Ecological and biogeographic processes drive the proteome evolution of snake venom
Corresponding Author
Tuany Siqueira-Silva
PIBi Lab – Laboratório de Pesquisas Integrativas em Biodiversidade, Universidade Federal de Sergipe, São Cristóvão, Sergipe, Brazil
Correspondence
Tuany Siqueira-Silva, Laboratório de Pesquisas Integrativas em Biodiversidade, Department of Biology, Universidade Federal de Sergipe, Av. Marechal Rondon, s/n - Jardim Rosa Elze, São Cristóvão - SE, 49100-000, Brazil.
Email: [email protected]
Search for more papers by this authorLuiz Antônio Gonzaga de Lima
PIBi Lab – Laboratório de Pesquisas Integrativas em Biodiversidade, Universidade Federal de Sergipe, São Cristóvão, Sergipe, Brazil
Search for more papers by this authorJônatas Chaves-Silveira
PIBi Lab – Laboratório de Pesquisas Integrativas em Biodiversidade, Universidade Federal de Sergipe, São Cristóvão, Sergipe, Brazil
Search for more papers by this authorTalita Ferreira Amado
BioMa – Biodiversity and Macroecology Lab, Universidad Rey Juan Carlos, Móstoles, Madrid, Spain
Search for more papers by this authorJulian Naipauer
UM-CFAR/ Sylvester CCC Argentina Consortium for Research and Training in Virally induced AIDS-Malignancies, Tumor Biology Program, Sylvester Comprehensive Cancer Center and Miami Center for AIDS Research, Department of Microbiology and Immunology, University of Miami Miller School of Medicine, Miami, Florida, USA
Search for more papers by this authorPablo Riul
Deptartamento de Sistemática e Ecologia, Universidade Federal da Paraíba, João Pessoa, Paraíba, Brazil
Search for more papers by this authorPablo Ariel Martinez
PIBi Lab – Laboratório de Pesquisas Integrativas em Biodiversidade, Universidade Federal de Sergipe, São Cristóvão, Sergipe, Brazil
Search for more papers by this authorCorresponding Author
Tuany Siqueira-Silva
PIBi Lab – Laboratório de Pesquisas Integrativas em Biodiversidade, Universidade Federal de Sergipe, São Cristóvão, Sergipe, Brazil
Correspondence
Tuany Siqueira-Silva, Laboratório de Pesquisas Integrativas em Biodiversidade, Department of Biology, Universidade Federal de Sergipe, Av. Marechal Rondon, s/n - Jardim Rosa Elze, São Cristóvão - SE, 49100-000, Brazil.
Email: [email protected]
Search for more papers by this authorLuiz Antônio Gonzaga de Lima
PIBi Lab – Laboratório de Pesquisas Integrativas em Biodiversidade, Universidade Federal de Sergipe, São Cristóvão, Sergipe, Brazil
Search for more papers by this authorJônatas Chaves-Silveira
PIBi Lab – Laboratório de Pesquisas Integrativas em Biodiversidade, Universidade Federal de Sergipe, São Cristóvão, Sergipe, Brazil
Search for more papers by this authorTalita Ferreira Amado
BioMa – Biodiversity and Macroecology Lab, Universidad Rey Juan Carlos, Móstoles, Madrid, Spain
Search for more papers by this authorJulian Naipauer
UM-CFAR/ Sylvester CCC Argentina Consortium for Research and Training in Virally induced AIDS-Malignancies, Tumor Biology Program, Sylvester Comprehensive Cancer Center and Miami Center for AIDS Research, Department of Microbiology and Immunology, University of Miami Miller School of Medicine, Miami, Florida, USA
Search for more papers by this authorPablo Riul
Deptartamento de Sistemática e Ecologia, Universidade Federal da Paraíba, João Pessoa, Paraíba, Brazil
Search for more papers by this authorPablo Ariel Martinez
PIBi Lab – Laboratório de Pesquisas Integrativas em Biodiversidade, Universidade Federal de Sergipe, São Cristóvão, Sergipe, Brazil
Search for more papers by this authorAbstract
Aim
The emergence of venom is an evolutionary innovation that favoured the diversification and survival of snakes. The composition of snake venoms is known in detail from venom gland proteomic data. However, there is still a gap of knowledge about the forces that lead to the expression of different toxins in different proportions in the venom cocktail across space and time.
