Journal of Molecular Evolution

, Volume 84, Issue 4, pp 162–173 | Cite as

Testing for the Occurrence of Selective Episodes During the Divergence of Otophysan Fishes: Insights from Mitogenomics

  • Alejandro D’Anatro
  • Facundo Giorello
  • Matías Feijoo
  • Enrique P. Lessa
Original Article

Abstract

How natural selection shapes biodiversity constitutes a topic of renewed interest during the last few decades. The division Otophysi comprises approximately two-thirds of freshwater fish diversity and probably underwent an extensive adaptive radiation derived from a single invasion of the supercontinent Pangaea, giving place to the evolution of the main five Otophysan lineages during a short period of time. Little is known about the factors involved in the processes that lead to lineage diversification among this group of fishes and identifying directional selection acting over protein-coding genes could offer clues about the processes acting on species diversification. The main objective of this study was to explore the otophysan mitochondrial genome evolution, in order to account for the possible signatures of selective events in this lineage, and to explore for the functional connotations of these molecular substitutions. Mainly, three different approaches were used: the “ω-based” BS-REL and MEME methods, implemented in the DATAMONKEY web server, and analysis of selection on amino acid properties, implemented in the software TreeSAAP. We found evidence of selective episodes along several branches of the evolutionary history of othophysan fishes. Analyses carried out using the BS-REL algorithm suggest episodic diversifying selection at basal branches of the otophysan lineage, which was also supported by analyses implemented in MEME and TreeSAAP. These results suggest that throughout the Siluriformes radiation, an important number of adaptive changes occurred in their mitochondrial genome. The metabolic consequences and ecological correlates of these molecular substitutions should be addressed in future studies.

