Sexual signal evolution and patterns of assortative mating across an intraspecific contact zone.

Contact zones provide important insights into the evolutionary processes that underlie lineage divergence and speciation. Here, we use a contact zone to ascertain speciation potential in the red-eyed treefrog (Agalychnis callidryas), a brightly coloured and polymorphic frog that exhibits unusually high levels of intraspecific variation. Populations of A. callidryas differ in a number of traits, several of which are known sexual signals that mediate premating reproductive isolation in allopatric populations. Along the Caribbean coast of Costa Rica, a ~100 km contact zone, situated between two phenotypically and genetically divergent parent populations, contains multiple colour pattern phenotypes and late-generation hybrids. This contact zone provides the opportunity to examine processes that are important in the earliest stages of lineage divergence. We performed analyses of colour pattern variation in five contact zone sites and six parental sites and found complex, continuous colour variation along the contact zone. We found discordance between the geographic distribution of colour pattern and previously described genomic population structure. We then used a parental site and contact zone site to measure assortative mating and directional selection from naturally-occurring amplectant mating pairs. We found assortative mating in a parental population, but no assortative mating in the contact zone. Furthermore, we uncovered evidence of directional preference towards the adjacent parental phenotype in the contact zone population, but no directional preference in the parent population. Combined, these data provide insights into potential dynamics at the contact zone borders and indicate that incipient speciation between parent populations will be slowed.

Comparative linkage mapping uncovers recombination suppression across massive chromosomal inversions associated with local adaptation in Atlantic silversides.

The role of recombination in genome evolution has long been studied in theory, but until recently empirical investigations had been limited to a small number of model species. Here, we compare the recombination landscape and genome collinearity between two populations of the Atlantic silverside (Menidia menidia), a small fish distributed across the steep latitudinal climate gradient of the North American Atlantic coast. We constructed separate linkage maps for locally adapted populations from New York and Georgia and their interpopulation laboratory cross. First, we used one of the linkage maps to improve the current silverside genome assembly by anchoring three large unplaced scaffolds to two chromosomes. Second, we estimated sex-specific recombination rates, finding 2.3-fold higher recombination rates in females than males-one of the most extreme examples of heterochiasmy in a fish. While recombination occurs relatively evenly across female chromosomes, it is restricted to only the terminal ends of male chromosomes. Furthermore, comparisons of female linkage maps revealed suppressed recombination along several massive chromosomal inversions spanning nearly 16% of the genome. These inversions segregate between locally adapted populations and coincide near perfectly with blocks of highly elevated genomic differentiation between wild populations. Finally, we discerned significantly higher recombination rates across chromosomes in the northern population compared to the southern. In addition to providing valuable resources for ongoing evolutionary and comparative genomic studies, our findings represent a striking example of structural variation that impacts recombination between adaptively divergent populations, providing empirical support for theorized genomic mechanisms facilitating adaptation despite gene flow.

Genetic isolation by distance underlies colour pattern divergence in red-eyed treefrogs (Agalychnis callidryas).

Investigating the spatial distribution of genetic and phenotypic variation can provide insights into the evolutionary processes that shape diversity in natural systems. We characterized patterns of genetic and phenotypic diversity to learn about drivers of colour-pattern diversification in red-eyed treefrogs (Agalychnis callidryas) in Costa Rica. Along the Pacific coast, red-eyed treefrogs have conspicuous leg colour patterning that transitions from orange in the north to purple in the south. We measured phenotypic variation of frogs, with increased sampling at sites where the orange-to-purple transition occurs. At the transition zone, we discovered the co-occurrence of multiple colour-pattern morphs. To explore possible causes of this variation, we generated a single nucleotide polymorphism data set to analyse population genetic structure, measure genetic diversity and infer the processes that mediate genotype-phenotype dynamics. We investigated how patterns of genetic relatedness correspond to individual measures of colour pattern along the coast, including testing for the role of hybridization in geographic regions where orange and purple phenotypic groups co-occur. We found no evidence that colour-pattern polymorphism in the transition zone arose through recent hybridization. Instead, a strong pattern of genetic isolation by distance indicates that colour-pattern variation was either retained through other processes such as ancestral colour polymorphisms or ancient secondary contact, or else it was generated by novel mutations. We found that phenotype changes along the Pacific coast more than would be expected based on genetic divergence and geographic distance alone. Combined, our results suggest the possibility of selective pressures acting on colour pattern at a small geographic scale.