Location
World.
Time period
Modern.
Major taxa studied
Elapidae and Viperidae.
Methods
We integrated proteomic data with phylogenetic comparative methods to understand how ecological and biogeographic processes drive the evolution of snake venom.
Results
We observed that more productive environments favour a more complex venom, with more toxins in similar proportions. We found that taxa that live on islands, where there is lower variability of resources, tended to present less complex venom dominated by few toxins. In such cases, the extent of an island's isolation seems to be a relevant factor for faster fixation of specific venom compositions.
Main conclusion
We show that ecological and biogeographic processes, which can act differentially over time and space, affect the gene expression of toxins in snake venoms.
Open Research
DATA AVAILABILITY STATEMENT
The data supporting the results are available via Dryad: https://doi.org/10.5061/dryad.nzs7h44qs
Supporting Information
Filename | Description |
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geb13359-sup-0001-Supinfo.docxWord document, 193.8 KB | Supplementary Material |
geb13359-sup-0002-FigS1.pdfPDF document, 37.5 KB | Fig S1 |
Please note: The publisher is not responsible for the content or functionality of any supporting information supplied by the authors. Any queries (other than missing content) should be directed to the corresponding author for the article.
REFERENCES
- Allen, A. P., Brown, J. H., & Gillooly, J. F. (2002). Global biodiversity, biochemical kinetics, and the energetic-equivalence rule. Science, 297(5586), 1545–1548. https://doi.org/10.1126/science.1072380
- Arnold, S. J. (1993). Foraging theory and prey size-predator size relations in snakes. In R. A. Seigel & J. T Collins (Eds.), Snakes: Ecology and Behavior ( 2nd ed., pp. 87–115). McGraw-Hill.
- Barlow, A., Pook, C. E., Harrison, R. A., & Wüster, W. (2009). Coevolution of diet and prey-specific venom activity supports the role of selection in snake venom evolution. Proceedings of the Royal Society B: Biological Sciences, 276, 2443–2449. https://doi.org/10.1098/rspb.2009.0048
- Barua, A., & Mikheyev, A. S. (2021). An ancient, conserved gene regulatory network led to the rise of oral venom systems. Proceedings of the National Academy of Sciences, 118(14), e2021311118. https://doi.org/10.1073/pnas.2021311118
- Barua, A., Mikheyev, A. S., & Russo, C. (2019). Many options, few solutions: Over 60 my snakes converged on a few optimal venom formulations. Molecular Biology and Evolution, 36, 1964–1974. https://doi.org/10.1093/molbev/msz125
- Booth, T. H., Nix, H. A., Busby, J. R., & Hutchinson, M. F. (2014). BIOCLIM: The first species distribution modelling package, its early applications and relevance to most current MaxEnt studies. Diversity and Distributions, 20, 1–9.
- Bouckaert, R., Vaughan, T. G., Barido-Sottani, J., Duchêne, S., Fourment, M., Gavryushkina, A., Heled, J., Jones, G., Kühnert, D., De Maio, N., Matschiner, M., Mendes, F. K., Müller, N. F., Ogilvie, H. A., Du Plessis, L., Popinga, A., Rambaut, A., Rasmussen, D., Siveroni, I., … Drummond, A. J. (2019). BEAST 2.5: An advanced software platform for Bayesian evolutionary analysis. PLoS Computational Biology, 15, 1–28. https://doi.org/10.1371/journal.pcbi.1006650
- Brito, J. C. (2004). Feeding ecology of Vipera latastei in northern Portugal: Ontogenetic shifts, prey size and seasonal variations. Herpetological Journal, 14(1), 13–19.
