Recovering the evolutionary history of Africa’s most diverse viper genus: morphological and molecular phylogeny of Bitis (Reptilia: Squamata: Viperidae)

Wittenberg, Rod D.; Jadin, Robert C.; Fenwick, Allyson M.; Gutberlet, Ronald L.

doi:10.1007/s13127-014-0185-3

Cited by 5 publications

(4 citation statements)

References 43 publications

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“…Although the relative abundance of protein families can be rapidly altered by genetic drift, (e.g., founder effect), some conserved toxins may act as reliable biomarkers for tracing evolutionary history. The venom compositions of the species in the viperine genus Bitis ( Table 2 ) show a perfect congruence with the phylogenetic relationships of this genus proposed by Wittenberg et al 2015 [ 150 ]. There is also evidence that snakes with unique venom represent species of ancient phylogenetic divergence (e.g., Calliophis and Dendroaspis [ 151 , 152 ] and Tropidolaemus wagleri [ 153 ].…”

Section: Discussionsupporting

confidence: 77%

A Review and Database of Snake Venom Proteomes

Tasoulis

Isbister

2017

Toxins

480

455

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Advances in the last decade combining transcriptomics with established proteomics methods have made possible rapid identification and quantification of protein families in snake venoms. Although over 100 studies have been published, the value of this information is increased when it is collated, allowing rapid assimilation and evaluation of evolutionary trends, geographical variation, and possible medical implications. This review brings together all compositional studies of snake venom proteomes published in the last decade. Compositional studies were identified for 132 snake species: 42 from 360 (12%) Elapidae (elapids), 20 from 101 (20%) Viperinae (true vipers), 65 from 239 (27%) Crotalinae (pit vipers), and five species of non-front-fanged snakes. Approximately 90% of their total venom composition consisted of eight protein families for elapids, 11 protein families for viperines and ten protein families for crotalines. There were four dominant protein families: phospholipase A2s (the most common across all front-fanged snakes), metalloproteases, serine proteases and three-finger toxins. There were six secondary protein families: cysteine-rich secretory proteins, l-amino acid oxidases, kunitz peptides, C-type lectins/snaclecs, disintegrins and natriuretic peptides. Elapid venoms contained mostly three-finger toxins and phospholipase A2s and viper venoms metalloproteases, phospholipase A2s and serine proteases. Although 63 protein families were identified, more than half were present in <5% of snake species studied and always in low abundance. The importance of these minor component proteins remains unknown.

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Section: Discussionsupporting

confidence: 77%

A Review and Database of Snake Venom Proteomes

Tasoulis

Isbister

2017

Toxins

480

455

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“…Commonly referred to as the African adders, Bitis is Africa's most taxonomically diverse and geographically widespread viperid genus, containing 18 extant species ( sensu Branch, ; Gower et al., ; Lenk, Herrmann, Joger, & Wink, ; Uetz, Freed, & Hošek, ) and one documented extinct Pleistocene species, Bitis olduvaiensis (Rage, ). Several studies have investigated the phylogeny of Bitis using morphological evidence (Ashe & Marx, ; Groombridge, ; Wittenberg, Jadin, Fenwick, & Gutberlet, ) and immunological distances (Lenk et al., ). Higher level phylogenies of Viperidae and Viperinae have also included Bitis (Alencar et al., ; Herrmann & Joger, , ; Herrmann, Joger, Lenk, & Wink, ; Lenk, Kalayabina, Wink, & Joger, ; Lenk et al., ; Pyron, Burbrink, & Wiens, ; Wüster, Peppin, Pook, & Walker, ; Šmíd & Tolley, ).…”

Section: Introductionmentioning

confidence: 99%

“…(Edwards, Vanhooydonck, Herrel, Measey, & Tolley, 2012;da Silva, Herrel, Measey, Vanhooydonck, & Tolley, 2014;da Silva & Tolley, 2017;Measey, Hopkins, & Tolley, 2009;Tolley et al, 2008) Branch, 1999;Gower et al, 2016;Uetz, Freed, & Hošek, 2017) and one documented extinct Pleistocene species, Bitis olduvaiensis (Rage, 1973). Several studies have investigated the phylogeny of Bitis using morphological evidence (Ashe & Marx, 1988;Groombridge, 1980;Wittenberg, Jadin, Fenwick, & Gutberlet, 2015) and immunological distances . Higher level phylogenies of Viperidae and Viperinae have also included Bitis (Alencar et al, 2016;Herrmann & Joger, 1995Lenk, Kalayabina, Wink, & Joger, 2001;Lenk et al, 1999;Pyron, Burbrink, & Wiens, 2013;Wüster, Peppin, Pook, & Walker, 2008;Šmíd & Tolley, 2019).…”

