Adaptive differentiation and rapid evolution of a soil bacterium along a climate gradient

Microbial community responses to environmental change are largely associated with ecological processes; however, the potential for microbes to rapidly evolve and adapt remains relatively unexplored in natural environments. To assess how ecological and evolutionary processes simultaneously alter the genetic diversity of a microbiome, we conducted two concurrent experiments in the leaf litter layer of soil over 18 mo across a climate gradient in Southern California. In the first experiment, we reciprocally transplanted microbial communities from five sites to test whether ecological shifts in ecotypes of the abundant bacterium, Curtobacterium, corresponded to past adaptive differentiation. In the transplanted communities, ecotypes converged toward that of the native communities growing on a common litter substrate. Moreover, these shifts were correlated with community-weighted mean trait values of the Curtobacterium ecotypes, indicating that some of the trait variation among ecotypes could be explained by local adaptation to climate conditions. In the second experiment, we transplanted an isogenic Curtobacterium strain and tracked genomic mutations associated with the sites across the same climate gradient. Using a combination of genomic and metagenomic approaches, we identified a variety of nonrandom, parallel mutations associated with transplantation, including mutations in genes related to nutrient acquisition, stress response, and exopolysaccharide production. Together, the field experiments demonstrate how both demographic shifts of previously adapted ecotypes and contemporary evolution can alter the diversity of a soil microbiome on the same timescale.

Faster-X adaptive differentiation under divergence-with-gene-flow in diploids and haplodiploids

Empirical data from diverse taxa indicate that the hemizygous portions of the genome (X/Z chromosomes) evolve more rapidly than their diploid counterparts. Faster-X theory predicts increased rates of adaptive substitutions between isolated species, yet little is known about species experiencing gene flow. Here we investigate how hemizygosity impacts genome-wide patterns of differentiation during adaptive divergence with gene flow, combining simulations under isolation-with-migration models, a meta-analysis of autosomes and sex-chromosomes from diverse taxa, and analysis of haplodiploid species. First, using deterministic and stochastic simulations, we show that elevated differentiation at hemizygous loci occurs when there is gene flow, irrespective of dominance. This faster-X adaptive differentiation stems from more efficient selection resulting in reduced probability of losing the beneficial allele, greater migration-selection threshold, greater allele frequency differences at equilibrium, and a faster time to equilibrium. Second, by simulating neutral variation linked to selected loci, we show that faster-X differentiation affects linked variation due to reduced opportunities for recombination between locally adaptive and maladaptive immigrant haplotypes. Third, after correcting for expected differences in effective population size, we find that most taxon pairs (24 out of 28) exhibit faster-X differentiation in the meta-analysis. Finally, using a novel approach combining demographic modeling and simulations, we found evidence for faster-X differentiation in haplodiploid pine-feeding hymenopteran species adapted to different host plants. Together, our results indicate that divergent selection with gene flow can lead to higher differentiation at selected and linked variation in hemizygous loci (i.e., faster-X adaptive differentiation), both in X/Z-chromosomes and haplodiploid species.

The role of neutral and adaptive genomic variation in population diversification and speciation in two ground squirrel species of conservation concern

Understanding the neutral (demographic) and adaptive processes leading to the differentiation of species and populations is a critical component of evolutionary and conservation biology. In this context, recently diverged taxa represent a unique opportunity to study the process of genetic differentiation. Northern and southern Idaho ground squirrels (Urocitellus brunneus – NIDGS, and U. endemicus - SIDGS, respectively) are a recently diverged pair of sister species that have undergone dramatic declines in the last 50 years and are currently found in metapopulations across restricted spatial areas with distinct environmental pressures. Here we genotyped single-nucleotide polymorphisms (SNPs) from buccal swabs with restriction site-associated DNA sequencing (RADseq). With these data we evaluated neutral genetic structure at both the inter- and intra-specific level, and identified putatively adaptive SNPs using population structure outlier and genotype-environment association (GEA) analyses. At the interspecific level, we found a clear separation between NIDGS and SIDGS, and evidence for adaptive differentiation relating to differences in hibernation. At the intraspecific level, we identified 3 Evolutionarily Significant Units for NIDGS and 2 for SIDGS plus multiple Management and Adaptive Units. Elevation appears to be the main driver of adaptive differentiation in NIDGS, while neutral variation patterns match and extend that identified in previous studies using microsatellite markers. For SIDGS, neutral substructure generally reflected the effect of natural geographic barriers, while adaptive variation reflected differences in land cover and temperature. These results clearly highlight the roles of neutral and adaptive processes for understanding species and population differentiation, which can have important conservation implications in threatened species.

Adaptive trade-offs in fish energetics and physiology: insights from adaptive differentiation among juvenile salmonids

Juveniles of different salmonid species often co-exist along environmental gradients, making them a useful model for identifying dominant trade-off axes and their stability within a biological hierarchy (e.g., from individuals to populations to species). In this perspective, we use multivariate trade-offs among juvenile coho salmon (Oncorhynchus kisutch) and rainbow trout (Oncorhynchus mykiss) as a case study to explore broader-scale patterns of trait association. Multivariate ordination identified a dominant trade-off axis between high growth, consumption, and growth efficiency versus high aerobic scope and active metabolism among individual juvenile rainbow trout and three ecologically divergent rainbow trout populations. This pattern suggests a dominant trade-off between growth and active metabolism among individuals and populations, facilitated by simple developmental controls on increased energy intake (larger digestive tract, potentially more risky foraging behavior). In contrast, the adaptive trade-off differentiating species appears to have shifted to maximizing growth and consumption (rainbow trout) versus maximizing growth efficiency (coho), based on evolved differences in foraging strategy and digestive physiology. The generality of these patterns remains uncertain, but trade-offs related to growth efficiency may be an underappreciated dimension of adaptive differentiation in fishes, and their relationship to digestive strategy and active metabolism warrants further investigation.