Extensive Population Structure Highlights an Apparent Paradox of Stasis in the Impala (Aepyceros melampus)

Genís Garcia-Erill; Xi Wang; Malthe S Rasmussen; Liam Quinn; Anubhab Khan; Laura D Bertola; Cindy G Santander; Renzo F Balboa; Joseph O Ogutu; Patrícia Pečnerová; Kristian Hanghøj; Josiah Kuja; Casia Nursyifa; Charles Masembe; Vincent Muwanika; Faysal Bibi; Ida Moltke; Hans R Siegismund; Anders Albrechtsen; Rasmus Heller

doi:10.1111/mec.17539

Extensive Population Structure Highlights an Apparent Paradox of Stasis in the Impala (Aepyceros melampus)

Genís Garcia-Erill^*, Xi Wang, Malthe S Rasmussen, Liam Quinn, Anubhab Khan, Laura D Bertola, Cindy G Santander, Renzo F Balboa, Joseph O Ogutu, Patrícia Pečnerová, Kristian Hanghøj, Josiah Kuja, Casia Nursyifa, Charles Masembe, Vincent Muwanika, Faysal Bibi, Ida Moltke, Hans R Siegismund, Anders Albrechtsen, Rasmus Heller^*

^*Corresponding author for this work

Department of Molecular Biology and Genetics - Bioinformatics Research Centre (BiRC)

Research output: Contribution to journal/Conference contribution in journal/Contribution to newspaper › Journal article › Research › peer-review

Abstract

Impalas are unusual among bovids because they have remained morphologically similar over millions of years—a phenomenon referred to as evolutionary stasis. Here, we sequenced 119 whole genomes from the two extant subspecies of impala, the common (Aepyceros melampus melampus) and black-faced (A. m. petersi) impala. We investigated the evolutionary forces working within the species to explore how they might be associated with its evolutionary stasis as a taxon. Despite being one of the most abundant bovid species, we found low genetic diversity overall, and a phylogeographic signal of spatial expansion from southern to eastern Africa. Contrary to expectations under a scenario of evolutionary stasis, we found pronounced genetic structure between and within the two subspecies with indications of ancient, but not recent, gene flow. Black-faced impala and eastern African common impala populations had more runs of homozygosity than common impala in southern Africa, and, using a proxy for genetic load, we found that natural selection is working less efficiently in these populations compared to the southern African populations. Together with the fossil record, our results are consistent with a fixed-optimum model of evolutionary stasis, in which impalas in the southern African core of the range are able to stay near their evolutionary fitness optimum as a generalist ecotone species, whereas eastern African impalas may struggle to do so due to the effects of genetic drift and reduced adaptation to the local habitat, leading to recurrent local extinction in eastern Africa and re-colonisation from the South.

Original language	English
Article number	e17539
Journal	Molecular Ecology
Volume	33
Issue	22
ISSN	0962-1083
DOIs	https://doi.org/10.1111/mec.17539
Publication status	Published - Nov 2024

Keywords

evolutionary stasis
impala
phylogeography
population genetics
whole genome sequencing

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10.1111/mec.17539Licence: CC BY-NC-ND

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Garcia-Erill, G., Wang, X., Rasmussen, MS., Quinn, L., Khan, A., Bertola, LD., Santander, CG., Balboa, RF., Ogutu, JO., Pečnerová, P., Hanghøj, K., Kuja, J., Nursyifa, C., Masembe, C., Muwanika, V., Bibi, F., Moltke, I., Siegismund, HR., Albrechtsen, A., & Heller, R. (2024). Extensive Population Structure Highlights an Apparent Paradox of Stasis in the Impala (Aepyceros melampus). Molecular Ecology, 33(22), Article e17539. https://doi.org/10.1111/mec.17539

@article{96fb671d757b400da3287625e6fccce6,

title = "Extensive Population Structure Highlights an Apparent Paradox of Stasis in the Impala (Aepyceros melampus)",

abstract = "Impalas are unusual among bovids because they have remained morphologically similar over millions of years—a phenomenon referred to as evolutionary stasis. Here, we sequenced 119 whole genomes from the two extant subspecies of impala, the common (Aepyceros melampus melampus) and black-faced (A. m. petersi) impala. We investigated the evolutionary forces working within the species to explore how they might be associated with its evolutionary stasis as a taxon. Despite being one of the most abundant bovid species, we found low genetic diversity overall, and a phylogeographic signal of spatial expansion from southern to eastern Africa. Contrary to expectations under a scenario of evolutionary stasis, we found pronounced genetic structure between and within the two subspecies with indications of ancient, but not recent, gene flow. Black-faced impala and eastern African common impala populations had more runs of homozygosity than common impala in southern Africa, and, using a proxy for genetic load, we found that natural selection is working less efficiently in these populations compared to the southern African populations. Together with the fossil record, our results are consistent with a fixed-optimum model of evolutionary stasis, in which impalas in the southern African core of the range are able to stay near their evolutionary fitness optimum as a generalist ecotone species, whereas eastern African impalas may struggle to do so due to the effects of genetic drift and reduced adaptation to the local habitat, leading to recurrent local extinction in eastern Africa and re-colonisation from the South.",

keywords = "evolutionary stasis, impala, phylogeography, population genetics, whole genome sequencing",

author = "Gen{\'i}s Garcia-Erill and Xi Wang and Malthe S Rasmussen and Liam Quinn and Anubhab Khan and Laura D Bertola and Cindy G Santander and Renzo F Balboa and Joseph O Ogutu and Patr{\'i}cia Pe{\v c}nerov{\'a} and Kristian Hangh{\o}j and Josiah Kuja and Casia Nursyifa and Charles Masembe and Vincent Muwanika and Faysal Bibi and Ida Moltke and Hans R Siegismund and Anders Albrechtsen and Rasmus Heller",

