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Jakovlic, I.

Publications and source records attributed to Jakovlic, I..

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Mitochondrial Genome-Based Phylogeny of Turbellarians and Evidence for Accelerated Mitochondrial Evolution in Symbiotic Species

BackgroundFlatworms are a highly diverse phylum with over 26,500 predominantly parasitic species. A minor portion of this diversity comprise predominantly free-living "turbellarians" Phylogenetic relationships within turbellarian orders remain debated, with recent mitochondrial genome studies also questioning the monophyly of the "Neoophora clade". Some unique mitochondrial gene features have also been observed in this group. Within Turbellaria, the order Rhabdocoela includes significant symbiotic lineages, such as the endosymbiotic Umagillidae, Pterastericolidae, and Graffillidae, and the ectosymbiotic Temnocephalidae, which notably exhibits characteristics akin to a parasitic lifestyle. Given evidence linking parasitic lifestyles to accelerated mitogenomic evolution, we hypothesize that similar patterns: symbiotic turbellarians have mitochondrial genomes that accelerate evolution compared to free-living turbellarians. This study presents the first complete mitochondrial genome of the ectosymbiont Craspedella pedum, provides mitogenomic insights into turbellarian phylogeny, and addressing our hypothesis. ResultsThe mitochondrial genome of Craspedella pedum is a circular DNA molecule of 18,456 base pairs, containing the standard 36 flatworm mitochondrial genes, a duplicated trnT, two cox1 pseudogene fragments, a putative atp8 gene, and several distinctive NCRs. Phylogenetic analyses based on 47 mitochondrial genomes, including the newly sequenced C. pedum and two assembled species from SRA database, using CAT-GTR model and BI and ML algorithms further confirmed that the paraphyly of the Neoophora clade and the basal position of Catenulida and Macrostomida. Different from previous study, Rhabdocoela forms a distinct clade within the turbellarians diverged immediately after Macrostomida before Polycladida and Tricladida. Within Rhabdocoela, C. pedum formed a direct sister clade with Typhloplanidae, suggesting a close phylogenetic relationship between the two. We also identified the paraphyletic of the Planoceridae of Polycladida and the unstable position of Planariidae within Tricladidain. Furthermore, we found a trend that the nad4L-nad4 gene box in turbellarians may have evolved from an overlapping state, to the insertion of a non-coding region (NCR), and subsequently to a separated configuration, correlating with species divergence. The selection pressure analysis showcased selective relaxation from free-living species of Rhabdocoela to symbiotic species of Rhabdocoela. Furthermore, we also detected a relaxation from certain tubellarian lineages to Rhabdocoela. Along with higher GORR and longer Brl, Rhabdocoela and its symbiotic group possesses a more rapidly evolving mitochondrial genome. ConclusionsThe mitochondrial genome of Craspedella pedum displays uncommon characteristics, combined extended branch lengths and elevated GORR, suggesting rapid evolution and extensive rearrangements. Our phylogenetic analysis, integrating additional mitogenome data, further corroborates the paraphyly of the Neoophora clade and offers novel insights into turbellarian phylogeny. For the first time, we confirmed the accelerated evolution of mitochondrial genomes in symbiotic tubellarians compared to free-living ones, as evidenced by a longer average Brl, a higher average GORR, and relaxed selection pressure. Additionally, with the same evidences, we found that Rhabdocoela also exhibited accelerated mitochondrial genome evolution in planarians.