- Brown, G. P., & Shine, R. (2007). Rain, prey and predators: Climatically driven shifts in frog abundance modify reproductive allometry in a tropical snake. Oecologia, 154(2), 361–368. https://doi.org/10.1007/s00442-007-0842-8
- Butler, M. A., & King, A. A. (2004). Phylogenetic comparative analysis: A modeling approach for adaptive evolution. The American Naturalist, 164(6), 683–695. https://doi.org/10.1086/426002
- Casewell, N. R., Wüster, W., Vonk, F. J., Harrison, R. A., & Fry, B. G. (2013). Complex cocktails: The evolutionary novelty of venoms. Trends in Ecology and Evolution, 28, 219–229. https://doi.org/10.1016/j.tree.2012.10.020
- Chamberlain, S. (2020). spocc: Interface to species occurrence data sources. R package version 1.1.0. https://cran.r-project.org/web/packages/spocc/index.html
- Chiba, T., & Sato, S. (2016). Climate-mediated changes in predator-prey interactions in the fossil record: A case study using shell-drilling gastropods from the Pleistocene Japan Sea. Paleobiology, 42, 257–268. https://doi.org/10.1017/pab.2015.38
- Clavel, J., Escarguel, G., & Merceron, G. (2015). mvMORPH: An R package for fitting multivariate evolutionary models to morphometric data. Methods in Ecology and Evolution, 6, 1311–1319.
- Conticello, S. G., Gilad, Y., Avidan, N., Ben-Asher, E., Levy, Z., & Fainzilber, M. (2001). Mechanisms for evolving hypervariability: The case of conopeptides. Molecular Biology and Evolution, 18, 120–131. https://doi.org/10.1093/oxfordjournals.molbev.a003786
- Creer, S., Chou, W. H., Malhotra, A., & Thorpe, R. S. (2002). Offshore insular variation in the diet of the Taiwanese bamboo viper Trimeresurus stejnegeri (Schmidt). Zoological Science, 19, 907–913. https://doi.org/10.2108/zsj.19.907
- Creer, S., Malhotra, A., Thorpe, R. S., Stöcklin, R., Favreau, P., & Chou, W. H. (2003). Genetic and ecological correlates of intraspecific variation in pitviper venom composition detected using matrix-assisted laser desorption time-of-flight mass spectrometry (MALDI-TOF-MS) and isoelectric focusing. Journal of Molecular Evolution, 56, 317–329. https://doi.org/10.1007/s00239-002-2403-4
- Daltry, J. C., Wüster, W., & Thorpe, R. S. (1996). Diet and snake venom evolution. Nature, 379, 537–540. https://doi.org/10.1038/379537a0
- Davies, E. L., & Arbuckle, K. (2019). Coevolution of snake venom toxic activities and diet: Evidence that ecological generalism favours toxicological diversity. Toxins, 11, 1–14. https://doi.org/10.3390/toxins11120711
- de Roodt, A. R., Boyer, L. V., Lanari, L. C., Irazu, L., Laskowicz, R. D., Sabattini, P. L., & Damin, C. F. (2016). Venom yield and its relationship with body size and fang separation of pit vipers from Argentina. Toxicon, 121, 22–29. https://doi.org/10.1016/j.toxicon.2016.08.013
- Deshimaru, M., Ogawa, T., Nakashima, K.-I., Nobuhisa, I., Chijiwa, T., Shimohigashi, Y., Fukumaki, Y., Niwa, M., Yamashina, I., Hattori, S., & Ohno, M. (1996). Accelerated evolution of crotalinae snake venom gland serine proteases. FEBS Letters, 397, 83–88. https://doi.org/10.1016/S0014-5793(96)01144-1
- Diniz-Filho, J. A. F., Jardim, L., Rangel, T. F., Holden, P. B., Edwards, N. R., Hortal, J., Santos, A. M. C., & Raia, P. (2019). Quantitative genetics of body size evolution on islands: An individual-based simulation approach. Biology Letters, 15, 20190481. https://doi.org/10.1098/rsbl.2019.0481
- Dynesius, M., & Jansson, R. (2000). Evolutionary consequences of changes in species’ geographical distributions driven by Milankovitch climate oscillations. Proceedings of the National Academy of Sciences USA, 97, 9115–9120. https://doi.org/10.1073/pnas.97.16.9115
- Feldman, A., Sabath, N., Pyron, R. A., Mayrose, I., & Meiri, S. (2016). Body sizes and diversification rates of lizards, snakes, amphisbaenians and the tuatara. Global Ecology and Biogeography, 25, 187–197. https://doi.org/10.1111/geb.12398
