BRANTA — Carlos Camacho Olmedo
Fine-scale population differentiation: ecological and evolutionary mechanisms involved
Institution: University of Seville
Supervisors: Jaime Potti
Details: PhD, 2018
Subject Keywords: Additive genetic variance, competition, demography, dispersal, habitat preferences, local adaptation, long-term trends, matching habitat choice, microevolution, microsatellites, morphological differentiation, natural selection, phenotypic divergence, population structure, tarsus length
Species Keywords: Pied Flycatcher, Ficedula hypoleuca
Dispersal and gene flow have traditionally been thought to counteract the effects of divergent selection and thus prevent evolutionary differentiation. However, recent research suggests that, if non-random, dispersal may promote population differentiation even at microgeographic scales. Examples of the eco-evolutionary consequences of non-random dispersal are still very scarce in the literature, possibly because long-term data from continuously monitored populations of marked individuals are needed. I document the effect of phenotype-dependent dispersal with respect to body size (tarsus length) on the evolutionary dynamics of a wild population of pied flycatchers (Ficedula hypoleuca) between 1988 and 2016. I characterized the natal dispersal patterns and phenotypic trajectories of dispersers and philopatric individuals originating from ecologically distinct (coniferous vs. deciduous), adjacent (1 km) habitats, and investigated the genetic architecture of, and patterns of selection on, tarsus length.
Pied flycatchers breeding in the oak and the pine forest showed strong divergence in tarsus length during the colonization phase of the pinewood, despite geographic proximity and extensive dispersal (ca. 25% of each cohort change habitats). However, the initial degree of differentiation was not sustained over the 29-year period. Differential dynamics of phenotype-dependent dispersal between habitats seem to be the key force shaping the phenotypic trajectories of the study populations. Males moving from the pine to the oak forest tended to be smaller over time, whereas those that remained in the pine forest tended to be larger. Dispersers from the oak to the pine forest also tended to be larger over time, and thus the positive trend of philopatric birds was furthermore reinforced. No clear evidence of phenotype-dependent dispersal was found in females but, importantly, an analysis of both sexes combined confirmed the patterns observed for males alone.
Temporal changes in breeding density and the level of nest-site competition could have provided the ecological mechanism for the habitat segregation of size classes. Breeding density increased in both habitats following nest-box addition. Nevertheless, due to the lack of natural cavities, nest-site competition –and therefore the relevance of body size in territorial contests– was probably magnified in the pinewood. Based on density and dispersal rates dynamics, it seems that the pine forest became progressively more attractive for pied flycatchers at the expense of a decrease in the attractiveness of the oakwood. Because large-dominant and small-subordinate males are generally sorted into preferred and non-preferred habitats, the steep increase in breeding density in the pinewood resulted in a shift in the patterns of phenotype-dependent dispersal. No evidence of adaptive habitat choice in relation to body size was found in this population possibly because, as demonstrated here, most pied flycatchers, regardless of their phenotype, return to the habitat they imprinted on as fledglings.
Quantitative genetic analyses revealed a substantial component of additive genetic variance underlying tarsus length, although there were substantial differences among pools of dispersers and philopatric birds. Specifically, individuals genetically predisposed to be larger preferentially dispersed into the oak forest. However, selection gradients on this group, unlike the other groups, were negative and, therefore, resulted in a negative response to selection. Dispersers to the oak forest actually showed a decline in tarsus length over time that, nevertheless, deviated from the lack of trend observed in the entire oak population. No such discrepancy was found in the pine forest, indicating a greater genetic contribution of dispersers to the pine forest in shaping the distribution of phenotypes within their recipient population. Examination of the breeding success of each group suggested that this unusual asymmetry resulted from uncoupled patterns of dispersal and gene flow in the oak forest, since the reproductive output of immigrants into the oakwood was lower than that of the other groups.
Overall, these results indicate that the effect of dispersal on microevolutionary processes may vary from being positive to non-existent depending on the habitat type, although the ecological factors responsible for such discrepancy remain to be elucidated. Collectively, the five chapters presented in this thesis represent a major step forward in our understanding of the specific role of gene flow on eco-evolutionary dynamics and phenotypic evolution.
Camacho, C., Canal, D. & Potti, J. 2016. Natal habitat imprinting counteracts the diversifying effects of phenotype-dependent dispersal in a spatially structured population. BMC Evolutionary Biology, 16:158.
Camacho, C., Canal, D. & Potti, J. 2015. Testing the matching habitat choice hypothesis in nature: phenotype−environment correlation and fitness in a songbird population. Evolutionary Ecology, 29: 873−886.
Camacho, C., Canal, D. & Potti, J. 2013. Non−random dispersal drives phenotypic divergence within a bird population. Ecology and Evolution, 3: 4841−4848.