Journal of Heredity Advance Access originally published online on June 1, 2006
Journal of Heredity 2006 97(3):206-217; doi:10.1093/jhered/esj034
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
Venom Evolution Widespread in Fishes: A Phylogenetic Road Map for the Bioprospecting of Piscine Venoms
From the Department of Ecology, Evolution, and Environmental Biology, Columbia University, 1200 Amsterdam Avenue, New York, NY 10027 (Leo Smith); Division of Vertebrate Zoology (Ichthyology), American Museum of Natural History, Central Park West at 79th Street, New York, NY 10024-5192 (Leo Smith); and Division of Invertebrate Zoology, American Museum of Natural History, Central Park West at 79th Street, New York, NY 10024-5192 (Wheeler)
Address correspondence to W. L. Smith at the address above, or e-mail: leosmith{at}amnh.org.
Knowledge of evolutionary relationships or phylogeny allows for effective predictions about the unstudied characteristics of species. These include the presence and biological activity of an organism's venoms. To date, most venom bioprospecting has focused on snakes, resulting in six stroke and cancer treatment drugs that are nearing U.S. Food and Drug Administration review. Fishes, however, with thousands of venoms, represent an untapped resource of natural products. The first step involved in the efficient bioprospecting of these compounds is a phylogeny of venomous fishes. Here, we show the results of such an analysis and provide the first explicit suborder-level phylogeny for spiny-rayed fishes. The results, based on 
1.1 million aligned base pairs, suggest that, in contrast to previous estimates of 200 venomous fishes, >1,200 fishes in 12 clades should be presumed venomous. This assertion was corroborated by a detailed anatomical study examining potentially venomous structures in >100 species. The results of these studies not only alter our view of the diversity of venomous fishes, now representing >50% of venomous vertebrates, but also provide the predictive phylogeny or "road map" for the efficient search for potential pharmacological agents or physiological tools from the unexplored fish venoms.
Until such fundamentals as the anatomical distribution of fish venoms have been determined, the pharmacological and chemical characterization of these compounds will continue to be unstudied.
—Halstead (1988, p. XXI) in the introduction to his treatise on venomous marine organisms.
Venomous organisms produce and use venom, a toxin injected using a specialized apparatus, for interactions with predators, prey, and competitors (Bulaj et al. 2003; Halstead 1970, 1988). Venoms and their associated delivery systems have evolved in animal groups ranging from the simple box jellyfish (Carybdea) to the black widow spider (Latrodectus), lionfish (Pterois), and cobra (Naja). To date, snakes, scorpions, and spiders have been the principal focus of research into potential pharmacological agents or physiological tools found in the toxins of venomous animals (Ault 2004; Tan et al. 2003). This research has already led to the development of six pharmaceuticals derived from snake venoms with functions ranging from anticoagulation to antiangiogenesis; these drugs are currently in various stages of U.S. Food and Drug Administration regulatory review (Ault 2004; Tan et al. 2003). In comparison to these terrestrial groups, venomous fishes have been largely ignored as a source of potential pharmaceuticals (Church and Hodgson 2002; Halstead 1988; Tan et al. 2003). In fact, recent studies (Church and Hodgson 2002; Sosa-Rosales et al. 2005) indicate that roughly one dozen toxins have been identified and/or characterized from venomous fishes. This deficiency is due, in part, to the lack of reliable estimates of the number and diversity of venomous fish species. The number of venomous fishes has typically been reported as 200 species (Church and Hodgson 2002; Haddad et al. 2003; Halstead 1970, 1988), but this value clearly underestimates the number of venomous fishes implied by the phylogenetic distribution of venom among ray-finned fishes. Given the potential pharmaceutical benefits offered by and the health threats posed by venomous fishes, it is surprising that no studies have ever examined the relationships of venomous fishes to infer the identity and number of venomous fish species. Phylogenies are crucial for predicting the distribution of such characteristics because they provide maximally efficient descriptions of organismic attributes, which allow for effective predictions about organismal characteristics that have not yet been studied (Raven et al. 1994; Systematics Agenda 2000 1994). For this reason, a complete understanding of the phylogeny of venomous fishes would also be extremely valuable for the efficient bioprospecting of piscine venoms. However, generating this phylogenetic road map for exploring the biological activity and distribution of piscine venoms requires sufficient resolution of the >18,000 species "acanthomorph problem," which remains the major task facing systematic ichthyology (Johnson 1993; Miya et al. 2003; Nelson 1989; Stiassny et al. 2004).