- Felsenstein, J. (1985). Phylogenies and the comparative method. The American Naturalist, 125, 1–15. https://doi.org/10.1086/284325
- Ferraz, C. R., Arrahman, A., Xie, C., Casewell, N. R., Lewis, R. J., Kool, J., & Cardoso, F. C. (2019). Multifunctional toxins in snake venoms and therapeutic implications: From pain to hemorrhage and necrosis. Frontiers in Ecology and Evolution, 7, 1–19. https://doi.org/10.3389/fevo.2019.00218
- Figueroa, A., McKelvy, A. D., Grismer, L. L., Bell, C. D., & Lailvaux, S. P. (2016). A species-level phylogeny of extant snakes with description of a new colubrid subfamily and genus. PLoS ONE, 11(9), e0161070. https://doi.org/10.1371/journal.pone.0161070
- Fry, B. G., Roelants, K., Champagne, D. E., Scheib, H., Tyndall, J. D. A., King, G. F., Nevalainen, T. J., Norman, J. A., Lewis, R. J., Norton, R. S., Renjifo, C., & Rodríguez De La Vega, R. C. (2009). The toxicogenomic multiverse: Convergent recruitment of proteins into animal venoms. Annual Review of Genomics and Human Genetics, 10, 483–511. https://doi.org/10.1146/annurev.genom.9.081307.164356
- Fujimi, T. J., Nakajyo, T., Nishimura, E., Ogura, E., Tsuchiya, T., & Tamiya, T. (2003). Molecular evolution and diversification of snake toxin genes, revealed by analysis of intron sequences. Gene, 313, 111–118. https://doi.org/10.1016/S0378-1119(03)00637-1
- Giorgianni, M. W., Dowell, N. L., Griffin, S., Kassner, V. A., Selegue, J. E., & Carroll, S. B. (2020). The origin and diversification of a novel protein family in venomous snakes. Proceedings of the National Academy of Sciences USA, 117, 10911–10920. https://doi.org/10.1073/pnas.1920011117
- Glaudas, X., Glennon, K. L., Martins, M., Luiselli, L., Fearn, S., Trembath, D. F., Jelić, D., & Alexander, G. J. (2019). Foraging mode, relative prey size and diet breadth: A phylogenetically explicit analysis of snake feeding ecology. Journal of Animal Ecology, 88, 757–767. https://doi.org/10.1111/1365-2656.12972
- Grundler, M. C. (2020). SquamataBase: A natural history database and R package for comparative biology of snake feeding habits. Biodiversity Data Journal, 8, e49943. https://doi.org/10.3897/BDJ.8.e49943
- Gutiérrez, J., Avila, C., Camacho, Z., & Lomonte, B. (1990). Ontogenetic changes in the venom of the snake Lachesis muta stenophrys (bushmaster) from Costa Rica. Toxicon, 28, 419–426. https://doi.org/10.1016/0041-0101(90)90080-Q
- Hansen, T. F., & Martins, E. P. (1996). Translating between microevolutionary process and macroevolutionary patterns: The correlation structure of interspecific data. Evolution, 50, 1404–1417. https://doi.org/10.1111/j.1558-5646.1996.tb03914.x
- Harris, R. J., Zdenek, C. N., Harrich, D., Frank, N., & Fry, B. G. (2020). An appetite for destruction: Detecting prey-selective binding of α-neurotoxins in the venom of Afro-Asian elapids. Toxins, 12(3), 205. https://doi.org/10.3390/toxins12030205
- Healy, K., Carbone, C., & Jackson, A. L. (2019). Snake venom potency and yield are associated with prey-evolution, predator metabolism and habitat structure. Ecology Letters, 22, 527–537. https://doi.org/10.1111/ele.13216
- Holding, M. L., Drabeck, D. H., Jansa, S. A., & Gibbs, H. L. (2016). Venom resistance as a model for understanding the molecular basis of complex coevolutionary adaptations. Integrative and Comparative Biology, 56, 1032–1043. https://doi.org/10.1093/icb/icw082
- Holt, B. G., Lessard, J.-P., Borregaard, M. K., Fritz, S. A., Araújo, M. B., Dimitrov, D., Fabre, P.-H., Graham, C. H., Graves, G. R., Jonsson, K. A., Nogués-Bravo, D., Wang, Z., Whittaker, R. J., Fjeldsa, J., & Rahbek, C. (2013). An update of Wallace's zoogeographic regions of the world. Science, 339, 74–79.
