David Canal

Heritability and genetic correlation between the sexes in a songbird sexual ornament

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 cross-fostering 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 mothers 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.

Lifetime fitness and age-related female ornament signalling: evidence for survival and fecundity selection in the pied flycatcher.

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.

Multiple mating opportunities boost protandry in a pied flycatcher population

Protandry, the earlier arrival of males than females to breeding areas, is widespread in birds, but its underlying mechanisms are far from well understood. The two, not mutually exclusive most highly supported hypotheses to explain avian protandry postulate that it has evolved from intrasexual male competition to acquire the best territories (“rank advantage” hypothesis) and/or to maximize the number of mates (“mate opportunity” hypothesis). We studied for two consecutive years the relative importance of both hypotheses in a population of pied flycatchers (Ficedula hypoleuca), a territorial songbird with a mixed mating strategy. We measured territory quality using a long-term dataset on nest occupation and breeding output, and we used molecular techniques to assess male fitness across the range of social and genetic mating options. Territory quality was unrelated to breeding date and had no influence on extra-pair paternity or social polygynous events. However, males breeding early increased their chances of becoming socially polygynous and/or of attaining extra-pair paternity and, as a consequence, increased their total reproductive success. These results support the “mate opportunity” hypothesis, suggesting that sexual selection is the main mechanism driving protandry in this population.

Male phenotype predicts extra-pair paternity in pied flycatchers

Consejeria de Medio Ambiente, Comunidad de Madrid and Delegacion de Medio Ambiente, Junta de Castilla-La Mancha gave us working permissions. This work was supported by projects PAC05-006-2 (to J.A.D.) and CGL2006-07481/BOS (to J.C. Senar). D.C. was supported by a grant from the Ministerio de Educacion y Ciencia (I3P-BDP2005).

Towards the simplification of MHC typing protocols: targeting classical MHC class II genes in a passerine, the pied flycatcher Ficedula hypoleuca

BackgroundMajor Histocompatibility Complex (MHC) has drawn the attention of evolutionary biologists due to its importance in crucial biological processes, such as sexual selection and immune response in jawed vertebrates. However, the characterization of classical MHC genes subjected to the effects of natural selection still remains elusive in many vertebrate groups. Here, we have tested the suitability of flanking intron sequences to guide the selective exploration of classical MHC genes driving the co-evolutionary dynamics between pathogens and their passerine (Aves, Order Passeriformes) hosts.FindingsIntronic sequences flanking the usually polymorphic exon 2 were isolated from different species using primers sitting on conserved coding regions of MHC class II genes (β chain). Taking the pied flycatcher Ficedula hypoleuca as an example, we demonstrate that careful primer design can evade non-classical MHC gene and pseudogene amplification. At least four polymorphic and expressed loci were co-replicated using a single pair of primers in five non-related individuals (N = 28 alleles). The cross-amplification and preliminary inspection of similar MHC fragments in eight unrelated songbird taxa suggests that similar approaches can also be applied to other species.ConclusionsIntron sequences flanking the usually polymorphic exon 2 may assist the specific investigation of classical MHC class II B genes in species characterized by extensive gene duplication and pseudogenization. Importantly, the evasion of non-classical MHC genes with a more specific function and non-functional pseudogenes may accelerate data collection and diminish lab costs. Comprehensive knowledge of gene structure, polymorphism and expression profiles may be useful not only for the selective examination of evolutionarily relevant genes but also to restrict chimera formation by minimizing the number of co-amplifying loci.

Nonrandom dispersal drives phenotypic divergence within a bird population

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.

Differentiation in neutral genes and a candidate gene in the pied flycatcher: Using biological archives to track global climate change

Global climate change is one of the major driving forces for adaptive shifts in migration and breeding phenology and possibly impacts demographic changes if a species fails to adapt sufficiently. In Western Europe, pied flycatchers (Ficedula hypoleuca) have insufficiently adapted their breeding phenology to the ongoing advance of food peaks within their breeding area and consequently suffered local population declines. We address the question whether this population decline led to a loss of genetic variation, using two neutral marker sets (mitochondrial control region and microsatellites), and one potentially selectively non-neutral marker (avian Clock gene). We report temporal changes in genetic diversity in extant populations and biological archives over more than a century, using samples from sites differing in the extent of climate change. Comparing genetic differentiation over this period revealed that only the recent Dutch population, which underwent population declines, showed slightly lower genetic variation than the historic Dutch population. As that loss of variation was only moderate and not observed in all markers, current gene flow across Western and Central European populations might have compensated local loss of variation over the last decades. A comparison of genetic differentiation in neutral loci versus the Clock gene locus provided evidence for stabilizing selection. Furthermore, in all genetic markers, we found a greater genetic differentiation in space than in time. This pattern suggests that local adaptation or historic processes might have a stronger effect on the population structure and genetic variation in the pied flycatcher than recent global climate changes.

Testing the matching habitat choice hypothesis in nature: phenotype-environment correlation and fitness in a songbird population

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 26-year 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.

Exploring heterozygosity-survival correlations in a wild songbird population: contrasting effects between juvenile and adult stages.

The relationship between genetic diversity and fitness, a major issue in evolutionary and conservation biology, is expected to be stronger in traits affected by many loci and those directly influencing fitness. Here we explore the influence of heterozygosity measured at 15 neutral markers on individual survival, one of the most important parameters determining individual fitness. We followed individual survival up to recruitment and during subsequent adult life of 863 fledgling pied flycatchers born in two consecutive breeding seasons. Mark-recapture analyses showed that individual heterozygosity did not influence juvenile or adult survival. In contrast, the genetic relatedness of parents was negatively associated with the offspring’s survival during the adult life, but this effect was not apparent in the juvenile (from fledgling to recruitment) stage. Stochastic factors experienced during the first year of life in this long-distance migratory species may have swamped a relationship between heterozygosity and survival up to recruitment.

North African hybrid sparrows (Passer domesticus, P. hispaniolensis) back from oblivion – ecological segregation and asymmetric mitochondrial introgression between parental species

Abstract A stabilized hybrid form of the house sparrow (Passer domesticus) and the Spanish sparrow (P. hispaniolensis) is known as Passer italiae from the Italian Peninsula and a few Mediterranean islands. The growing attention for the Italian hybrid sparrow and increasing knowledge on its biology and genetic constitution greatly contrast the complete lack of knowledge of the long‐known phenotypical hybrid sparrow populations from North Africa. Our study provides new data on the breeding biology and variation of mitochondrial DNA in three Algerian populations of house sparrows, Spanish sparrows, and phenotypical hybrids. In two field seasons, the two species occupied different breeding habitats: Spanish sparrows were only found in rural areas outside the cities and bred in open‐cup nests built in large jujube bushes. In contrast, house sparrows bred only in the town centers and occupied nesting holes in walls of buildings. Phenotypical hybrids were always associated with house sparrow populations. House sparrows and phenotypical hybrids started breeding mid of March, and most pairs had three successive clutches, whereas Spanish sparrows started breeding almost one month later and had only two successive clutches. Mitochondrial introgression is strongly asymmetric because about 75% of the rural Spanish sparrow population carried house sparrow haplotypes. In contrast, populations of the Italian hybrid form, P. italiae, were genetically least diverse among all study populations and showed a near‐fixation of house sparrow haplotypes that elsewhere were extremely rare or that were even unique for the Italian Peninsula. Such differences between mitochondrial gene pools of Italian and North African hybrid sparrow populations provide first evidence that different demographic histories have shaped the extant genetic diversity observed on both continents.