Yılmaz, V. M. | Search bioRxiv

bioRxiv2025

Dissecting Cold Tolerance in Drosophila ananassae: A Multi-Phenotypic and Bulk Segregant Analysis

As a major element of the environment, temperature impacts the geographical ranges of insects. Therefore, the worldwide distribution of insects follows adaptation to wide ranges of temperature. A population of Drosophila ananassae from the ancestral region showed variation in cold tolerance levels. The ancestral Bangkok population also differed from the derived Kathmandu population regarding cold tolerance. However, the phenotypic variation was only measured by chill coma assays, and no further characterization of the cold tolerance phenotype was performed. Here, we aimed to further characterize the iso-female lines of Bangkok and Kathmandu populations and the recombinant inbred lines generated from the ancestral population using lethal time and cold shock mortality in addition to chill coma recovery time. We showed that cold tolerance phenotypes differ between sexes, the additional phenotypes do not correlate significantly to chill coma recovery time, and some recombinant inbred lines have extreme phenotypes with higher tolerance than the tolerant founder or lower tolerance than the sensitive founder. We performed bulk segregant analysis using the recombinant inbred lines that exhibited extreme chill coma recovery time to identify genomic regions responsible for the phenotype. We identified 16 regions with significant association with the phenotype and showed that the genes in the putative regions were enriched in muscle development, metabolic processes, and cytoskeletal protein binding. Our results provide further evidence for the need for multiple cold tolerance phenotypes and shed light on the genetic architecture of adaptive phenotypic changes in natural populations of Drosophila.

evolutionary biology↗

bioRxiv2024

Navigating the Cold: Integrative Transcriptome Sequencing Approach Reveals Ionoregulatory and Whole-Body Responses to Cold Acclimation in Drosophila ananassae

Understanding how species adapt to changing environments is a major goal in evolutionary biology and can elucidate the impact of climate change. Climate imposes inevitable effects on the geographical distribution of insects as their body temperature primarily depends on the environment. The vinegar fly Drosophila ananassae expanded from its tropical ancestral range to more temperate regions, which requires adaptation to colder temperatures. Transcriptome and genome-wide association studies focusing on the ancestral-range population identified the targets of selection related to ionoregulatory tissues. However, how cosmopolitan D. ananassae adapted to colder environments, where low temperatures last longer, is still unknown. Here, we present a study on the effect of long-term cold exposure on D. ananassae, examining the gene expression variation in the whole body and the ionoregulatory tissues, namely the hindgut and the Malpighian tubule. To elucidate molecular mechanisms of cold adaptation during species expansion, we included cold-tolerant and cold-sensitive strains from the ancestral species range and cold-tolerant strains from the derived species range. We show that cold acclimation improves cold tolerance and results in differential expression of more than half of the transcriptome in the ionoregulatory tissues and the whole body. Notably, we provide complementary insight into molecular processes at four levels: strains, populations, phenotypes, and tissues. By determining the biochemical pathways of phenotypic plasticity underlying cold tolerance, our results enhance our understanding of how environmental changes affect thermal adaptation in natural populations. SignificanceThe physiological mechanisms underlying cold tolerance of insects are complex. Our study integrates tissue-specific responses with whole-body response to cold and compares these responses in different populations, phenotypes, and strains of the vinegar fly Drosophila ananassae. The study reveals that the response to extended cold in the renal and intestinal tissues are different, that the tissue-specific responses can be masked in the whole body, and that the transcriptomic response to extended cold can depend on population of origin, cold tolerance phenotype, or strain. Overall, this study sheds light on insect cold adaptation in terms of transcriptomic response to cold acclimation in the ionoregulatory tissues and whole bodies.

evolutionary biology↗