 10.1038/ncomms1213 | www.nature.com/naturecommunications © 2011 Macmillan Publishers Limited. All rights reserved. Estimated survival (Phi) Snow depth (cm) Estimated survival (Phi) n ATu RE Co MMun ICATIons | Do I: 10.1038/ncomms1213 ARTICLE 0.5 0.5 0.5 0.4 0.4 0.4 0.3 0.3 0.3 0.2 0.2 0.2 0.1 0.1 0.1 29 97 198 157 219 174 205 114 24 82 170 179 347 393 625 468 558 348 0 0 0 1910 1940 1970 1980 1990 2000 2010 1960 1970 1980 1990 2000 2010 Year Year Year Figure 4 | Temporal changes in the frequency of the brown morph in Finland on different scales. (a) Historical data on colour morph frequencies in the early century (1911–1945) and mid-century (1946–1980) based on skins from the Zoological museum collection (u niversity of Helsinki). Each symbol represents the mean frequencies of seven 5-year periods ( ± s.e.m.). (b) Frequency of the brown morph in the study population based on captured breeding birds between 1981 and 2008. s hown are mean annual frequencies of the brown morph in 5-year periods ( ± s.e.m.). (c) n ationwide population frequency of brown individuals based on all breeding birds ringed or recaptured by amateur ringers in Finland and colour scored as either grey or brown. s ymbols are as in b. Total sample size is given along the x axis. The method of scoring colour morphs in a and b (filled diamonds) differs from the method used in c (filled dots), such that the averages and slope of the trend are not directly comparable, although the direction is. Our second main finding is a clear temporal shift towards a higher proportion of the brown morph in the population. In general, such a pattern is microevolution (change in allele frequen- 20 cies driven by selection), genetic drift (stochastic change in allele frequency) or phenotypic plasticity (environmentally induced change in expressed phenotype) . We show that the increase of the brown tawny owl morph occurs in a representative (nationwide) sample of the entire Finnish population of tawny owls (thousands of individuals), which makes it unlikely that random genetic drift drives this trend. e Th observed trend concerns phenotypes, but we 1980 1985 1990 1995 2000 2005 2010 1980 1985 1990 1995 2000 2005 2010 here demonstrate that tawny owl morphs are under tight genetic Year Year control in a manner that is consistent with a one locus–two allele genetic architecture. In addition, we demonstrate that phenotypic Figure 5 | Factors explaining the increase in the proportion of the plasticity does not explain the trend. We therefore believe that brown morph in the study population. n umber of brown (a) and grey the increase in the proportion of brown tawny owls during the last (b) survivors (denoted by diamonds, solid line), immigrants (circles, two decades constitutes a microevolutionary change. dashed line) and recruits (triangles, dashed-dotted line) in the breeding A recent review concluded that three study systems provide population during the study period. evidence for microevolutionary changes over time with a puta- tive link to climate change. es Th e are: a shift in the critical photo - period that ae ff cts diapause in pitcher-plant mosquitoes , shifts in which is not a visual predator. Furthermore, the brown morph is the distribution of chromosomal arrangements and Adh alleles in 28 4,5 in fact considered to be more cryptic , although this need not hold Drosophila , and quantitative genetic evidence that timing of breed- under snow-rich conditions. Second, colouration may, through ing in red squirrels Tamiasciurus hudsonicus advanced in concert pleiotropic effect be associated with another property that is the with climate warming . For the first two examples, climate change real target of selection. Increasing evidence, both on molecular could not be firmly established as the causal agent of the temporal 3 34 and individual level, suggests that the differential performance of change . Recent developments in quantitative genetics suggest that morphs across environments can be caused by genetic covariation the last example is not as