Asymmetric song recognition does not influence gene flow in an emergent songbird hybrid zone

ABSTRACT Hybrid zones can be used to examine the mechanisms, like song recognition, that affect reproductive isolation and speciation. Song has mixed support as a driver of speciation; we did not find song to be associated with reproductive isolation in White-crowned Sparrow subspecies (Zonotrichia leucophrys pugetensis and Z. l. gambelii). We examined an emerging secondary contact zone in these subspecies by measuring song variation, song recognition, plumage, morphology, and mitochondrial DNA (mtDNA). Plumage and morphological characters provided evidence of hybridization in the contact zone, with some birds possessing intermediate phenotype and song characteristics, and some possessing discordant phenotype and mitochondrial haplotype. Playback experiments revealed asymmetric song recognition: male pugetensis displayed greater response to their own song than gambelii song, whereas gambelii did not discriminate significantly. If female choice operates similarly to male song discrimination, we predicted asymmetric gene flow, resulting in a greater number of hybrids with gambelii mtDNA. Contrary to our prediction, more gambelii and putative hybrids in the contact zone possessed pugetensis mtDNA haplotypes, possibly due to greater pugetensis abundance and female-biased dispersal. LAY SUMMARY Hybrid zones, or boundaries where closely related populations or species interbreed, provide an opportunity to study factors affecting reproductive isolation and speciation. Many songbirds exhibit preference for local song types which may facilitate reproductive isolation. Recent contact between White-crowned Sparrows (Zonotrichia leucophrys pugetensis and Z. l. gambelii) appears to have resulted in hybridization in the Washington Cascade mountains. We investigated the role that song recognition may play in determining whether the two subspecies interbreed in the new contact zone. In playback experiments, male pugetensis recognized their own subspecies song more than that of gambelii, whereas gambelii did not discriminate. This difference in song discrimination correlates with the presence of geographic song variation. Pugetensis has regional dialects, distinguishes among different dialects, and is exposed to less song variation, thus may be less likely to recognize foreign songs. Gambelii is exposed to more song variation, and thus may be more likely to recognize foreign songs. Genetic results indicated greater movement of pugetensis mitochondrial DNA into gambelii-like individuals, suggesting that female pugetensis hybridized more frequently than female gambelii. This result was contrary to what we expected from the playback experiment results (if female choice mirrored male discrimination behavior). Asymmetric hybridization may be explained by some combination of differences in relative population growth/size, female dispersal, or female choice. Our results underscore the complexity of hybrid zones and the importance of investigating multiple possible mechanisms. RESUMEN Las zonas híbridas pueden usarse para examinar los mecanismos, como el reconocimiento del canto, que afectan el aislamiento reproductivo y la especiación. El canto cuenta con un apoyo parcial como impulsor de la especiación; nosotros no encontramos que el canto esté asociado con el aislamiento reproductivo en las subespecies Zonotrichia leucophrys pugetensis y Z. l. gambelii. Examinamos una zona emergente de contacto secundario en estas subespecies midiendo la variación del canto, el reconocimiento del canto, el plumaje, la morfología y el ADN mitocondrial (ADNmt). El plumaje y los caracteres morfológicos proporcionaron evidencia de hibridación en la zona de contacto, con algunas aves poseyendo características fenotípicas y de canto intermedias, y algunas poseyendo fenotipo discordante y haplotipo mitocondrial. Los experimentos de playback revelaron un reconocimiento asimétrico del canto: el macho pugetensis mostró una mayor respuesta a su propio canto que al canto de gambelii, mientras que gambelii no discriminó significativamente. Si la elección femenina opera de manera similar a la discriminación del canto de los machos, predijimos un flujo génico asimétrico, resultando en una mayor cantidad de híbridos con ADNmt de gambelii. Contrariamente a nuestra predicción, más gambelii e híbridos putativos en la zona de contacto poseyeron haplotipos de ADNmt de pugetensis, posiblemente debido a una mayor abundancia de pugetensis y a una dispersión sesgada hacia las hembras.