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

Monica Guerrini,Alan Crabtree,Clizia Gennai,Dimitri Giunchi,Panicos Panayides,Iñigo Zuberogoitia,Paolo M Politi,Filippo Barbanera,Alex S Copland,Olga Babushkina,Valerio Ketmaier

doi:10.1371/journal.pone.0098574

Monica Guerrini, Alan Crabtree + Show 9 more

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https://doi.org/10.1371/journal.pone.0098574

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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.

Highlights

Distribution, dynamics and genetic structure of natural populations can be severely affected by dispersal [1,2,3], i.e. the movement of an organism from its birthplace to its first breeding site or from one breeding site to another [4,5]
Sexing The Chromo Helicase DNA (CHD) gene was amplified in all barn swallows: 92 birds were identified as males while 94 as females
There are a few studies focusing on migratory bird species and relying on the use of molecular DNA markers

Summary

Introduction

Distribution, dynamics and genetic structure of natural populations can be severely affected by dispersal [1,2,3], i.e. the movement of an organism from its birthplace to its first breeding site (natal dispersal) or from one breeding site to another (breeding dispersal) [4,5]. Dispersal may be significantly different between sexes, as has been well documented in birds and mammals [3,4,6]. The costs/benefits of such asymmetry usually depend on the life history and the mating system of a given species [7]. Dispersal tends to be female-biased in birds and male-biased in mammals [4,8,9]. Given that dispersal can significantly affect gene flow among populations [10], the dispersing sex may appear as genetically less structured. Accounting for sex is fundamental to find out potential differences in dispersal [10,11] and to reliably infer the genetic structure of populations, as the latter could be driven mainly by the philopatric sex [12]

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