Venomous ray-finned fishes are diverse with representatives spread across four orders (Church and Hodgson 2002; Haddad et al. 2003; Halstead 1988; Smith-Vaniz et al. 2001; Vetrano et al. 2002) and habitats ranging from mountain streams to coral reefs and oceanic midwaters (Nelson 1994). Their envenomations cause at least 50,000 reported injuries per year with symptoms ranging from blisters to intense pain, fever, and death (Haddad et al. 2003; Halstead 1970, 1988; Vetrano et al. 2002). The known venomous fishes are currently distributed among the catfishes (Siluriformes) and six groups of "acanthomorphs" or spiny-rayed fishes (Church and Hodgson 2002; Halstead 1970, 1988; Nelson 1994; Smith-Vaniz et al. 2001): toadfishes (Batrachoidiformes); scorpionfishes (Scorpaeniformes: Scorpaenoidei); surgeonfishes, scats, and rabbitfishes (Perciformes: Acanthuroidei); saber-toothed blennies (Perciformes: Blennioidei); jacks (Perciformes: Percoidei); and stargazers and weeverfishes (Perciformes: Trachinoidei). The distantly related catfishes (Nelson 1994; Stiassny et al. 2004) are not included in this analysis, but it is clear that envenomation structures have been gained and/or lost multiple times within the order (Friel J, personal communication; Smith WL, unpublished data). The remaining venomous fish groups are nested within the acanthomorph problem or Nelson's (1989) "bush at the top of the tree," which refers to our poor, and often contradictory, understanding of the relationships of the 18,000 species of spiny-rayed fishes that represent the crown group of bony fish evolution (Johnson 1993; Miya et al. 2003; Nelson 1994; Stiassny et al. 2004). Our knowledge of the relationships of the venomous fish groups within the context of the acanthomorph problem is also poor, with recent studies (Chen et al. 2003; Miya et al. 2003; Smith and Wheeler 2004; Tang et al. 1999) challenging the integrity of many of these venomous assemblages. The incongruence between these recent studies and the traditional classification (Nelson 1994) only highlight the need for a large-scale phylogenetic analysis examining the relationships among spiny-rayed fishes as a whole to delimit venomous fish clades.
To resolve relationships among venomous spiny-rayed fishes, we analyzed 4,700 bp in 233 species (approximately 1.1 Mb), including representatives of all suborders and venomous groups within the Acanthomorpha. The results of this study will allow us to (1) hypothesize the number and identity of venomous species, (2) hypothesize the number of times that venom apparatuses have originated by delimiting all venomous clades, and (3) make effective predictions about venomous fishes and venom evolution by providing a predictive phylogenetic framework or road map.
 |
Materials and Methods |
|---|
 Top Materials and Methods ResultsSupplementary MaterialReferences |
|---|
Taxon Sampling
The 233 analyzed taxa include 228 representatives from all suborders and orders of spiny-rayed fishes (Acanthomorpha) and two aulopiform and three myctophiform outgroups, with the Atlantic sabretooth (Coccorella atlantica) as the root. Representatives of all venomous acanthomorph groups (i.e., Meiacanthus blennies, thalassophrynine toadfishes, scatophagids, scomberoidine carangids, uranoscopids, siganids, acanthurids, trachinids, and scorpaenoids) and their putative allies were included to rigorously examine the evolution of venomous fishes. Species considered venomous in our molecular analysis have had the presence of venom confirmed, or it has been confirmed in one of their congeners (Church and Hodgson 2002; Halstead 1970, 1988; Smith-Vaniz et al. 2001; Sosa-Rosales et al. 2005).
