Evidence for Resistance to Coagulotoxic Effects of Australian Elapid Snake Venoms by Sympatric Prey (Blue Tongue Skinks) but Not by Predators (Monitor Lizards)

Some Australian elapids possess potently procoagulant coagulotoxic venoms which activate the zymogen prothrombin into the functional enzyme thrombin. Although the activity of Australian elapid prothrombin-activators has been heavily investigated with respect to the mammalian, and in particular, huma...

Full description

Bibliographic Details
Main Authors: Nicholas J. Youngman, Joshua Llinas, Bryan G. Fry
Format: Article
Language:English
Published: MDPI AG 2021-08-01
Series:Toxins
Subjects:
Online Access:https://www.mdpi.com/2072-6651/13/9/590
_version_ 1797517089657847808
author Nicholas J. Youngman
Joshua Llinas
Bryan G. Fry
author_facet Nicholas J. Youngman
Joshua Llinas
Bryan G. Fry
author_sort Nicholas J. Youngman
collection DOAJ
description Some Australian elapids possess potently procoagulant coagulotoxic venoms which activate the zymogen prothrombin into the functional enzyme thrombin. Although the activity of Australian elapid prothrombin-activators has been heavily investigated with respect to the mammalian, and in particular, human clotting cascades, very few studies have investigated the activity of their venom upon reptile plasmas. This is despite lizards representing both the primary diet of most Australian elapids and also representing natural predators. This study investigated the procoagulant actions of a diverse range of Australian elapid species upon plasma from known prey species within the genera <i>Tiliqua</i> (blue tongue skinks) as well as known predator species within the genera <i>Varanus</i> (monitor lizards). In addition to identifying significant variation in the natural responses of the coagulation cascade between species from the genera <i>Tiliqua</i> and <i>Varanus</i> relative to each other, as well as other vertebrate lineages, notable differences in venom activity were also observed. Within the genus <i>Tiliqua</i>, both <i>T. rugosa</i> and <i>T. scincoides</i> plasma displayed significant resistance to the procoagulant activity of <i>Pseudechis porphyriacus</i> venom, despite being susceptible to all other procoagulant elapid venoms. These results indicate that <i>T. rugosa</i> and <i>T. scincoides</i> have evolved resistance within their plasma to the coagulotoxic venom activity of the sympatric species <i>P. porphyriacus</i>. Other venoms were able to activate <i>Tiliqua</i> prothrombin, which suggests that the lessened activity of <i>P. porphyriacus</i> venom is not due to modifications of the prothrombin and may instead be due to a serum factor that specifically binds to <i>P. porphyriacus</i> toxins, as has been previously seen for squirrels resistant to rattlesnake venom. In contrast, none of the predatory lizards studied (<i>Varanus giganteus</i>, <i>V. mertensi</i> and <i>V. varius</i>) demonstrated resistance to the venom. This suggests that the mechanical protection afforded by thick osteodermic scales, and prey handling behaviour, removes a selection pressure for the evolution of resistance in these large predatory lizards. These results therefore reveal differential interactions between venoms of snakes with sympatric lizards that are on opposite sides of the predator–prey arms race.
first_indexed 2024-03-10T07:09:56Z
format Article
id doaj.art-bc323f73ba1e436b861f74602bd7552f
institution Directory Open Access Journal
issn 2072-6651
language English
last_indexed 2024-03-10T07:09:56Z
publishDate 2021-08-01
publisher MDPI AG
record_format Article
series Toxins
spelling doaj.art-bc323f73ba1e436b861f74602bd7552f2023-11-22T15:30:37ZengMDPI AGToxins2072-66512021-08-0113959010.3390/toxins13090590Evidence for Resistance to Coagulotoxic Effects of Australian Elapid Snake Venoms by Sympatric Prey (Blue Tongue Skinks) but Not by Predators (Monitor Lizards)Nicholas J. Youngman0Joshua Llinas1Bryan G. Fry2Venom Evolution Lab, School of Biological Sciences, University of Queensland, St Lucia, QLD 4072, AustraliaUnusual Pet Vets, Jindalee, QLD 4074, AustraliaVenom Evolution Lab, School of Biological Sciences, University of Queensland, St Lucia, QLD 4072, AustraliaSome Australian elapids possess potently procoagulant coagulotoxic venoms which activate the zymogen prothrombin into the functional