Patrik Karell

Climate change drives microevolution in a wild bird

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.

Population dynamics in a cyclic environment: consequences of cyclic food abundance on tawny owl reproduction and survival

1. Understanding which factors regulate population dynamics may help us to understand how a population would respond to environmental change, and why some populations are declining. 2. In southern Finland, vole abundance shows a three-phased cycle of low, increase and decrease phases, but these have been fading out in recent years. During five such cycles (1981-1995), all tawny owls Strix aluco were censused in a 250-km(2) study area, and their reproduction and survival were monitored. 3. Males and females showed similar dynamics, but experienced breeders recruited more offspring and had higher survival than first breeders. Offspring recruitment, but not survival of breeding individuals varied in accordance with vole abundance. 4. The populations numerical response to prey abundance was primarily due to first-breeding individuals entering the population in the increase phase when immigration was the highest. First-breeding birds were younger, but experienced breeders were older in more favourable vole years. 5. A stage-specific matrix population model integrating survival and fecundity showed that, despite obvious variation in fecundity between vole cycle phases, this variation had limited importance for overall tawny owl population dynamics, but that the survival of experienced breeders during the low phase is most important for population growth. 6. Model and data agreed that the vole cycle drives the dynamics of this avian predator by limiting the recruitment of new breeders during the low phase. Population dynamics hence differ not only from the classic example of the species in a more temperate region in the UK where the number of territories is stable across years, but also from the dynamics of other avian vole predators in Fennoscandia where the recurring crash in vole abundance drastically lowers adult survival thereby creating vacancies.

Blood parasites mediate morph-specific maintenance costs in a colour polymorphic wild bird

Parasites can mediate profound negative effects on host fitness. Colour polymorphism has been suggested to covary genetically with intrinsic physiological properties. Tawny owl colour polymorphism is highly heritable with two main morphs, grey and brown. We show that experimental medication acts to reduce blood parasites and that medicated grey females maintain body mass during breeding, whereas medicated brown females decline in body mass similar to control females of both morphs. We find no effect of medication on general immunoglobulin levels, antigen‐specific humoral response or H/L ratio. In the descriptive data, both morphs have similar blood parasite infection rates, but blood parasite infection is associated with decreased body mass in brown but not in grey females. We conclude that blood parasite infection primarily has somatic costs, which differ between the two highly heritable tawny owl colour morphs with more pronounced costs in the grey (little pigmented) morph than in the brown (heavily pigmented) morph. Because our descriptive results imply the opposite pattern, our findings highlight the need of experimental manipulation when studying heritable variation in hosts’ response to parasitism.

Tawny owl reproduction and offspring sex ratios under variable food conditions

Tawny owl reproduction and offspring sex ratios have been considered to depend on the abundance of small voles. We studied reproductive performance (laying date, clutch and brood size) during 1995–2003 and offspring sex ratios from 1999 to 2003 in relation to the abundance of small voles and food delivered to the nest in a tawny owl population in southern Finland. Abundance of small voles (field and bank voles) was based on trappings in the field, and estimates of food delivery was based on diet analysis of food remains in the nest boxes. In this population, reproductive output was not related to the abundance of small voles. Analysis of food delivered to the nest showed that the prey weight per offspring varied more than twofold between years and revealed that this difference was mainly related to the proportion of water voles in the diet. Only the number of water voles correlated with laying dates. Offspring sex ratios were weakly male biased (55%) but did not differ from parity. Sex ratios were not related to the abundance of small voles, and we found no evidence that parents delivered more food to nests with proportionally more offspring of the larger (female) sex. Our results underline the notion that populations may differ in their sex allocation pattern, and suggest such differences may be due to diet.

Demographic routes to variability and regulation in bird populations

There is large interspecific variation in the magnitude of population fluctuations, even among closely related species. The factors generating this variation are not well understood, primarily because of the challenges of separating the relative impact of variation in population size from fluctuations in the environment. Here, we show using demographic data from 13 bird populations that magnitudes of fluctuations in population size are mainly driven by stochastic fluctuations in the environment. Regulation towards an equilibrium population size occurs through density-dependent mortality. At small population sizes, population dynamics are primarily driven by environment-driven variation in recruitment, whereas close to the carrying capacity K, variation in population growth is more strongly influenced by density-dependent mortality of both juveniles and adults. Our results provide evidence for the hypothesis proposed by Lack that population fluctuations in birds arise from temporal variation in the difference between density-independent recruitment and density-dependent mortality during the non-breeding season.

Heritability, plasticity and canalization of Ural owl egg size in a cyclic environment

Avian egg size is highly variable on the population level, but is considered inflexible on the individual level. On the basis of 2969 measurements of individual eggs collected during 1981–2005, we analysed heritability, plasticity and selection on egg size in the Ural owl, a long‐lived bird that preys on voles. Vole abundance varied in a 3‐year cycle, creating varying food supply across the cycle’s phases. Ural owl egg size is heritable (h2 = 60%). Ural owls lay larger eggs in improved food conditions. On the basis of repeated breeding records of 59 females that bred in all vole cycle phases, we show that intra‐individual adjustment (plasticity) explained 22.4% of the variation in egg size across phases. Egg size was under stabilizing selection. Extremely small and extremely large eggs had reduced hatchability, and individuals who laid either large or small eggs had lower lifetime fledgling production than the ones laying intermediately sized eggs. Our findings illustrate how maternal investment in egg size can both be heritable and highly responsive to variable environmental conditions, and suggest that variation in the investment in egg size across individuals is canalized.