rigorous a demonstration of microevolu- between colouration (melanization) and a physiological property, tion as initially suggested. We show that warming of winter climate 14,18,29–32 such as metabolism or immune function . Third, pleiotropic leads to reduced selection against the brown morph, and we demon- effects between energy homoeostasis and melanin pigmentation strate that at the same time the frequency of the brown morph in can lead to differential predation pressure if the melanistic (brown) the Finnish population increases to a level that is above the historic morph has higher energetic requirements and needs to forage record of the species. Intuitively, a release of selection on a highly more and thus becomes more susceptible to predation under harsh heritable trait should lead to a microevolutionary response, and we winter conditions. Additional research is needed in establishing the provide statistical evidence that selection (rather than immigra- possible pleiotropic link between genes expressing colouration and tion or local recruitment) indeed drives the observed increase in physiological properties. Nevertheless, the observed pattern with the frequency of the brown morph. On the other hand, our survival an interaction between winter harshness and morph suggests that analysis does not show a selective advantage of the brown morph: intrinsic differences between the morphs drive their propensity for survival during the last (warm) winters was approximately equal for survival. the grey and brown morphs. Furthermore, the brown morph has n ATu RE Co MMun ICATIons | 2:208 | Do I: 10.1038/ncomms1213 | www.nature.com/naturecommunications © 2011 Macmillan Publishers Limited. All rights reserved. N individuals Frequency of brown ARTICLE nATuRE CoMMunICATIons | DoI: 10.1038/ncomms1213 no reproductive advantage. How can the frequency of the brown Capture–mark–recapture modelling and model selection. Survival of adult grey and brown tawny owls was estimated using capture–mark–recapture methodol- increase despite an absence of selective advantages? We believe that ogy on live encounters data (Cormack–Jolly–Seber model) of 1,065 observations as yet unknown details of the genetics provide the link between the of 466 tawny owls Supplementary Table S3, using the programme MARK . We climate-driven change in selection and the observed increase in used a sliding-window approach (all possible time windows between 5 and 44 days the frequency of the brown morph. In particular, we currently lack were considered) to find the relevant time period during which survival (full-time detailed quantitative understanding of how the selective mechanism dependent CMR model, Φ p ) correlated best with climate (average temperature (t) (t) and snow depth). Annual survival of tawny owls was highly correlated with operates on the genotypes. This is because if one accepts that morph temperature and snow depth (Supplementary Table S4). Measures of temperature inheritance patterns are caused by a one locus–two allele model and snow depth from the time window that correlated best with annual tawny with brown dominance over grey (as our findings suggest), there owl survival were selected as covariates for further modelling (Supplementary are two genotypes that produce a brown morph (heterozygous Bg Table S4). We tested for the effects of real covariates by replacing the dummy variable ‘time dependence (t)’ with interactions of colour morph and prey and homozygous BB), but we necessarily measure selection on these abundance (col*vole), temperature (col*temp) and snow depth (col*snow) in two combined (that is, morph-based). One possibility is that winter both survival (Φ) estimation as well as recapture (p). We applied model climate-driven selection against the heterozygote is less than selec- averaging on the candidate models to get a more conservative estimate of Φ tion against the homozygote. Indeed, if pleiotropic effects of the and p. Although averaging is performed over all candidate models, the weighting putative grey and brown