Biology subjects

Behrman, E. L.

Publications and source records attributed to Behrman, E. L..

8 recordsLinked to original sources

bioRxiv2026

Intragenic epistasis in couch potato shapes life history traits and climatic adaptation in Drosophila melanogaster

Populations adapting to heterogeneous environments often harbor many alleles that covary with environmental gradients, yet how so many adaptive variants can be maintained and show signatures of local adaptation remains unclear. Epistatic non-additive interactions among alleles may concentrate fitness effects at specific allelic combinations to shape complex traits and facilitate adaptation. We evaluate compositional epistasis among three intronic SNPs in the couch potato (cpo) gene, each independently clinal along the North American latitudinal gradient, using recombinant outbred populations fixed for distinct three-locus combinations. Flies carrying all three temperate alleles (cpoTTA) or all three tropical alleles (cpoCGT) show non-additive increases in traits associated with fitness in their respective environments: dormancy, starvation resistance, and lipid storage in temperate flies and fecundity in tropical flies. Intermediate genotype combinations generally show weaker and negative deviations from additive predictions. Temperate genotypes show reduced cpo expression and independently create predicted transcription factor binding sites, suggesting a regulatory basis for the observed phenotypic effects. Consistent with selection shaping haplotype frequencies against a backdrop of ongoing recombination, the temperate and tropical genotypes are enriched above random expectation across the latitudinal cline, with directionally consistent but non-significant seasonal patterns. Our findings demonstrate that non-additive interactions among non-coding variants within a single gene can produce large, pleiotropic fitness effects and shape genotype distributions in natural populations, providing a mechanism by which a small number of regulatory variants can underlie complex climatic adaptation.

evolutionary biology↗

bioRxiv2026

Climate predicts wMel Wolbachia frequency variation in Drosophila melanogaster, but genomic variation reflects a recent incomplete cytoplasmic sweep

Maternally transmitted Wolbachia occupy roughly half of terrestrial arthropod species, but the factors maintaining their variable population frequencies are poorly understood. In Drosophila melanogaster, the wMel Wolbachia variant occurs at intermediate and variable frequencies globally. We document rapid wMel frequency shifts up to 0.33 between consecutive weeks in experimental and natural orchards in the eastern United States, with frequencies peaking at intermediate temperatures and declining at thermal extremes. Seven years of seasonal sampling at a Pennsylvania orchard showed wMel frequencies consistently higher in summer than fall, consistent with temperature-dependent maternal transmission. Bayesian models applied to 248 locations across five continents and 42 years of sampling corroborated the previously described wMel frequency cline in eastern Australia but found no latitudinal pattern on any other continent. Precipitation seasonality and driest-quarter precipitation were the strongest global predictors, absorbing the among-continent wMel frequency variation that latitude left unexplained. Wet-season temperature predicted wMel frequency in Australia, where the wettest quarter coincides with summer and peak host reproduction. Analysis of 339 individually sequenced wMel genomes identified 38 wMel SNPs associated with latitude, but these associations did not persist after accounting for cytoplasmic lineage structure, and 35 of the 38 were private to a remnant southwestern European lineage. Our results establish that local climatic conditions shape wMel frequencies globally, plausibly through effects on maternal transmission fidelity that depend on the seasonal alignment of warm temperatures with host reproduction. wMel genomic variation, in contrast, reflects the incomplete replacement of ancestral wMelCS by wMel, rather than local adaptation.

evolutionary biology↗

bioRxiv2025

Natural evolution of intermale sexual behavior by multiple pheromone switches among Drosophila species