- Jansson, R. (2003). Global patterns in endemism explained by past climatic change. Proceedings of the Royal Society B: Biological Sciences, 270, 583–590.
- Johnson, J. B., & Omland, K. S. (2004). Model selection in ecology and evolution. Trends in Ecology & Evolution, 19(2), 101–108.
- Juárez, P., Comas, I., González-Candelas, F., & Calvete, J. J. (2008). Evolution of snake venom disintegrins by positive Darwinian selection. Molecular Biology and Evolution, 25, 2391–2407. https://doi.org/10.1093/molbev/msn179
- Kazandjian, T. D., Petras, D., Robinson, S. D., van Thiel, J., Greene, H. W., Arbuckle, K., Barlow, A., Carter, D. A., Wouters, R. M., Whiteley, G., & Wagstaff, S. C. (2021). Convergent evolution of pain-inducing defensive venom components in spitting cobras. Science, 371(6527), 386–390.
- Kini, R. M. (2003). Excitement ahead: Structure, function and mechanism of snake venom phospholipase A2 enzymes. Toxicon, 42, 827–840. https://doi.org/10.1016/j.toxicon.2003.11.002
- Kordiš, D., & Gubenšek, F. (2000). Adaptive evolution of animal toxin multigene families. Gene, 261, 43–52. https://doi.org/10.1016/S0378-1119(00)00490-X
- Laws, A. N. (2017). Climate change effects on predator–prey interactions. Current Opinion in Insect Science, 23, 28–34. https://doi.org/10.1016/j.cois.2017.06.010
- Losos, J. B., & Ricklefs, R. E. (2009). Adaptation and diversification on islands. Nature, 457, 830–836. https://doi.org/10.1038/nature07893
- Luiselli, L., Capizzi, D., Filippi, E., Anibaldi, C., Rugiero, L., & Capula, M. (2007). Comparative diets of three populations of an aquatic snake (Natrix tessellata, Colubridae) from Mediterranean streams with different hydric regimes. Copeia, 2, 426–435.
10.1643/0045-8511(2007)7[426:CDOTPO]2.0.CO;2 Google Scholar
- Luiselli, L., Capula, M., & Shine, R. (1996). Reproductive output, costs of reproduction, and ecology of the smooth snake, Coronella austriaca, in the eastern Italian Alps. Oecologia, 106, 100–110. https://doi.org/10.1007/BF00334412
- Lyons, K., Dugon, M. M., & Healy, K. (2020). Diet breadth mediates the prey specificity of venom potency in snakes. Toxins, 12(2), 74. https://doi.org/10.3390/toxins12020074
- MacArthur, R. H., & Wilson, E. O. (1967). The theory of island biogeography. Princeton University Press.
10.1111/j.1463-6409.2007.00280.x Google Scholar
- Martinez, P. A., Gouveia, S. F., dos Santos, L. M., Carvalho, F. H. A., & Olalla-Tárraga, M. (2021). Ecological and historical legacies on global diversity gradients in marine elapid snakes. Austral Ecology, 46, 3–7.