Acquisition of Nucleotide Sequences
Fish tissues were preserved in 70%–95% ethanol prior to extraction of DNA. Total DNA was extracted from muscle or fin clips using a Qiagen (Valencia, CA) DNeasy Tissue Extraction Kit following the manufacturer's protocol. Polymerase chain reaction (PCR) was used to amplify four segments, representing five genes, from the mitochondrial and nuclear genomes. Double-stranded amplifications were performed in a 25-µl volume containing one Ready-To-Go PCR bead (Amersham Biosciences, Piscataway, NJ), 1.25 µl of each primer, and 2–5 µl of undiluted extracted DNA. To amplify and sequence these five gene regions, the following primer pairs were used (primer sequences can be found in Smith and Wheeler 2004): 12S, tRNAVal, 16S fragment—primers 12SL13-L and TitusI-H, remaining 16S fragment—primers 16S ar-L and 16S br-H, 28S fragment—primers 28SV and 28SJJ, and histone H3 fragment—primers H3a-L and H3b-H. The analysis resulted in an alignment of 4,721 aligned nucleotides (based on the implied alignment, Wheeler 2003a). Amplifications for all fragments were carried out in 30–40 cycles with the following temperature profile: initial denaturation for 6 min at 94°C, denaturation for 45–60 s at 94°C, annealing for 45–60 s at 46°C–49°C, and extension for 1–2 min at 72°C, with an additional terminal extension at 72°C for 6 min. The double-stranded amplification products were desalted and concentrated using an ArrayIt PCR Product Purification Kit (TeleChem International, Sunnyvale, CA) on a Beckman BIOMEK 2000 laboratory automated pipetting workstation with minor modifications to the manufacturer's protocol. Both strands of the purified PCR fragments were used as templates and directly cycle sequenced using the original amplification primers and an ABI Prism Dye Terminator Reaction Kit V1.1. The sequencing reactions were cleaned with standard isopropyl-ethanol precipitation and resuspended in 10 µl formamide. The nucleotides were sequenced on an ABI 3700 or ABI 3730xl automated DNA sequencer. Contigs were built in SEQUENCHER 3.1 (Gene Codes, Ann Arbor, MI) using DNA sequences from the complementary heavy and light strands. Sequences were edited in SEQUENCHER and BIOEDIT (Hall 1999). All novel sequences were submitted to GenBank and assigned accession numbers (DQ532831-DQ533482) or were taken from our previous studies (Smith and Wheeler 2004; Sparks and Smith 2004a,b; see supplementary information). Histone H3 was unable to be amplified in the brotulid (Brosmophycis) and the 12S/tRNAVal genes were unable to be sequenced in toadfishes (Batrachoidifomes except Perulibatrachus) and the soldierfish (Gymnapistes), so the unavailable data were treated as missing.
Phylogenetic Analyses
The parsimony analysis was run using direct optimization (Wheeler 1996), fixed states optimization (Wheeler 1999), and iterative pass (Wheeler 2003b) as implemented in the program POY 3.0 (Wheeler WC, Gladstein DS, DeLaet J, unpublished; http://research.amnh.org/scicomp/projects/poy.php) using default values unless listed otherwise below and run on the American Museum of Natural History (AMNH) parallel computing cluster.
The analysis began by generating 500 random addition sequences each under fixed states optimization and direct optimization for a total of 1,000 starting points for the analysis. These random addition sequences were improved with tree fusing (Goloboff 1999; specifying: fuselimit 5000, fitchtrees, and fusemingroup 3), tree bisection and reconnection (TBR) branch swapping, and 400 parsimony ratchet replicates (Nixon 1999; specifying: ratchettbr; ratchetseverity 3; ratchetpercent 40). This initial searching took 35 days on the AMNH parallel computing cluster and resulted in eight most parsimonious trees with a length of 27,625 steps. These optimal trees were submitted to POY for further TBR branch swapping, tree fusing (specifying: fuselimit 5000, fitchtrees, and fusemingroup 3), and 100 rounds of parsimony ratcheting (specifying: ratchettbr; ratchetseverity 3; ratchetpercent 40) using iterative pass and exact, which provide more thorough and less heuristic searches. This final round of the analysis took an additional 32 days.
The length of the resulting implied alignment was verified in NONA 3.0 (Goloboff PA, unpublished; http://www.cladistics.com). To estimate the robustness of the phylogenetic hypotheses recovered, Bremer supports and jackknife resampling percentages were calculated. Jackknife resampling analyses were performed using NONA (1,000 replications, five random addition sequences per replication), and Bremer supports were calculated with default values using TREEROT 2b (Sorenson MD, unpublished; http://people.bu.edu/msoren/TreeRot.html) in conjunction with PAUP* 4.0b10 (Swofford DL, unpublished; http://paup.csit.fsu.edu/). Character evolution on the recovered topologies was examined using NONA and WINCLADA 0.99 (Nixon KC, unpublished; http://www.cladistics.com).
Morphological Examination
After completing the molecular phylogeny, we examined preserved museum specimens for the presence of both a venom delivery structure (e.g., spine, teeth) and a conspicuous venom gland to test the effectiveness of our phylogeny for predicting the distribution of venomous spiny-rayed fishes. Testing using these anatomical features has been the dominant method for establishing whether a fish is venomous because venomous fishes must have both a toxin, housed in a discrete gland, and a specialized delivery system (Halstead 1970, 1988). Previous studies have shown that both the gland and the delivery system are visible by dissection in all groups except venomous jacks (Fishelson 1974; Halstead 1988).
