Haplotype-resolved chromosome-level genome assemblies of four Diamesa species reveal the genetic basis of cold tolerance and high-altitude adaptations in arctic chironomids
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Abstract
Arctic and alpine insects face extreme environmental stressors, yet the genomic basis of their adaptation remains poorly understood. Here, we present the first haplotype-resolved, chromosome-level genomes for four species of Diamesa (Diptera: Chironomidae), a genus of cold-adapted midges inhabiting glacial and high-altitude freshwater ecosystems. Using PacBio HiFi sequencing and Hi-C scaffolding, we assembled high-quality genomes with chromosome-level resolution and high k-mer completeness. Phylogenomic analyses support Diamesinae as sister to other Chironomidae except Podonominae, and genomic comparisons provide evidence for introgression between the evolutionary distinct D. hyperborea and D. tonsa . Comparative genomic analyses across 20 Diptera species revealed significant gene family contractions in Diamesa associated with oxygen transport and metabolism, suggesting adaptations to high-altitude, low-oxygen environments. Conversely, expansions were detected in histone-related and Toll-like receptor gene families, likely enhancing chromatin remodeling and immune regulation under cold stress. A single gene family encoding glucose dehydrogenase was significantly expanded across all cold-adapted species studied, implicating its role in cryoprotectant synthesis and oxidative stress mitigation. Notably, Diamesa species exhibit the largest gene family contraction at any node, with minimal overlap in expansions with other cold-adapted Diptera, indicating lineage-specific adaptation. Our findings support the hypothesis that genome size condensation and selective gene family changes underpin survival in cold environments. These genome assemblies represent a valuable resource for investigating adaptation, speciation, and conservation in cold-specialist insects. Future work integrating gene expression and population genomics will further illuminate the evolutionary resilience of Diamesa in a warming world.
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ABSTRACTArctic and alpine insects face extreme environmental stressors, yet the genomic basis of their adaptation remains poorly understood. Here, we present the first haplotype-resolved, chromosome-level genomes for four species of Diamesa (Diptera: Chironomidae), a genus of cold-adapted midges inhabiting glacial and high-altitude freshwater ecosystems. Using PacBio HiFi sequencing and Hi-C scaffolding, we assembled high-quality genomes with chromosome-level resolution and high k-mer completeness. Phylogenomic analyses support Diamesinae as sister to other Chironomidae except Podonominae, and genomic comparisons provide evidence for introgression between the evolutionary distinct D. hyperborea and D. tonsa. Comparative genomic analyses across 20 Diptera species revealed significant gene family contractions in Diamesa associated with …
ABSTRACTArctic and alpine insects face extreme environmental stressors, yet the genomic basis of their adaptation remains poorly understood. Here, we present the first haplotype-resolved, chromosome-level genomes for four species of Diamesa (Diptera: Chironomidae), a genus of cold-adapted midges inhabiting glacial and high-altitude freshwater ecosystems. Using PacBio HiFi sequencing and Hi-C scaffolding, we assembled high-quality genomes with chromosome-level resolution and high k-mer completeness. Phylogenomic analyses support Diamesinae as sister to other Chironomidae except Podonominae, and genomic comparisons provide evidence for introgression between the evolutionary distinct D. hyperborea and D. tonsa. Comparative genomic analyses across 20 Diptera species revealed significant gene family contractions in Diamesa associated with oxygen transport and metabolism, suggesting adaptations to high-altitude, low-oxygen environments. Conversely, expansions were detected in histone-related and Toll-like receptor gene families, likely enhancing chromatin remodeling and immune regulation under cold stress. A single gene family encoding glucose dehydrogenase was significantly expanded across all cold-adapted species studied, implicating its role in cryoprotectant synthesis and oxidative stress mitigation. Notably, Diamesa species exhibit the largest gene family contraction at any node, with minimal overlap in expansions with other cold-adapted Diptera, indicating lineage-specific adaptation. Our findings support the hypothesis that genome size condensation and selective gene family changes underpin survival in cold environments. These genome assemblies represent a valuable resource for investigating adaptation, speciation, and conservation in cold-specialist insects. Future work integrating gene expression and population genomics will further illuminate the evolutionary resilience of Diamesa in a warming world.Competing Interest StatementThe authors have declared no competing interest.Footnotes↵# Indicates shared senior authorshipFunder Information DeclaredThe Research Council of Norway, https://ror.org/00epmv149, 326819, 270068
This work has been peer reviewed in GigaScience (see https://doi.org/10.1093/gigascience/giaf160), which carries out open, named peer-review. These reviews are published under a CC-BY 4.0 license and were as follows:
Reviewer 2: Chao Bian
This paper, entitled 'Haplotype-resolved chromosome-level genome assemblies of four Diamesa species reveal the genetic basis of cold tolerance and high-altitude adaptations in arctic chironomids', provided four chromosome-level genomes of Diamesa by using PCABIO HIFI. Phylogenetics and gene families were identified in this study.
However, I strongly suggest authors to show then expansion result by using some figures. Only expansion introduction is too weak.
The genome size condensation is also limited and have no sufficient evidence.
Some suggestions: The format of the abstract should be largely revised.
Line 35-37, this sentence is too heavy to understanding, split it to be clearer.
Line 123-126, the cycle for temperature profile can be removed. I think no need to introduce this too detailed.