genomics↗

The Phylogeny and the Evolution of Parasitic Strategies in Trematoda

Trematodes are obligatory parasites that generally must transmit between hosts to complete their life cycle. They parasitize varying numbers of intermediate hosts (0, 1 or 2), but the evolutionary history of these strategies and the ancestral states remain unknown. We conducted the ancestral state reconstruction of the number of intermediate hosts using mitogenomic (Trematoda) and nuclear-genomic (Neodermata) topologies. Aspidogastrea was identified as the sister-group ("basal") to all other Trematoda using a range of approaches, so it is crucial for studying the evolutionary history of trematodes. However, there is only one transcriptome available for this lineage, and mitochondrial genomes (mitogenomes) remain unavailable. Herein, we sequenced mitogenomes of two aspidogastreans: Aspidogaster ijimai and Aspidogaster conchicola. As the ancestral state reconstruction analysis is topology-sensitive, we tested multiple phylogenetic strategies, comprising the outgroup selection, phylogenetic models, partitioning strategies, and topological constraints. These mitogenomic phylogenies exhibited pronounced topological instability, with Aspidogastrea resolved as the "basal" radiation in most, but not all, topologies. Based on our analyses, Cestoda was the optimal outgroup choice, and the "heterogeneous" CAT-GTR model in PhyloBayes was the optimal model choice. We inferred the time tree and conducted ancestral state reconstruction analyses using this "optimal" topology, as well as constrained mitogenomic and nuclear genomic topologies. Results were ambiguous for some lineages, but scenario that received the strongest support is the direct life cycle (no intermediate hosts) in the ancestors of Trematoda (proto-trematodes) and Aspidogastrea (proto-aspidogastreans), while the ancestor of Digenea (proto-digeneans) had two intermediate hosts. The inferred scenario indicates that host strategies are relatively plastic among trematodes, putatively comprising several independent host gains, and multiple host losses. We propose a timeline for these events and discuss the role that alternating sexual and asexual generations putatively played in the evolution of complex parasitic life histories in digeneans.

evolutionary biology↗

Positive Selection on Rare Variants Underlying the Cold Adaptation of Wild Boar

The wide geographical distribution of Eurasian wild boar (Sus scrofa) offers a natural experiment to study the thermoregulation. Here, we conducted whole-genome resequencing and chromatin profiling experiments on the local populations from cold regions (northern and northeastern Asia) and warm regions (southeastern Asia and southern China). Using genome-wide scans of four methods, we detected candidate genes underlying cold-adaptation with significant enrichment of pathways related to thermogenesis, fat cell development, and adipose tissue regulation. We also found two enhancer variants under positive selection, an intronic variant of IGF1R (rs341219502) and an exonic variant of BRD4 (rs327139795), which showed the highest differentiation between cold and warm region populations of wild boar and domestic pigs. Moreover, these rare variants were absent in outgroup species and warm-region wild boar but nearly fixed in cold-region populations, suggesting their de novo origins in cold-region populations. The experiments of CUT&Tag chromatin profiling showed that rs341219502 of IGF1R is associated with the gain of three novel transcription factors involving regulatory changes in enhancer function, while rs327139795 of BRD4 could result in the loss of a phosphorylation site due to amino acid alteration. We also found three genes (SLCO1C1, PDE3A, and TTC28) with selection signals in both wild boar and native human populations from Siberia, which suggests convergent molecular adaptation in mammals. Our study shows the adaptive evolution of genomic molecules underlying the remarkable environmental flexibility of wild boar.

evolutionary biology↗

Parasitism and locomotory capacity calibrate the mitogenomic evolutionary rates in Bilateria

The evidence that parasitic lineages exhibit elevated evolutionary rates is limited to Arthropoda and inconsistent. Similarly, the evidence that mitogenomic evolution is faster in species with low locomotory capacity (LC) is limited to a handful of animal lineages. We hypothesised that these two variables are associated and that LC is a major underlying factor driving the elevated evolutionary rates in parasites. We tested this hypothesis by studying mitogenomic evolutionary patterns in 10,911 bilaterian species classified according to their locomotory capacity and parasitic/free-living life history (LH). Evolutionary rates were significantly elevated in endoparasites, ectoparasites with reduced LC, and free-living lineages with reduced LC, but not in ectoparasites and parasitoids with high LC. Nematoda and Arachnida were the only lineages where parasitism was not associated with faster evolution. We propose that LC may also explain these two major outliers. Overall, the LH categorisation explained 35-37%, LC categorisation 26-28%, and together they explained 41-44% of the variance in branch lengths across the Bilateria. Our findings suggest that these two variables play a major role in calibrating the molecular clock in bilaterian animals.