The presence or absence of a venom apparatus was examined in 102 museum specimens spread across 42 families (Table 1). Our sampling focused on species that are predicted to be venomous (e.g., additional scorpionfishes, surgeonfishes, rabbitfishes), species listed as possibly venomous in previous studies (e.g., Halstead 1970), or species that were closely allied to the venomous clades recovered in our phylogeny.
|
The estimates for venomous cartilaginous and lobe-finned fishes were taken from the literature (as given in Table 2). Because the distribution and number of venomous ray-finned fishes have not been studied as extensively, these numbers were estimated using the previously reported distribution of venom in spiny-rayed fishes (Supplementary Table 1), the results of our examination of 102 museum specimens (Table 1), previously published phylogenies and taxonomies (Nelson 1994 and references listed in Tables 1 and 2), our current phylogeny, and the current number of described species in each clade (Froese and Pauly 2004). If the distribution of venom within a small clade that lacks diagnosed subgroups (e.g., Acanthurus surgeonfishes) was unclear because both venomous and nonvenomous forms have been noted, a range is given. Because the phylogeny and distribution of venom in catfishes is less well known and not examined in the current study, the estimated number of venomous catfishes was never extended beyond the level of the family. Therefore, the listed values for catfishes are clearly underestimates because there are countless anecdotal reports (Froese and Pauly 2004; Halstead 1970, 1988) of venom in other catfish families and the presence or absence of venom in most catfish families has not been reported.
|
|
Results |
|---|
|
TopMaterials and MethodsResultsSupplementary MaterialReferences |
|---|
Molecular Phylogeny
The phylogenetic analysis resulted in a single most parsimonious hypothesis with 27,395 steps (Figures 1 and 2). This cladogram had a consistency index of 0.37 and a retention index of 0.57 when parsimony-uninformative characters were retained (based on the implied alignment). Our results are largely congruent with the traditional classification of spiny-rayed fishes (Nelson 1994). Approximately two-thirds of the orders, suborders, and families that were represented by multiple species were recovered as monophyletic groups. The only order containing venomous species resolved as monophyletic in our phylogeny was the toadfishes (Batrachoidiformes). The remaining spiny-rayed fish orders with venomous species, Scorpaeniformes (scorpionfishes) and Perciformes (perchlike fishes), were resolved as polyphyletic, corroborating the results of recent studies (Chen et al. 2003; Johnson 1993; Miya et al. 2003; Smith and Wheeler 2004; Tang et al. 1999). Based on our phylogeny, venom apparatuses have originated 11 independent times in spiny-rayed fishes (Figures 1 and 2), nearly doubling previous estimates (Halstead 1988). Furthermore, our results, in combination with studies on the phylogeny of catfishes (de Pinna 1993; Hardman 2002), suggest that >1,200 fish species should be presumed venomous (Table 2), and it is likely that 1,500–2,000 ray-finned fishes may be venomous when catfishes are examined in detail. Clearly, this greatly increases the previous estimate of
200 venomous fish species (Church and Hodgson 2002; Haddad et al. 2003; Halstead 1970, 1988; Vetrano et al. 2002; Supplementary Table 1). Our results also indicate that the most common venom apparatus (Halstead 1970, 1988), venom glands associated with fin spines, have convergently evolved in nine of the 11 venomous spiny-rayed fish clades (blue or hatched blue branches in Figure 1). The four remaining envenomation structures (i.e., teeth, dorsal opercular spines, central opercular spines, and cleithral spines; Halstead 1970, 1988; Smith-Vaniz et al. 2001) are unreversed and uniquely derived.
|
|
95% jackknife support are marked with an "*." Venomous fishes are indicated by the use of gray branches.Morphological Examination
The results of our morphological examination (Table 1) provide evidence that our molecular phylogeny is highly effective at predicting the presence or absence of venom glands in spiny-rayed fishes. Of the 43 families examined in the morphological study, we were unable to find a conspicuous venom gland or any indications of a venom apparatus in 24 families (Table 1), despite previous suggestions that some species in these groups were venomous (e.g., Chelidonichthys, Zanclus).