We have identified a Drosophila species which exhibits spontaneous and robust intermale sexual behavior. D. santomea males distinguish conspecific sexes but court both vigorously and seldom attack. Elevated intermale courtship stems from at least three evolutionarily derived pheromonal changes. In males, the sexually monomorphic cuticular pheromone 7-tricosene promotes rather than inhibits courtship and the courtship-inhibiting olfactory pheromone cVA is reduced 84-92% compared to close relatives. The third switch is in D. santomea females, where cVA suppresses rather than promotes sexual receptivity. Female cVA aversion and male cVA reduction may have co-evolved to maintain efficient intraspecific mating but prevent hybridization with the sympatric sibling species D. yakuba. High intermale courtship and low cVA also co-occur and appear selectively derived in a distant monomorphic species D. persimilis, implying pheromonal and social behavioral convergence. Changes in pheromone valence and levels may therefore explain the recent evolutionary emergence of intermale sexual behavior in Drosophila.

evolutionary biology↗

bioRxiv2024

Drosophila melanogaster pigmentation demonstrates adaptive phenotypic parallelism but genomic unpredictability over multiple timescales

Populations are capable of responding to environmental change over ecological timescales via adaptive tracking. However, the translation from patterns of allele frequency change to rapid adaptation of complex traits remains unresolved. We used abdominal pigmentation in Drosophila melanogaster as a model phenotype to address the nature, genetic architecture, and repeatability of rapid adaptation in the field. We show that D. melanogaster pigmentation evolves as a highly parallel and deterministic response to shared environmental gradients across latitude and season in natural North American populations. We then experimentally evolved replicate, genetically diverse fly populations in field mesocosms to remove any confounding effects of demography and/or cryptic structure that may drive patterns in wild populations; we show that pigmentation rapidly responds, in parallel, in fewer than fifteen generations. Thus, pigmentation evolves concordantly in response to spatial and temporal climatic gradients. We next examined whether phenotypic differentiation was associated with allele frequency change at loci with established links to genetic variance in pigmentation in natural populations. We found that across all spatial and temporal scales, phenotypic patterns were associated with variation at pigmentation-related loci, and the sets of genes we identified in each context were largely nonoverlapping. Therefore, our findings suggest that parallel phenotypic evolution is associated with distinct components of the polygenic architecture shifting across each environmental gradient to produce redundant adaptive patterns.

evolutionary biology↗

bioRxiv2022

How predictable is rapid evolution?

Although evolution is historically considered a slow, gradual process, it is now clear that evolution can occur rapidly over generational timescales. It remains unclear both how predictable rapid evolution is and what timescales are ecologically relevant due to a paucity of longitudinal studies. We use a common garden approach to measure genetic-based change in complex, fitness-associated traits that are important for climatic adaptation in wild Drosophila over multiple timescales: an estimated 1-16 generations within each year and 48-89 generations over five consecutive years. Evolution is fast and pervasive with parallel patterns of rapid evolution in three distinct locations that span 4{o} latitude. Developmental time evolves consistently across seasons with flies collected in spring developing faster than those collected in autumn. The evolutionary trajectory of stress traits (heat knockdown and starvation) depends on the severity of the preceding winter: harsh winters result in a predictable evolutionary trajectory with high stress tolerance in spring flies that declines in the subsequent generations across the summer. Flies collected after mild winters do not evolve in a predictable pattern but may utilize an alternative strategy as plasticity for chill coma recovery and starvation evolves across seasons. Overall, winter severity determines the predictability of rapid seasonal evolution, but there are also long-term shifts in the phenotypic correlations and allele frequencies that indicate long-term population changes that have broader implications for how organisms respond to the changing climate. Significance StatementAdaptive tracking may result in rapid evolution over short timescales, but the repeatability and predictability of rapid adaptation is less well resolved without long-term, multi-year analyses. Here, we collect wild flies at regular intervals across five years to determine what traits evolve consistently over seasons and which environmental variables predict this rapid evolution. Traditional temperate seasonal patterns of harsh winters are crucial for normal selection patterns, although independently changing phenotypic and genetic correlations help the populations respond to long-term shifts over years, particularly in response to heat stress. This has the implication that populations may be flexible within certain genetic constraints to adapt to changing climatic temperatures.

evolutionary biology↗

bioRxiv2021

Drosophila Evolution over Space and Time (DEST) - A New Population Genomics Resource