colour genes indeed cause the differential by QAIC model weights ensures that the information in the best fitting models contributes most. survival of tawny owl morphs then a heterozygote brown individual Further methodological details are provided in the Supplementary Methods. may well perform differently than a homozygous brown individual. In the buzzard Buteo buteo, Mendelian inheritance of colour genes has been suggested to underlie the plumage colour polymorphism References observed in that species with a selective advantage for the hetero- 1. Davis, M. B. & Shaw, R. G. Range shifts and adaptive responses to quaternary zygous morph . From a population-genetic perspective, such a ‘hid- climate. Science 292, 763–679 (2001). 2. Parmesan, C. Ecological and evolutionary responses to recent climate change. den’ heterozygote advantage in combination with a temporal release Annu. Rev. Ecol. Evol. Syst. 37, 637–669 (2006). of selection has the potential to explain both the maintenance of 3. Gienapp, P., Teplitsky, C., Alho, S., Mills, J. A. & Merilä, J. Climate change and the brown morph in the population and the increase in frequency evolution: disentangling environmental and genetic responses. Mol. Ecol. 17, of the brown morph, despite the fact that selection continuously 167–178 (2008). acts against the brown morph (model developed in Supplementary 4. Umina, P. A., Weeks, A. R., Kearney, M. R., McKechnie, S. W. & Hoffmann, A. A rapid shift in a classical clinal pattern in Drosophila reflecting climate change. Information). This hypothesis is testable once the molecular genetic Science 308, 691–693 (2005). basis of tawny owl plumage colour polymorphism has been clarified 5. Balanya, J., Oller, J. M., Huey, R. B., Gilchrist, G. W. & Serra, L. Global genetic and selection on the genotypic level can be estimated. change tracks global climate warming in Drosophila subobscura. Science 313, Our study demonstrates a climate change driven alteration of 1773–1775 (2006). selection on a heritable trait coupled with a population-level evo- 6. Ozgul, A. et al. The dynamics of phenotypic change and the shrinking sheep of St. Kilda. Science 325, 464–467 (2009). lutionary response; all of which are required for long-term survival 7. Réale, D., McAdam, A. G., Boutin, S. & Berteaux, D. Genetic and plastic of species. Because colour polymorphism is highly heritable, studies responses of a northern mammal to climate change. Proc. R. Soc. Lond. B 270, on these systems are likely to provide important benchmark insights 591–596 (2003). in the effects of environmental change on population level changes, 8. Teplitsky, C., Mills, J. A., Alho, J. S., Yarrall, J. W. & Merilä, J. Bergmann’s not only in terms of phenotypic changes , but also in terms of rule and climate change revisited: disentangling environmental and genetic responses in a wild bird population. Proc. Natl Acad. Sci. USA 105, changes in genetic diversity and the evolvability of organisms 13492–13496 (2008). (see also Supplementary Information) and changes in latitudinal 9. Sheldon, B. C. Genetic perspectives on the evolutionary consequences of distributions of morphs in colour polymorphic species . climate change in birds. in Ee ff ct of Climate Change on Birds (eds Møller, A. P, Fiedler, W. & Berthold, P.) 149–168 (Oxford University Press, 2010). 10. Sumner, F. B. Genetic and distributional studies of three subspecies of Methods Data sets. Tawny owls were studied from 1981 to 2008 in a study area of Peromyscus. J. Genet. 23, 275–376 (1930). 11. Fisher, R. A. & Ford, E. B. e Th spread of a gene in natural conditions in a colony about 250 km in Southern Finland (60°15N′, 24°15E′). The study area is of the moth Panaxia dominula L. Heredity 1, 143–174 (1947). dominated by mixed forests, agricultural areas and small freshwater courses and was established in 1977–78. From 1980 onwards ~125 nest boxes in suitable 12. Majerus, M. E. N. Melanism, Evolution in Action. (Oxford University Press, habitats were available for tawny owls to breed in. Considerable effort was put 1998). 