Gene flow through dispersal has traditionally been thought to function as a force opposing evolutionary differentiation. However, directional gene flow may actually reinforce divergence of populations in close proximity. This study documents the phenotypic differentiation over more than two decades in body size (tarsus length) at a very short spatial scale (1.1 km) within a population of pied flycatchers Ficedula hypoleuca inhabiting deciduous and coniferous habitats. Unlike females, males breeding in the deciduous forest were consistently larger than those from the managed coniferous forest. This assortment by size is likely explained by preset habitat preferences leading to dominance of the largest males and exclusion of the smallest ones toward the nonpreferred coniferous forest coupled with directional dispersal. Movements of males between forests were nonrandom with respect to body size and flow rate, which might function to maintain the phenotypic variation in this heritable trait at such a small spatial scale. However, a deeply rooted preference for the deciduous habitat might not be in line with its quality due to the increased levels of breeding density of hole-nesting competitors therein. These results illustrate how eco-evolutionary scenarios can develop under directional gene flow over surprisingly small spatial scales. Our findings come on top of recent studies concerning new ways in which dispersal and gene flow can influence microevolution.
The genetic correlation between the sexes in the expression of secondary sex traits in wild vertebrate populations has attracted very few previous empirical efforts of field researchers. In southern European populations of pied flycatchers, a sexually selected male ornament is also expressed by a proportion of females. Additive genetic variances in ornament size and expression, transmission mechanisms (autosomal vs Z-linkage) and maternal effects are examined by looking at patterns of familial resemblance across three generations. Size of the secondary sex trait has a genetic basis common to both sexes, with estimated heritability being 0.5 under an autosomal model of inheritance. Significant additive genetic variance in males was also confirmed through a crossfostering experiment. Heritability analyses were only partially consistent with previous molecular genetics evidence, as only two out of the three predictions supported Z-linkage and lack of significant mother-daughter resemblance could be due to small sample sizes caused by limited female trait expression. Therefore, the evidence was mixed as to the contribution of the Z chromosome and autosomal genes to trait size. The threshold heritability of trait expression in females was lower, around 0.3, supporting autosomal-based trait expression in females. Environmental (birth date) and parental effects on ornament size mediated by the mother's condition after accounting for maternal and paternal genetic influences are also highlighted. The genetic correlation between the sexes did not differ from one, indicating that selection on the character on either sex entails a correlated response in the opposite sex.
Extra-pair paternity has the potential to increase male reproductive success and in turn the potential for sexual selection to act on male traits predicting extra pair mate success. There is large variation among European populations of pied flycatchers (Ficedula hypoleuca) in the extent to which male traits predict success in extra pair mating behaviour. In an Iberian population with a relatively high proportion of extra-pair young multiple male traits were involved in extra pair paternity success. Cuckolder males had larger tarsi and more attractive sex ornaments (blacker dorsal plumage and larger forehead patches) than the individuals they cuckolded, results not replicated in other populations. Previous studies in the species have shown that all traits associated with achieving success in extra pair paternity in our population are heritable and likely reliable indicators of male quality. Siring additional young was an advantageous strategy for males as it did not imply loss of paternity in their own nests. Our results, thus, suggest that this behaviour may enhance the evolution of male traits associated to success in extra-pair paternity in this population.
Ornaments displayed by females have often been denied evolutionary interest due to their frequently reduced expression relative to males, habitually attributed to a genetic correlation between the sexes. We estimated annual and lifetime reproductive success of female pied flycatchers (Ficedula hypoleuca) and applied capture-mark-recapture models to analyse annual survival rates in relation to the patterns of expression (absence/presence) of an ornament displayed by all males and a fraction of females. Overall, the likelihood of expressing the ornament increased nonlinearly with female age and was due to within-individual variation, not to the selective appearance or disappearance of ornament-related expression of phenotypes in the population. Accordingly, expressing the forehead patch in a given year did not influence survival probability. However, those females expressing the ornament at early ages (1-2 years old) enjoyed survival advantages throughout lifetime. Although ornamented females had higher lifetime fecundity and fledging success, their yearly reproductive performance, in terms of fledging productivity, decreased as they aged so that, late in life, ornamented females reared fewer offspring than nonexpressing females of the same age. In addition, both strategies (expressing vs. not expressing the trait) returned similar fitness payoffs in terms of recruited offspring. Our results support the hypothesis that fecundity and survival selection are involved in the displaying of this 'male' ornament by females.
The matching habitat choice hypothesis holds that individuals with different phenotypes actively select the habitats to which they are best adapted, hence maximizing fitness. Despite the potential implications of matching habitat choice for many ecological and evolutionary processes, very few studies have tested its predictions. Here, we use a 26year dataset on a spatially structured population of pied flycatchers (Ficedula hypoleuca) to test whether phenotype-dependent dispersal and habitat selection translate into increased fitness, as measured by recruitment success. In our study system, males at the extremes of the body size range segregate into deciduous and coniferous forests through nonrandom dispersal. According to the matching habitat choice hypothesis, fitness of large-sized males is expected to be higher in the deciduous habitat, where they preferentially settle to breed, while the reverse would be true for small-sized males, which are more frequent in the coniferous forest. Our results showed that recruitment success in the coniferous forest increased non-linearly with body size, with males at the middle of the size range having higher fitness than both large and small-sized males. However, no clear trend was observed in the deciduous forest where males of either size had similar fitness. After empirically discarding other important processes potentially confounding matching habitat choice, as genotype-and body condition-dependent dispersal, competitive exclusion remains the most likely force shaping the nonrandom distribution of male pied flycatchers. A conclusive demonstration of the operation and occurrence of matching habitat choice in nature remains therefore to be done.
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