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Beltz, J. K.

Publications and source records attributed to Beltz, J. K..

5 recordsLinked to original sources

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↗

High-resolution mapping of a rapidly evolving complex trait reveals genotype-phenotype stability and an unpredictable genetic architecture of adaptation

The extent to which adaptation can be predicted is unknown. Here, we leveraged a longitudinal sampling design to test the efficacy of genomic prediction of trait evolution in an ecologically-relevant setting. Specifically, we monitored genome-wide allele frequencies and pigmentation variation in genetically diverse populations of Drosophila melanogaster across seven generations of evolution in both field mesocosms and a controlled, lab-based setting. At two points during trait evolution, we conducted a high-powered quantification of trait architecture that produced a well-resolved genotype-phenotype map. While we were able to use this map to correctly infer the direction of pigmentation evolution in both the field and lab mesocosms, the particular loci responding to selection, and thus the architecture of adaptation itself, was largely unpredictable. Further, we quantified a striking stability of the genotype-phenotype map, even across independent and genetically diverged populations. Our results hold implications for both the promise and limitations of genomic prediction.

evolutionary biology↗

The microbiota elicits compensatory adaptation in a seasonally-adapting animal host

Seasonal adaptation in Drosophila melanogaster is a model for understanding the evolutionary responses of organisms to cyclical environmental changes, including roles played by associated microorganisms ( microbiota). Here we examined how the microbiota influences D. melanogaster seasonal adaptation by rearing flies in outdoor mesocosms, fed diets inoculated with different bacterial strains that have distinct influences on the flies life history. The bacterial treatments influenced fly population dynamics and microbiota composition over a summer-to-fall season. The developmental phenotype of the treated flies initially differed but converged over time in flies reared with a complete microbial community. Conversely, rearing the flies free of their colonizing microorganisms revealed that the bacterial treatments led to evolution of distinct developmental phenotypes. The development time of flies from the different treatments consistently adapted to compensate for the direct influence of the bacteria on host development; e.g., flies evolved faster development times if they were inoculated with microbes that slowed development. This compensatory trend was apparent in flies reared in a second location and season, and is consistent with a previous report of wild-sampled flies whose development phenotype segregated with their microbiota composition. Together, these results reveal that microbiota-dependent selection consistently elicits compensatory adaptation in seasonally-evolving flies, which we conclude is a mechanism whereby horizontally-acquired, low-fidelity microbial partners can shape the evolution of their animal hosts. ImportanceUnderstanding how organisms adapt to seasonal change can model evolutionary responses in a broader changing world. Drosophila melanogaster is a powerful model for studying these dynamics, especially when considering the influence of transient yet impactful colonizing microorganisms. This study reveals that microbial partners can drive consistent, compensatory adaptation in host development across seasons and locations. By demonstrating that flies evolve faster development times in response to microbes that slow a model hosts period of growth and development, this work highlights one way that the microbiota can influence adaptation in their animal hosts. These findings also provide evidence that low-fidelity, horizontally-acquired microbes can exert selective pressures strong enough to shape host life history traits. These insights underscore the microbiotas role as an ecological and evolutionary force.

microbiology↗

Seasonal evolution of Drosophila melanogaster abdominal pigmentation is associated with a multifarious selective landscape

Pigmentation has been widely studied by evolutionary biologists due to both ease of measure and relationship to fitness. Drosophila melanogaster pigmentation has represented a particularly useful avenue of investigation, as extensive genetic tools have enabled the characterization of the traits complex architecture. Drosophila pigmentation also varies predictably across space and time in wild populations, suggesting pigmentation is a component of adaptation to local environmental conditions. Despite this, the impact of D. melanogaster pigmentation on fitness, and the environmental factors that drive the evolution of pigmentation, are not well understood. To address this gap, we experimentally evolved replicated D. melanogaster populations in field mesocosms to determine whether and how pigmentation evolves in response to environmental variation. We found that pigmentation rapidly and predictably adapted to a direct manipulation of temperature, supportive of melanization playing a role in thermoregulation. However, we also determined that pigmentation responded adaptively to direct manipulations of numerous additional factors, including intraspecific competition, diet, and the microbiome. These findings suggest that the selective landscape acting on pigmentation is complex and multifaceted, and that patterns of melanization may be driven, at least in part, by indirect selection due to correlations with other fitness-related traits.

evolutionary biology↗

Variation in Resource Environment Drives Adaptive Divergence in Drosophila melanogaster

Natural populations often experience heterogeneity in the quality and abundance of environmentally acquired resources across both space and time, and this variation can influence population demographics and evolutionary dynamics. In this study, we directly manipulated diet in replicate populations of Drosophila melanogaster cultured in experimental mesocosms in the field. We found no significant effect of resource variation on demographic patterns. Furthermore, while resource variation altered the patterns of phenotypic and genomic evolution, this effect is secondary to population responses to seasonally fluctuating selective pressures. Seasonal adaptation was observed for all traits assayed and elicited genome-wide signatures of selection; in contrast, adaptation to the resource environment was trait-specific and exhibited an oligogenic architecture. This illustrates the capacity of populations to adapt to a specific axis of variation (the resource environment) without hindering the adaptive response to seasonal change. This in turn, suggests that resource variation may be an important force driving fluctuating selection across natural populations, ultimately contributing to the maintenance of genetic and phenotypic variation.

evolutionary biology↗