Our study constitutes, to our knowledge, the first empirical evidence of climate-driven change in selection on a heritable trait. Work on climate change induced evolution typically concerns the documentation of temporal trends in traits that are assumed to be fitness-related (for example, phenology), possibly linked with an exploration of the genetic underpinning of such traits3
. 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 changes25
. 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 natural 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 variable environmental conditions lies at the heart of theory behind the evolution of genetic polymorphism26
. There are three non-mutually exclusive explanations for why the brown tawny owl morph may be more sensitive to harsh winter conditions. First, colouration itself may be the target of selection; for example, predation on brown individuals may be more severe under snow-rich conditions. The main tawny owl predator, however, is the eagle owl Bubo bubo27
, which is not a visual predator. Furthermore, the brown morph is in fact considered to be more cryptic28
, although this need not hold under snow-rich conditions. Second, colouration may, through pleiotropic effect be associated with another property that is the real target of selection. Increasing evidence, both on molecular and individual level, suggests that the differential performance of morphs across environments can be caused by genetic covariation between colouration (melanization) and a physiological property, such as metabolism or immune function14
. Third, pleiotropic effects between energy homoeostasis and melanin pigmentation can lead to differential predation pressure if the melanistic (brown) morph has higher energetic requirements and needs to forage more and thus becomes more susceptible to predation under harsh winter conditions. Additional research is needed in establishing the possible pleiotropic link between genes expressing colouration and physiological properties. Nevertheless, the observed pattern with an interaction between winter harshness and morph suggests that intrinsic differences between the morphs drive their propensity for survival.
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 frequencies driven by selection), genetic drift (stochastic change in allele frequency) or phenotypic plasticity (environmentally induced change in expressed phenotype)3
. 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. The observed trend concerns phenotypes, but we here demonstrate that tawny owl morphs are under tight genetic control in a manner that is consistent with a one locus–two allele genetic architecture. In addition, we demonstrate that phenotypic plasticity does not explain the trend. We therefore believe that the increase in the proportion of brown tawny owls during the last two decades constitutes a microevolutionary change.
A recent review3
concluded that three study systems provide evidence for microevolutionary changes over time with a putative link to climate change. These are: a shift in the critical photoperiod that affects diapause in pitcher-plant mosquitoes33
, shifts in the distribution of chromosomal arrangements and Adh
alleles in Drosophila4
, and quantitative genetic evidence that timing of breeding in red squirrels Tamiasciurus hudsonicus
advanced in concert with climate warming7
. For the first two examples, climate change could not be firmly established as the causal agent of the temporal change3
. Recent developments in quantitative genetics34
suggest that the last example is not as rigorous a demonstration of microevolution as initially suggested. We show that warming of winter climate leads to reduced selection against the brown morph, and we demonstrate that at the same time the frequency of the brown morph in the Finnish population increases to a level that is above the historic record of the species. Intuitively, a release of selection on a highly heritable trait should lead to a microevolutionary response, and we provide statistical evidence that selection (rather than immigration or local recruitment) indeed drives the observed increase in the frequency of the brown morph. On the other hand, our survival analysis does not show a selective advantage of the brown morph: survival during the last (warm) winters was approximately equal for the grey and brown morphs. Furthermore, the brown morph has no reproductive advantage. How can the frequency of the brown increase despite an absence of selective advantages? We believe that as yet unknown details of the genetics provide the link between the climate-driven change in selection and the observed increase in the frequency of the brown morph. In particular, we currently lack detailed quantitative understanding of how the selective mechanism operates on the genotypes. This is because if one accepts that morph inheritance patterns are caused by a one locus–two allele model with brown dominance over grey (as our findings suggest), there are two genotypes that produce a brown morph (heterozygous Bg
and homozygous BB
), but we necessarily measure selection on these two combined (that is, morph-based). One possibility is that winter climate-driven selection against the heterozygote is less than selection against the homozygote. Indeed, if pleiotropic effects of the putative grey and brown colour genes indeed cause the differential survival of tawny owl morphs then a heterozygote brown individual 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 observed in that species with a selective advantage for the heterozygous morph35
. From a population-genetic perspective, such a 'hidden' heterozygote advantage in combination with a temporal release of selection has the potential to explain both the maintenance of the brown morph in the population and the increase in frequency of the brown morph, despite the fact that selection continuously acts against the brown morph (model developed in Supplementary Information
). This hypothesis is testable once the molecular genetic basis of tawny owl plumage colour polymorphism has been clarified and selection on the genotypic level can be estimated.
Our study demonstrates a climate change driven alteration of selection on a heritable trait coupled with a population-level evolutionary response; all of which are required for long-term survival of species. Because colour polymorphism is highly heritable, studies on these systems are likely to provide important benchmark insights in the effects of environmental change on population level changes, not only in terms of phenotypic changes36
, but also in terms of changes in genetic diversity and the evolvability of organisms (see also Supplementary Information
) and changes in latitudinal distributions of morphs in colour polymorphic species37