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Complete mitochondrial genomes and updated divergence time of the two freshwater clupeids endemic to Lake Tanganyika (Africa) suggest intralacustrine speciation

BACKGROUND: The hydrogeological history of Lake Tanganyika paints a complex image of several colonization and adaptive radiation events. The initial basin was formed around 9–12 million years ago (MYA) from the predecessor of the Malagarasi–Congo River and only 5–6 MYA, its sub-basins fused to produ...

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Autores principales: Milec, Leona J. M., Vanhove, Maarten P. M., Bukinga, Fidel Muterezi, De Keyzer, Els L. R., Kapepula, Vercus Lumami, Masilya, Pascal Mulungula, Mulimbwa, N’Sibula, Wagner, Catherine E., Raeymaekers, Joost A. M.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9635120/
https://www.ncbi.nlm.nih.gov/pubmed/36329403
http://dx.doi.org/10.1186/s12862-022-02085-8
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author Milec, Leona J. M.
Vanhove, Maarten P. M.
Bukinga, Fidel Muterezi
De Keyzer, Els L. R.
Kapepula, Vercus Lumami
Masilya, Pascal Mulungula
Mulimbwa, N’Sibula
Wagner, Catherine E.
Raeymaekers, Joost A. M.
author_facet Milec, Leona J. M.
Vanhove, Maarten P. M.
Bukinga, Fidel Muterezi
De Keyzer, Els L. R.
Kapepula, Vercus Lumami
Masilya, Pascal Mulungula
Mulimbwa, N’Sibula
Wagner, Catherine E.
Raeymaekers, Joost A. M.
author_sort Milec, Leona J. M.
collection PubMed
description BACKGROUND: The hydrogeological history of Lake Tanganyika paints a complex image of several colonization and adaptive radiation events. The initial basin was formed around 9–12 million years ago (MYA) from the predecessor of the Malagarasi–Congo River and only 5–6 MYA, its sub-basins fused to produce the clear, deep waters of today. Next to the well-known radiations of cichlid fishes, the lake also harbours a modest clade of only two clupeid species, Stolothrissa tanganicae and Limnothrissa miodon. They are members of Pellonulini, a tribe of clupeid fishes that mostly occur in freshwater and that colonized West and Central-Africa during a period of high sea levels during the Cenozoic. There is no consensus on the phylogenetic relationships between members of Pellonulini and the timing of the colonization of Lake Tanganyika by clupeids. RESULTS: We use short-read next generation sequencing of 10X Chromium libraries to sequence and assemble the full mitochondrial genomes of S. tanganicae and L. miodon. We then use Maximum likelihood and Bayesian inference to place them into the phylogeny of Pellonulini and other clupeiforms, taking advantage of all available full mitochondrial clupeiform genomes. We identify Potamothrissa obtusirostris as the closest living relative of the Tanganyika sardines and confirm paraphyly for Microthrissa. We estimate the divergence of the Tanganyika sardines around 3.64 MYA [95% CI: 0.99, 6.29], and from P. obtusirostris around 10.92 MYA [95% CI: 6.37–15.48]. CONCLUSIONS: These estimates imply that the ancestor of the Tanganyika sardines diverged from a riverine ancestor and entered the proto-lake Tanganyika around the time of its formation from the Malagarasi–Congo River, and diverged into the two extant species at the onset of deep clearwater conditions. Our results prompt a more thorough examination of the relationships within Pellonulini, and the new mitochondrial genomes provide an important resource for the future study of this tribe, e.g. as a reference for species identification, genetic diversity, and macroevolutionary studies. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12862-022-02085-8.