evolutionary biology↗

The nanopore sequencing of a Chinese rhesus macaque revealed patterns of methylation, recombination, and selection for structural variations

Rhesus macaques (Macaca mulatta) are the most extensively studied nonhuman primate species for human biomedical modeling. However, little is known about the biological pattern of genome-wide structural variations (SVs) and the evolutionary forces underlying SVs. Here, we conducted genomic sequencing and analyses based on Nanopore long reads and Illumina short reads technology. We called SVs between the two subspecies (China vs. India), using three methods of assembly-based and long-reads-based algorithms. Interestingly, we found significantly more SVs in X-chromosome than in autosomes, consistent with the expectation of the faster-X divergence at the subspecies level. With the fine-scale methylation frequencies and recombination rates, we found duplications with significantly lower methylation frequencies while higher recombination rates than other types of SVs, suggesting a higher level of transcriptional and evolutionary potential for duplications than for other SVs types. A genome-wide scan of selective sweep revealed that over 3% of SVs are under positive selection. Moreover, X chromosome showed significantly higher number of positively selected SVs than do autosomes, suggesting the "faster-X effect" of SVs. Our study revealed a different evolutionary importance for duplications compared with other SVs forms. We also revealed the "faster-X effect" of SVs, which could provide raw material upon which positive selection can further play.

genomics↗

Drivers of interlineage variability in mitogenomic evolutionary rates in flatworms (Platyhelminthes) are multifactorial

The forces driving interlineage variability in the evolutionary rates (both sequence and architecture) of mitochondrial genomes are often inconsistent and unpredictable. Herein we studied the impacts of multiple variables using 223 flatworm (Platyhelminthes) species and phylogenetic multilevel regression models. We found that: 1. Mitogenomic sequence evolution is faster in parasites associated with the thermally stable environment of endothermic hosts, but the overall impact of thermic habitat is small; 2. Mitogenome sizes are smaller in parasites of endothermic hosts, but the effects are small and inconsistent; 3. Mitogenomic gene order rearrangements (GORR) are positively correlated with mitogenomic size; 4. The expected positive correlation between GORR and sequence evolution is lineage-specific, and non-parasitic species exhibited a strong negative correlation; 5. Longevity has negligible impacts on mitogenomic evolution; 6. Parasitic (Neodermata) flatworm lineages exhibit higher evolutionary rates than non-parasitic lineages; 7. The effective population size has negligible impacts on mitogenomic evolution; 8. Comparatively, parasitism had by far the greatest impact on the mitogenomic evolution, but due to the monophyletic origin of this life-history strategy, alternative hypotheses cannot be rejected. A large number of factors impact the mitogenomic evolution in flatworms, with lineage-specific relative contributions, which sometimes produces incongruent lineage-specific mitogenomic evolution patterns.

evolutionary biology↗

Evolutionary history of inversions in the direction of architecture-driven mutational pressures in crustacean mitochondrial genomes

Inversions of the origin of replication (ORI) of mitochondrial genomes produce asymmetrical mutational pressures that can cause artefactual clustering in phylogenetic analyses. It is therefore an absolute prerequisite for all molecular evolution studies that use mitochondrial data to account for ORI events in the evolutionary history of their dataset. The number of ORI events in crustaceans remains unknown; several studies reported ORI events in some crustacean lineages on the basis of fully inversed (e.g. negative vs. positive) GC skew patterns, but studies of isolated lineages could have easily overlooked ORI events that produced merely a reduction in the skew magnitude. In this study, we used a comprehensive taxonomic approach to systematically study the evolutionary history of ORI events in crustaceans using all available mitogenomes and combining signals from lineage-specific skew magnitude and direction (+ or -), cumulative skew diagrams, and gene rearrangements. We inferred 24 putative ORI events (14 of which have not been proposed before): 17 with relative confidence, and 7 speculative. Most of these were located at lower taxonomic levels, but there are indications of ORIs that occurred at or above the order-level: Copepoda, Isopoda, and putatively in Branchiopoda and Poecilostomatida+Cyclopoida. Several putative ORI events did not result in fully inversed skews. In many lineages skew plots were not informative for the prediction of replication origin and direction of mutational pressures, but inversions of the mitogenome fragment comprising the ancestral CR (rrnS-CR-trnI) were rather good predictors of skew inversions. We also found that skew plots can be a useful tool to indirectly infer the relative strengths of mutational/purifying pressures in some crustacean lineages: when purifying pressures outweigh mutational, GC skew plots are strongly affected by the strand distribution of genes, and when mutational > purifying, GC skew plots can be even completely (apparently) unaffected by the strand distribution of genes. This observation has very important repercussions for phylogenetic and evolutionary studies, as it implies that not only the relatively rare ORI events, but also much more common gene strand switches and same-strand rearrangements can produce mutational bursts, which in turn affect phylogenetic and evolutionary analyses. We argue that such compositional biases may produce misleading signals not only in phylogenetic but also in other types of evolutionary analyses (dN/dS ratios, codon usage bias, base composition, branch length comparison, etc.), and discuss several such examples. Therefore, all studies aiming to study the evolution of mtDNA sequences should pay close attention to architectural rearrangements.