Keywords

Molecular evolution Natural selection Adaptation Speciation Fish 

Supplementary material

239_2017_9790_MOESM1_ESM.tif (186 kb)
Figure OR1. Results obtained with MEME analyses in Datamonkey web server when ATP6 gene sequences were analyzed. Branches that have experienced substitutions, based on most likely joint maximum likelihood ancestral reconstructions at a given site, are labeled as count of synonymous substitutions:count of non-synonymous substitutions. The thickness of each branch is proportional to the minimal number of single nucleotide substitutions mapped to the branch. Branches are colored according to the magnitude of the empirical Bayes factor (EBF) for the event of positive selection: red—evidence for positive selection, teal—evidence for neutral evolution or negative selection, black—no information (taken from Murrell et al. 2012) (TIF 185 KB)
239_2017_9790_MOESM2_ESM.tif (195 kb)
Figure OR2. Results obtained with MEME analyses in Datamonkey web server when ATP8 gene sequences were analyzed. Branches that have experienced substitutions, based on most likely joint maximum likelihood ancestral reconstructions at a given site, are labeled as count of synonymous substitutions:count of non-synonymous substitutions. The thickness of each branch is proportional to the minimal number of single nucleotide substitutions mapped to the branch. Branches are colored according to the magnitude of the empirical Bayes factor (EBF) for the event of positive selection: red—evidence for positive selection, teal—evidence for neutral evolution or negative selection, black—no information (taken from Murrell et al. 2012) (TIF 195 KB)
239_2017_9790_MOESM3_ESM.tif (189 kb)
Figure OR3. Results obtained with MEME analyses in Datamonkey web server when COX1 gene sequences were analyzed. Branches that have experienced substitutions, based on most likely joint maximum likelihood ancestral reconstructions at a given site, are labeled as count of synonymous substitutions:count of non-synonymous substitutions. The thickness of each branch is proportional to the minimal number of single nucleotide substitutions mapped to the branch. Branches are colored according to the magnitude of the empirical Bayes factor (EBF) for the event of positive selection: red—evidence for positive selection, teal—evidence for neutral evolution or negative selection, black—no information (taken from Murrell et al. 2012) (TIF 189 KB)
239_2017_9790_MOESM4_ESM.tif (4 mb)
Figure OR4. Results obtained with MEME analyses in Datamonkey web server when COX3 gene sequences were analyzed. Branches that have experienced substitutions, based on most likely joint maximum likelihood ancestral reconstructions at a given site, are labeled as count of synonymous substitutions:count of non-synonymous substitutions. The thickness of each branch is proportional to the minimal number of single nucleotide substitutions mapped to the branch. Branches are colored according to the magnitude of the empirical Bayes factor (EBF) for the event of positive selection: red—evidence for positive selection, teal—evidence for neutral evolution or negative selection, black—no information (taken from Murrell et al. 2012) (TIF 4109 KB)
239_2017_9790_MOESM5_ESM.tif (3.8 mb)
Figure OR5. Results obtained with MEME analyses in Datamonkey web server when CYTB gene sequences were analyzed. Branches that have experienced substitutions, based on most likely joint maximum likelihood ancestral reconstructions at a given site, are labeled as count of synonymous substitutions:count of non-synonymous substitutions. The thickness of each branch is proportional to the minimal number of single nucleotide substitutions mapped to the branch. Branches are colored according to the magnitude of the empirical Bayes factor (EBF) for the event of positive selection: red—evidence for positive selection, teal—evidence for neutral evolution or negative selection, black—no information (taken from Murrell et al. 2012) (TIF 3855 KB)
239_2017_9790_MOESM6_ESM.tif (6.5 mb)
Figure OR6. Results obtained with MEME analyses in Datamonkey web server when ND1 gene sequences were analyzed. Branches that have experienced substitutions, based on most likely joint maximum likelihood ancestral reconstructions at a given site, are labeled as count of synonymous substitutions:count of non-synonymous substitutions. The thickness of each branch is proportional to the minimal number of single nucleotide substitutions mapped to the branch. Branches are colored according to the magnitude of the empirical Bayes factor (EBF) for the event of positive selection: red—evidence for positive selection, teal—evidence for neutral evolution or negative selection, black—no information (taken from Murrell et al. 2012) (TIF 6661 KB)
239_2017_9790_MOESM7_ESM.tif (3.7 mb)
Figure OR7. Results obtained with MEME analyses in Datamonkey web server when ND2 gene sequences were analyzed. Branches that have experienced substitutions, based on most likely joint maximum likelihood ancestral reconstructions at a given site, are labeled as count of synonymous substitutions:count of non-synonymous substitutions. The thickness of each branch is proportional to the minimal number of single nucleotide substitutions mapped to the branch. Branches are colored according to the magnitude of the empirical Bayes factor (EBF) for the event of positive selection: red—evidence for positive selection, teal—evidence for neutral evolution or negative selection, black—no information (taken from Murrell et al. 2012) (TIF 3819 KB)
239_2017_9790_MOESM8_ESM.tif (208 kb)
Figure OR8. Results obtained with MEME analyses in Datamonkey web server when ND3 gene sequences were analyzed. Branches that have experienced substitutions, based on most likely joint maximum likelihood ancestral reconstructions at a given site, are labeled as count of synonymous substitutions:count of non-synonymous substitutions. The thickness of each branch is proportional to the minimal number of single nucleotide substitutions mapped to the branch. Branches are colored according to the magnitude of the empirical Bayes factor (EBF) for the event of positive selection: red—evidence for positive selection, teal—evidence for neutral evolution or negative selection, black—no information (taken from Murrell et al. 2012) (TIF 207 KB)
239_2017_9790_MOESM9_ESM.tif (199 kb)
Figure OR9. Results obtained with MEME analyses in Datamonkey web server when ND4 gene sequences were analyzed. Branches that have experienced substitutions, based on most likely joint maximum likelihood ancestral reconstructions at a given site, are labeled as count of synonymous substitutions:count of non-synonymous substitutions. The thickness of each branch is proportional to the minimal number of single nucleotide substitutions mapped to the branch. Branches are colored according to the magnitude of the empirical Bayes factor (EBF) for the event of positive selection: red—evidence for positive selection, teal—evidence for neutral evolution or negative selection, black—no information (taken from Murrell et al. 2012) (TIF 199 KB)
239_2017_9790_MOESM10_ESM.tif (10.4 mb)
Figure OR10. Results obtained with MEME analyses in Datamonkey web server when ND5 gene sequences were analyzed. Branches that have experienced substitutions, based on most likely joint maximum likelihood ancestral reconstructions at a given site, are labeled as count of synonymous substitutions:count of non-synonymous substitutions. The thickness of each branch is proportional to the minimal number of single nucleotide substitutions mapped to the branch. Branches are colored according to the magnitude of the empirical Bayes factor (EBF) for the event of positive selection: red—evidence for positive selection, teal—evidence for neutral evolution or negative selection, black—no information (taken from Murrell et al. 2012) (TIF 10690 KB)
239_2017_9790_MOESM11_ESM.tif (4.5 mb)
Figure OR11. Three-dimensional structure of: A) ATP6 (PDB accession number: 1C17_M), B) COX1 (10CC_A), C) COX3 (10CC_C), D) CYTB (1BCC_C), E) ND1 (4HE8_H), F) ND2 (4HE8_N), G) ND3 (4HE8_A), H) ND4 (4HE8_M), and I) ND5 (4HE8_L). Arrows indicate position of the sites in the protein under directional natural selection, as suggested by MEME analyses (TIF 4582 KB)

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Copyright information

© Springer Science+Business Media New York 2017

Authors and Affiliations

  • Alejandro D’Anatro
    • 1
  • Facundo Giorello
    • 1
  • Matías Feijoo
    • 1
  • Enrique P. Lessa
    • 1
  1. 1.Departamento de Ecología y Evolución, Facultad de CienciasUniversidad de la RepúblicaMontevideoUruguay

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