note = "Publisher Copyright: {\textcopyright} 2024 The Author(s). Molecular Ecology published by John Wiley & Sons Ltd.",

year = "2024",

month = nov,

doi = "10.1111/mec.17539",

language = "English",

volume = "33",

journal = "Molecular Ecology",

issn = "0962-1083",

publisher = "Wiley-Blackwell Publishing Ltd",

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Garcia-Erill, G, Wang, X, Rasmussen, MS, Quinn, L, Khan, A, Bertola, LD, Santander, CG, Balboa, RF, Ogutu, JO, Pečnerová, P, Hanghøj, K, Kuja, J, Nursyifa, C, Masembe, C, Muwanika, V, Bibi, F, Moltke, I, Siegismund, HR, Albrechtsen, A & Heller, R 2024, 'Extensive Population Structure Highlights an Apparent Paradox of Stasis in the Impala (Aepyceros melampus)', Molecular Ecology, vol. 33, no. 22, e17539. https://doi.org/10.1111/mec.17539

Extensive Population Structure Highlights an Apparent Paradox of Stasis in the Impala (Aepyceros melampus). / Garcia-Erill, Genís; Wang, Xi; Rasmussen, Malthe S et al.
In: Molecular Ecology, Vol. 33, No. 22, e17539, 11.2024.

Research output: Contribution to journal/Conference contribution in journal/Contribution to newspaper › Journal article › Research › peer-review

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T1 - Extensive Population Structure Highlights an Apparent Paradox of Stasis in the Impala (Aepyceros melampus)

AU - Garcia-Erill, Genís

AU - Wang, Xi

AU - Rasmussen, Malthe S

AU - Quinn, Liam

AU - Khan, Anubhab

AU - Bertola, Laura D

AU - Santander, Cindy G

AU - Balboa, Renzo F

AU - Ogutu, Joseph O

AU - Pečnerová, Patrícia

AU - Hanghøj, Kristian

AU - Kuja, Josiah

AU - Nursyifa, Casia

AU - Masembe, Charles

AU - Muwanika, Vincent

AU - Bibi, Faysal

AU - Moltke, Ida

AU - Siegismund, Hans R

AU - Albrechtsen, Anders

AU - Heller, Rasmus

PY - 2024/11

Y1 - 2024/11

N2 - Impalas are unusual among bovids because they have remained morphologically similar over millions of years—a phenomenon referred to as evolutionary stasis. Here, we sequenced 119 whole genomes from the two extant subspecies of impala, the common (Aepyceros melampus melampus) and black-faced (A. m. petersi) impala. We investigated the evolutionary forces working within the species to explore how they might be associated with its evolutionary stasis as a taxon. Despite being one of the most abundant bovid species, we found low genetic diversity overall, and a phylogeographic signal of spatial expansion from southern to eastern Africa. Contrary to expectations under a scenario of evolutionary stasis, we found pronounced genetic structure between and within the two subspecies with indications of ancient, but not recent, gene flow. Black-faced impala and eastern African common impala populations had more runs of homozygosity than common impala in southern Africa, and, using a proxy for genetic load, we found that natural selection is working less efficiently in these populations compared to the southern African populations. Together with the fossil record, our results are consistent with a fixed-optimum model of evolutionary stasis, in which impalas in the southern African core of the range are able to stay near their evolutionary fitness optimum as a generalist ecotone species, whereas eastern African impalas may struggle to do so due to the effects of genetic drift and reduced adaptation to the local habitat, leading to recurrent local extinction in eastern Africa and re-colonisation from the South.

AB - Impalas are unusual among bovids because they have remained morphologically similar over millions of years—a phenomenon referred to as evolutionary stasis. Here, we sequenced 119 whole genomes from the two extant subspecies of impala, the common (Aepyceros melampus melampus) and black-faced (A. m. petersi) impala. We investigated the evolutionary forces working within the species to explore how they might be associated with its evolutionary stasis as a taxon. Despite being one of the most abundant bovid species, we found low genetic diversity overall, and a phylogeographic signal of spatial expansion from southern to eastern Africa. Contrary to expectations under a scenario of evolutionary stasis, we found pronounced genetic structure between and within the two subspecies with indications of ancient, but not recent, gene flow. Black-faced impala and eastern African common impala populations had more runs of homozygosity than common impala in southern Africa, and, using a proxy for genetic load, we found that natural selection is working less efficiently in these populations compared to the southern African populations. Together with the fossil record, our results are consistent with a fixed-optimum model of evolutionary stasis, in which impalas in the southern African core of the range are able to stay near their evolutionary fitness optimum as a generalist ecotone species, whereas eastern African impalas may struggle to do so due to the effects of genetic drift and reduced adaptation to the local habitat, leading to recurrent local extinction in eastern Africa and re-colonisation from the South.

KW - evolutionary stasis

KW - impala

KW - phylogeography

KW - population genetics

KW - whole genome sequencing

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U2 - 10.1111/mec.17539

DO - 10.1111/mec.17539

M3 - Journal article

C2 - 39373069

AN - SCOPUS:85205938993

SN - 0962-1083

VL - 33

JO - Molecular Ecology

JF - Molecular Ecology

IS - 22

M1 - e17539

ER -

Extensive Population Structure Highlights an Apparent Paradox of Stasis in the Impala (Aepyceros melampus)

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Keywords

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