Section: Introductionmentioning

confidence: 99%

Ancient habitat shifts and organismal diversification are decoupled in the African viper genus Bitis (Serpentes: Viperidae)

Barlow

Wüster

Kelly

et al. 2019

Journal of Biogeography

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Aim The expansion of open habitats during the mid‐Miocene has been hypothesized as a driver of allopatric speciation for many African taxa. This habitat‐dependent mode of diversification has been implicated in the shift from C3 (e.g. forest/woodland) to C4 dominated systems (i.e. open savanna, grasslands) in a number of African squamates. We examined this hypothesis using a genus of African viperid snakes (Bitis) with both open habitat and forest‐dwelling representatives. Location Africa. Methods A comprehensive multilocus dataset was used to generate a calibrated species tree using a multispecies coalescent model. Individual gene trees and patterns of nuclear allele sharing were used to assess species monophyly and isolation. To test the habitat‐dependent evolution hypothesis, we generated an ancestral character state reconstruction for open and closed habitats using the dated phylogeny. This was related to the timing of open habitat expansion and forest/woodland contraction in Africa. Results The genus Bitis originated in the Oligocene, with species level diversification in the late Miocene/Pliocene. Four well‐supported clades correspond to the recognized subgenera Bitis, Keniabitis, Macrocerastes and Calechidna. Several previously unrecognized lineages potentially represent cryptic species. Main conclusions Habitat‐dependent evolution does not appear to have been a main driver for generic level viperine diversification: the ancestral state for Bitis was open habitat and at least one clade moved into forest in the Miocene, long after forest had contracted and fragmented. Forest‐dependent species diversified only in the late Miocene, presumably as forest became further reduced in extent, fitting an allopatric model of speciation. Although our results do not favour a general pattern of habitat‐dependent diversification in Bitis, cladogenesis within the subgenus Calechidna for “arenicolous” species (Bitis caudalis complex) and “rupicolous” species (B. atropos‐cornuta complex), corresponds to the aridification of southwest Africa. This suggests there are subtleties not captured in the broad open habitat category, which are relevant for understanding the role of habitat‐dependent evolution.

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“…By combining published studies on venom proteomes with published phylogenies it can be shown that the venoms of some snake genera co-vary with phylogenetic distance. An example of this is the venom proteomes of the viper genus Bitis [21], which closely mirror the phylogeny of this genus as proposed by Wittenberg et.al [22]. .Several studies have demonstrated prey-specific toxicity in snake venom [23,24].…”

Section: Introductionmentioning

confidence: 58%

Activity of two key toxin groups in Australian elapid venoms show a strong correlation to phylogeny but not to diet

et al. 2020

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Background The relative influence of diet and phylogeny on snake venom activity is a poorly understood aspect of snake venom evolution. We measured the activity of two enzyme toxin groups – phospholipase A2 (PLA2), and L-amino acid oxidase (LAAO) – in the venom of 39 species of Australian elapids (40% of terrestrial species diversity) and used linear parsimony and BayesTraits to investigate any correlation between enzyme activity and phylogeny or diet. Results PLA2 activity ranged from 0 to 481 nmol/min/mg of venom, and LAAO activity ranged from 0 to 351 nmol/min/mg. Phylogenetic comparative methods, implemented in BayesTraits showed that enzyme activity was strongly correlated with phylogeny, more so for LAAO activity. For example, LAAO activity was absent in both the Vermicella and Pseudonaja/Oxyuranus clade, supporting previously proposed relationships among these disparate taxa. There was no association between broad dietary categories and either enzyme activity. There was strong evidence for faster initial rates of change over evolutionary time for LAAO (delta parameter mean 0.2), but no such pattern in PLA2 (delta parameter mean 0.64). There were some exceptions to the phylogenetic patterns of enzyme activity: different PLA2 activity in the ecologically similar sister-species Denisonia devisi and D. maculata; large inter-specific differences in PLA2 activity in Hoplocephalus and Austrelaps. Conclusions We have shown that phylogeny is a stronger influence on venom enzyme activity than diet for two of the four major enzyme families present in snake venoms. PLA2 and LAAO activities had contrasting evolutionary dynamics with the higher delta value for PLA2 Some species/individuals lacked activity in one protein family suggesting that the loss of single protein family may not incur a significant fitness cost.

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Recovering the evolutionary history of Africa’s most diverse viper genus: morphological and molecular phylogeny of Bitis (Reptilia: Squamata: Viperidae)

Cited by 5 publications

References 43 publications

A Review and Database of Snake Venom Proteomes

A Review and Database of Snake Venom Proteomes

Ancient habitat shifts and organismal diversification are decoupled in the African viper genus Bitis (Serpentes: Viperidae)

Activity of two key toxin groups in Australian elapid venoms show a strong correlation to phylogeny but not to diet

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