Experimental evidence for ecological selection on genome variation in the wild

Understanding natural selection's effect on genetic variation is a major goal in biology, but the genome-scale consequences of contemporary selection are not well known. In a release and recapture field experiment we transplanted stick insects to native and novel host plants and directly measured allele frequency changes within a generation at 186 576 genetic loci. We observed substantial, genome-wide allele frequency changes during the experiment, most of which could be attributed to random mortality (genetic drift). However, we also documented that selection affected multiple genetic loci distributed across the genome, particularly in transplants to the novel host. Host-associated selection affecting the genome acted on both a known colour-pattern trait as well as other (unmeasured) phenotypes. We also found evidence that selection associated with elevation affected genome variation, although our experiment was not designed to test this. Our results illustrate how genomic data can identify previously underappreciated ecological sources and phenotypic targets of selection

Genome divergence and diversification within a geographic mosaic of coevolution

Despite substantial interest in coevolution's role in diversification, examples of coevolution contributing to speciation have been elusive. Here, we build upon past studies that have shown both coevolution between South Hills crossbills and lodgepole pine (Pinus contorta), and high levels of reproductive isolation between South Hills crossbills and other ecotypes in the North American red crossbill (Loxia curvirostra) complex. We used genotyping by sequencing to generate population genomic data and applied phylogenetic and population genetic analyses to characterize the genetic structure within and among nine of the ecotypes. Although genome-wide divergence was slight between ecotypes (FST = 0.011–0.035), we found evidence of relative genetic differentiation (as measured by FST) between and genetic cohesiveness within many of them. As expected for nomadic and opportunistic breeders, we detected no evidence of isolation by distance. The one sedentary ecotype, the South Hills crossbill, was genetically most distinct because of elevated divergence at a small number of loci rather than pronounced overall genome-wide divergence. These findings suggest that mechanisms related to recent local coevolution between South Hills crossbills and lodgepole pine (e.g. strong resource-based density dependence limiting gene flow) have been associated with genome divergence in the face of gene flow. Our results further characterize a striking example of coevolution driving speciation within perhaps as little as 6000 years

Stick insect genomes reveal natural selection's role in parallel speciation.

Natural selection can drive the repeated evolution of reproductive isolation, but the genomic basis of parallel speciation remains poorly understood. We analyzed whole-genome divergence between replicate pairs of stick insect populations that are adapted to different host plants and undergoing parallel speciation. We found thousands of modest-sized genomic regions of accentuated divergence between populations, most of which are unique to individual population pairs. We also detected parallel genomic divergence across population pairs involving an excess of coding genes with specific molecular functions. Regions of parallel genomic divergence in nature exhibited exceptional allele frequency changes between hosts in a field transplant experiment. The results advance understanding of biological diversification by providing convergent observational and experimental evidence for selection's role in driving repeatable genomic divergence

Progress and Promise in using Arabidopsis to Study Adaptation, Divergence, and Speciation

Fundamental questions remain to be answered on how lineages split and new species form. The Arabidopsis genus, with several increasingly well characterized species closely related to the model system A. thaliana, provides a rare opportunity to address key questions in speciation research. Arabidopsis species, and in some cases populations within a species, vary considerably in their habitat preferences, adaptations to local environments, mating system, life history strategy, genome structure and chromosome number. These differences provide numerous open doors for understanding the role these factors play in population divergence and how they may cause barriers to arise among nascent species. Molecular tools available in A. thaliana are widely applicable to its relatives, and together with modern comparative genomic approaches they will provide new and increasingly mechanistic insights into the processes underpinning lineage divergence and speciation. We will discuss recent progress in understanding the molecular basis of local adaptation, reproductive isolation and genetic incompatibility, focusing on work utilizing the Arabidopsis genus, and will highlight several areas in which additional research will provide meaningful insights into adaptation and speciation processes in this genus