Hybridization but No Evidence for Backcrossing and Introgression in a Sympatric Population of Great Reed Warblers and Clamorous Reed Warblers

Hybridization is observed frequently in birds, but often it is not known whether the hybrids are fertile and if backcrossing occurs. The breeding ranges of the great reed warbler (Acrocephalus arundinaceus) and the clamorous reed warbler (A. stentoreus) overlap in southern Kazakhstan and a previous study has documented hybridization in a sympatric population. In the present study, we first present a large set of novel microsatellite loci isolated and characterised in great reed warblers. Secondly, we evaluate whether hybridization in the sympatric breeding population has been followed by backcrossing and introgression. We isolated 181 unique microsatellite loci in great reed warblers. Of 41 loci evaluated, 40 amplified and 30 were polymorphic. Bayesian clustering analyses based on genotype data from 23 autosomal loci recognised two well-defined genetic clusters corresponding to the two species. Individuals clustered to a very high extent to either of these clusters (admixture proportions ≥0.984) with the exception of four previously suggested arundinaceus–stentoreus hybrid birds that showed mixed ancestry (admixture proportions 0.495–0.619). Analyses of simulated hybrids and backcrossed individuals showed that the sampled birds do not correspond to first–fourth-generation backcrosses, and that fifth or higher generation backcrosses to a high extent resemble ‘pure’ birds at this set of markers. We conclude that these novel microsatellite loci provide a useful molecular resource for Acrocephalus warblers. The time to reach reproductive isolation is believed to be very long in birds, approximately 5 Myrs, and with an estimated divergence time of 2 Myrs between these warblers, some backcrossing and introgression could have been expected. However, there was no evidence for backcrossing and introgression suggesting that hybrids are either infertile or their progeny inviable. Very low levels of introgression cannot be excluded, which still may be an important factor as a source of new genetic variation.

[1]  Albert J. Vilella,et al.  The genome of a songbird , 2010, Nature.

[2]  M. M. Hansen,et al.  Admixture analysis of stocked brown trout populations using mapped microsatellite DNA markers: indigenous trout persist in introgressed populations , 2009, Biology Letters.

[3]  L. Excoffier,et al.  Gene flow and species delimitation. , 2009, Trends in ecology & evolution.

[4]  M. Vera,et al.  Efficiency of markers and methods for detecting hybrids and introgression in stocked populations , 2009, Conservation Genetics.

[5]  N. Mundy,et al.  An analysis of population genetic differentiation and genotype–phenotype association across the hybrid zone of carrion and hooded crows using microsatellites and MC1R , 2009, Molecular ecology.

[6]  L. Excoffier,et al.  The Hidden Side of Invasions: Massive Introgression by Local Genes , 2008, Evolution; international journal of organic evolution.

[7]  M. Kronforst Gene flow persists millions of years after speciation in Heliconius butterflies , 2008, BMC Evolutionary Biology.

[8]  E. Nielsen,et al.  hybridlab (version 1.0): a program for generating simulated hybrids from population samples , 2006 .

[9]  B. Faivre,et al.  Spreading introgression in the wake of a moving contact zone , 2006, Molecular ecology.

[10]  Urban Olsson,et al.  Phylogeny and classification of the avian superfamily Sylvioidea. , 2006, Molecular phylogenetics and evolution.

[11]  C. Primmer,et al.  Efficiency of model‐based Bayesian methods for detecting hybrid individuals under different hybridization scenarios and with different numbers of loci , 2005, Molecular ecology.

[12]  J. Mallet Hybridization as an invasion of the genome. , 2005, Trends in ecology & evolution.

[13]  C. Oosterhout,et al.  Micro-Checker: Software for identifying and correcting genotyping errors in microsatellite data , 2004 .

[14]  B. Grant,et al.  CONVERGENT EVOLUTION OF DARWIN'S FINCHES CAUSED BY INTROGRESSIVE HYBRIDIZATION AND SELECTION , 2004, Evolution; international journal of organic evolution.

[15]  B. Hansson,et al.  Molecular evidence of a reed warbler × great reed warbler hybrid (Acrocephalus scirpaceus × A. arundinaceus) in Belgium , 2004, Journal of Ornithology.

[16]  E. Taylor,et al.  Evidence for bimodal hybrid zones between two species of char (Pisces: Salvelinus) in northwestern North America , 2003, Journal of evolutionary biology.

