Climate Change Outpaces Adaptive Potential Via Hybridization in Nesting Female Saltmarsh and Nelson's Sparrows

Hybridization and introgression can promote adaptive potential and evolutionary resilience in response to increased pressures of climate change; they can also disrupt local adaptation and lead to outbreeding depression. We investigated female fitness consequences of hybridization in two sister species that are endemic to a threatened tidal marsh ecosystem: Saltmarsh (Ammospiza caudacutus) and Nelson's (Ammospiza nelsoni) sparrows. We found increasing nest flooding rates due to rising sea levels are outpacing potential adaptive benefits of hybridization due to very low overall nesting success in both the Nelson's and Saltmarsh sparrows. In the center of the hybrid zone across two years, we determined the success of 201 nests of 104 pure and admixed Saltmarsh and Nelson's Sparrow females, genotyped using a panel of single nucleotide polymorphisms (SNPs) from double digest restriction-site associated DNA (ddRAD) sequencing. We evaluated 5 metrics of female fitness and modeled nesting success in relation to genotypic, environmental, and nesting characteristics. We found differential fitness among Saltmarsh, Nelson's, and hybrid females, such that birds with predominantly Saltmarsh Sparrow alleles had higher reproductive success than birds with predominantly Nelson's Sparrows alleles, and hybrids were intermediate. Fledging success increased with two known tidal marsh nesting adaptations: nest height and nesting synchrony with tidal cycles. We found a positive relationship between hybrid index and fitness in daily nest survival in 2016, but not in 2017, likely due to differing levels of precipitation and nest flooding between years. The strongest and most consistent predictors of daily nest survival were nesting synchrony with lunar tidal flooding cycles and daily maximum tide height. Fitness patterns suggest that there may be an adaptive benefit of interspecific geneflow for the Nelson's Sparrow at the detriment of the Saltmarsh Sparrow; however, flooding rates are so high in many years they mask any fitness differences between the species, and all females had poor nesting success, regardless of genetic makeup. & BULL; This study explores female fitness consequences of hybridization between Saltmarsh and Nelson's Sparrows.& BULL; We evaluated 5 metrics of female fitness, and modeled nesting success in relation to genotype, environment, and nesting characteristics.& BULL; We found differential fitness among Saltmarsh, Nelson's, and hybrid females, such that birds with more Saltmarsh Sparrow alleles had higher reproductive success than birds with predominantly Nelson's Sparrow alleles, and hybrids had intermediate success.& BULL; The most consistent predictors of nest survival and fledging success were daily maximum tide height and female nesting adaptations that mitigate the risk of nest flooding.& BULL; High rates of nest flooding due to rising sea levels may be masking species-specific effects and fitness consequences of hybridization due to very low overall nesting success in both species. La hibridacion y la introgresion pueden promover el potencial adaptativo y la resiliencia evolutiva en respuesta a las crecientes presiones del cambio climatico; tambien pueden interrumpir la adaptacion local y llevar a depresion hibrida. Investigamos las consecuencias de la hibridacion en la aptitud biologica de las hembras en dos especies hermanas endemicas de un ecosistema amenazado de marismas de marea: Ammospiza caudacutus y A. nelsoni. Encontramos que las crecientes tasas de inundacion de nidos debido al aumento del nivel del mar estan superando los posibles beneficios adaptativos de la hibridacion debido al muy bajo exito general de nidificacion tanto en A. nelsoni como en A. caudacutus. En el centro de la zona hibrida, durante dos anos determinamos el exito de 201 nidos de 104 hembras puras y mezcladas de A. caudacutus y A. nelsoni, genotipadas mediante un panel de polimorfismos de un solo nucleotido obtenidos mediante secuenciacion de ADN asociada al sitio de restriccion de doble digestion. Evaluamos cinco metricas de aptitud de las hembras y modelamos el exito de nidificacion en relacion con caracteristicas genotipicas, ambientales y de nidificacion. Encontramos una aptitud diferencial entre las hembras de A. caudacutus, A. nelsoni y las hibridas, de modo que las aves con alelos predominantemente de A. caudacutus tuvieron un mayor exito reproductivo que las aves con alelos predominantemente de A. nelsoni, y las hibridas estuvieron en una posicion intermedia. El exito de emplumamiento aumento con dos adaptaciones conocidas para la nidificacion en marismas de marea: la altura del nido y la sincronizacion de la nidificacion con los ciclos de las mareas. Encontramos una relacion positiva entre el indice de hibridacion y la aptitud en la supervivencia diaria de los nidos en 2016, pero no en 2017, probablemente debido a diferentes niveles de precipitacion e inundacion de los nidos entre anos. Los predictores mas fuertes y consistentes de la supervivencia diaria de los nidos fueron la sincronizacion de la nidificacion con los ciclos de inundacion lunar y la altura maxima diaria de la marea. Los patrones de aptitud sugieren que puede haber un beneficio adaptativo del flujo genetico inter-especifico para A. nelsoni a expensas de A. caudacutus; sin embargo, las tasas de inundacion son tan altas en muchos anos que enmascaran cualquier diferencia de aptitud entre las especies, y todas las hembras tuvieron un bajo exito de nidificacion, independientemente de su composicion genetica.