13. Galeotti, P., Rubolini, D., Dunn, P. O. & Fasola, M. Colour polymorphism in into finding the nests of all tawny owls in the study population by searching for birds: causes and functions. J. Evol. Biol. 16, 635–646 (2003). natural nest sites and new boxes set up by private individuals in the approximate area where hooting individuals had been recorded earlier in spring and where 14. Roulin, A. The evolution, maintenance and adaptive function of genetic colour polymorphism in birds. Biol. Rev. 79, 1–34 (2004). a breeding thus was expected. The same monitoring scheme was used by K.A. and 15. Mundy, N. I. A window on the genetics of evolution: MC1R and plumage T.K. during all years and the effort remained similar in all years. The majority of all breeding male and female owls in the study population were caught, ringed colouration in birds. Proc. R. Soc. Lond. B. 272, 1633–1640 (2005). 16. Hoekstra, H. E. Genetics, development and evolution of adaptive pigmentation and their reproductive output was measured. Plumage colouration was scored in vertebrates. Heredity 97, 222–234 (2006). using a semi-continuous ordinal scale (range from 4 (grey) to 14 (reddish-brown)) on all breeding individuals on each encounter (N = 1116 records of 491 individuals) 17. Gasparini, J. et al. Strength and cost of an induced immune response are using a standardized and repeatable scoring that shows colouration is independ- associated with a heritable melanin-based colour trait in female tawny owls. J. Anim. Ecol. 78, 608–616 (2009). ent of age and sex . Museum skin specimens collected by the public between 18. Brommer, J. E., Ahola, K. & Karstinen, T. The colour of fitness: plumage 1915 and 1980 and stored by the Natural History Museum, University of Helsinki, (N = 126) were colour scored in the same way as in the study population. National coloration and lifetime reproductive success in the tawny owl. Proc. R. Soc. Lond. B. 272, 935–940 (2005). level tawny owl colour morph data collected by ornithologists in Finland were 19. Lynch, M. & Walsh, B. Genetics and Analysis of Quantitative Traits (Sinauer, obtained from the Finnish Ringing Centre. We extracted the data on all records of adult ringed and recaptured tawny owls in Finland to which colour morph (grey 1998). 20. Saladin, V., Ritschard, M., Roulin, A., Bize, P. & Richner, H. Analysis of genetic or brown) had been assigned during 1961–2008 (30% of all data, 3,194/10,601 parentage in the tawny owls (Strix aluco) reveals extra-pair paternity is low. records). Genetics. We used a REML linear mixed model (‘animal model’) to estimate J. Ornithol. 148, 113–116 (2007). heritability of plumage colouration. The additive genetic effects were estimated 21. Intergovernmental Panel on Climate Change (IPCC). Climate change 2007: Synthesis report. Fourth assessment report, http://www.ipcc.ch/ (2007). using pedigree-derived estimates of relatedness across all individuals . We tested 22. Ims, R. A., Henden, J.- A. & Killengreen, S. T. Collapsing population cycles. whether parent–offspring resemblance (83 nests with 318 offspring, data from 2006 to 2009) followed a purely additive genetic model, or a one locus–two allele Trends Ecol. Evol. 23, 79–86 (2008). 23. Brommer, J. E., Pietiäinen, H., Ahola, K., Karell, P., Karstinen, T. & Kolunen, H. model under Hardy–Weinberg equilibrium, in which either ‘brown’ or ‘grey’ e r Th eturn of the vole cycle in southern Finland refutes the generality of were dominant over the other allele. nATuRE CoMMunICATIons | 2:208 | DoI: 10.1038/ncomms1213 | www.nature.com/naturecommunications © 2011 Macmillan Publishers Limited. All rights reserved. nATuRE CoMMunICATIons | DoI: 10.1038/ncomms1213 ARTICLE the loss of cycles through ‘climatic forcing’. Global Change Biol. 16, 577–586 38. White, G. C. & Burnham, K. P. Program MARK: survival estimation from (2010). populations of marked animals. Bird Study 46, S120–S138 (1999). 