Ural Owl Predation on Field Voles and Bank Voles by Size, Sex and Reproductive State

Predation on selected individuals from a population may have consequences for the prey population. We studied predation of breeding Ural owls (Strix uralensis) in southern Finland on their two main prey species, field voles (Microtus agrestis) and bank voles (Myodes glareolus), which fluctuate in abundance between years. We identified sex, body mass and reproductive state of the voles in Ural owl nests and of voles caught by snap-trapping in the study area. Our results showed that Ural owls preyed proportionally more upon reproductively active field voles than expected, whereas no such bias was found for predation on bank voles. There was no difference in sex ratio between preyed upon and trapped field voles or bank voles. Ural owls captured heavier individuals of both field voles and bank voles than expected, and in field voles, but not bank voles, reproductively active individuals were heavier than reproductively inactive individuals. We discuss how differences in social organisation, dispersal and reproductive behaviour may differently affect predation vulnerability of field voles and bank voles. In contrast to the pattern documented in other owl species, we find that Ural owls select larger and reproductively active voles, and may thereby exert a higher population-dynamical impact on vole populations than expected solely from the numbers of voles preyed upon.

A possible link between parasite defence and residual reproduction

Life‐history theory centres around trade‐offs between current and future reproduction, but we have little understanding of how such trade‐offs are mediated. We supplementary fed Ural owls (Strix uralensis) during the nestling period and quantified parents’ current and future life‐history components as well as their physiological health by monitoring haematocrit, leucocyte profile, intra‐ and extracellular blood parasites. Feeding led to reduced parental effort but did not improve offspring viability, male parasite defence, or parental survival. Intracellular leucocytozoan infection was reduced in fed females which lasted to the following years reproductive season (carry‐over effect), when fed females also laid larger and earlier clutches. Leucocytozoon infection therefore may mediate the life‐history trade‐off between current and residual reproduction in this species.

Pale and dark morphs of tawny owls show different patterns of telomere dynamics in relation to disease status

Parasites are expected to exert long-term costs on host fecundity and longevity. Understanding the consequences of heritable polymorphic variation in disease defence in wild populations is essential in order to predict evolutionary responses to changes in disease risk. Telomeres have been found to shorten faster in malaria-diseased individuals compared with healthy ones with negative effects on longevity and thereby fitness. Here, we study the impact of haemosporidian blood parasites on telomere dynamics in tawny owls, which display a highly heritable plumage colour polymorphism. Previously, it has been shown that blood parasites have morph-specific impact on body mass maintenance. Here, we show that telomeres shortened faster in individuals with shorter breeding lifespan. Telomere length was negatively associated with the degree of pheomelanic brown coloration and shorter in infected than uninfected individuals. The rate of telomere shortening between breeding seasons was faster in darker pheomelanic individuals and suppression of parasite intensity between seasons was associated with faster telomere shortening in the paler individuals but not in darker ones. We propose that morph-specific physiological profiles cause differential telomere shortening and that this is likely to be a mechanism involved in previously documented environment-driven survival selection against the pheomelanic morph in this population.

Data from: Increased male bias in eider ducks can be explained by sex-specific survival of prime-age breeders

In contrast to theoretical predictions of even adult sex ratios, males are dominating in many bird populations. Such bias among adults may be critical to population growth and viability. Nevertheless, demographic mechanisms for biased adult sex ratios are still poorly understood. Here, we examined potential demographic mechanisms for the recent dramatic shift from a slight female bias among adult eider ducks (Somateria mollissima) to a male bias (about 65% males) in the Baltic Sea, where the species is currently declining. We analysed a nine-year dataset on offspring sex ratio at hatching based on molecularly sexed ducklings of individually known mothers. Moreover, using demographic data from long-term individual-based capture-recapture records, we investigated how sex-specific survival at different ages after fledgling can modify the adult sex ratio. More specifically, we constructed a stochastic two-sex matrix population model and simulated scenarios of different survival probabilities for males and females. We found that sex ratio at hatching was slightly female-biased (52.8%) and therefore unlikely to explain the observed male bias among adult birds. Our stochastic simulations with higher survival for males than for females revealed that despite a slight female bias at hatching, study populations shifted to a male-biased adult sex ratio (> 60% males) in a few decades. This shift was driven by prime reproductive-age individuals (≥5-year-old), with sex-specific survival of younger age classes playing a minor role. Hence, different age classes contributed disproportionally to population dynamics. We argue that an alternative explanation for the observed male dominance among adults–sex-biased dispersal–can be considered redundant and is unlikely, given the ecology of the species. The present study highlights the importance of considering population structure and age-specific vital rates when assessing population dynamics and management targets.