evolutionary biology↗

Mitochondrial architecture rearrangements produce asymmetrical nonadaptive mutational pressures that subvert the phylogenetic reconstruction in Isopoda

The phylogeny of Isopoda, a speciose order of crustaceans, remains unresolved, with different datasets often producing starkly incongruent phylogenetic hypotheses. We hypothesised that extreme diversity in their life histories might be causing compositional heterogeneity/heterotachy in their mitochondrial genomes, and compromising the phylogenetic reconstruction. We tested the effects of different datasets (mitochondrial, nuclear, nucleotides, amino acids, concatenated genes, individual genes, gene orders), phylogenetic algorithms (assuming data homogeneity, heterogeneity, and heterotachy), and partitioning; and found that almost all of them produced unique topologies. As we also found that mitogenomes of Asellota and two Cymothoida families (Cymothoidae and Corallanidae) possess inversed base (GC) skew patterns in comparison to other isopods, we concluded that inverted skews cause long-branch attraction phylogenetic artefacts between these taxa. These asymmetrical skews are most likely driven by multiple independent inversions of origin of replication (i.e., nonadaptive mutational pressures). Although the PhyloBayes CAT-GTR algorithm managed to attenuate some of these artefacts (and outperform partitioning), mitochondrial data have limited applicability for reconstructing the phylogeny of Isopoda. Regardless of this, our analyses allowed us to propose solutions to some unresolved phylogenetic debates, and support Asellota are the most likely candidate for the basal isopod branch. As our findings show that architectural rearrangements can produce major compositional biases even on short evolutionary timescales, the implications are that proving the suitability of data via composition skew analyses should be a prerequisite for every study that aims to use mitochondrial data for phylogenetic reconstruction, even among closely related taxa.

evolutionary biology↗

PhyloSuite: an integrated and scalable desktop platform for streamlined molecular sequence data management and evolutionary phylogenetics studies

Multi-gene and genomic datasets have become commonplace in the field of phylogenetics, but many of the existing tools are not designed for such datasets, which makes the analysis time-consuming and tedious. We therefore present PhyloSuite, a user-friendly workflow desktop platform dedicated to streamlining molecular sequence data management and evolutionary phylogenetics studies. It employs a plugin-based system that integrates a number of useful phylogenetic and bioinformatic tools, thereby streamlining the entire procedure, from data acquisition to phylogenetic tree annotation, with the following features: (i) point-and-click and drag-and-drop graphical user interface, (ii) a workspace to manage and organize molecular sequence data and results of analyses, (iii) GenBank entries extraction and comparative statistics, (iv) a phylogenetic workflow with batch processing capability, (v) elaborate bioinformatic analysis for mitochondrial genomes. The aim of PhyloSuite is to enable researchers to spend more time playing with scientific questions, instead of wasting it on conducting standard analyses. The compiled binary of PhyloSuite is available under the GPL license at https://github.com/dongzhang0725/PhyloSuite/releases, implemented in Python and runs on Windows, Mac OSX and Linux.

bioinformatics↗