Male-biased gene flow across an avian hybrid zone: evidence from mitochondrial and microsatellite DNA

Abstract

Mating pattern and gene flow were studied in the contact zone between two morphologically very similar Chiffchaff taxa (Phylloscopus collybita, P. brehmii) in SW France and northern Spain. Mating was assortative in brehmii, but not in collybita. Mixed matings were strongly asymmetric (excess of collybita male × brehmii female pairs), but did produce viable offspring in some cases. Sequence divergence of the mitochondrial cytochrome b gene was 4.6%. Haplotypes segregated significantly with phenotype (only five ‘mismatches’ among 94 individuals), demonstrating that mitochondrial gene flow was very restricted. The estimated proportion of F1 hybrids in the reproductive population was significantly lower than expected under a closed population model, indicating strong selection against hybrids. Genetic typing of 101 individuals at four microsatellite loci also showed significant population differentiation, but nuclear gene flow was estimated to be 75 times higher than mitochondrial gene flow. This strong discrepancy is probably due to unisexual hybrid sterility (Haldane’s rule). Thus, there is a strong, but incomplete, reproductive barrier between these taxa.

When east meets west: population structure of a high-latitude resident species, the boreal chickadee (Poecile hudsonicus)

“…Several species show evidence of sex-biased dispersal Milot et al, 2000;Helbig et al, 2001;Austin et al, 2003;Bensch et al, 2006), including the yellow warbler which, while a long distance migrant, showed similar patterns of population differentiation, at comparable sampling sites, to the boreal chickadee Milot et al, 2000). Yellow warbler populations also showed higher levels of population differentiation at mtDNA genes than microsatellite loci.…”

Are Iberian ChiffchaffsPhylloscopus (collybita) brehmiilong-distance migrants? An analysis of flight-related morphology

“…This type of selection against hybrids has been suggested to be involved in the maintenance of morphological differences at either side of a migratory divide in Willow Warblers despite existing gene flow (Bensch et al 1999). Among leaf warblers, song divergence seems to be the major pre-reproductive isolating mechanism (Helbig et al 2001, Irwin et al 2001. However, song differences are not sufficient for brehmii and collybita to remain isolated, as they are unable to completely discriminate each other by song alone (Helbig et al 2001, Bensch et al 2002.…”

“…Among leaf warblers, song divergence seems to be the major pre-reproductive isolating mechanism (Helbig et al 2001, Irwin et al 2001. However, song differences are not sufficient for brehmii and collybita to remain isolated, as they are unable to completely discriminate each other by song alone (Helbig et al 2001, Bensch et al 2002. The high frequency of hybrids between brehmii and collybita in the contact zone suggests that post-reproductive isolating mechanisms are important, and our results support the idea that migratory divergence might contribute to the maintenance of the divide at the Pyrenees, despite considerable genetic interchange.…”

“…These two forms differ at the molecular level (4.6% divergence in the cytochrome b gene), and also have a different song (Helbig et al 1996). Remarkably, these differences have persisted over time despite noticeable gene flow, as shown by microsatellite analyses and direct identification of hybrids (Helbig et al 2001, Bensch et al 2002.…”

Haldane's rule in the 21st century

“…Studies include work on taxa with male heterogamety, where maternally inherited loci are seen to introgress further than autosomal and paternally inherited loci (for example, in the Mus musculus-M. domesticus hybrid zone, mitochondrial DNA introgresses to a greater degree than autosomal loci (Raufaste et al, 2005)), as well as taxa with female heterogamety (where biparentally inherited loci are seen to introgress deeper than maternally inherited ones; Jiggins et al, 1997;Helbig et al, 2001;Cianchi et al, 2003;Kronforst et al, 2006). As a particularly comprehensive example, Carling and Brumfield (2008) studied cline width in a (female-heterogametic) avian hybrid zone and found that Z-linked and mitochondrial genes introgressed less deeply than autosomal markers, which is consistent with HR.…”