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spelling pubmed-96351202022-11-05 Complete mitochondrial genomes and updated divergence time of the two freshwater clupeids endemic to Lake Tanganyika (Africa) suggest intralacustrine speciation Milec, Leona J. M. Vanhove, Maarten P. M. Bukinga, Fidel Muterezi De Keyzer, Els L. R. Kapepula, Vercus Lumami Masilya, Pascal Mulungula Mulimbwa, N’Sibula Wagner, Catherine E. Raeymaekers, Joost A. M. BMC Ecol Evol Research BACKGROUND: The hydrogeological history of Lake Tanganyika paints a complex image of several colonization and adaptive radiation events. The initial basin was formed around 9–12 million years ago (MYA) from the predecessor of the Malagarasi–Congo River and only 5–6 MYA, its sub-basins fused to produce the clear, deep waters of today. Next to the well-known radiations of cichlid fishes, the lake also harbours a modest clade of only two clupeid species, Stolothrissa tanganicae and Limnothrissa miodon. They are members of Pellonulini, a tribe of clupeid fishes that mostly occur in freshwater and that colonized West and Central-Africa during a period of high sea levels during the Cenozoic. There is no consensus on the phylogenetic relationships between members of Pellonulini and the timing of the colonization of Lake Tanganyika by clupeids. RESULTS: We use short-read next generation sequencing of 10X Chromium libraries to sequence and assemble the full mitochondrial genomes of S. tanganicae and L. miodon. We then use Maximum likelihood and Bayesian inference to place them into the phylogeny of Pellonulini and other clupeiforms, taking advantage of all available full mitochondrial clupeiform genomes. We identify Potamothrissa obtusirostris as the closest living relative of the Tanganyika sardines and confirm paraphyly for Microthrissa. We estimate the divergence of the Tanganyika sardines around 3.64 MYA [95% CI: 0.99, 6.29], and from P. obtusirostris around 10.92 MYA [95% CI: 6.37–15.48]. CONCLUSIONS: These estimates imply that the ancestor of the Tanganyika sardines diverged from a riverine ancestor and entered the proto-lake Tanganyika around the time of its formation from the Malagarasi–Congo River, and diverged into the two extant species at the onset of deep clearwater conditions. Our results prompt a more thorough examination of the relationships within Pellonulini, and the new mitochondrial genomes provide an important resource for the future study of this tribe, e.g. as a reference for species identification, genetic diversity, and macroevolutionary studies. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12862-022-02085-8. BioMed Central 2022-11-03 /pmc/articles/PMC9635120/ /pubmed/36329403 http://dx.doi.org/10.1186/s12862-022-02085-8 Text en © The Author(s) 2022 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research
Milec, Leona J. M.
Vanhove, Maarten P. M.
Bukinga, Fidel Muterezi
De Keyzer, Els L. R.
Kapepula, Vercus Lumami
Masilya, Pascal Mulungula
Mulimbwa, N’Sibula
Wagner, Catherine E.
Raeymaekers, Joost A. M.
Complete mitochondrial genomes and updated divergence time of the two freshwater clupeids endemic to Lake Tanganyika (Africa) suggest intralacustrine speciation
title Complete mitochondrial genomes and updated divergence time of the two freshwater clupeids endemic to Lake Tanganyika (Africa) suggest intralacustrine speciation
title_full Complete mitochondrial genomes and updated divergence time of the two freshwater clupeids endemic to Lake Tanganyika (Africa) suggest intralacustrine speciation
title_fullStr Complete mitochondrial genomes and updated divergence time of the two freshwater clupeids endemic to Lake Tanganyika (Africa) suggest intralacustrine speciation
title_full_unstemmed Complete mitochondrial genomes and updated divergence time of the two freshwater clupeids endemic to Lake Tanganyika (Africa) suggest intralacustrine speciation
title_short Complete mitochondrial genomes and updated divergence time of the two freshwater clupeids endemic to Lake Tanganyika (Africa) suggest intralacustrine speciation
title_sort complete mitochondrial genomes and updated divergence time of the two freshwater clupeids endemic to lake tanganyika (africa) suggest intralacustrine speciation
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9635120/
https://www.ncbi.nlm.nih.gov/pubmed/36329403
http://dx.doi.org/10.1186/s12862-022-02085-8
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