Geographically consistent hybridization dynamics between the Black-crested and Tufted titmouse with evidence of hybrid zone expansion

ABSTRACT We studied hybridization between the Black-crested and Tufted titmouse across two geographically distinct transects that differ in the timing of secondary contact by hundreds to thousands of years. We found that hybridization patterns correspond to localized hybrid swarms and that the titmouse hybrid zone is likely slowly expanding over time, a product of short post-natal dispersal distances coupled with weak or absent selection against admixture. We show the southern part of the hybrid zone located in Texas is four times wider than the northern region of hybridization in Oklahoma, which is likely due to geographic differences in hybrid zone age. Despite differences in width, most individuals in both transects are advanced-generation hybrids and backcrosses, suggesting geographically consistent hybridization dynamics. We documented a strong correlation between genotypes and plumage index, suggesting that hybridization has not yet resulted in the decoupling of plumage and genome-wide ancestry as observed in some other avian hybrid zones. Although our results suggest the ongoing expansion of the hybrid zone, the rate of expansion appears to be slow, on the scale of tens of meters a year, and it will likely take hundreds of thousands to millions of years before homogenization of the parental populations. While we did not find support for partial reproductive isolation in the hybrid zone itself, there is the possibility that ecological or sexual selection limits introgression into allopatric regions. Broadly, the results of our study highlight the value of multiple, geographically distant, transects across a hybrid zone for assessing the evolutionary dynamics of hybridizing lineages. LAY SUMMARY We studied hybridization patterns between Black-crested and Tufted titmice in two areas of their contact zone that differ in the age of onset of hybridization by hundreds or thousands of years. We show that northern (younger) parts of the hybrid zone have a genetic transition four times narrower than the southern (older) region, which plausibly reflects the differences in the hybrid zone age or is a result of differences in the breadth of the ecotone between titmouse habitats in the north and south. Our results suggest that the Black-crested and Tufted titmouse hybrid zone might be in the process of slowly expanding following selectively neutral hybridization dynamics, although we cannot completely rule out a possible role of ecological or sexual selection in limiting gene flow outside of the hybrid zone. RESUMEN Estudiamos la hibridación entre Baeolophus atricristatus y B. bicolor a través de dos transectos geográficamente distintos que difieren en el momento del contacto secundario por cientos a miles de años. Encontramos que los patrones de hibridación corresponden a enjambres híbridos localizados y que la zona híbrida de Baeolophus probablemente se está expandiendo lentamente con el tiempo, producto de distancias cortas de dispersión postnatal, junto con una selección débil o ausente en contra de la mezcla genética. Mostramos que la parte sur de la zona híbrida ubicada en Texas es cuatro veces más ancha que la región norte de hibridación en Oklahoma, lo cual probablemente se debe a diferencias geográficas en la edad de la zona híbrida. A pesar de las diferencias en el ancho, la mayoría de los individuos en ambos transectos son híbridos de generaciones avanzadas y retrocruzas, lo que sugiere dinámicas de hibridación geográficamente consistentes. Documentamos una fuerte correlación entre los genotipos y el índice de plumaje, lo que sugiere que la hibridación aún no se ha traducido en el desacople del plumaje y la ancestralidad a nivel de todo el genoma, como se observa en algunas otras zonas híbridas de aves. Aunque nuestros resultados sugieren la expansión en curso de la zona híbrida, la tasa de expansión parece ser muy lenta, en la escala de decenas de metros por año, y probablemente tomará cientos de miles a millones de años antes de la homogeneización de las poblaciones parentales. Aunque no encontramos apoyo para el aislamiento reproductivo parcial en la zona híbrida en sí misma, existe la posibilidad de que la selección ecológica o sexual limite la introgresión en regiones alopátricas. En términos generales, los resultados de nuestro estudio destacan el valor de múltiples transectos geográficamente distantes a través de una zona híbrida para evaluar las dinámicas evolutivas de linajes hibridizantes.