Because of the diverse phylogenetic distribution of venomous fin spines, it is not surprising that there is variation in the morphology of these structures (Figures 1 and 3). The venomous toadfishes (Figure 3A) have a distinct venom gland surrounding their dorsal spines; this is in contrast to nonvenomous dorsal spines in other toadfish species that lack a venom gland (Figure 3B). All fishes with venomous spines (except the toadfishes and jacks) have distinct anterolateral grooves on the lateral surfaces of the fin spines (Figure 3C), where the venom gland is situated. Interestingly, the only clade in which we predict a reversal from the presence to the absence of venomous fin-spine glands (the velvetfish and prowfish clade; Figure 1) shows a reversion in the fin spines to the primitive condition where the anterolateral grooves are absent (Figure 3D). During the course of this morphological investigation, three scorpionfish genera (Neomerinthe, Pontinus, and Sebastolobus) were found to have a modified venom apparatus. Our examination of six species in these three genera indicates that anterolateral grooves are present in all six species, but conspicuous venom glands associated with these grooves are lacking. However, the caudal margin of their fin spines have conspicuous glandular tissue (Figure 3F) that differs significantly from the typical muscle tissue found on the posterior margin of the spines in most nonvenomous spiny-rayed fishes (e.g., toadfishes, Figure 3B). We tentatively identify this structure as a venom gland, pending further study. Interestingly, these three genera, although classified into two families, form a clade in recent molecular analyses (Smith and Wheeler 2004, unpublished data).
|
To illustrate the remarkable similarity of venomous fin spines across the diversity of venomous spiny-rayed fishes, the dorsal-fin spine of a rabbitfish is shown (Figure 3G) for comparison to the distantly related scorpaenoid Ptarmus (Figure 3E). Finally, the highly modified venomous spines in Synanceia stonefishes show their distinct venom glands and venom duct (Halstead 1988; Figure 3H).
The other venom apparatuses examined in this study were remarkably similar to previous descriptions (e.g., Halstead 1988). Briefly, the opercular spines of venomous (Figure 3I) and nonvenomous (Figure 3J) toadfishes are shown to illustrate the presence of an opercular venom gland surrounding an opercular spine. A similar morphology is seen in the weeverfishes where the opercular venom gland surrounds the distal margin of the dorsal opercular spine (Figure 3K). Finally, a venomous fang from a saber-toothed blenny is shown, highlighting the grooved tooth that delivers the venom (Figure 3L).
The results of our survey of museum specimens clearly indicate that our phylogeny is effective at predicting the presence or absence of venom in spiny-rayed fishes. Because of this high level of predictability, our estimates of the number of fishes predicted to be venomous were unaltered by the results of our museum survey, with one exception. Because the fin-spine morphology of the scorpionfish genera Neomerinthe, Pontinus, and Sebastolobus has not been previously described and the morphology of the "probable" venom gland has not been examined histologically, we have used a range for the estimated number of venomous scorpionfishes that either includes or excludes the species classified in these three genera, until additional study confirms the presence of venom in these fishes. The results of this museum survey provide strong corroborative evidence for our hypothesis that the presence of venom in fishes has been drastically underestimated in previous reviews.
Road Map for the Bioprospecting of Piscine Venoms
In addition to its use for understanding the evolution and diversity of venomous fishes, our phylogeny can be used to make predictions about the biological activity of the venoms themselves. An example (Systematics Agenda 2000 1994) of the predictive power of phylogenies for bioprospecting comes from the plant kingdom. The drug paclitaxel (TaxolTM), which is used to treat ovarian and breast cancer, was originally extracted from the bark of the threatened Pacific Yew (Taxus brevifolia), but each dose required the destruction of several trees. Fortunately, our understanding of the relationships among yews led researchers to examine its close relatives for similar natural products, resulting in the discovery that the leaves of the European Yew (Taxus baccata) had 10-deacetylbaccatin III, which could be used as a precursor to synthesize paclitaxel without harm to yew populations. Our results provide biochemists with a similar predictive road map for the efficient testing and tracing of venoms for beneficial compounds. Without this road map, it would be prohibitively expensive and time consuming to isolate and characterize the thousands of venoms that are found in spiny-rayed fishes.
The generation of a piscine venom road map is particularly helpful for expanding our current limited understanding of fish venom biological activity. Recent reviews (Church and Hodgson 2002; Halstead 1988; Sosa-Rosales et al. 2005) indicate that fewer than one dozen fish venoms have been characterized and identified (Supplementary Table 1); therefore, this sampling only allows for a few preliminary trends to be noted. First, fish venoms are unusual in that only one to a few toxins per species possess all of the lethal or hemolytic activity (Church and Hodgson 2002). This is in stark contrast to cone snails or terrestrial animals, which often have hundreds of venoms per species (e.g., Bulaj et al. 2003). This small number of venoms per species will allow natural-product chemists to more easily trace the evolution of these individual toxins without the confounding homology problems inherent in studies tracing venoms in species with hundreds of toxins (e.g., gene identification, gene loss, gene duplication). Despite limited venom diversity within species, fish venoms exhibit a surprisingly wide range of pharmacological effects, including neuromuscular, cytolytic, hemolytic, and particularly cardiovascular activity (reviewed in Church and Hodgson 2002). Clearly, additional study may overturn these preliminary observations, but our current knowledge provides the starting point for future bioprospecting of fish venoms as potential pharmacological agents and physiological tools.
