iiinova — where your digital self keeps evolving

Finally, we used the parameters quantified from experiment in an evolutionary rescue model and found that our focal population has the potential to track warming as projected under moderate emissions scenarios.

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We took a standard GWA approach to identify variants associated with acute heat tolerance (here, thermal knockdown time). The diffuse signal throughout the genome for this trait suggested a potentially much more polygenic basis for prolonged vs acute heat tolerance.

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We identified hundreds of SNPs with systematic allele frequency differences between the heat-selected and control replicate populations, signal that was clustered into several distinct regions on each of the three chromosomes.

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Survival was reduced by 25% in the heat-selection treatment, with survivors of heat selection being roughly 10% smaller, and exhibiting significantly lower adult heat tolerance than those reared in control conditions.

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To quantify how much variation in thermal tolerance exists within a natural mosquito pop., we collected Aedes sierrensis wild from a mid-latitude population in Solano County, CA, reared them in common garden for two generations, and split F3 larvae into ‘control’ and ‘heat-selection’ groups.

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To circumvent the biosafety risks of working with many mosquito spp., we studied the western tree hole mosquito, Aedes sierrensis – a non-human disease vector. It is widely distributed across a large climate gradient, and easy to collect, rear, and manipulate in lab settings.

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Then, as predicted from our pop. expansion/truncation experiment, the indoor-favored alleles became selected against during population collapse in the outdoor mesocosm (again w/ cool chromosomal-arm level heterogeneity). 20/n

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We found that there was far greater overlap in the SNPs identified during expansion in the indoor and outdoor mesocosms than expected by chance, with the dominant direction of allele frequency movement concordant across indoor and outdoor expansion. 19/n

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Indeed, we found that two overlapping inversions on chromosome 3R (In3RK and In3RP), which segregate globally in D. mel pop’s, were favored in opposite directions across pop. expansion and truncation 16/n

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Quantifying expansion-favored allele trajectories during truncation, when stress-tolerance traits were favored, we observed a genome-wide trend reversion in allele frequencies, a signal of antagonistic pleiotropy underlying trade-offs! (w/ cool chromosome-level differences in this dynamic) 14/n

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Across the 9 gen’s of population expansion, when reproduction-associated traits are favored, we found evidence of strong, parallel adaption across our replicates (selection coeff’s > 10% per gen., similar to those quantified in the field). 13/n

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They then mimicked the pop. crash that occurs in the field during fall by removing all food and water from the replicate cages and sampling the surviving flies until all had perished. This sampling thus isolated groups of flies based on relative stress tolerance. 12/n

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Furthermore, we recently showed that patterns of genomic variation across independent study years is best predicted by the ecological phase (e.g., pop. expansion, peak density, or collapse) over which allele frequencies were quantified (10.1038/s41586-024-07834-x) 8/n

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We suspected this repeatability may result from fundamental life-history trade-offs that emerge in response to boom-bust dynamics, an ecological process that is ubiquitous to Drosophila and many other taxa 5/n

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Finally, we compared our results to a study using the same mesocosm in 2014 (DOI: 10.1126/science.abj7484). We found the targets of selection to be predictable across the independent bouts of adaptation, and largely driven by selection on sensory perception pathways.

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A more nuanced examination of the dynamics of sets of SNPs within individual replicate populations demonstrated that the direction of selection can fluctuate more than 5 times (!) throughout the experiment (B = target SNPs; C = matched controls)

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Measuring allele freq. shifts across all weekly intervals showed that the dominant direction of selection oftentimes reversed directions (blue points, below), indicating that fluctuating selection was revealed by our high resolution sampling.

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We took this approach to identify sets of SNPs across 10 time points (t1->11) and measured their dynamics in the left-out cage on increasingly shorter intervals. This revealed that evolutionary change occurs even on weekly intervals! (t1->2, below)

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To infer changes in the direction of selection throughout the experiment, we identified SNPs shifting systematically in 11 cages and measured the frequency change of the rising allele in the 12th. Check out this schematic by Sharon Greenblum from DOI: 10.1126/science.abj7484

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PCA indicated that variance in allele frequencies across all collected samples was dominated by collection time (A/B). Regression of allele frequencies throughout the experiment yielded 1000’s of SNP’s shifting systematically across replicates (C).

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In a tour-de-force, collaborative effort, we sampled 12 outdoor mesocosms at 12 time pts between July and December (~12 gen’s). The populations expanded during summer, hit a peak density in fall, and ultimately crashing following the first freeze. (schematic by Rashpal Dhillon rushstudio.ca)

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So, during the summer of 2021, I loaded my van and drove from California to Philadelphia.

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