Comparative phylogeography reveals widespread cryptic diversity driven by ecology in Panamanian birds

Abstract

Widespread species often harbor unrecognized genetic diversity, and investigating the factors associated with such cryptic variation can help us better understand the forces driving diversification. Here, we identify potential cryptic species based on a comprehensive dataset of COI mitochondrial DNA barcodes from 2,333 individual Panamanian birds across 429 species, representing 391 (59%) of the 659 resident landbird species of the country, as well as opportunistically sampled waterbirds. We complement this dataset with additional publicly available mitochondrial loci, such as ND2 and cytochrome b, obtained from whole mitochondrial genomes from 20 taxa. Using barcode identification numbers (BINs), we find putative cryptic species in 19% of landbird species, highlighting hidden diversity in the relatively well-described avifauna of Panama. Whereas some of these mitochondrial divergence events corresponded with recognized geographic features that likely isolated populations, such as the Cordillera Central highlands, the majority (74%) of lowland splits were between eastern and western populations. The timing of these splits are not temporally coincident across taxa, suggesting that historical events, such as the formation of the Isthmus of Panama and Pleistocene climatic cycles, were not the primary drivers of cryptic diversification. Rather, we observed that forest species, understory species, insectivores, and strongly territorial species--all traits associated with lower dispersal ability--were all more likely to have multiple BINs in Panama, suggesting strong ecological associations with cryptic divergence. Additionally, hand-wing index, a proxy for dispersal capability, was significantly lower in species with multiple BINs, indicating that dispersal ability plays an important role in generating diversity in Neotropical birds. Together, these results underscore the need for evolutionary studies of tropical bird communities to consider ecological factors along with geographic explanations, and that even in areas with well-known avifauna, avian diversity may be substantially underestimated. LAY SUMMARY- What factors are common among bird species with cryptic diversity in Panama? What role do geography, ecology, phylogeographic history, and other factors play in generating bird diversity? - 19% of widely-sampled bird species form two or more distinct DNA barcode clades, suggesting widespread unrecognized diversity. - Traits associated with reduced dispersal ability, such as use of forest understory, high territoriality, low hand-wing index, and insectivory, were more common in taxa with cryptic diversity. Filogeografia comparada revela amplia diversidad criptica causada por la ecologia en las aves de Panama RESUMENEspecies extendidas frecuentemente tiene diversidad genetica no reconocida, y investigando los factores asociados con esta variacion criptica puede ayudarnos a entender las fuerzas que impulsan la diversificacion. Aqui, identificamos especies cripticas potenciales basadas en un conjunto de datos de codigos de barras de ADN mitocondrial de 2,333 individuos de aves de Panama en 429 especies, representando 391 (59%) de las 659 especies de aves terrestres residentes del pais, ademas de algunas aves acuaticas muestreada de manera oportunista. Adicionalmente, complementamos estos datos con secuencias mitocondriales disponibles publicamente de otros loci, tal como ND2 o citocroma b, obtenidos de los genomas mitocondriales completos de 20 taxones. Utilizando los numeros de identificacion de codigo de barras (en ingles: BINs), un sistema taxonomico numerico que proporcina una estimacion imparcial de la diversidad potencial a nivel de especie, encontramos especies cripticas putativas en 19% de las especies de aves terrestres, lo que destaca la diversidad oculta en la avifauna bien descrita de Panama. Aunque algunos de estos eventos de divergencia conciden con caracteristicas geograficas que probablemente aislaron las poblaciones, la mayoria (74%) de la divergencia en las tierras bajas se encuentra entre las poblaciones orientales y occidentales. El tiempo de esta divergencia no coincidio entre los taxones, sugiriendo que eventos historicos tales como la formacion del Istmo de Panama y los ciclos climaticos del pleistoceno, no fueron los principales impulsores de la especiacion. En cambio, observamos asociaciones fuertes entre las caracteristicas ecologicas y la divergencia mitocondriale: las especies del bosque, sotobosque, con una dieta insectivora, y con territorialidad fuerte mostraton multiple BINs probables. Adicionalmente, el indice mano-ala, que esta asociado a la capacidad de dispersion, fue significativamente menor en las especies con BINs multiples, sugiriendo que la capacidad de dispersion tiene un rol importamente en la generacion de la diversidad de las aves neotropicales. Estos resultos demonstran la necesidad de que estudios evolutivos de las comunidades de aves tropicales consideren los factores ecologicos en conjunto con las explicaciones geograficos. Palabras clave: biodiversidad tropical, biogeografia, codigos de barras, dispersion, especies cripticas