Ultimately, our study provides the first explicit suborder-level phylogeny of spiny-rayed fishes, which we used to delimit venomous clades. Using the predictive capabilities of phylogeny, prior knowledge of the distribution of venomous fishes, and an extensive survey for the presence or absence of conspicuous venom glands in spiny-rayed fishes, we have estimated the number and identity of venomous ray-finned fishes. Our results suggest at least a sixfold increase in the number of venomous species and a nearly twofold increase in the number of origins of envenomation structures. Additionally, our phylogeny provides a framework for studying the biological activity of piscine venoms in a predictive, evolutionary context. The next step in their bioprospecting is additional isolation and characterization of toxins from several species within each of the 11 venomous spiny-rayed fish clades. These preliminary assays can then be used, in conjunction with our phylogeny and further fine-scaled systematic studies (i.e., species-level phylogenies), to target species with venoms that provide novel structures or have desirable qualities for use as research tools or lead compounds for drugs. In an era when traditional bioprospecting and high-throughput screening of mass-produced combinatorial libraries have failed to meet expectations for the development of novel pharmaceutical compounds (Newman et al. 2003), a fresh approach is clearly needed. The phylogenetic approach favored by Halstead (1988, see quote above) and highlighted here serves as a model for the efficient discovery and exploitation of untapped natural products, which continue to play the dominant role in the discovery of leads for novel pharmaceuticals (Newman et al. 2003).
|
Supplementary Material |
|---|
|
TopMaterials and MethodsResultsSupplementary MaterialReferences |
|---|
Supplementary Table 1 and other supplementary information are available online at http://jhered.oxfordjournals.org/.
|
Acknowledgments |
|---|
We are indebted to R. DeSalle, J. Faivovich, H. Gee, T. Grant, S. Schaefer, J. Smith, K. Smith, J. Sparks, M. Stiassny, and two anonymous reviewers for thoughtful discussions about this project and/or making valuable suggestions on previous drafts. We graciously thank J. Randall for providing several of the digital images used in Figure 1. This project was supported by funding from the AMNH, AMNH Lerner-Gray Program for Marine Research, Columbia University, National Aeronautics and Space Administration-Ames Fundamental Space Biology Program, and National Science Foundation DEB-0405246 to M. Stiassny and W.L.S. This project would not have been possible without the computational resources at the AMNH, so we gratefully acknowledge all funding agencies and personnel who have helped build and develop Computational Sciences at the AMNH and its parallel computing cluster. We graciously thank D. Bray, B. Brown, D. Catania, W. Eschmeyer, P. Hastings, C. Klepadlo, J. McCosker, R. Rosenblatt, S. Schaefer, M. Stiassny, and H. Walker for hospitality during collection visits, providing access to specimens in their care, and/or loan of specimens. This work would not have been possible without the help of numerous friends and colleagues worldwide who provided tissue samples, reprints of relevant research, suggestions, or unpublished information: P. Baverstock, M. Bell, A. Bentley, E. Bermingham, T. Bertozzi, B. Bowen, L. Britt, C. Burridge, K. Carpenter, M. Craig, A. Dettai, S. Donnellan, P. Doukakis, H. Endo, M. Fahay, C. Ferraris, J. Friel, the Gahan family, A. Gill, A. Gosztonyi, V. Guida, R. Hanel, P. Hastings, G. Herrera, J. Holt, D. Jerry, J. Kaiser, C. Klepadlo, A. Larson, H. Larson, R. Lea, G. Lecointre, J. Leis, P. Loiselle, N. Lovejoy, O. Lucanus, A. Mahon, J. Marliave, J. Martinez, R. Mayden, R. McDowall, M. McGrouther, M. Mok, C. Nock, D. O'Meally, J. Orr, T. Orrell, J. Paxton, K. Pearson, T. Pietsch, D. Pondella, J. Quattro, Reef and Fin (Stamford, CT), R. Rosenblatt, R. Schelly, A. Simons, W. Smith-Vaniz, K. Tang, C. Thacker, H. Walker, E. Wiley, and Y. Yamanoue.
|
Footnotes |
|---|
Corresponding Editor: Rob DeSalle
Received April 19, 2005
Accepted March 6, 2006
|
References |
|---|
|
TopMaterials and MethodsResultsSupplementary MaterialReferences |
|---|
-
Alterman L. (1995) Toxins and toothcombs: potential allospecific chemical defenses in Nyciticebus and Perodicticus.. In Alterman L, Doyle GA, Izard MK (Eds.). Creatures of the dark (Plenum Press, New York) pp. 413–424.