- Martinez, P. A., Zurano, J. P., Amado, T. F., Penone, C., Betancur-R, R., Bidau, C. J., & Jacobina, U. P. (2015). Chromosomal diversity in tropical reef fishes is related to body size and depth range. Molecular Phylogenetics and Evolution, 93, 1–4. https://doi.org/10.1016/j.ympev.2015.07.002
- McElroy, T., McReynolds, C. N., Gulledge, A., Knight, K. R., Smith, W. E., & Albrecht, E. A. (2017). Differential toxicity and venom gland gene expression in Centruroides vittatus. PLoS ONE, 12, 1–17. https://doi.org/10.1371/journal.pone.0184695
- Morales-Barbero, J., Gouveia, S. F., & Martinez, P. A. (2021). Historical climatic instability predicts the inverse latitudinal pattern in speciation rate of modern mammalian biota. Journal of Evolutionary Biology, 34(2), 339–351.
- Nei, M., Gu, X., & Sitnikova, T. (1997). Evolution by the birth-and-death process in multigene families of the vertebrate immune system. Proceedings of the National Academy of Sciences USA, 94, 7799–7806. https://doi.org/10.1073/pnas.94.15.7799
- Novosolov, M., Rodda, G. H., Gainsbury, A. M., & Meiri, S. (2018). Dietary niche variation and its relationship to lizard population density. Journal of Animal Ecology, 87, 285–292. https://doi.org/10.1111/1365-2656.12762
- O’Shea, M. (1996). A guide to the snakes of Papua New Guinea ( 1st ed.). Independent Group Pty Ltd.
- Ogawa, T., Chijiwa, T., Oda-Ueda, N., & Ohno, M. (2005). Molecular diversity and accelerated evolution of C-type lectin-like proteins from snake venom. Toxicon, 45, 1–14. https://doi.org/10.1016/j.toxicon.2004.07.028
- Prestt, I. (1971). An ecological study of the viper Vipera berus in southern Britain. Journal of Zoology, 164(3), 373–418. https://doi.org/10.1111/j.1469-7998.1971.tb01324.x
10.1111/j.1469-7998.1971.tb01324.x Google Scholar
- R Core Team. (2020). R: A language and environment for statistical computing. R Foundation for Statistical Computing.
- Rambaut, A., Drummond, A. J., Xie, D., Baele, G., & Suchard, M. A. (2018). Posterior summarization in Bayesian phylogenetics using Tracer 1.7. Systematic Biology, 67, 901–904. https://doi.org/10.1093/sysbio/syy032
- Revell, L. J. (2012). phytools: An R package for phylogenetic comparative biology (and other things). Methods in Ecology and Evolution, 3, 217–223. https://doi.org/10.1111/j.2041-210X.2011.00169.x
- Rodríguez, C., Rollins-Smith, L., Ibáñez, R., Durant-Archibold, A. A., & Gutiérrez, M. (2017). Toxins and pharmacologically active compounds from species of the family Bufonidae (Amphibia, Anura). Journal of Ethnopharmacology, 198, 235–254. https://doi.org/10.1016/j.jep.2016.12.021
- Roelants, K., Fry, B. G., Norman, J. A., Clynen, E., Schoofs, L., & Bossuyt, F. (2010). Identical skin toxins by convergent molecular adaptation in frogs. Current Biology, 20, 125–130. https://doi.org/10.1016/j.cub.2009.11.015
- Salazar, J. C., del Rosario Castañeda, M., Londoño, G. A., Bodensteiner, B. L., & Muñoz, M. M. (2019). Physiological evolution during adaptive radiation: A test of the island effect in Anolis lizards. Evolution, 73, 1241–1252.
- Sandel, B., Arge, L., Dalsgaard, B., Davies, R. G., Gaston, K. J., Sutherland, W. J., & Svenning, J.-C. (2011). The influence of late quaternary climate-change velocity on species endemism. Science, 334, 660–664. https://doi.org/10.1126/science.1210173
- Schluter, D. (1988). The evolution of finch communities on islands and continents: Kenya vs. Galapagos. Ecological Monographs, 58, 229–249.
