Proteomic similarity of the Littorinid snails in the evolutionary context

Background The introduction of DNA-based molecular markers made a revolution in biological systematics. However, in cases of very recent divergence events, the neutral divergence may be too slow, and the analysis of adaptive part of the genome is more informative to reconstruct the recent evolutiona...

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Main Authors: Arina L. Maltseva, Marina A. Varfolomeeva, Arseniy A. Lobov, Polina Tikanova, Marina Panova, Natalia A. Mikhailova, Andrei I. Granovitch
Format: Article
Language:English
Published: PeerJ Inc. 2020-02-01
Series:PeerJ
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Online Access:https://peerj.com/articles/8546.pdf
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author Arina L. Maltseva
Marina A. Varfolomeeva
Arseniy A. Lobov
Polina Tikanova
Marina Panova
Natalia A. Mikhailova
Andrei I. Granovitch
author_facet Arina L. Maltseva
Marina A. Varfolomeeva
Arseniy A. Lobov
Polina Tikanova
Marina Panova
Natalia A. Mikhailova
Andrei I. Granovitch
author_sort Arina L. Maltseva
collection DOAJ
description Background The introduction of DNA-based molecular markers made a revolution in biological systematics. However, in cases of very recent divergence events, the neutral divergence may be too slow, and the analysis of adaptive part of the genome is more informative to reconstruct the recent evolutionary history of young species. The advantage of proteomics is its ability to reflect the biochemical machinery of life. It may help both to identify rapidly evolving genes and to interpret their functions. Methods Here we applied a comparative gel-based proteomic analysis to several species from the gastropod family Littorinidae. Proteomes were clustered to assess differences related to species, geographic location, sex and body part, using data on presence/absence of proteins in samples and data on protein occurrence frequency in samples of different species. Cluster support was assessed using multiscale bootstrap resampling and the stability of clustering—using cluster-wise index of cluster stability. Taxon-specific protein markers were derived using IndVal method. Proteomic trees were compared to consensus phylogenetic tree (based on neutral genetic markers) using estimates of the Robinson–Foulds distance, the Fowlkes–Mallows index and cophenetic correlation. Results Overall, the DNA-based phylogenetic tree and the proteomic similarity tree had consistent topologies. Further, we observed some interesting deviations of the proteomic littorinid tree from the neutral expectations. (1) There were signs of molecular parallelism in two Littoraria species that phylogenetically are quite distant, but live in similar habitats. (2) Proteome divergence was unexpectedly high between very closely related Littorina fabalis and L. obtusata, possibly reflecting their ecology-driven divergence. (3) Conservative house-keeping proteins were usually identified as markers for cryptic species groups (“saxatilis” and “obtusata” groups in the Littorina genus) and for genera (Littoraria and Echinolittorina species pairs), while metabolic enzymes and stress-related proteins (both potentially adaptively important) were often identified as markers supporting species branches. (4) In all five Littorina species British populations were separated from the European mainland populations, possibly reflecting their recent phylogeographic history. Altogether our study shows that proteomic data, when interpreted in the context of DNA-based phylogeny, can bring additional information on the evolutionary history of species.
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spelling doaj.art-d0c81e8556594010843641f9d033d7eb2023-12-03T10:31:15ZengPeerJ Inc.PeerJ2167-83592020-02-018e854610.7717/peerj.8546Proteomic similarity of the Littorinid snails in the evolutionary contextArina L. Maltseva0Marina A. Varfolomeeva1Arseniy A. Lobov2Polina Tikanova3Marina Panova4Natalia A. Mikhailova5Andrei I. Granovitch6Department of Invertebrate Zoology, St. Petersburg State University, St. Petersburg, RussiaDepartment of Invertebrate Zoology, St. Petersburg State University, St. Petersburg, RussiaDepartment of Invertebrate Zoology, St. Petersburg State University, St. Petersburg, RussiaDepartment of Invertebrate Zoology, St. Petersburg State University, St. Petersburg, RussiaDepartment of Invertebrate Zoology, St. Petersburg State University, St. Petersburg, RussiaDepartment of Invertebrate Zoology, St. Petersburg State University, St. Petersburg, RussiaDepartment of Invertebrate Zoology, St. Petersburg State University, St. Petersburg, RussiaBackground The introduction of DNA-based molecular markers made a revolution in biological systematics. However, in cases of very recent divergence events, the neutral divergence may be too slow, and the analysis of adaptive part of the genome is more informative to reconstruct the recent evolutionary history of young species. The advantage of proteomics is its ability to reflect the biochemical machinery of life. It may help both to identify rapidly evolving genes and to interpret their functions. Methods Here we applied a comparative gel-based proteomic analysis to several species from the gastropod family Littorinidae. Proteomes were clustered to assess differences related to species, geographic location, sex and body part, using data on presence/absence of proteins in samples and data on protein occurrence frequency in samples of different species. Cluster support was assessed using multiscale bootstrap resampling and the stability of clustering—using cluster-wise index of cluster stability. Taxon-specific protein markers were derived using IndVal method. Proteomic trees were compared to consensus phylogenetic tree (based on neutral genetic markers) using estimates of the Robinson–Foulds distance, the Fowlkes–Mallows index and cophenetic correlation. Results Overall, the DNA-based phylogenetic tree and the proteomic similarity tree had consistent topologies. Further, we observed some interesting deviations of the proteomic littorinid tree from the neutral expectations. (1) There were signs of molecular parallelism in two Littoraria species that phylogenetically are quite distant, but live in similar habitats. (2) Proteome divergence was unexpectedly high between very closely related Littorina fabalis and L. obtusata, possibly reflecting their ecology-driven divergence. (3) Conservative house-keeping proteins were usually identified as markers for cryptic species groups (“saxatilis” and “obtusata” groups in the Littorina genus) and for genera (Littoraria and Echinolittorina species pairs), while metabolic enzymes and stress-related proteins (both potentially adaptively important) were often identified as markers supporting species branches. (4) In all five Littorina species British populations were separated from the European mainland populations, possibly reflecting their recent phylogeographic history. Altogether our study shows that proteomic data, when interpreted in the context of DNA-based phylogeny, can bring additional information on the evolutionary history of species.https://peerj.com/articles/8546.pdfTaxonomyCryptic speciesPhylogenetic markersOutliersProteomicsLittorinidae
spellingShingle Arina L. Maltseva
Marina A. Varfolomeeva
Arseniy A. Lobov
Polina Tikanova
Marina Panova
Natalia A. Mikhailova
Andrei I. Granovitch
Proteomic similarity of the Littorinid snails in the evolutionary context
PeerJ
Taxonomy
Cryptic species
Phylogenetic markers
Outliers
Proteomics
Littorinidae
title Proteomic similarity of the Littorinid snails in the evolutionary context
title_full Proteomic similarity of the Littorinid snails in the evolutionary context
title_fullStr Proteomic similarity of the Littorinid snails in the evolutionary context
title_full_unstemmed Proteomic similarity of the Littorinid snails in the evolutionary context
title_short Proteomic similarity of the Littorinid snails in the evolutionary context
title_sort proteomic similarity of the littorinid snails in the evolutionary context
topic Taxonomy
Cryptic species
Phylogenetic markers
Outliers
Proteomics
Littorinidae
url https://peerj.com/articles/8546.pdf
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AT marinapanova proteomicsimilarityofthelittorinidsnailsintheevolutionarycontext
AT nataliaamikhailova proteomicsimilarityofthelittorinidsnailsintheevolutionarycontext
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