Ault A. (2004) Ventures with venoms. The Scientist 18:43–45.
Bulaj G, Buczek O, Goodsell I, Jimenez EC, Kranski J, Nielsen JS, Garrett JE, Olivera BM. (2003) Efficient oxidative folding of conotoxins and the radiation of venomous cone snails. Proc Natl Acad Sci USA 100:Suppl. 2, 14562–14568.
Cameron AM and Endean R. (1972) Refutation of the venomous reputations of three teleost fishes. Toxicon 10:335–336.[Medline]
Chen W-J, Bonillo C, Lecointre G. (2003) Repeatability of clades as a critetion of reliability: a case study for molecular phylogeny of Acanthomorpha (Teleostei) with larger number of taxa. Mol Phylogenet Evol 26:262–288.[CrossRef][ISI][Medline]
Church JE and Hodgson WC. (2002) The pharmacological activity of fish venoms. Toxicon 40:1083–1093.[Medline]
de Pinna MCC. (1993) Higher-level phylogeny of Siluriformes, with a new classification of the order (Teleostei, Ostariophysi) (PhD dissertation). (City University of New York, New York)1–482.
de Plater G, Martin L, Milburn PJ. (1995) A pharmacological and biochemical investigation of the venom from the platypus (Ornithorhynchus anatinus). Toxicon 33:157–169.[Medline]
Fishelson L. (1974) Histology and ultrastructure of the recently found buccal toxic gland in the fish Meiacanthus nigrolineatus (Blennididae). Copeia 1974:386–392.[CrossRef]
Froese R and Pauly D (eds), 2004. Fishbase (version 11/2004). Available from: http://www.fishbase.org.
Goloboff PA. (1999) Analyzing large data sets in reasonable times: solutions for composite optima. Cladistics 15:415–428.[CrossRef]
Haddad V Jr, Martins IA, Makyama HM. (2003) Injuries caused by scorpionfishes (Scorpaena plumieri Bloch, 1789 and Scorpaena brasiliensis Cuvier, 1829) in the southwestern Atlantic Ocean (Brazilian coast): epidemiologic, clinic, and therapeutic aspects of 23 stings in humans. Toxicon 42:79–83.[Medline]
Hall TA. (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98.
Halstead BW. (1970) Poisonous and venomous marine animals of the world. (U.S. Government Printing Office, Washington, DC) vol 3:.
Halstead BW. (1988) Poisonous and venomous marine animals of the world 2nd ed (The Darwin Press, Inc, Princeton, NJ).
Hardman M. (2002) The phylogenetic relationships among extant catfishes, with special reference to Ictaluridae (Otophysi: Siluriformes) (PhD dissertation). (University of Illinois, Urbana-Champaign, IL) pp. 1–206.
Imamura H. (2004) Phylogenetic relationships and a new classification of the superfamily Scorpaenoidea (Actinopterygii: Perciformes). Species Divers 9:1–36.
Ishida M. (1994) Phylogeny of the suborder Scorpaenoidei (Pisces: Scorpaeniformes). Bull Nansei Natl Fish Res Inst 27:1–112.
Jackson K. (2003) The evolution of venom-delivery systems in snakes. Zool J Linn Soc 137:337–354.[CrossRef]
Johnson GD. (1993) Percomorph phylogeny: progress and problems. Bull Mar Sci 52:3–28.
