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Male-Biased Gene Flow Across an Avian Hybrid Zone: Evidence from Mitochondrial and Microsatellite DNA

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Male-Biased Gene Flow Across an Avian Hybrid Zone: Evidence from Mitochondrial and Microsatellite DNA Male-biased gene flow across an avian hybrid zone: evidence from mitochondrial and microsatellite DNA Helbig, AJ; Salomon, M; Bensch, Staffan; Seibold, I Published in: Journal of evolutionary biology DOI: 10.1046/j.1420-9101.2001.00273.x 2001 Link to publication Citation for published version (APA): Helbig, AJ., Salomon, M., Bensch, S., & Seibold, I. (2001). Male-biased gene flow across an avian hybrid zone: evidence from mitochondrial and microsatellite DNA. Journal of evolutionary biology, 14(2), 277-287. https://doi.org/10.1046/j.1420-9101.2001.00273.x Total number of authors: 4 General rights Unless other specific re-use rights are stated the following general rights apply: Copyright and moral rights for the publications made accessible in the public portal are retained by the authors and/or other copyright owners and it is a condition of accessing publications that users recognise and abide by the legal requirements associated with these rights. • Users may download and print one copy of any publication from the public portal for the purpose of private study or research. • You may not further distribute the material or use it for any profit-making activity or commercial gain • You may freely distribute the URL identifying the publication in the public portal Read more about Creative commons licenses: https://creativecommons.org/licenses/ Take down policy If you believe that this document breaches copyright please contact us providing details, and we will remove access to the work immediately and investigate your claim. LUND UNIVERSITY PO Box 117 221 00 Lund +46 46-222 00 00 Male-biased gene ¯ow across an avian hybrid zone: evidence from mitochondrial and microsatellite DNA A. J. HELBIG,* M. SALOMON, S. BENSCHà &I.SEIBOLD* *University of Greifswald, Vogelwarte Hiddensee, Kloster, Germany Universite de Rennes I, UFR SVE Campus de Beaulieu, Rennes, France àMolecular Population Biology Lab, Department of Animal Ecology, University of Lund, Lund, Sweden Keywords: Abstract Haldane's rule; Mating pattern and gene ¯ow were studied in the contact zone between two hybrid zone; morphologically very similar Chiffchaff taxa (Phylloscopus collybita, P. brehmii) leaf-warblers; in SW France and northern Spain. Mating was assortative in brehmii, but not microsatellites; in collybita. Mixed matings were strongly asymmetric (excess of collybita mtDNA; male ´ brehmii female pairs), but did produce viable offspring in some cases. reproductive isolation. Sequence divergence of the mitochondrial cytochrome b gene was 4.6%. Haplotypes segregated signi®cantly with phenotype (only ®ve `mismatches' among 94 individuals), demonstrating that mitochondrial gene ¯ow was very restricted. The estimated proportion of F1 hybrids in the reproductive population was signi®cantly lower than expected under a closed population model, indicating strong selection against hybrids. Genetic typing of 101 individuals at four microsatellite loci also showed signi®cant population differentiation, but nuclear gene ¯ow was estimated to be 75 times higher than mitochondrial gene ¯ow. 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. to indicate that there is a barrier to gene ¯ow. Introduction Mechanisms constituting such barriers may be pre- In the Palearctic bird fauna there are many cases of zygotic (positive assortative mating among parental contact zones, where two phenotypically similar but phenotypes) or post-zygotic (reduced ®tness in one or distinct taxa come into contact and hybridize to a both sexes of the hybrids). limited extent (Haffer, 1989, 1992; Hewitt, 1996; In interspeci®c crosses, the situation is quite frequent Martens, 1996). These hybrid zones are generally that only one sex among the hybrids is less viable, sterile interpreted as zones of secondary contact of closely or has strongly impaired fertility. Haldane (1922) poin- related taxa which diverged in geographical isolation, ted out that in such cases it is the heterogametic sex but have not reached the state of complete reproduc- which is sterile, a fact that has come to be known as tive incompatibility. Even if the frequency of hybrid- `Haldane's rule' (review: Wu et al., 1996). In organisms ization has been assessed, the extent of gene ¯ow where the heterogametic sex is the female, as in birds across such zones is generally not known, because and lepidoptera, unisexual hybrid sterility should con- hybrid viability and hybrid ®tness are dif®cult to stitute a much stronger barrier to mitochondrial than to measure in nature. The fact that phenotypes on both nuclear gene ¯ow (Sperlich, 1993). In bird taxa which sides of a hybrid zone remain distinct is generally taken differentiated (in allopatry) with respect to their mtDNA, such differentiation should be maintained in zones of secondary contact even in the face of ongoing (nuclear) Correspondence: Andreas J. Helbig, University of Greifswald, Vogelwarte gene ¯ow. This situation