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Poikela, N.

Publications and source records attributed to Poikela, N..

6 recordsLinked to original sources

Adaptive introgression improves heat-tolerance despite barriers to gene flow: a case study in Drosophila flavomontana and Drosophila montana

As global temperatures rise and heat waves become more frequent, populations must adapt rapidly to avoid local extinctions. Adaptive introgression allows species to quickly acquire adaptive genetic material from close relatives. However, certain genomic regions, containing barrier loci, may resist introgression. We experimentally tested whether strong heat stress selection can overcome such barriers and facilitate the transfer of adaptive alleles to improve heat tolerance. We also examined whether chromosomal inversions, which can tightly link adaptive and barrier loci through reduced recombination, promote or prevent introgression. We conducted a hybridize, evolve, and re-sequence experiment by crossing the heat-sensitive D. flavomontana with the more heat-tolerant D. montana, exposing heat-selection lines to transient heat for three generations while maintaining control lines. We also mapped long-term barriers to gene flow between natural populations using a demographically explicit genome scan. The heat-selection lines exhibited approximately twice the introgression and higher male fertility under heat stress compared to control lines and the heat-sensitive parental D. flavomontana. This introgression was primarily located in colinear autosomal regions and correlated with improved heat tolerance. Some introgression occurred also in inverted autosomal regions in the heat-selection lines but not in the control lines. The X chromosome, with three overlapping inversions, resisted introgression in both heat-selection and control lines, thereby maintaining a strong species barrier. Finally, genetic barriers in the control lines significantly overlapped with long-term barriers, but this overlap was less pronounced in the heat-selection lines. Our study demonstrates that strong selection can lead to adaptive introgression despite long-standing genetic barriers. These findings highlight that introgression can serve as a rapid source of adaptive genetic material under stressful thermal conditions, potentially mitigating climate-induced population extinctions.

evolutionary biology↗

A chromosomal inversion accumulates adaptive and barrier loci in a cold-adapted insect species

Chromosomal inversions can play a crucial role in population adaptation and divergence by reducing gene flow and preserving adaptive allelic combinations between populations with different arrangements. However, demonstrating this empirically is challenging due to numerous interacting processes with similar genomic signatures affecting inversion evolution. In this study, we characterized a large (9.5Mb) polymorphic inversion in the cold-adapted and widely distributed species, Drosophila montana, using long- and short-read sequencing across several populations. The origin of this inversion predates the divergence of North American (NA) and Fennoscandian (North European) populations, suggesting it emerged in the ancestral D. montana population in the Rocky Mountains of NA. Despite the species expansion across the northern hemisphere, this inversion has remained exclusive to the Rocky Mountains populations, where it is fixed in the southernmost high-elevation population and appears at lower frequencies in the more northern and lower-elevation populations. By independently mapping SNPs linked to climate adaptation and barriers to gene flow (barrier loci; identified through reduced migration rates), we found enrichment of both within the inversion, with barrier and adaptive regions partially overlapping. However, the inversion was not enriched for SNPs related to cold tolerance. These findings suggest that inversions may maintain associations between multiple adaptive and barrier loci, effectively coupling them, and that locally adaptive regions may act as barriers to gene flow. Our study provides empirical evidence that inversions can contribute to population adaptation and divergence by reducing gene flow, maintaining adaptive allelic combinations, and facilitating the coupling of different barriers to gene flow. SignificanceChromosomal inversions, genomic rearrangements with reversed gene order, are important drivers of population adaptation and divergence, but demonstrating this empirically is challenging due to complex interacting processes that produce similar genomic signatures. We characterized and analysed a large polymorphic inversion in Drosophila montana, a cold-adapted and widely distributed insect, using whole-genome sequencing data, phenotypic experiments, and recent methodological developments. This inversion is found only in mountain populations and is enriched with SNPs potentially associated with climate adaptation, as well as regions that act as barriers to gene flow, with these regions partially overlapping. These results suggest that adaptive loci can act as barriers to gene flow and that inversions help maintain adaptive allelic combinations and associations between multiple barrier loci, thereby contributing to population adaptation and divergence.

evolutionary biology↗

Genomic incompatibilities are persistent barriers when speciation happens with gene flow in Formica ants

A current goal of speciation research is to identify the loci underlying reproductive barriers between species. Locating such barrier loci in empirical data is difficult due to the often complex demographic history of diverged taxa and the heterogeneity in evolutionary forces across the genome. Here we take advantage of a natural case of hybridization between two wood ant species (Formica aquilonia and F. polyctena) to identify regions of reduced long-term gene flow using demographically explicit scans of non-admixed genomes. In addition we identify candidate Bateson-Dobzhansky-Muller incompatibilities (BDMIs) through an imbalanced recombinant haplotype frequency analysis of natural F. aquilonia x F. polyctena hybrid genomes. Both approaches find barriers that are scattered across the genome. Furthermore, candidate BDMIs significantly overlap with the long-term barriers identified by gIMble, indicating that incompatibilities have persisted despite divergence with gene flow between the wood ant species. Intriguingly, BDMIs interact in a network and the number of pairwise interactions a BDMI has correlates with its long-term barrier strength: hub-like BDMIs with many pairwise interactions reduce gene flow more effectively. Finally in regards to function, long-term barriers identified by gIMble arise outside regions of both gene coding sequences (CDS) and transposable elements. In contrast, regions where long-term barriers and BDMIs co-locate are significantly associated with introns, implying a potential role of alternative splicing or gene regulation in incompatibilities, rather than CDS divergence. Overall, our results highlight the underappreciated impact of multilocus BDMIs and the need to consider network connectivity of BDMIs in future work. SignificanceDetecting barrier loci that reduce gene flow between closely related species is a common goal of speciation research. However, reliable detection of barrier loci is difficult due to confounding signals in genomic data. Here we take advantage of two different, recently developed approaches and find that barrier loci between wood ant species are scattered across the genome, and despite on-going gene flow, maintain two distinct species. We reveal that genomic regions that are incompatible between the two species can act as persistent barriers, despite theoretical predictions for their collapse under gene flow. Connectivity between incompatibilities also seems to play an important role in barrier persistence. These results highlight the need to consider connectivity between barrier loci in future speciation research.

