Positive selection on panpulmonate mitogenomes provide new clues on adaptations to terrestrial life

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Abstract

Background

Transitions from marine to intertidal and terrestrial habitats resulted in a significant adaptive radiation within the Panpulmonata (Gastropoda: Heterobranchia). This clade comprises several groups that invaded the land realm independently and in different time periods, e.g., Ellobioidea, Systellomatophora, and Stylommatophora. Thus, mitochondrial genomes of panpulmonate gastropods are promising to screen for adaptive molecular signatures related to land invasions.

Results

We obtained three complete mitochondrial genomes of terrestrial panpulmonates, i.e., the ellobiid Carychium tridentatum, and the stylommatophorans Arion rufus and Helicella itala. Our dataset consisted of 50 mitogenomes comprising almost all major panpulmonate lineages. The phylogenetic tree based on mitochondrial genes supports the monophyly of the clade Panpulmonata. Terrestrial lineages were sampled from Ellobioidea (1 sp.) and Stylommatophora (9 spp.). The branch-site test of positive selection detected significant non-synonymous changes in the terrestrial branches leading to Carychium (Ellobiodea) and Stylommatophora. These convergent changes occurred in the cob and nad5 genes (OXPHOS complex III and I, respectively).

Conclusions

The convergence of the non-synonymous changes in cob and nad5 suggest possible ancient episodes of positive selection related to adaptations to non-marine habitats. The positively selected sites in our data are in agreement with previous results in vertebrates suggesting a general pattern of adaptation to the new metabolic requirements. The demand for energy due to the colonization of land (for example, to move and sustain the body mass in the new habitat) and the necessity to tolerate new conditions of abiotic stress may have changed the physiological constraints in the early terrestrial panpulmonates and triggered adaptations at the mitochondrial level.

Electronic supplementary material

The online version of this article (doi:10.1186/s12862-016-0735-8) contains supplementary material, which is available to authorized users.

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TranslatorX: multiple alignment of nucleotide sequences guided by amino acid translations

Federico Abascal, Rafael Zardoya, Maximilian J Telford (2010)

We present TranslatorX, a web server designed to align protein-coding nucleotide sequences based on their corresponding amino acid translations. Many comparisons between biological sequences (nucleic acids and proteins) involve the construction of multiple alignments. Alignments represent a statement regarding the homology between individual nucleotides or amino acids within homologous genes. As protein-coding DNA sequences evolve as triplets of nucleotides (codons) and it is known that sequence similarity degrades more rapidly at the DNA than at the amino acid level, alignments are generally more accurate when based on amino acids than on their corresponding nucleotides. TranslatorX novelties include: (i) use of all documented genetic codes and the possibility of assigning different genetic codes for each sequence; (ii) a battery of different multiple alignment programs; (iii) translation of ambiguous codons when possible; (iv) an innovative criterion to clean nucleotide alignments with GBlocks based on protein information; and (v) a rich output, including Jalview-powered graphical visualization of the alignments, codon-based alignments coloured according to the corresponding amino acids, measures of compositional bias and first, second and third codon position specific alignments. The TranslatorX server is freely available at http://translatorx.co.uk.

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Codon-substitution models for heterogeneous selection pressure at amino acid sites.

Shira N Goldman, Q. Z. Yang, Gloria A. Pedersen … (2000)

Comparison of relative fixation rates of synonymous (silent) and nonsynonymous (amino acid-altering) mutations provides a means for understanding the mechanisms of molecular sequence evolution. The nonsynonymous/synonymous rate ratio (omega = d(N)d(S)) is an important indicator of selective pressure at the protein level, with omega = 1 meaning neutral mutations, omega 1 diversifying positive selection. Amino acid sites in a protein are expected to be under different selective pressures and have different underlying omega ratios. We develop models that account for heterogeneous omega ratios among amino acid sites and apply them to phylogenetic analyses of protein-coding DNA sequences. These models are useful for testing for adaptive molecular evolution and identifying amino acid sites under diversifying selection. Ten data sets of genes from nuclear, mitochondrial, and viral genomes are analyzed to estimate the distributions of omega among sites. In all data sets analyzed, the selective pressure indicated by the omega ratio is found to be highly heterogeneous among sites. Previously unsuspected Darwinian selection is detected in several genes in which the average omega ratio across sites is 1. Genes undergoing positive selection include the beta-globin gene from vertebrates, mitochondrial protein-coding genes from hominoids, the hemagglutinin (HA) gene from human influenza virus A, and HIV-1 env, vif, and pol genes. Tests for the presence of positively selected sites and their subsequent identification appear quite robust to the specific distributional form assumed for omega and can be achieved using any of several models we implement. However, we encountered difficulties in estimating the precise distribution of omega among sites from real data sets.

