Heterogeneidad ambiental y evolución del tamaño de puesta en el herrerillo común (Cyanistes caeruleus) : testando la hipótesis de la adaptación local

Abstract

Environmental heterogeneity creates a range of habitats of different quality for species, which exert distinct selective pressures that will shape the genotype and, consequently, the phenotype of organisms. Traditionally, evolutionary models considered both the large-scale environmental heterogeneity and geographical barriers as the main promoters for adaptive population divergence. However, recent research shows that small scale environmental heterogeneity, together with nonrandom dispersal, can promote genotypic and phenotypic population differentiation, sometimes even leading to local adaptation. In this thesis, I document the effect of fine-scale environmental heterogeneity on the evolutionary dynamics of a wild population of blue tits (Cyanistes caeruleus). I characterized various abiotic and biotic factors in different adjacent forest formations, which form a continuous woodland extending across the two opposing slopes of a valley, and analysed how such environmental heterogeneity promotes the adaptive divergence between populations and shapes a habitat-dependent optimal clutch size. To this end, this thesis has been divided into two parts. The first part shows how environmental heterogeneity influences the offspring’s phenotype; while the second part demonstrates how such heterogeneity, together with non-random dispersal, has promoted the genotypic and phenotypic divergence within the blue tit population, as well as the evolution of a habitat-dependent and locally adapted optimal clutch size. The forest formations extending along the valley exhibited distinct selective pressures for blue tits during reproduction, as they differed in a wide variety of abiotic and biotic factors. The forest formations of the east-facing slope of the valley (a Holm oak forest and a dry Pyrenean oak forest), unlike the forest formations of the westfacing slope (a Scots pine forest and a humid Pyrenean oak forest), received more solar radiation, had more insolation time and temperature, and showed lower humidity, tree cover and food availability. Moreover, the presence of ectoparasites (prevalence of Ceratophyllus gallinae fleas and Protocalliphora azurea blowflies, and abundance of Culicoides biting midges) was higher in nests of the east-facing slope of the valley, while the presence of haemoparasites (microfilariae) infecting adult blue tits did not vary along the continuous woodland. The presence of Nasonia vitripennis parasitoids, which in turn parasitize P. azurea pupae, was higher in nests of the west-facing slope of the valley. Blue tits adjusted their reproductive effort to the forest type where they bred. The laying date was earlier in deciduous (dry and humid Pyrenean oak forests) than in evergreen (Scots pine and Holm oak forests) forests, whilst the clutch size was the lowest in the Scots pine forest and the highest in the humid Pyrenean oak forest, with intermediate values found in the Holm oak and dry Pyrenean oak forests. The clutch size determined the number of offspring a blue tit pair raised in a single reproductive event, since there were no habitat-dependent differences in hatching success nor fledgling success. Although the oxidative status and immune system of nestlings (measured at 13 days after hatching) varied between forest types, the offspring quality, in terms of mean body mass and body condition, was similar across the woodland. No effects of ectoparasites on blue tit reproduction, nestling oxidative status or nestling immune system were detected; however, the presence of fleas in nests was associated with a lower body mass for small, marginal nestlings and a higher number of nestlings in a nest. For their part, the presence of biting midges and microfilariae was negatively related to nestling and adult body mass, respectively. Results from natal dispersal showed a strong philopatry, with first-year blue tits being recaptured as reproductive adults in their natal slope of the valley. Accordingly, population genetic analyses revealed the existence of two genetic clusters, with blue tits from each cluster associated with the slope they inhabit. The two genetic populations showed divergence in clutch size, exceeding the level of differentiation expected based on genetic drift, hence suggesting that natural selection has favoured different clutch sizes in the two slopes of the valley. A brood size manipulation experiment demonstrated the existence of a habitat-dependent optimal clutch size; an experimental increase of the brood size provoked a decrease in the offspring condition, in terms of mean body mass and body condition, in the two forest types where the experiment was carried out (dry and humid Pyrenean oak forests), mainly because parents did not increase their feeding effort. Overall, the results of this thesis evidence that environmental heterogeneity at a fine scale can promote the genotypic and phenotypic population divergence, even in organisms with a potentially high dispersal capacity, such as birds. The different chapters presented in this thesis demonstrate how, even in a continuous and heterogeneous woodland, natural selection may favour adaptive divergence and, consequently, local adaptation for life-history traits, such as clutch size.