evolutionary biology↗

Transposable elements in a cold-tolerant fly species, Drosophila montana: a link to adaptation to the harsh cold environments

BackgroundSubstantial discoveries during the past century have revealed that transposable elements (TEs) can play a crucial role in genome evolution by affecting gene expression and inducing genetic rearrangements, among other molecular and structural effects. Yet, our knowledge on the role of TEs in adaptation to extreme climates is still at its infancy. The availability of long-read sequencing has opened up the possibility to identify and study potential functional effects of TEs with higher precision. In this work, we used Drosophila montana as a model for cold-adapted organisms to study the association between TEs and adaptation to harsh climates. ResultsUsing the PacBio long-read sequencing technique, we de novo identified and manually curated TE sequences in five Drosophila montana genomes from eco-geographical distinct populations. We identified 489 new TE consensus sequences which represented 92% of the total TE consensus in D. montana. Overall, 11-13% of the D. montana genome is occupied by TEs, which as expected are non-randomly distributed across the genome. We identified five potentially active TE families, most of them from the retrotransposon class of TEs. Additionally, we found TEs present in the five analyzed genomes that were located nearby previously identified cold tolerant genes. Some of these TEs contain promoter elements and transcription binding sites. Finally, we detected TEs nearby fixed and polymorphic inversion breakpoints. ConclusionsOur research revealed a significant number of newly identified TE consensus sequences in the genome of D. montana, suggesting that non-model species should be studied to get a comprehensive view of the TE repertoire in Drosophila species and beyond. Genome annotations with the new D. montana library allowed us to identify TEs located nearby cold tolerant genes, and present at high population frequencies, that contain regulatory regions and are thus good candidates to play a role in D. montana cold stress response. Finally, our annotations also allow us to identify for the first time TEs present in the breakpoints of three D. montana inversions.

genomics↗

Latitudinal variation in cold tolerance and the role of vrille and vitellogenin in enhancing cold adaptation in highly cold-tolerant insect species

BackgroundTracing the association between insect cold tolerance and latitudinally and locally varying environmental conditions, as well as key morphological traits and molecular mechanisms, is essential for understanding the processes involved in adaptation. We explored these issues in two closely-related species, Drosophila montana and Drosophila flavomontana, originating from diverse climatic locations across several latitudes on the coastal and mountainous regions of North America. We also investigated the association between sequence variation in one of the key circadian clock genes, vrille, and cold tolerance in both species. Finally, we studied the impact of vrille on fly cold tolerance and cold acclimation ability by silencing it with RNA interference in D. montana. ResultsWe performed a principal component analysis (PCA) on variables representing bioclimatic conditions on the study sites and used latitude as a proxy of photoperiod. PC1 separated the mountainous continental sites from the coastal ones based on temperature variability and precipitation, while PC2 arranged the sites based on summer and annual mean temperatures. Cold tolerance tests showed D. montana to be more cold-tolerant than D. flavomontana and chill coma resistance (CTmin) of this species showed an association with PC2. Chill coma recovery time (CCRT) of both species improved towards northern latitudes, and in D. flavomontana this trait was also associated with PC1. D. flavomontana flies were darkest in the coast and in the northern mountainous populations, but coloration showed no linkage with cold tolerance. Body size decreased towards cold environments in both species, but only within D. montana populations largest flies showed fastest recovery from cold. Finally, both the sequence analysis and RNAi study on vrille suggested this gene to play an essential role in D. montana cold resistance and acclimation, but not in recovery time. ConclusionsOur study demonstrates the complexity of insect cold tolerance and emphasizes the need to trace its association with multiple environmental variables and morphological traits to identify potential agents of natural selection. It also shows that a circadian clock gene vrille is essential both for short- and long-term cold acclimation, potentially elucidating the connection between circadian clock system and cold tolerance.

evolutionary biology↗

Reinforcement targets sexual or postmating prezygotic reproductive barriers depending on species abundance and population history

The impact of different reproductive barriers on species or population isolation may vary in different stages of speciation depending on evolutionary forces acting within species and through species interactions. Genetic incompatibilities between interacting species are expected to reinforce prezygotic barriers in sympatric populations and create character displacement between conspecific populations living within and outside the area of sympatry. The outcome of reinforcement has been suggested to be affected by the strength of postzygotic barriers, the history of species coexistence, and the impact of species abundancies on females discrimination against heterospecific males. We tested these predictions in Drosophila montana and Drosophila flavomontana populations from different geographic regimes. All barriers between D. montana females and D. flavomontana males were extremely strong, while in the reciprocal cross postzygotic isolation was less effective and the target of reinforcement varied according to population type. In long-established sympatric populations, where D. flavomontana is abundant, reinforcement targeted sexual isolation, and in populations, where this species is a new invader and rare, reinforcement targeted postmating prezygotic barriers. Reinforcement of these barriers also created respective barriers between different D. flavomontana populations. These findings show that interspecies interactions have far-reaching effects on strengthening species barriers and promoting speciation.

evolutionary biology↗