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Selecting optimal partitioning schemes for phylogenomic datasets

Robert Lanfear, Brett Calcott, David Kainer … (2014)

Background Partitioning involves estimating independent models of molecular evolution for different subsets of sites in a sequence alignment, and has been shown to improve phylogenetic inference. Current methods for estimating best-fit partitioning schemes, however, are only computationally feasible with datasets of fewer than 100 loci. This is a problem because datasets with thousands of loci are increasingly common in phylogenetics. Methods We develop two novel methods for estimating best-fit partitioning schemes on large phylogenomic datasets: strict and relaxed hierarchical clustering. These methods use information from the underlying data to cluster together similar subsets of sites in an alignment, and build on clustering approaches that have been proposed elsewhere. Results We compare the performance of our methods to each other, and to existing methods for selecting partitioning schemes. We demonstrate that while strict hierarchical clustering has the best computational efficiency on very large datasets, relaxed hierarchical clustering provides scalable efficiency and returns dramatically better partitioning schemes as assessed by common criteria such as AICc and BIC scores. Conclusions These two methods provide the best current approaches to inferring partitioning schemes for very large datasets. We provide free open-source implementations of the methods in the PartitionFinder software. We hope that the use of these methods will help to improve the inferences made from large phylogenomic datasets.

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Author and article information

Contributors

Pedro E. Romero: pedro.romero@senckenberg.de

Alexander M. Weigand: alexander.weigand@uni-due.de

Markus Pfenninger: pfenninger@bio.uni-frankfurt.de

Journal

Journal ID (nlm-ta): BMC Evol Biol

Journal ID (iso-abbrev): BMC Evol. Biol

Title: BMC Evolutionary Biology

Publisher: BioMed Central (London )

ISSN (Electronic): 1471-2148

Publication date (Electronic): 22 August 2016

Publication date PMC-release: 22 August 2016

Publication date Collection: 2016

Volume: 16

Issue: 1

Electronic Location Identifier: 164

Affiliations

[1 ]Senckenberg Biodiversity and Climate Research Centre (BiK-F), Senckenberganlage 25, 60325 Frankfurt am Main, Germany

[2 ]Institute for Ecology, Evolution & Diversity, Faculty of Biological Sciences, Goethe University Frankfurt, Max-von-Laue-Straße 13, 60438 Frankfurt am Main, Germany

[3 ]Museo de Historia Natural, Universidad Nacional Mayor de San Marcos, Av. Arenales 1256, Apartado 14-0434, Lima 14, Peru

[4 ]Aquatic Ecosystem Research, University of Duisburg-Essen, Universitätsstraße 5, 45141 Essen, Germany

[5 ]Centre for Water and Environmental Research (ZWU), University of Duisburg-Essen, Universitätsstraße 2, 45117 Essen, Germany

Article

Publisher ID: 735

DOI: 10.1186/s12862-016-0735-8

PMC ID: 4994307

PubMed ID: 27549326

SO-VID: 7700c267-89cf-4170-9929-ff976deb2d05

License:

Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

History

Date received : 29 February 2016

Date accepted : 8 August 2016

Funding

Funded by: Consejo Nacional de Ciencia, Tecnología e Innovación Tecnológica (CONCYTEC)

Award ID: 291-2014-FONDECYT

Award Recipient : Pedro E. Romero

Custom metadata

ScienceOpen disciplines: Evolutionary Biology

Keywords: codon models,land invasion,mitogenomics,panpulmonata,positive selection

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ScienceOpen disciplines: Evolutionary Biology

Keywords: codon models, land invasion, mitogenomics, panpulmonata, positive selection

Positive selection on panpulmonate mitogenomes provide new clues on adaptations to terrestrial life

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Marine Life Science & Technology

Most cited references 67

TranslatorX: multiple alignment of nucleotide sequences guided by amino acid translations

Codon-substitution models for heterogeneous selection pressure at amino acid sites.

Selecting optimal partitioning schemes for phylogenomic datasets

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