Large-scale patterns of genetic variation in a female-biased dispersing passerine: the importance of sex-based analyses

Abstract

Dispersal affects the distribution, dynamics and genetic structure of natural populations, and can be significantly different between sexes. However, literature records dealing with the dispersal of migratory birds are scarce, as migratory behaviour can notably complicate the study of dispersal. We used the barn swallow Hirundo rustica as model taxon to investigate patterns of genetic variability in males and in females of a migratory species showing sex-biased dispersal. We collected blood samples (n = 186) over the period 2006 to 2011 from adults (H. r. rustica subspecies) nesting in the same breeding site at either high (Ireland, Germany and Russia) or low (Spain, Italy and Cyprus) latitude across Europe. We amplified the Chromo Helicase DNA gene in all birds in order to warrant a sex-balanced sample size (92 males, 94 females). We investigated both uniparental (mitochondrial ND2 gene) and biparental (microsatellite DNA: 10 loci) genetic systems. The mtDNA provided evidence for demographic expansion yet no significant partition of the genetic variability was disclosed. Nevertheless, a comparatively distant Russian population investigated in another study, whose sequences were included in the present dataset, significantly diverged from all other ones. Different to previous studies, microsatellites highlighted remarkable genetic structure among the studied populations, and pointed to the occurrence of differences between male and female barn swallows. We produced evidence for non-random patterns of gene flow among barn swallow populations probably mediated by female natal dispersal, and we found significant variability in the philopatry of males of different populations. Our data emphasize the importance of taking into account the sex of sampled individuals in order to obtain reliable inferences on species characterized by different patterns of dispersal between males and females.

Figure 1. Barn swallow breeding populations sampled in this study.

(1): SPA, Spain; (2): IRE, Ireland; (3): ITA, Italy; (4): GER, Germany; (5): CYP, Cyprus; (6): RUS, Russia. Mitochondrial DNA sequences available in the GenBank were obtained from Russian populations of Krasnodar (7, KRD) and Medvedevo (8, MED) (Table S1).

Figure 2. Median-Joining network of barn swallow populations computed on mtDNA haplotypes with network.

Size of circles is proportional to the haplotype frequency. The colour of each population is indicated as well as the number of each haplotype. A length bar to compute the number of mutational changes was provided (see also Table S1). The inset showed Mismatch Distribution (MD) of the mtDNA pairwise differences (observed: dotted; expected: line) computed on the whole dataset (n = 76). The expected curve was obtained from simulated values computed from the data under the model of demographic expansion (H₀). The Harpending's raggedness index (r) was given with the P value of the SSD test as well as Tajima's D, Fu's F _S and R ₂ statistics.

Figure 3. The Principal Component Analysis performed using the average pairwise F _ST distance values among STR genotypes.

The percentage of total variance explained by each of the first two components is given. (A) All individuals. (B) Only males. (C) Only females.

Figure 4. Bayesian admixture analysis as inferred using structure.

The ΔK calculated according to Evanno et al. was optimal for K = 2 in all computations. Each population was represented by a pie chart whose segments were proportional to the number of specimens assigned to cluster I (black), to cluster II (white) or which showed admixed genotypes (grey). Threshold value for assignment to each cluster was Q_i = 0.80 (Table S4). (A) All individuals. (B) Only males. (C) Only females.