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Physiological constraints dictate toxin spatial heterogeneity in snake venom glands

BACKGROUND: Venoms are ecological innovations that have evolved numerous times, on each occasion accompanied by the co-evolution of specialised morphological and behavioural characters for venom production and delivery. The close evolutionary interdependence between these characters is exemplified b...

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Autores principales: Kazandjian, Taline D., Hamilton, Brett R., Robinson, Samuel D., Hall, Steven R., Bartlett, Keirah E., Rowley, Paul, Wilkinson, Mark C., Casewell, Nicholas R., Undheim, Eivind A. B.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9238143/
https://www.ncbi.nlm.nih.gov/pubmed/35761243
http://dx.doi.org/10.1186/s12915-022-01350-y
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author Kazandjian, Taline D.
Hamilton, Brett R.
Robinson, Samuel D.
Hall, Steven R.
Bartlett, Keirah E.
Rowley, Paul
Wilkinson, Mark C.
Casewell, Nicholas R.
Undheim, Eivind A. B.
author_facet Kazandjian, Taline D.
Hamilton, Brett R.
Robinson, Samuel D.
Hall, Steven R.
Bartlett, Keirah E.
Rowley, Paul
Wilkinson, Mark C.
Casewell, Nicholas R.
Undheim, Eivind A. B.
author_sort Kazandjian, Taline D.
collection PubMed
description BACKGROUND: Venoms are ecological innovations that have evolved numerous times, on each occasion accompanied by the co-evolution of specialised morphological and behavioural characters for venom production and delivery. The close evolutionary interdependence between these characters is exemplified by animals that control the composition of their secreted venom. This ability depends in part on the production of different toxins in different locations of the venom gland, which was recently documented in venomous snakes. Here, we test the hypothesis that the distinct spatial distributions of toxins in snake venom glands are an adaptation that enables the secretion of venoms with distinct ecological functions. RESULTS: We show that the main defensive and predatory peptide toxins are produced in distinct regions of the venom glands of the black-necked spitting cobra (Naja nigricollis), but these distributions likely reflect developmental effects. Indeed, we detected no significant differences in venom collected via defensive ‘spitting’ or predatory ‘biting’ events from the same specimens representing multiple lineages of spitting cobra. We also found the same spatial distribution of toxins in a non-spitting cobra and show that heterogeneous toxin distribution is a feature shared with a viper with primarily predatory venom. CONCLUSIONS: Our findings suggest that heterogeneous distributions of toxins are not an adaptation to controlling venom composition in snakes. Instead, it likely reflects physiological constraints on toxin production by the venom glands, opening avenues for future research on the mechanisms of functional differentiation of populations of protein-secreting cells within adaptive contexts. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12915-022-01350-y.
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spelling pubmed-92381432022-06-29 Physiological constraints dictate toxin spatial heterogeneity in snake venom glands Kazandjian, Taline D. Hamilton, Brett R. Robinson, Samuel D. Hall, Steven R. Bartlett, Keirah E. Rowley, Paul Wilkinson, Mark C. Casewell, Nicholas R. Undheim, Eivind A. B. BMC Biol Research Article BACKGROUND: Venoms are ecological innovations that have evolved numerous times, on each occasion accompanied by the co-evolution of specialised morphological and behavioural characters for venom production and delivery. The close evolutionary interdependence between these characters is exemplified by animals that control the composition of their secreted venom. This ability depends in part on the production of different toxins in different locations of the venom gland, which was recently documented in venomous snakes. Here, we test the hypothesis that the distinct spatial distributions of toxins in snake venom glands are an adaptation that enables the secretion of venoms with distinct ecological functions. RESULTS: We show that the main defensive and predatory peptide toxins are produced in distinct regions of the venom glands of the black-necked spitting cobra (Naja nigricollis), but these distributions likely reflect developmental effects. Indeed, we detected no significant differences in venom collected via defensive ‘spitting’ or predatory ‘biting’ events from the same specimens representing multiple lineages of spitting cobra. We also found the same spatial distribution of toxins in a non-spitting cobra and show that heterogeneous toxin distribution is a feature shared with a viper with primarily predatory venom. CONCLUSIONS: Our findings suggest that heterogeneous distributions of toxins are not an adaptation to controlling venom composition in snakes. Instead, it likely reflects physiological constraints on toxin production by the venom glands, opening avenues for future research on the mechanisms of functional differentiation of populations of protein-secreting cells within adaptive contexts. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12915-022-01350-y. BioMed Central 2022-06-27 /pmc/articles/PMC9238143/ /pubmed/35761243 http://dx.doi.org/10.1186/s12915-022-01350-y 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 Article
Kazandjian, Taline D.
Hamilton, Brett R.
Robinson, Samuel D.
Hall, Steven R.
Bartlett, Keirah E.
Rowley, Paul
Wilkinson, Mark C.
Casewell, Nicholas R.
Undheim, Eivind A. B.
Physiological constraints dictate toxin spatial heterogeneity in snake venom glands
title Physiological constraints dictate toxin spatial heterogeneity in snake venom glands
title_full Physiological constraints dictate toxin spatial heterogeneity in snake venom glands
title_fullStr Physiological constraints dictate toxin spatial heterogeneity in snake venom glands
title_full_unstemmed Physiological constraints dictate toxin spatial heterogeneity in snake venom glands
title_short Physiological constraints dictate toxin spatial heterogeneity in snake venom glands
title_sort physiological constraints dictate toxin spatial heterogeneity in snake venom glands
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9238143/
https://www.ncbi.nlm.nih.gov/pubmed/35761243
http://dx.doi.org/10.1186/s12915-022-01350-y
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