has indeed been well docu- Hiddensee, D-18565 Kloster, Germany. Tel.: (49)-38300±212; fax: (49)-38300±50441; mented in two geographically separate contact zones e-mail: [email protected] between the Collared Ficedula albicollis and the Pied J. EVOL. BIOL. 14 (2001) 277±287 ã 2001 BLACKWELL SCIENCE LTD 277 278 A. J. HELBIG ET AL. Flycatcher F. hypoleuca (TegelstroÈ m & Gelter, 1990; Materials and methods Gelter et al., 1992; Sñtre et al., 1997a,b; 1999). Mating between these partially sympatric species is assortative, Field investigations but they hybridize frequently on the island of Gotland (Sweden) and, more rarely, elsewhere (Haffer, 1993). The collybita ± brehmii contact zone was mapped by Male hybrids were shown to be generally fertile, M. Salomon (with help of Joel Bried) in the years although some ®tness reduction relative to males of 1981±87, 1991±92 and 1995±97 in SW France and the parental phenotypes does exist (Saetre et al., 1999). northern Spain. Within the zone of sympatry, where Female hybrids, in contrast, appeared to be sterile, as both taxa occur (Fig. 1), the composition of mated pairs none were ever found to reproduce in the wild and no was studied during the breeding season. Chiffchaffs mitochondrial gene ¯ow was detected between the two usually form socially monogamous pairs and both sexes taxa. are strongly territorial at the height of the nesting In the present paper we examine the extent of season. Territories were located by listening for the interbreeding and gene ¯ow across another avian hybrid typical song. Males were then lured into mist nets by zone, that between two Chiffchaff taxa of the species-rich song playback from a recorder placed underneath the leaf±warbler genus Phylloscopus (Sylviidae). Based on net. Each individual was ringed and a blood sample was previous studies (Helbig et al., 1996; Salomon et al., taken from the ulnar vein (years 1991±92,1995 only). 1997) we regard the common Chiffchaff P. [c.] collybita Females did not respond as well to song playback, but and the Iberian Chiffchaff P. [c.] brehmii as members of were usually easy to identify as they ¯ew around the the superspecies Phylloscopus [collybita], which includes singing male giving their taxon-speci®c contact calls further allospecies on the Canary Islands (canariensis), in (see sonogram in Salomon, 1987). Females calling in the Caucasus and Himalayas (sindianus) and in Siberia close proximity to a territorial male were assumed to be (tristis). P. collybita and P. brehmii form a narrow zone of paired to that male. In almost all cases, only a single contact and local sympatry in extreme SW France and female was noticed on any given territory. Some pairs northern Spain. They differ mostly in vocalizations, both were observed when feeding nestlings, when both territorial songs and calls, which allow unambiguous partners frequently uttered their diagnostic contact ®eld identi®cation of pure phenotypes of either sex. calls. Morphologically the two forms are very similar, although Some males utter a song containing elements of the males in the contact zone can be distinguished in the typical songs of both taxa. These are called `mixed- hand by a combination of three measurements (Salomon singers'. The phenomenon is well known among closely et al., 1997). In areas where both occur, collybita and related passerine bird species (Helb et al., 1985; Sorjonen, brehmii males are interspeci®cally territorial. Mixed pairs 1986). In general, song development in oscine passerines have been noted in the past, but the composition of pairs involves a prominent learning component (Catchpole & in the contact zone has only been studied based on small Slater, 1995). Mixed singers may be hybrids, or they may sample sizes (Salomon, 1987). Mitochondrial DNA have acquired their song by partially copying a hetero- sequences (cytochrome b gene) between the two forms speci®c tutor. Chiffchaffs in the ®eld were classi®ed into differed by 4.6%, and a limited sample from the contact one of three acoustic phenotypes: collybita, brehmii or zone (21 brehmii,19collybita) did not reveal any mixing mixed singer. Classi®cation of males was usually based of haplotypes between the taxa (Helbig et al., 1993, on territorial song. Both sexes could also be identi®ed by 1996). their contact calls. Male and female `mixed singers' give We here examine the extent of gene ¯ow between distinct calls different from either pure phenotype (son- collybita and brehmii based on three sources of informa- ograms see Salomon, 1987; 1989). Although female tion: (1) the composition of breeding pairs in a large part chiffchaffs do not sing, we use the term `mixed singers' of the contact zone based on ®eld observations over also for females in order to have a uniform label for birds several years; (2) the extent of congruence between of both sexes producing mixed vocalizations. In this way phenotype (determined acoustically) and mitochondrial we determined the composition of a total of 260 mated haplotype in a large sample of individuals; and (3) the pairs spread over approximately 2000 km2 in the area of degree of nuclear genetic differentiation using microsat- sympatry.
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