24. Karell, P., Ahola, K., Karstinen, T., Zolei, A. & Brommer, J. E. Population 39. Burnham, K. P. & Anderson, D. R. Model Selection and Inference—A Practical dynamics in a cyclic environment: Consequences of cyclic food abundance Information Theoretical Approach (Springer, 1998). on tawny owl reproduction and survival. J. Anim. Ecol. 78, 150–162 (2009). 25. Charmantier, A., McCleery, R. H., Cole, L. R., Perrins, C., Kruuk, L. E. B. & Acknowledgments Sheldon, B. C. Adaptive phenotypic plasticity in response to climate change in This is report number 9 of Kimpari Bird Projects (KBP). We thank the other members of a wild bird population. Science 320, 800–803 (2008). KBP—Juhani Ahola, Pentti Ahola, Bo Ekstam, Arto Laesvuori and Martti Virolainen— 26. Fisher, R. A. e G Th enetical Theory of Natural Selection (Clarendon Press, 1930). for the many hours spent conducting fieldwork. We thank all bird ringers in Finland who 27. Mikkola, H. Owls of Europe. (T & A. D. Poyser, 1983). have provided data on tawny owl colour morphs, Martti Hildén for help with Museum 28. Gehlbach, F. R. e Eas Th tern Screech owl: Life History, Ecology, and Behaviour skins and Hannu Pietiäinen for insightful comments on the manuscript. P.K. was in the Suburbs and Countryside. (Texas A&M, 1994). supported by the Academy of Finland (projects 1118484 and 1131390 to J.E.B.) and 29. Ducrest, A.- L., Keller, L. & Roulin, A. Pleiotropy in the melanocortin system, J.E.B. was employed as an Academy Researcher. coloration and behavioural syndromes. Trends Ecol. Evol. 23, 502–510 (2008). 30. Piault, R., Gasparini, J., Bize, P., Jenni-Eiermann, S. & Roulin, A. Pheomelanin- based coloration and the ability to cope with variation in food supply and Author contributions parasitism. Am. Nat. 174, 548–556 (2009). Data from the study population were collected by K.A., T.K. and data on skin specimen 31. Stütz, A. M., Morrison, C. D. & Argyropoulos, G. The Agouti-related protein by P.K. J.V. provided national data on tawny owl ringing data. Analyses and writing was and its role in energy homeostasis. Peptides 26, 1771–1781 (2005). done by P.K. and J.E.B. 32. Boswell, T. & Takeuchi, S. Recent developments in our understanding of the avian melanocortin system: its involvement in the regulation of pigmentation Additional information and energy homeostasis. Peptides 26, 1733–1743 (2005). Supplementary Information accompanies this paper at http://www.nature.com/ 33. Bradshaw, W. E. & Holzapfel, C. M. Genetic shi ft in photoperiodic response naturecommunications correlated with global warming. Proc. Natl Acad. Sci. USA 98, 14509–14511 (2001). 34. Hadfield, J. D., Wilson, A. J., Garant, D., Sheldon, B. C. & Kruuk, L. E. B. The Competing financial interests: The authors declare no competing financial interests. misuse of BLUP in ecology and evolution. Am. Nat. 175, 116–125 (2010). Reprints and permission information is available online at http://npg.nature.com/ 35. Krüger, O., Lindström, J. & Amos, W. Maladaptive mate choice maintained by reprintsandpermissions/ heterozygote advantage. Evolution 55, 1207–1214 (2001). 36. Galeotti, P., Rubolini, D., Sacchi, R. & Fasola, M. Global changes and animal How to cite this article: Karell, P. et al. Climate change drives microevolution in a wild phenotypic responses: melanin-based plumage redness of scops owls increased bird. Nat. Commun. 2:208 doi: 10.1038/ncomms1213 (2011). with temperature and rainfall during the last century. Biol. Lett. 5, 532–534 (2009). License: This work is licensed under a Creative Commons Attribution-NonCommercial- 37. Roulin, A., Burri, R. & Antoniazza, S. Owl melanin-based plumage redness is more frequent near than away from the equator: implications on the effect of Share Alike 3.0 Unported License. To view a copy of this license, visit http:// climate change on biodiversity. Biol. J. Linn. Soc. (in the press). creativecommons.org/licenses/by-nc-sa/3.0/ nATuRE CoMMunICATIons | 2:208 | DoI: 10.1038/ncomms1213 | www.nature.com/naturecommunications © 2011 Macmillan Publishers Limited. 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Published: Feb 22, 2011

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