Exploring polymorphic interspecies structural variants in Eucalyptus: Unravelling Their Role in Reproductive Isolation and Adaptive Divergence
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Abstract
Structural variants (SVs) play a significant role in speciation and adaptation in many species, yet few studies have explored the prevalence and impact of different categories of SVs. We conducted a comparative analysis of long-read assembled reference genomes of closely related Eucalyptus species to identify candidate SVs potentially influencing speciation and adaptation. Interspecies SVs can be either fixed differences, or polymorphic in one or both species. To describe SV patterns, we employed short-read whole-genome sequencing on over 600 individuals of E. melliodora and E. sideroxylon , along with recent high quality genome assemblies. We aligned reads and genotyped interspecies SVs predicted between species reference genomes. Our results revealed that 49,756 of 58,025 and 39,536 of 47,064 interspecies SVs could be typed with short reads, in E. melliodora and E. sideroxylon respectively. Focusing on inversions and translocations, symmetric SVs which are readily genotyped within both populations, 24 were found to be structural divergences, 2,623 structural polymorphisms, and 928 shared structural polymorphisms. We assessed the functional significance of fixed interspecies SVs by examining differences in estimated recombination rates and genetic differentiation between species, revealing a complex history of natural selection. Shared structural polymorphisms displayed enrichment of potentially adaptive genes. Understanding how different classes of genetic mutations contribute to genetic diversity and reproductive barriers is essential for understanding how organisms enhance fitness, adapt to changing environments, and diversify. Our findings reveal the prevalence of interspecies SVs and elucidate their role in genetic differentiation, adaptive evolution, and species divergence within and between populations.
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respectively. Focusing on inversions and translocations, symmetric SVs which are readily genotyped within both populations, 24 were found to be structural divergences, 2,623 structural polymorphisms, and 928 shared structural polymorphisms. We assessed the functional significance of fixed interspecies SVs by examining differences in estimated recombination rates and genetic differentiation between species, revealing a complex history of natural selection. Shared structural polymorphisms displayed enrichment of potentially adaptive genes.
Reviewer 2: Lejun Ouyang Structural variation plays an important role in the domestication and adaptability of species. The author compared the structural variation between E. melliodora and E. sideroxylon populations. This is a very interesting study, but it feels that the author is just statistical …
respectively. Focusing on inversions and translocations, symmetric SVs which are readily genotyped within both populations, 24 were found to be structural divergences, 2,623 structural polymorphisms, and 928 shared structural polymorphisms. We assessed the functional significance of fixed interspecies SVs by examining differences in estimated recombination rates and genetic differentiation between species, revealing a complex history of natural selection. Shared structural polymorphisms displayed enrichment of potentially adaptive genes.
Reviewer 2: Lejun Ouyang Structural variation plays an important role in the domestication and adaptability of species. The author compared the structural variation between E. melliodora and E. sideroxylon populations. This is a very interesting study, but it feels that the author is just statistical data. However, the biological problems caused by these differences have not been condensed, such as the impact of structural variation on recombination. What effect does it have on the differentiation of the two populations? Is it promoting or inhibiting? Secondly, the author's writing is not very clear, and some of the results are described too simply, resulting in unclear conclusions. When formatting pictures, try to avoid nesting pictures, and use A, B, C, etc. to represent them. However, some obvious issues, but not limited, are listed above. Here are other minor issues:
- Lines 62-64: References are required.
- Lines 145-150: It is recommended to put it in the materials and methods section.
- The Synteny and structural variation annotation section requires a detailed explanation of the results in Figure 2 and Table 2.
- It is recommended to make Table 2 into a picture, the effect will be better.
- The form should be a three-line grid.
- Why does the recombination rate in Table 3 have positive and negative errors at the genome level, but only negative errors at the chromosome average level?
- 219-220 It is recommended that methods not appear in the results section. It is recommended to put it in the methods section.
- The Structural variation genotyping in the results section needs to be modified.
- Figure 6 is a bit confusing. It is recommended to revise it to make it clearer.
- The results section of Figure 7 is not clearly described and the notes are not clear. What do the different colors represent?
- Lines 263-264: It is recommended that methods should not appear in the results section, but can be placed in the materials and methods section.
- It is recommended that Figure 8 be divided into Figure 8A and Figure 8B. Try not to have pictures within pictures, which can easily lead to unclear references.
- Lines 276-281: It is recommended to put it in the method section.
- Lines 289-290: It is recommended to put it in the method section.
- Lines 307-308: E. melliodora and E. sideroxylon italics
- Lines 311-318, lines 320-321: It is recommended to put them in the method section.
- Lines 338-339: E. melliodora and E. sideroxylon italics.
- Line 342: It is recommended to put it in the discussion.
- It is recommended to change Figure 9B, Figure 10B and Figure 11B to Figure
- Line 561: Add references.
