Pitfalls and windfalls of detecting demographic declines using population genetics in long-lived species.

Detecting recent demographic changes is a crucial component of species conservation and management, as many natural populations face declines due to anthropogenic habitat alteration and climate change. Genetic methods allow researchers to detect changes in effective population size (N e ) from sampling at a single timepoint. However, in species with long lifespans, there is a lag between the start of a decline in a population and the resulting decrease in genetic diversity. This lag slows the rate at which diversity is lost, and therefore makes it difficult to detect recent declines using genetic data. However, the genomes of old individuals can provide a window into the past, and can be compared to those of younger individuals, a contrast that may help reveal recent demographic declines. To test whether comparing the genomes of young and old individuals can help infer recent demographic bottlenecks, we use forward-time, individual-based simulations with varying mean individual lifespans and extents of generational overlap. We find that age information can be used to aid in the detection of demographic declines when the decline has been severe. When average lifespan is long, comparing young and old individuals from a single timepoint has greater power to detect a recent (within the last 50 years) bottleneck event than comparing individuals sampled at different points in time. Our results demonstrate how longevity and generational overlap can be both a hindrance and a boon to detecting recent demographic declines from population genomic data.

Hybridization and range expansion in tamarisk beetles (Diorhabda spp.) introduced to North America for classical biological control.

With the global rise of human-mediated translocations and invasions, it is critical to understand the genomic consequences of hybridization and mechanisms of range expansion. Conventional wisdom is that high genetic drift and loss of genetic diversity due to repeated founder effects will constrain introduced species. However, reduced genetic variation can be countered by behavioral aspects and admixture with other distinct populations. As planned invasions, classical biological control (biocontrol) agents present important opportunities to understand the mechanisms of establishment and spread in a novel environment. The ability of biocontrol agents to spread and adapt, and their effects on local ecosystems, depends on genomic variation and the consequences of admixture in novel environments. Here, we use a biocontrol system to examine the genome-wide outcomes of introduction, spread, and hybridization in four cryptic species of a biocontrol agent, the tamarisk beetle (Diorhabda carinata, D. carinulata, D. elongata, and D. sublineata), introduced from six localities across Eurasia to control the invasive shrub tamarisk (Tamarix spp.) in western North America. We assembled a de novo draft reference genome and applied RADseq to over 500 individuals across laboratory cultures, the native ranges, and the introduced range. Despite evidence of a substantial genetic bottleneck among D. carinulata in N. America, populations continue to establish and spread, possibly due to aggregation behavior. We found that D. carinata, D. elongata, and D. sublineata hybridize in the field to varying extents, with D. carinata × D. sublineata hybrids being the most abundant. Genetic diversity was greater at sites with hybrids, highlighting potential for increased ability to adapt and expand. Our results demonstrate the complex patterns of genomic variation that can result from introduction of multiple ecotypes or species for biocontrol, and the importance of understanding them to predict and manage the effects of biocontrol agents in novel ecosystems.

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.

Minimal prezygotic isolation between ecologically divergent sibling species.

Divergence in mating signals typically accompanies speciation. We examine two ecologically divergent sibling species of crickets to assess the degree and timing of the evolution of prezygotic reproductive isolation. Gryllus saxatilis occurs in rocky habitats throughout western North America with long-winged individuals capable of long-distance dispersal; Gryllus navajo is endemic to red-rock sandstone areas of south-eastern Utah and north-eastern Arizona and has short-winged individuals only capable of limited dispersal. Previous genetic work suggested some degree of introgression and/or incomplete lineage sorting is likely. Here we: (1) use restriction site associated DNA sequencing (RAD-seq) genetic data to describe the degree of genetic divergence among species and populations; (2) examine the strength of prezygotic isolation by (i) quantifying differences among male mating songs, and (ii) testing whether females prefer G. saxatilis or G. navajo calling songs. Our results show that genetically distinct "pure" species populations and genetically intermediate populations exist. Male mating songs are statistically distinguishable, but the absolute differences are small. In playback experiments, females from pure populations had no preference based on song; however, females from a genetically intermediate population preferred G. navajo song. Together these results suggest that prezygotic isolation is minimal, and mediated by female behaviour in admixed populations.