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

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.

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Limited population structure but signals of recent selection in introduced African Fig Fly(Zaprionus indianus) in North America

Erickson,

Bangerter,

Gunter

et al. 2024

Preprint

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Invasive species have devastating consequences for human health, food security, and the environment. Many invasive species adapt to new ecological niches following invasion, but little is known about the early steps of adaptation. Here we examine population genomics of a recently introduced drosophilid in North America, the African Fig Fly, Zaprionus indianus. This species is likely intolerant of subfreezing temperatures and recolonizes temperate environments yearly. We generated a new chromosome-level genome assembly for Z. indianus. Using resequencing of over 200 North American individuals collected over four years in temperate Virginia, plus a single collection from subtropical Florida, we tested for signatures of recolonization, population structure, and adaptation within invasive populations. We show founding populations are sometimes small and contain close genetic relatives, yet temporal population structure and differentiation of populations is mostly absent across recurrent recolonization events. Although we find limited signals of genome-wide spatial or temporal population structure, we identify haplotypes on the X chromosome that are repeatedly differentiated between Virginia and Florida populations. These haplotypes show signatures of natural selection and are not found in African populations. We also find evidence for several large structural polymorphisms segregating within North America populations and show X chromosome evolution in invasive populations is strikingly different from the autosomes. These results show that despite limited population structure, populations may rapidly evolve genetic differences early in an invasion. Further uncovering how these genomic regions influence invasive potential and success in new environments will advance our understanding of how organisms evolve in changing environments.

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A cosmopolitan inversion facilitates seasonal adaptation in overwintering Drosophila

Cited by 3 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

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

Limited population structure but signals of recent selection in introduced African Fig Fly(Zaprionus indianus) in North America

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