La investigación de la distribución espacial de la variación genética y fenotípica puede proporcionar información sobre los procesos evolutivos que dan forma a la diversidad en los sistemas naturales. Caracterizamos patrones de diversidad genética y fenotípica para conocer los impulsores de la diversificación de patrones de color en ranas con ojos rojos (Agalychnis callidryas) en Costa Rica. A lo largo de la costa del Pacífico, las ranas con ojos rojos tienen un patrón de color llamativo en las patas que cambia de naranja en el norte a púrpura en el sur. Medimos la variación fenotípica de las ranas en los sitios del Pacífico, con un mayor muestreo en los sitios donde ocurre la transición de naranja a púrpura. En la zona de transición, descubrimos la co-ocurrencia de múltiples morfos de patrones de color. Para explorar las posibles causas de esta variación, generamos un conjunto de datos SNP con secuenciación RAD para analizar la estructura genética de la población, medir la diversidad genética e inferir los procesos que median la dinámica genotipo-fenotipo. Investigamos cómo los patrones de parentesco genético se corresponden con medidas individuales de patrón de color a lo largo de la costa, incluidas las pruebas del papel de la hibridación en regiones geográficas donde coexisten grupos fenotípicos naranja y morado. No encontramos evidencia de que el polimorfismo del patrón de color en la zona de transición surgiera a través de una hibridación o introgresión reciente. En cambio, un fuerte patrón de aislamiento genético por distancia indica que la variación del patrón de color se retuvo a través de otros procesos, como los polimorfismos de color ancestrales, el contacto secundario antiguo o la generada por mutaciones novedosas. Descubrimos que el fenotipo de color cambia a lo largo de la costa del Pacífico más de lo que se esperaría solo por la divergencia genética y la distancia geográfica. Combinados, nuestros resultados sugieren la posibilidad de que las presiones selectivas actúen sobre el patrón de color a pequeña escala geográfica.

Genetic and phenotypic evidence of a contact zone between divergent colour morphs of the iconic red-eyed treefrog.

Hybrid zones act as natural laboratories where divergent genomes interact, providing powerful systems for examining the evolutionary processes underlying biological diversity. In this study, we characterized patterns of genomic and phenotypic variation resulting from hybridization between divergent intraspecific lineages of the Neotropical red-eyed treefrog (Agalychnis callidryas). We found genetic evidence of a newly discovered contact zone and phenotypic novelty in leg colour-a trait suspected to play a role in mediating assortative mating in this species. Analysis of hybrid ancestry revealed an abundance of later-generation Fn individuals, suggesting persistence of hybrids in the contact zone. Hybrids are predominantly of southern ancestry but are phenotypically more similar to northern populations. Genome-wide association mapping revealed QTL with measurable effects on leg-colour variation, but further work is required to dissect the architecture of this trait and establish causal links. Further, genomic cline analyses indicated substantial variation in patterns of introgression across the genome. Directional introgression of loci associated with different aspects of leg colour are inherited from each parental lineage, creating a distinct hybrid colour pattern. We show that hybridization can generate new phenotypes, revealing the evolutionary processes that potentially underlie patterns of phenotypic diversity in this iconic polytypic frog. Our study is consistent with a role of hybridization and sexual selection in lineage diversification, evolutionary processes that have been implicated in accelerating divergence in the most phenotypically diverse species.