Line 147, "Prior" should be 'prior'.
Please add the "RRID" and version for the used software.
Line 191, 'samtools' should be 'SAMtools'.
The detailed parameters also need to be shown.
For the table 2, this table is bit in disorder. Please move the Hifi read covergage, Hic read coverage and Consensus quanlity, Kmer both, heterozygosity to half bottom of this table.
Line 327, 337, Align subheadings to the left margin. Do not indent.
Line 338, 'between' revised to 'among'.
I suggested the authors to initial a figure to show the expansion of Glucose dehydrogenase.
Line 359, 1066 should be '1,066'.
For the data records, where did the sequenced deposited? There was no NCBI project ID in this study.
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ABSTRACTArctic and alpine insects face extreme environmental stressors, yet the genomic basis of their adaptation remains poorly understood. Here, we present the first haplotype-resolved, chromosome-level genomes for four species of Diamesa (Diptera: Chironomidae), a genus of cold-adapted midges inhabiting glacial and high-altitude freshwater ecosystems. Using PacBio HiFi sequencing and Hi-C scaffolding, we assembled high-quality genomes with chromosome-level resolution and high k-mer completeness. Phylogenomic analyses support Diamesinae as sister to other Chironomidae except Podonominae, and genomic comparisons provide evidence for introgression between the evolutionary distinct D. hyperborea and D. tonsa. Comparative genomic analyses across 20 Diptera species revealed significant gene family contractions in Diamesa associated with …
ABSTRACTArctic and alpine insects face extreme environmental stressors, yet the genomic basis of their adaptation remains poorly understood. Here, we present the first haplotype-resolved, chromosome-level genomes for four species of Diamesa (Diptera: Chironomidae), a genus of cold-adapted midges inhabiting glacial and high-altitude freshwater ecosystems. Using PacBio HiFi sequencing and Hi-C scaffolding, we assembled high-quality genomes with chromosome-level resolution and high k-mer completeness. Phylogenomic analyses support Diamesinae as sister to other Chironomidae except Podonominae, and genomic comparisons provide evidence for introgression between the evolutionary distinct D. hyperborea and D. tonsa. Comparative genomic analyses across 20 Diptera species revealed significant gene family contractions in Diamesa associated with oxygen transport and metabolism, suggesting adaptations to high-altitude, low-oxygen environments. Conversely, expansions were detected in histone-related and Toll-like receptor gene families, likely enhancing chromatin remodeling and immune regulation under cold stress. A single gene family encoding glucose dehydrogenase was significantly expanded across all cold-adapted species studied, implicating its role in cryoprotectant synthesis and oxidative stress mitigation. Notably, Diamesa species exhibit the largest gene family contraction at any node, with minimal overlap in expansions with other cold-adapted Diptera, indicating lineage-specific adaptation. Our findings support the hypothesis that genome size condensation and selective gene family changes underpin survival in cold environments. These genome assemblies represent a valuable resource for investigating adaptation, speciation, and conservation in cold-specialist insects. Future work integrating gene expression and population genomics will further illuminate the evolutionary resilience of Diamesa in a warming world.Competing Interest StatementThe authors have declared no competing interest.Footnotes↵# Indicates shared senior authorshipFunder Information DeclaredThe Research Council of Norway, https://ror.org/00epmv149, 326819, 270068
This work has been peer reviewed in GigaScience (see https://doi.org/10.1093/gigascience/giaf160), which carries out open, named peer-review. These reviews are published under a CC-BY 4.0 license and were as follows:
Reviewer 1: shijun xiao
Using the first haplotype resolved, chromosome-level genomes for four species of Diamesa, authors provide a valuable resource for investigating adaptation, speciation, and conservation in cold-specialist insects and they analyized the genomic reason, including significant gene family contractions and expansions, for their cold environment adaptations. It effectively highlights the ecological importance of Diamesa midges and the novelty of generating haplotype-resolved, chromosome-level genomes, providing a strong rationale for the study. I think the manuscript could be accepted after authors address the following minor issues: 1．The QV values in Table 2 were evaluated using Hi-C data. Could you clarify the rationale for this approach? In general, Hi-C data are not suitable for assessing genome quality; instead, whole-genome short reads are more appropriate for such evaluations. The relatively low QV value of 20 might be due to the use of Hi-C data, as high-quality short-read evaluations typically yield QV values around 30. If short-read data are available, I recommend re-evaluating the genome quality with Merqury using those reads. If short reads are not available, please provide a reasonable justification for the use of Hi-C data, or retain only the QV evaluation based on HiFi read alignments. 2．The title of the manuscript mentions that the genome assemblies are at the chromosome level, and the Conclusions section also refers to chromosome numbers. It would be helpful to include the number of chromosomes in Table 2, which would provide a more intuitive representation of chromosome features and highlight differences among the species. 3．Based on Supplementary Figure 2 and Table 2, it can be observed that the haplotype carrying the fourth scaffold has a slightly larger genome size and more protein-coding genes than the other haplotype, although the difference is not very pronounced. Could the authors clarify whether this is due to a biological feature of Diamesinae species or a consequence of the assembly process? 4．In addition, BUSCO results are only reported as overall completeness, without distinguishing between single-copy and duplicated genes. It would be helpful to provide this information, as it would give a more complete picture of genome quality and potential assembly artifacts.
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