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Structural variants (SVs) play a significant role in speciation and adaptation in many species, yet few studies have explored the prevalence and impact of different categories of SVs. We conducted a comparative analysis of long-read assembled reference genomes of closely related Eucalyptus species to identify candidate SVs potentially influencing speciation and adaptation. Interspecies SVs can be either fixed differences, or polymorphic in one or both species. To describe SV patterns, we employed short-read whole-genome sequencing on over 600 individuals of E. melliodora and E. sideroxylon, along with recent high quality genome assemblies. We aligned reads and genotyped interspecies SVs predicted between species reference genomes. Our results revealed that 49,756 of 58,025 and 39,536 of 47,064 interspecies SVs could be typed with short …
Structural variants (SVs) play a significant role in speciation and adaptation in many species, yet few studies have explored the prevalence and impact of different categories of SVs. We conducted a comparative analysis of long-read assembled reference genomes of closely related Eucalyptus species to identify candidate SVs potentially influencing speciation and adaptation. Interspecies SVs can be either fixed differences, or polymorphic in one or both species. To describe SV patterns, we employed short-read whole-genome sequencing on over 600 individuals of E. melliodora and E. sideroxylon, along with recent high quality genome assemblies. We aligned reads and genotyped interspecies SVs predicted between species reference genomes. Our results revealed that 49,756 of 58,025 and 39,536 of 47,064 interspecies SVs could be typed with short reads, in E. melliodora and E. sideroxylon
Reviewer 1: Jakob Butler Ferguson et al have performed a thorough analysis of two species of Eucalyptus, quantifying the extent of structural variation between assembled genomes of the species and determining how prevalent those variations are across a selection of wild material. I believe this study is of sufficient quality for publication in GigaScience, if some minor inconsistencies and grammatical issues are addressed, and a few supporting analyses are performed. The major changes I would like to see include the addition of a syri plot of the complete set of SVs between E. melliodora and E. sideroxylon. I believe this, along with correcting the scale on the plots of recombination in Figure S6/S7 would allow for a better comparison of how recombination rate is interacting with the SVs. I would also suggest a more formal test of enrichment for COG terms, to better support the statements of "enrichment" in the discussion. Suggested changes by line: Line 142 - This section is quite short, I would either merge this section into the Genome scaffolding (and annotation) section, or expand on the results of the gene annotation. Line 182 - (Supplementary Figure S4) Line 183 (and throughout) - Please be consistent with your references to tables and figures. Line 186 - delete comma after 28.63% Line 194 - These are density plots rather than histograms Figure 4 - Both axes are labelled as PC1 Line 217 (page 10, line numbers are doubled up) - This seems repetitive, perhaps "…especially as they may also represent divergent sequences". Line 221 (page 11) - Please insert "and" before polymorphic translocations Line 223 - You have stated that those not successfully genotyped in both species are private or artefacts earlier in the paragraph, please reduce the repetition. Figure 6 - I don't find this figure particularly informative (and somewhat confusing to interpret). I think showing the percentages of each different SV in a visual form implies a level of equivalence in genomic impact, which is difficult to reconcile with the raw difference in numbers. I think a supplemental table with the focus on the percentages would illustrate the point better. Line 246 - There is no mention in the methods about what r threshold was used to declare a pair "correlated", please state it here or in the methods. Line 265 - This line was confusing to interpret. A suggested alteration: "significant value. After attempting to functionally annotating all genes across the genome and placing them within COG categories, 247 of the total 281 gene candidates in SSPs were annotated. These genes were enriched for...." Line 266 - I would like to see a formal enrichment analysis rather than "increased/decreased association", so we could have a clearer picture of which gene functions are truly over/underrepresented in SSPs. You could subsequently limit Figure 8 to those that show a difference. Line 275 - The grammar of this title is a bit off, perhaps "Effect of syntenic, rearranged, unaligned regions and genes on recombination rates" Line 276 - This is the first mention of p, please define it as recombination rate Line 283 - The supplemental Figure S6 and S7 seem to have regions of heightened recombination, but this is difficult to interpret and compare with the current variable axis scales. Please make these consistent. I would also like to see the syri graph of the two aligned genomes, as this would allow for a visual comparison of SV regions with recombination rate. Line 290 - How were p-values adjusted? Line 294 - More information about this 'significantly' higher recombination rate would be good, either in the figure or further expanded in the text. Line 307 - Italics for species names (repeated in Figure 10 and Figure 11 caption) Line 310 - Similar problem to line 275 Figure 10 - Having Figure 9b repeated in Figure 10 and Figure 11 is unnecessary. Line 336 - Vertical lines show average FST, not p Line 341 - Similar problem to line 275 Line 356 - translocations should be plural Line 367 - Vertical lines show average SNP density, not p Line 391 - This is the first mention of barrier loci, please define Line 413 - As mentioned above, I would recommend a formal enrichment test to support this statement Line 428 - Grammar is poor here, please correct Line 490 - Please make this a complete sentence Line 499 - Please state how the Hi-C map was manually edited, and what informed the position of those edits. Line 508 - Please provide an example of how well your LAI score of ~18 compares. The LAI paper seems to intimate that 10 is low quality? Line 513 - Missing bracket for version number Line 536 - Syntenic rather than synteny Line 717 - Formatting error in references Supp table S3-S4-S5 - Space between E. and sideroxylon
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