- Shine, R. (1981). Venomous snakes in cold climates: Ecology of the Australian genus Drysdalia (Serpentes: Elapidae). Copeia, 1, 14–25. https://doi.org/10.2307/1444037
- Shine, R. (1991). Intersexual dietary divergence and the evolution of sexual dimorphism in snakes. The American Naturalist, 138(1), 103–122.
- Slagboom, J., Kool, J., Harrison, R. A., & Casewell, N. R. (2017). Haemotoxic snake venoms: Their functional activity, impact on snakebite victims and pharmaceutical promise. British Journal of Haematology, 177, 947–959.
- Sridharan, S., & Kini, R. M. (2015). Snake venom natriuretic peptides: Potential molecular probes. BMC Pharmacology and Toxicology, 16, A87. https://doi.org/10.1186/2050-6511-16-S1-A87
10.1186/2050-6511-16-S1-A87 Google Scholar
- Tasoulis, T., & Isbister, G. K. (2017). A review and database of snake venom proteomes. Toxins, 9(9), 290. https://doi.org/10.3390/toxins9090290
- Toledo, L. F., Sazima, I., & Haddad, C. F. B. (2011). Behavioural defences of anurans: An overview. Ethology Ecology and Evolution, 23, 1–25. https://doi.org/10.1080/03949370.2010.534321
- van der Bijl, W. (2018). phylopath: Easy phylogenetic path analysis in R. PeerJ, 2018(6), e4718.
- von Hardenberg, A., & Gonzalez-Voyer, A. (2013). Disentangling evolutionary cause-effect relationships with phylogenetic confirmatory path analysis. Evolution, 67, 378–387. https://doi.org/10.1111/j.1558-5646.2012.01790.x
- Wagenmakers, E. J., & Farrell, S. (2004). AIC model selection using Akaike weights. Psychonomic Bulletin and Review, 11, 192–196. https://doi.org/10.3758/BF03206482
- Waide, R. B., Willig, M. R., Steiner, C. F., Mittelbach, G., Gough, L., Dodson, S. I., Juday, G. P., & Parmenter, R. (1999). The relationship between productivity and species richness. Annual Review of Ecology and Systematics, 30(1), 257–300. https://doi.org/10.1146/annurev.ecolsys.30.1.257
10.1146/annurev.ecolsys.30.1.257 Google Scholar
- Winemiller, K. O., & Pianka, E. R. (1990). Organization in natural assemblages of desert lizards and tropical fishes. Ecological Monographs, 60, 27–55. https://doi.org/10.2307/1943025
- Wong, E. S. W., & Belov, K. (2012). Venom evolution through gene duplications. Gene, 496, 1–7. https://doi.org/10.1016/j.gene.2012.01.009
- Woolfit, M., & Bromham, L. (2005). Population size and molecular evolution on islands. Proceedings of the Royal Society B: Biological Sciences, 272, 2277–2282. https://doi.org/10.1098/rspb.2005.3217
- Zancolli, G., Calvete, J. J., Cardwell, M. D., Greene, H. W., Hayes, W. K., Hegarty, M. J., Herrmann, H. W., Holycross, A. T., Lannutti, D. I., Mulley, J. F., Sanz, L., Travis, Z. D., Whorley, J. R., Wüster, C. E., & Wüster, W. (2019). When one phenotype is not enough: Divergent evolutionary trajectories govern venom variation in a widespread rattlesnake species. Proceedings of the Royal Society B: Biological Sciences, 286(1898), 20182735. https://doi.org/10.1098/rspb.2018.2735
- Zancolli, G., & Casewell, N. R. (2020). Venom systems as models for studying the origin and regulation of evolutionary novelties. Molecular Biology and Evolution, 37, 2777–2790. https://doi.org/10.1093/molbev/msaa133
- Zhang, Y. (2015). Why do we study animal toxins? Dong wu xue yan jiu = Zoological Research, 36, 183–222.
- Župunski, V., Kordiš, D., & Gubenšek, F. (2003). Adaptive evolution in the snake venom Kunitz/BPTI protein family. FEBS Letters, 547, 131–136. https://doi.org/10.1016/S0014-5793(03)00693-8