enzyme thrombin. Although the activity of Australian elapid prothrombin-activators has been heavily investigated with respect to the mammalian, and in particular, human clotting cascades, very few studies have investigated the activity of their venom upon reptile plasmas. This is despite lizards representing both the primary diet of most Australian elapids and also representing natural predators. This study investigated the procoagulant actions of a diverse range of Australian elapid species upon plasma from known prey species within the genera <i>Tiliqua</i> (blue tongue skinks) as well as known predator species within the genera <i>Varanus</i> (monitor lizards). In addition to identifying significant variation in the natural responses of the coagulation cascade between species from the genera <i>Tiliqua</i> and <i>Varanus</i> relative to each other, as well as other vertebrate lineages, notable differences in venom activity were also observed. Within the genus <i>Tiliqua</i>, both <i>T. rugosa</i> and <i>T. scincoides</i> plasma displayed significant resistance to the procoagulant activity of <i>Pseudechis porphyriacus</i> venom, despite being susceptible to all other procoagulant elapid venoms. These results indicate that <i>T. rugosa</i> and <i>T. scincoides</i> have evolved resistance within their plasma to the coagulotoxic venom activity of the sympatric species <i>P. porphyriacus</i>. Other venoms were able to activate <i>Tiliqua</i> prothrombin, which suggests that the lessened activity of <i>P. porphyriacus</i> venom is not due to modifications of the prothrombin and may instead be due to a serum factor that specifically binds to <i>P. porphyriacus</i> toxins, as has been previously seen for squirrels resistant to rattlesnake venom. In contrast, none of the predatory lizards studied (<i>Varanus giganteus</i>, <i>V. mertensi</i> and <i>V. varius</i>) demonstrated resistance to the venom. This suggests that the mechanical protection afforded by thick osteodermic scales, and prey handling behaviour, removes a selection pressure for the evolution of resistance in these large predatory lizards. These results therefore reveal differential interactions between venoms of snakes with sympatric lizards that are on opposite sides of the predator–prey arms race.https://www.mdpi.com/2072-6651/13/9/590coagulotoxinsplasma<i>Pseudechis</i><i>Pseudonaja</i>resistance<i>Tiliqua</i>
spellingShingle Nicholas J. Youngman
Joshua Llinas
Bryan G. Fry
Evidence for Resistance to Coagulotoxic Effects of Australian Elapid Snake Venoms by Sympatric Prey (Blue Tongue Skinks) but Not by Predators (Monitor Lizards)
Toxins
coagulotoxins
plasma
<i>Pseudechis</i>
<i>Pseudonaja</i>
resistance
<i>Tiliqua</i>
title Evidence for Resistance to Coagulotoxic Effects of Australian Elapid Snake Venoms by Sympatric Prey (Blue Tongue Skinks) but Not by Predators (Monitor Lizards)
title_full Evidence for Resistance to Coagulotoxic Effects of Australian Elapid Snake Venoms by Sympatric Prey (Blue Tongue Skinks) but Not by Predators (Monitor Lizards)
title_fullStr Evidence for Resistance to Coagulotoxic Effects of Australian Elapid Snake Venoms by Sympatric Prey (Blue Tongue Skinks) but Not by Predators (Monitor Lizards)
title_full_unstemmed Evidence for Resistance to Coagulotoxic Effects of Australian Elapid Snake Venoms by Sympatric Prey (Blue Tongue Skinks) but Not by Predators (Monitor Lizards)
title_short Evidence for Resistance to Coagulotoxic Effects of Australian Elapid Snake Venoms by Sympatric Prey (Blue Tongue Skinks) but Not by Predators (Monitor Lizards)
title_sort evidence for resistance to coagulotoxic effects of australian elapid snake venoms by sympatric prey blue tongue skinks but not by predators monitor lizards
topic coagulotoxins
plasma
<i>Pseudechis</i>
<i>Pseudonaja</i>
resistance
<i>Tiliqua</i>
url https://www.mdpi.com/2072-6651/13/9/590
work_keys_str_mv AT nicholasjyoungman evidenceforresistancetocoagulotoxiceffectsofaustralianelapidsnakevenomsbysympatricpreybluetongueskinksbutnotbypredatorsmonitorlizards
AT joshuallinas evidenceforresistancetocoagulotoxiceffectsofaustralianelapidsnakevenomsbysympatricpreybluetongueskinksbutnotbypredatorsmonitorlizards
AT bryangfry evidenceforresistancetocoagulotoxiceffectsofaustralianelapidsnakevenomsbysympatricpreybluetongueskinksbutnotbypredatorsmonitorlizards