The Fast and the Furriest: Investigating the Rate of Selection on Mammalian Toxins

The evolution of venom and the selection pressures that act on toxins have been increasingly researched within toxinology in the last two decades, in part due to the exceptionally high rates of diversifying selection observed in animal toxins. In 2015, Sungar and Moran proposed the ‘two-speed’ model...

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Main Authors: Leah Lucy Joscelyne Fitzpatrick, Vincent Nijman, Rodrigo Ligabue-Braun, K. Anne-Isola Nekaris
Format: Article
Language:English
Published: MDPI AG 2022-12-01
Series:Toxins
Subjects:
Online Access:https://www.mdpi.com/2072-6651/14/12/842
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author Leah Lucy Joscelyne Fitzpatrick
Vincent Nijman
Rodrigo Ligabue-Braun
K. Anne-Isola Nekaris
author_facet Leah Lucy Joscelyne Fitzpatrick
Vincent Nijman
Rodrigo Ligabue-Braun
K. Anne-Isola Nekaris
author_sort Leah Lucy Joscelyne Fitzpatrick
collection DOAJ
description The evolution of venom and the selection pressures that act on toxins have been increasingly researched within toxinology in the last two decades, in part due to the exceptionally high rates of diversifying selection observed in animal toxins. In 2015, Sungar and Moran proposed the ‘two-speed’ model of toxin evolution linking evolutionary age of a group to the rates of selection acting on toxins but due to a lack of data, mammals were not included as less than 30 species of venomous mammal have been recorded, represented by elusive species which produce small amounts of venom. Due to advances in genomics and transcriptomics, the availability of toxin sequences from venomous mammals has been increasing. Using branch- and site-specific selection models, we present the rates of both episodic and pervasive selection acting upon venomous mammal toxins as a group for the first time. We identified seven toxin groups present within venomous mammals, representing Chiroptera, Eulipotyphla and Monotremata: KLK1, Plasminogen Activator, Desmallipins, PACAP, CRiSP, Kunitz Domain One and Kunitz Domain Two. All but one group (KLK1) was identified by our results to be evolving under both episodic and pervasive diversifying selection with four toxin groups having sites that were implicated in the fitness of the animal by TreeSAAP (Selection on Amino Acid Properties). Our results suggest that venomous mammal ecology, behaviour or genomic evolution are the main drivers of selection, although evolutionary age may still be a factor. Our conclusion from these results indicates that mammalian toxins are following the two-speed model of selection, evolving predominately under diversifying selection, fitting in with other younger venomous taxa like snakes and cone snails—with high amounts of accumulating mutations, leading to more novel adaptions in their toxins.
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spelling doaj.art-0ecbcf7f771c4b4d9fb42699ff0e41f52023-11-24T18:26:44ZengMDPI AGToxins2072-66512022-12-01141284210.3390/toxins14120842The Fast and the Furriest: Investigating the Rate of Selection on Mammalian ToxinsLeah Lucy Joscelyne Fitzpatrick0Vincent Nijman1Rodrigo Ligabue-Braun2K. Anne-Isola Nekaris3Nocturnal Primate Research Group, Department of Social Sciences, Oxford Brookes University, Oxford OX3 0BP, UKNocturnal Primate Research Group, Department of Social Sciences, Oxford Brookes University, Oxford OX3 0BP, UKDepartment of Pharmacosciences, Federal University of Health Sciences of Porto Alegre (UFCSPA), Avenida Sarmento Leite 245, Porto Alegre 90050-130, BrazilNocturnal Primate Research Group, Department of Social Sciences, Oxford Brookes University, Oxford OX3 0BP, UKThe evolution of venom and the selection pressures that act on toxins have been increasingly researched within toxinology in the last two decades, in part due to the exceptionally high rates of diversifying selection observed in animal toxins. In 2015, Sungar and Moran proposed the ‘two-speed’ model of toxin evolution linking evolutionary age of a group to the rates of selection acting on toxins but due to a lack of data, mammals were not included as less than 30 species of venomous mammal have been recorded, represented by elusive species which produce small amounts of venom. Due to advances in genomics and transcriptomics, the availability of toxin sequences from venomous mammals has been increasing. Using branch- and site-specific selection models, we present the rates of both episodic and pervasive selection acting upon venomous mammal toxins as a group for the first time. We identified seven toxin groups present within venomous mammals, representing Chiroptera, Eulipotyphla and Monotremata: KLK1, Plasminogen Activator, Desmallipins, PACAP, CRiSP, Kunitz Domain One and Kunitz Domain Two. All but one group (KLK1) was identified by our results to be evolving under both episodic and pervasive diversifying selection with four toxin groups having sites that were implicated in the fitness of the animal by TreeSAAP (Selection on Amino Acid Properties). Our results suggest that venomous mammal ecology, behaviour or genomic evolution are the main drivers of selection, although evolutionary age may still be a factor. Our conclusion from these results indicates that mammalian toxins are following the two-speed model of selection, evolving predominately under diversifying selection, fitting in with other younger venomous taxa like snakes and cone snails—with high amounts of accumulating mutations, leading to more novel adaptions in their toxins.https://www.mdpi.com/2072-6651/14/12/842mammalsselection ratesdN/dSvenom evolutionPrimatesEulipotyphla
spellingShingle Leah Lucy Joscelyne Fitzpatrick
Vincent Nijman
Rodrigo Ligabue-Braun
K. Anne-Isola Nekaris
The Fast and the Furriest: Investigating the Rate of Selection on Mammalian Toxins
Toxins
mammals
selection rates
dN/dS
venom evolution
Primates
Eulipotyphla
title The Fast and the Furriest: Investigating the Rate of Selection on Mammalian Toxins
title_full The Fast and the Furriest: Investigating the Rate of Selection on Mammalian Toxins
title_fullStr The Fast and the Furriest: Investigating the Rate of Selection on Mammalian Toxins
title_full_unstemmed The Fast and the Furriest: Investigating the Rate of Selection on Mammalian Toxins
title_short The Fast and the Furriest: Investigating the Rate of Selection on Mammalian Toxins
title_sort fast and the furriest investigating the rate of selection on mammalian toxins
topic mammals
selection rates
dN/dS
venom evolution
Primates
Eulipotyphla
url https://www.mdpi.com/2072-6651/14/12/842
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