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Snakes on an African plain: the radiation of Crotaphopeltis and Philothamnus into open habitat (Serpentes: Colubridae)

BACKGROUND: The African continent is comprised of several different biomes, although savanna is the most prevalent. The current heterogeneous landscape was formed through long-term vegetation shifts as a result of the global cooling trend since the Oligocene epoch. The overwhelming trend was a shift...

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Autores principales: Engelbrecht, Hanlie M., Branch, William R., Tolley, Krystal A.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: PeerJ Inc. 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8351568/
https://www.ncbi.nlm.nih.gov/pubmed/34434643
http://dx.doi.org/10.7717/peerj.11728
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author Engelbrecht, Hanlie M.
Branch, William R.
Tolley, Krystal A.
author_facet Engelbrecht, Hanlie M.
Branch, William R.
Tolley, Krystal A.
author_sort Engelbrecht, Hanlie M.
collection PubMed
description BACKGROUND: The African continent is comprised of several different biomes, although savanna is the most prevalent. The current heterogeneous landscape was formed through long-term vegetation shifts as a result of the global cooling trend since the Oligocene epoch. The overwhelming trend was a shift from primarily forest, to primarily savanna. As such, faunal groups that emerged during the Paleogene/Neogene period and have species distributed in both forest and savanna habitat should show a genetic signature of the possible evolutionary impact of these biome developments. Crotaphopeltis and Philothamnus (Colubridae) are excellent taxa to investigate the evolutionary impact of these biome developments on widespread African colubrid snakes, and whether timing and patterns of radiation are synchronous with biome reorganisation. METHODS: A phylogenetic framework was used to investigate timing of lineage diversification. Phylogenetic analysis included both genera as well as other Colubridae to construct a temporal framework in order to estimate radiation times for Crotaphopeltis and Philothamnus. Lineage diversification was estimated in Bayesian Evolutionary Analysis Sampling Trees (BEAST), using two mitochondrial markers (cyt–b, ND4), one nuclear marker (c–mos), and incorporating one fossil and two biogeographical calibration points. Vegetation layers were used to classify and confirm species association with broad biome types (‘closed’ = forest, ‘open’ = savanna/other), and the ancestral habitat state for each genus was estimated. RESULTS: Philothamnus showed an ancestral state of closed habitat, but the ancestral habitat type for Crotaphopeltis was equivocal. Both genera showed similar timing of lineage diversification diverging from their sister genera during the Oligocene/Miocene transition (ca. 25 Mya), with subsequent species radiation in the Mid-Miocene. Philothamnus appeared to have undergone allopatric speciation during Mid-Miocene forest fragmentation. Habitat generalist and open habitat specialist species emerged as savanna became more prevalent, while at least two forest associated lineages within Crotaphopeltis moved into Afromontane forest habitat secondarily and independently. DISCUSSION: With similar diversification times, but contrasting ancestral habitat reconstructions, we show that these genera have responded very differently to the same broad biome shifts. Differences in biogeographical patterns for the two African colubrid genera is likely an effect of distinct life-history traits, such as the arboreous habits of Philothamnus compared to the terrestrial lifestyle of Crotaphopeltis.
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spelling pubmed-83515682021-08-24 Snakes on an African plain: the radiation of Crotaphopeltis and Philothamnus into open habitat (Serpentes: Colubridae) Engelbrecht, Hanlie M. Branch, William R. Tolley, Krystal A. PeerJ Biodiversity BACKGROUND: The African continent is comprised of several different biomes, although savanna is the most prevalent. The current heterogeneous landscape was formed through long-term vegetation shifts as a result of the global cooling trend since the Oligocene epoch. The overwhelming trend was a shift from primarily forest, to primarily savanna. As such, faunal groups that emerged during the Paleogene/Neogene period and have species distributed in both forest and savanna habitat should show a genetic signature of the possible evolutionary impact of these biome developments. Crotaphopeltis and Philothamnus (Colubridae) are excellent taxa to investigate the evolutionary impact of these biome developments on widespread African colubrid snakes, and whether timing and patterns of radiation are synchronous with biome reorganisation. METHODS: A phylogenetic framework was used to investigate timing of lineage diversification. Phylogenetic analysis included both genera as well as other Colubridae to construct a temporal framework in order to estimate radiation times for Crotaphopeltis and Philothamnus. Lineage diversification was estimated in Bayesian Evolutionary Analysis Sampling Trees (BEAST), using two mitochondrial markers (cyt–b, ND4), one nuclear marker (c–mos), and incorporating one fossil and two biogeographical calibration points. Vegetation layers were used to classify and confirm species association with broad biome types (‘closed’ = forest, ‘open’ = savanna/other), and the ancestral habitat state for each genus was estimated. RESULTS: Philothamnus showed an ancestral state of closed habitat, but the ancestral habitat type for Crotaphopeltis was equivocal. Both genera showed similar timing of lineage diversification diverging from their sister genera during the Oligocene/Miocene transition (ca. 25 Mya), with subsequent species radiation in the Mid-Miocene. Philothamnus appeared to have undergone allopatric speciation during Mid-Miocene forest fragmentation. Habitat generalist and open habitat specialist species emerged as savanna became more prevalent, while at least two forest associated lineages within Crotaphopeltis moved into Afromontane forest habitat secondarily and independently. DISCUSSION: With similar diversification times, but contrasting ancestral habitat reconstructions, we show that these genera have responded very differently to the same broad biome shifts. Differences in biogeographical patterns for the two African colubrid genera is likely an effect of distinct life-history traits, such as the arboreous habits of Philothamnus compared to the terrestrial lifestyle of Crotaphopeltis. PeerJ Inc. 2021-08-06 /pmc/articles/PMC8351568/ /pubmed/34434643 http://dx.doi.org/10.7717/peerj.11728 Text en ©2021 Engelbrecht et al. https://creativecommons.org/licenses/by/4.0/This is an open access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, reproduction and adaptation in any medium and for any purpose provided that it is properly attributed. For attribution, the original author(s), title, publication source (PeerJ) and either DOI or URL of the article must be cited.
spellingShingle Biodiversity
Engelbrecht, Hanlie M.
Branch, William R.
Tolley, Krystal A.
Snakes on an African plain: the radiation of Crotaphopeltis and Philothamnus into open habitat (Serpentes: Colubridae)
title Snakes on an African plain: the radiation of Crotaphopeltis and Philothamnus into open habitat (Serpentes: Colubridae)
title_full Snakes on an African plain: the radiation of Crotaphopeltis and Philothamnus into open habitat (Serpentes: Colubridae)
title_fullStr Snakes on an African plain: the radiation of Crotaphopeltis and Philothamnus into open habitat (Serpentes: Colubridae)
title_full_unstemmed Snakes on an African plain: the radiation of Crotaphopeltis and Philothamnus into open habitat (Serpentes: Colubridae)
title_short Snakes on an African plain: the radiation of Crotaphopeltis and Philothamnus into open habitat (Serpentes: Colubridae)
title_sort snakes on an african plain: the radiation of crotaphopeltis and philothamnus into open habitat (serpentes: colubridae)
topic Biodiversity
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8351568/
https://www.ncbi.nlm.nih.gov/pubmed/34434643
http://dx.doi.org/10.7717/peerj.11728
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