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Phylomitogenomic analyses on collembolan higher taxa with enhanced taxon sampling and discussion on method selection.

ABSTRACT: Collembola are a basal group of Hexapoda renowned for both unique morphological characters and significant ecological roles. However, a robust and plausible phylogenetic relationship between its deeply divergent lineages has yet to be achieved. We carried out a mitophylogenomic study based on a so far the most comprehensive mitochondrial genome dataset. Our data matrix contained mitogenomes of 31 species from almost all major families of all four orders, with 16 mitogenomes newly sequenced and annotated. We compared the linear arrangements of genes along mitochondria across species. Then we conducted 13 analyses each under a different combination of character coding, partitioning scheme and heterotachy models, and assessed their performance in phylogenetic inference. Several hypothetical tree topologies were also tested. Mitogenomic structure comparison revealed that most species share the same gene order of putative ancestral pancrustacean pattern, while seven species from Onychiuridae, Poduridae and Symphypleona bear different levels of gene rearrangements, indicating phylogenetic signals. Tomoceroidea was robustly recovered for the first time in the presence of all its families and subfamilies. Monophyly of Onychiuroidea was supported using unpartitioned models alleviating LBA. Paronellidae was revealed polyphyletic with two subfamilies inserted independently into Entomobryidae. Although Entomobryomorpha has not been well supported, more than half of the analyses obtained convincing topologies by placing Tomoceroidea within or near remaining Entomobryomorpha. The relationship between elongate-shaped and spherical-shaped collembolans still remained ambiguous, but Neelipleona tend to occupy the basal position in most trees. This study showed that mitochondrial genomes could provide important information for reconstructing the relationships among Collembola when suitable analytical approaches are implemented. Of all the data refining and model selecting schemes used in this study, the combination of nucleotide sequences, partitioning model and exclusion of third codon positions performed better in generating more reliable tree topology and higher node supports than others.

SUBMITTER: Sun X

PROVIDER: S-EPMC7153868 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Assessing the importance of different taxa for inferring evolutionary history is a critical, but underutilized, aspect of systematics. Quantifying the importance of all taxa within a dataset provides an empirical measurement that can establish a ranking of extant taxa for ecological study and/or quantify the relative importance of newly announced or redescribed specimens to enable the disentangling of novelty and inferential influence. Here, we illustrate the use of taxon influence indices through analysis of both molecular and morphological datasets, introducing a modified Bayesian approach to the taxon influence index that accounts for model and topological uncertainty. Quantification of taxon influence using the Bayesian approach produced clear rankings for both dataset types. Bayesian taxon rankings differed from maximum likelihood (ML)-derived rankings from a mitogenomic dataset, and the highest ranking taxa exhibited the largest interquartile range in influence estimate, suggesting variance in the estimate must be taken into account when the ranking of taxa is the feature of interest. Application of the Bayesian taxon influence index to a recent morphological analysis of the Tully Monster (Tullimonstrum) reveals that it exhibits consistently low inferential importance across two recent treatments of the taxon with alternative character codings. These results lend support to the idea that taxon influence indices may be robust to character coding and therefore effective for morphological analyses. These results underscore a need for the development of approaches to, and application of, taxon influence analyses both for the purpose of establishing robust rankings for future inquiry and for explicitly quantifying the importance of individual taxa. Quantifying the importance of individual taxa refocuses debates in morphological studies from questions of character choice/significance and taxon sampling to explicitly analytical techniques, and guides discussion of the context of new discoveries.

Project description:BACKGROUND:Malagasy tenrecs belong to the Afrotherian clade of placental mammals and comprise three subfamilies divided in eight genera (Tenrecinae: Tenrec, Echinops, Setifer and Hemicentetes; Oryzorictinae: Oryzorictes, Limnogale and Microgale; Geogalinae:Geogale). The diversity of their morphology and incomplete taxon sampling made it difficult until now to resolve phylogenies based on either morphology or molecular data for this group. Therefore, in order to delineate the evolutionary history of this family, phylogenetic and dating analyses were performed on a four nuclear genes dataset (ADRA2B, AR, GHR and vWF) including all Malagasy tenrec genera. Moreover, the influence of both taxon sampling and data partitioning on the accuracy of the estimated ages were assessed. RESULTS:Within Afrotheria the vast majority of the nodes received a high support, including the grouping of hyrax with sea cow and the monophyly of both Afroinsectivora (Macroscelidea + Afrosoricida) and Afroinsectiphillia (Tubulidentata + Afroinsectivora). Strongly supported relationships were also recovered among all tenrec genera, allowing us to firmly establish the grouping of Geogale with Oryzorictinae, and to confirm the previously hypothesized nesting of Limnogale within the genus Microgale. The timeline of Malagasy tenrec diversification does not reflect a fast adaptive radiation after the arrival on Madagascar, indicating that morphological specializations have appeared over the whole evolutionary history of the family, and not just in a short period after colonization. In our analysis, age estimates at the root of a clade became older with increased taxon sampling of that clade. Moreover an augmentation of data partitions resulted in older age estimates as well, whereas standard deviations increased when more extreme partition schemes were used. CONCLUSION:Our results provide as yet the best resolved gene tree comprising all Malagasy tenrec genera, and may lead to a revision of tenrec taxonomy. A timeframe of tenrec evolution built on the basis of this solid phylogenetic framework showed that morphological specializations of the tenrecs may have been affected by environmental changes caused by climatic and/or subsequent colonization events. Analyses including various taxon sampling and data partitions allow us to point out some possible pitfalls that may lead to biased results in molecular dating; however, further analyses are needed to corroborate these observations.

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Phylomitogenomic analyses on collembolan higher taxa with enhanced taxon sampling and discussion on method selection.

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