[17]  B. Hansson,et al.  Hybridisation between great reed warblers Acrocephalus arundinaceus and clamorous reed warblers A. stentoreus: morphological and molecular evidence. , 2003 .

[18]  A. Helbig,et al.  Amplified fragment length polymorphism analysis identifies hybrids between two subspecies of warblers , 2002, Molecular ecology.

[19]  C. Randler Avian hybridization, mixed pairing and female choice , 2002, Animal Behaviour.

[20]  L. Gustafsson,et al.  Hybridization and adaptive mate choice in flycatchers , 2001, Nature.

[21]  M W Bruford,et al.  Genetic diversity and introgression in the Scottish wildcat , 2001, Molecular ecology.

[22]  J. Sambrook,et al.  Molecular Cloning: A Laboratory Manual , 2001 .

[23]  P. Salgueiro,et al.  Fifty Seychelles warbler (Acrocephalus sechellensis) microsatellite loci polymorphic in Sylviidae species and their cross‐species amplification in other passerine birds , 2000, Molecular ecology.

[24]  J. Mallet,et al.  Bimodal hybrid zones and speciation. , 2000, Trends in ecology & evolution.

[25]  P. Donnelly,et al.  Inference of population structure using multilocus genotype data. , 2000, Genetics.

[26]  P. Wirtz Mother species–father species: unidirectional hybridization in animals with female choice , 1999, Animal Behaviour.

[27]  H. Ellegren,et al.  A simple and universal method for molecular sexing of non-ratite birds , 1999 .

[28]  A. Helbig,et al.  Molecular phylogeny of Palearctic-African Acrocephalus and Hippolais Warblers (Aves: Sylviidae). , 1999, Molecular phylogenetics and evolution.

[29]  Dennis Hasselquist,et al.  POLYGYNY IN GREAT REED WARBLERS: A LONG-TERM STUDY OF FACTORS CONTRIBUTING TO MALE FITNESS , 1998 .

[30]  T. Dowling,et al.  The role of hybridization and introgression in the diversification of animals , 1997 .

[31]  Loren H. Rieseberg,et al.  Hybrid Origins of Plant Species , 1997 .

[32]  B. Grant,et al.  High Survival of Darwin's Finch Hybrids: Effects of Beak Morphology and Diets , 1996 .

[33]  L. Rieseberg,et al.  Hybridization in the Catalina Island Mountain Mahogany (Cercocarpus traskiae): RAPD Evidence , 1995 .

[34]  A. Jeffreys,et al.  Isolation of human simple repeat loci by hybridization selection. , 1994, Human molecular genetics.

[35]  B. Grant,et al.  Hybridization of Bird Species , 1992, Science.

[36]  E. Mayr Handbook of the Birds of Europe, the Middle East and North Africa: The Birds of the Western Palearctic. Volume 1: Ostrich to Ducks. Stanley Cramp , 1978 .

[37]  W. Hollander,et al.  Introgressive Hybridization , 1949, The Yale Journal of Biology and Medicine.

[38]  T. Price Speciation in birds , 2008 .

[39]  J. Mallet Hybrid speciation , 2007, Nature.

[40]  T. Glenn,et al.  Isolating microsatellite DNA loci. , 2005, Methods in enzymology.

[41]  M. Wink,et al.  Ein Drossel- x Teichrohrsänger-HybrideAcrocephalus arundinaceus xA. scirpaceus und der Nachweis seiner Elternschaft , 2005, Journal für Ornithologie.

[42]  G. Barrowclough,et al.  GENETIC AND PHENOTYPIC DIFFERENTIATION IN A WOOD WARBLER (GENUS DENDROICA) HYBRID ZONE , 2003 .

[43]  J. Goudet FSTAT, a program to estimate and test gene diversities and fixation indices (version 2.9.3). Updated from Goudet (1995) , 2001 .

[44]  S Rozen,et al.  Primer3 on the WWW for general users and for biologist programmers. , 2000, Methods in molecular biology.

[45]  N. Mundy,et al.  Tandem repeats and heteroplasmy in the mitochondrial DNA control region of the loggerhead shrike (Lanius ludovicianus). , 1996, The Journal of heredity.

[46]  F. Lemaire Mixed Song, Interspecific Competition and Hybridisation in the Reed and Marsh Warblers (Acrocephalus Scirpaceus and Palustris) , 1977 .