Drosophila melanogaster is a leading model in population genetics and genomics, and a growing number of whole-genome datasets from natural populations of this species have been published over the last 20 years. A major challenge is the integration of these disparate datasets, often generated using different sequencing technologies and bioinformatic pipelines, which hampers our ability to address questions about the evolution and population structure of this species. Here we address these issues by developing a bioinformatics pipeline that maps pooled sequencing (Pool-Seq) reads from D. melanogaster to a hologenome consisting of fly and symbiont genomes and estimates allele frequencies using either a heuristic (PoolSNP) or a probabilistic variant caller (SNAPE-pooled). We use this pipeline to generate the largest data repository of genomic data available for D. melanogaster to date, encompassing 271 population samples from over 100 locations in >20 countries on four continents based on a combination of 121 unpublished and 150 previously published genomic datasets. Several of these locations have been sampled at different seasons across multiple years. This dataset, which we call Drosophila Evolution over Space and Time (DEST), is coupled with sampling and environmental meta-data. A web-based genome browser and web portal provide easy access to the SNP dataset. Our aim is to provide this scalable platform as a community resource which can be easily extended via future efforts for an even more extensive cosmopolitan dataset. Our resource will enable population geneticists to analyze spatio-temporal genetic patterns and evolutionary dynamics of D. melanogaster populations in unprecedented detail.

genomics↗

bioRxiv2018

Natural variation in couch potato mediates rapid evolution of learning and reproduction in natural populations of Drosophila melanogaster

Learning is a general mechanism of adaptive behavioural plasticity whose benefits and costs depend on the environment. Thus, seasonal oscillations in temperate environments between winter and summer might produce cyclical selection pressures that would drive rapid evolution of learning performance in multivoltine populations. To test this hypothesis, we investigated the evolutionary dynamics of learning ability over this rapid seasonal timescale in a natural population of Drosophila melanogaster. Associative learning was tested in common garden-raised flies collected from nature in the spring and fall over three consecutive years. The spring flies consistently learned better than fall flies, revealing seasonal evolution of improved learning performance in nature. Fecundity showed the opposite seasonal pattern, suggesting a trade-off between learning and reproduction. This trade-off also held within population: more fecund individual females learned less well. This trade-off is mediated at least in part by natural polymorphism in the RNA binding protein couch potato (cpo), with a genotype favoured during summer showing poorer learning performance and higher fecundity than a genotype favoured over winter. Thus, seasonal environments can drive rapid cyclical evolution of learning performance, but the evolutionary dynamics may be driven by trade-offs generated by pleiotropic effects of causative alleles selected for other reasons.

evolutionary biology↗

bioRxiv2017

Rapid seasonal evolution in innate immunity of wild Drosophila melanogaster

Understanding the rate of evolutionary change and the genetic architecture that facilitates rapid adaptation is a current challenge in evolutionary biology. Comparative studies show that genes with immune function are among the most rapidly evolving genes in a range of taxa. Here, we use immune defense in natural populations of D. melanogaster to understand the rate of evolution in natural populations and the genetics underlying the rapid change. We probed the immune system using the natural pathogens Enterococcus faecalis and Providencia rettgeri to measure post-infection survival and bacterial load of wild D. melanogaster populations collected across seasonal time along a latitudinal transect on the eastern North America (Massachusetts, Pennsylvania, and Virginia). There are pronounced and repeatable changes in the immune response over approximately 10 generations between the spring and fall populations with a significant but less distinct difference among geographic locations. Genes with known immune function are not enriched among alleles that cycle with seasonal time, but the immune function of a subset of seasonally cycling alleles in immune genes was tested using reconstructed outbred populations. We find that flies containing seasonal alleles in Thioester-containing protein 3 (Tep3) have different functional responses to infection and that epistatic interactions among seasonal Tep3 and Drosomycin-like 6 (Dro6) alleles produce the immune phenotypes observed in natural populations. This rapid, cyclic response to seasonal environmental pressure broadens our understanding of the complex ecological and genetic interactions determining the evolution of immune defense in natural populations.

evolutionary biology↗