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

Abstract 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...

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Main Authors: Leona J. M. Milec, Maarten P. M. Vanhove, Fidel Muterezi Bukinga, Els L. R. De Keyzer, Vercus Lumami Kapepula, Pascal Mulungula Masilya, N’Sibula Mulimbwa, Catherine E. Wagner, Joost A. M. Raeymaekers
Format: Article
Language:English
Published: BMC 2022-11-01
Series:BMC Ecology and Evolution
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Online Access:https://doi.org/10.1186/s12862-022-02085-8
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author Leona J. M. Milec
Maarten P. M. Vanhove
Fidel Muterezi Bukinga
Els L. R. De Keyzer
Vercus Lumami Kapepula
Pascal Mulungula Masilya
N’Sibula Mulimbwa
Catherine E. Wagner
Joost A. M. Raeymaekers
author_facet Leona J. M. Milec
Maarten P. M. Vanhove
Fidel Muterezi Bukinga
Els L. R. De Keyzer
Vercus Lumami Kapepula
Pascal Mulungula Masilya
N’Sibula Mulimbwa
Catherine E. Wagner
Joost A. M. Raeymaekers
author_sort Leona J. M. Milec
collection DOAJ
description Abstract 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.
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spelling doaj.art-e78347a4463d4bf2be85f3c2a6d2c44f2022-12-22T03:58:00ZengBMCBMC Ecology and Evolution2730-71822022-11-0122111710.1186/s12862-022-02085-8Complete mitochondrial genomes and updated divergence time of the two freshwater clupeids endemic to Lake Tanganyika (Africa) suggest intralacustrine speciationLeona J. M. Milec0Maarten P. M. Vanhove1Fidel Muterezi Bukinga2Els L. R. De Keyzer3Vercus Lumami Kapepula4Pascal Mulungula Masilya5N’Sibula Mulimbwa6Catherine E. Wagner7Joost A. M. Raeymaekers8Faculty of Biosciences and Aquaculture, Nord UniversityCentre for Environmental Sciences, Research Group Zoology: Biodiversity and Toxicology, Hasselt UniversityCentre de Recherche en Hydrobiologie-Uvira (CRH-Uvira)Laboratory of Biodiversity and Evolutionary Genomics, Department of Biology, KU LeuvenCentre de Recherche en Hydrobiologie-Uvira (CRH-Uvira)Centre de Recherche en Hydrobiologie-Uvira (CRH-Uvira)Centre de Recherche en Hydrobiologie-Uvira (CRH-Uvira)University of WyomingFaculty of Biosciences and Aquaculture, Nord UniversityAbstract 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.https://doi.org/10.1186/s12862-022-02085-8Great LakesClupeiformesMitogenomeTime calibrationPhylogenetics
spellingShingle Leona J. M. Milec
Maarten P. M. Vanhove
Fidel Muterezi Bukinga
Els L. R. De Keyzer
Vercus Lumami Kapepula
Pascal Mulungula Masilya
N’Sibula Mulimbwa
Catherine E. Wagner
Joost A. M. Raeymaekers
Complete mitochondrial genomes and updated divergence time of the two freshwater clupeids endemic to Lake Tanganyika (Africa) suggest intralacustrine speciation
BMC Ecology and Evolution
Great Lakes
Clupeiformes
Mitogenome
Time calibration
Phylogenetics
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 Great Lakes
Clupeiformes
Mitogenome
Time calibration
Phylogenetics
url https://doi.org/10.1186/s12862-022-02085-8
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