A cosmopolitan inversion facilitates seasonal adaptation in overwintering <i>Drosophila</i>

In many species, polymorphic genomic inversions underlie complex phenotypic polymorphisms and facilitate local adaptation in the face of gene flow. Multiple polymorphic inversions can co-occur in a genome, but the prevalence, evolutionary significance, and limits to complexity of genomic inversion landscapes remain poorly understood. Here, we examine genome-wide genetic variation in one of Europe's most destructive forest pests, the spruce bark beetle Ips typographus, scan for polymorphic inversions, and test whether inversions are associated with key traits in this species. We analyzed 240 individuals from 18 populations across the species’ European range and, using a whole-genome resequencing approach, identified 27 polymorphic inversions covering approximately 28% of the genome. The inversions vary in size and in levels of intra-inversion recombination, are highly polymorphic across the species range, and often overlap, forming a complex genomic architecture. We found no support for mechanisms such as directional selection, overdominance and associative overdominance that are often invoked to explain the presence of large inversion polymorphisms in the genome. This suggests that inversions are either neutral or maintained by the combined action of multiple evolutionary forces. We also found that inversions are enriched in odorant receptor genes encoding elements of recognition pathways for host plants, mates, and symbiotic fungi. Our results indicate that the genome of this major forest pest of growing social, political, and economic importance harbors one of the most complex inversion landscapes described to date and raise questions about the limits of intraspecific genomic architecture complexity.

show abstract

Drosophila melanogasterpigmentation demonstrates adaptive phenotypic parallelism but genomic unpredictability over multiple timescales

Berardi,

Rhodes,

Berner

et al. 2024

Preprint

View full text Add to dashboard Cite

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 inDrosophila melanogasteras a model phenotype to address the nature, genetic architecture, and repeatability of rapid adaptation in the field. We show thatD. melanogasterpigmentation 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 ten 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 an unpredictable genomic response, with distinct components of the polygenic architecture shifting across each environmental gradient to produce redundant adaptive patterns.Significance StatementShifts in global climate conditions have heightened our need to understand the dynamics and pace of adaptation in natural populations. In order to anticipate the population-level response to rapidly changing environmental conditions, we need to understand whether trait evolution is predictable over short timescales, and whether the genetic basis of adaptation is shared or distinct across multiple timescales. Here, we explored parallelism in the adaptive response of a complex phenotype,D. melanogasterpigmentation, to shared conditions that varied over multiple spatiotemporal scales. Our results demonstrate that while phenotypic adaptation proceeds as a predictable response to environmental gradients, even over short timescales, the genetic basis of the adaptive response is variable and nuanced across spatial and temporal contexts.

show abstract

A cosmopolitan inversion facilitates seasonal adaptation in overwintering Drosophila

Cited by 6 publications

References 136 publications

Acceleration of Drosophila subobscura evolutionary response to global warming in Europe

Acceleration of Drosophila subobscura evolutionary response to global warming in Europe

Complex Genomic Landscape of Inversion Polymorphism in Europe's Most Destructive Forest Pest

Drosophila melanogasterpigmentation demonstrates adaptive phenotypic parallelism but genomic unpredictability over multiple timescales

Contact Info

Product

Resources

About