Karmakar S, Muhuri DC, Dasgupta SC, Nagchaudhuri AK, Gomez A. (2004) Isolation of a haemorrhagic protein toxin (SA-HT) from the Indian venomous butterfish (Scatophagus argus, Linn) sting extract. Indian J Exp Biol 42:452–460.[Medline]
Mebs D. (1999) Studies on biological and enzymatic activities of salivary glands from the European hedgehog (Erinaceus europaeus). Toxicon 37:1635–1638.[Medline]
Miya M, Takeshima H, Endo H, Ishiguro NB, Inoue JG, Mukai T, Satoh TP, Yamaguchi M, Kawaguchi A, Mabuchi K, Shirai SM, Nishida M. (2003) Major patterns of higher teleostean phylogenies: a new perspective based on 100 complete mitochondrial DNA sequences. Mol Phylogenet Evol 26:121–138.[CrossRef][ISI][Medline]
Nelson G. (1989) Phylogeny of major fish groups. In Fernholm B, Bremer K, Jörnvall K (Eds.). The hierarchy of life: molecules and morphology in phylogenetic analysis (Excerpta Medica, Amsterdam, the Netherlands) pp. 325–336.
Nelson JS. (1994) Fishes of the World. 3rd ed (John Wiley and Sons, New York).
Newman DJ, Cragg GM, Snader KM. (2003) Natural products as sources of new drugs over the period 1981–2002. J Nat Prod 66:1022–1037.[CrossRef][Medline]
Nixon KC. (1999) The parsimony ratchet, a new method for rapid parsimony analysis. Cladistics 15:407–414.[CrossRef][ISI]
Poss SG. (1982) Taxonomy and systematics of the velvetfishes (Pisces: Aploactinidae) (PhD dissertation) (University of Michigan, Ann Arbor, MI) pp. 1–376.
Randall JE, Allen GR, Steene RC. (1997) Fishes of the Great Barrier Reef and Coral Sea 2nd ed (University of Hawaii Press, Honolulu, HI).
Raven PH, Bean MJ, Davis FW, Eaton GP, Haines SG, Hezir J, Jackson JBC, Leinberger CB, Meyer JL, Molin WA, Morin NR, Nevling LI, Orians GH, Risser PG, Robbins RJ, Savage JM, Sparrow RD, Tschinkel VJ, Wheeler QD, Fischer EA, Stine DD, Adams PA, Grossblatt N. (1994) A biological survey for the nation (National Research Council, Washington, DC).
Rifkin J and Williamson J. (1996) Venomous fish. Venomous and poisonous marine animals: a medical and biological handbook (University of New South Wales PressIn Williamson JA, Fenner PJ, Burnett JW, Rifkin JF (Eds.). , Sydney, Australia)354–395.
Russell FE and Boger CM. (1981) Gila monster: its biology, venom and bite—a review. Toxicon 19:341–359.[Medline]
Smith WL and Wheeler WC. (2004) Polyphyly of the mail-cheeked fishes (Teleostei: Scorpaeniformes): evidence from mitochondrial and nuclear sequence data. Mol Phylogenet Evol 32:627–646.[CrossRef][ISI][Medline]
Smith-Vaniz WF, Satapoomin U, Allen GR. (2001) Meiacanthus urostigma, a new fangblenny from the northeastern Indian Ocean, with discussion and examples of mimicry in species of Meiacanthus (Teleostei: Blenniidae: Nemophini). Aqua J Ichthyol Aquat Biol 5:25–43.
Sosa-Rosales JI, Piran-Soares AA, Farsky SH, Takehara HA, Lima C, Lopes-Ferreira M. (2005) Important biological activities induced by Thalassophryne maculosa fish venom. Toxicon 45:155–161.[Medline]
Southcott RV. (1975) Australian venomous and poisonous fishes (Southcott, Mitcham, Australia).
Sparks JS and Smith WL. (2004a) Phylogeny and biogeography of the Malagasy and Australasian rainbowfishes (Teleostei: Melanotaenioidei): Gondwanan vicariance and evolution in freshwater. Mol Phylogenet Evol 33:719–734.[CrossRef][ISI][Medline]
Sparks JS and Smith WL. (2004b) Phylogeny and biogeography of cichlid fishes (Teleostei: Perciformes: Cichlidae). Cladistics 20:501–517.[CrossRef][ISI]
Stiassny MLJ, Wiley EO, Johnson GD, de Carvalho MR. (2004) Gnathostome fishes. In Cracraft J and Donoghue MJ (Eds.). Assembling the tree of life (Oxford University Press, Oxford) pp. 429.
Systematics Agenda 2000, 1994. Systematics agenda 2000: charting the biosphere. In: Technical Report. New York: Systematics Agenda 2000; 1–34.
Tan PTJ, Khan AM, Brusic V. (2003) Bioinformatics for venom and toxin sciences. Brief Bioinform 4:53–62.
Tang KL, Berendzen PB, Wiley EO, Morrissey JF, Winterbottom R, Johnson GD. (1999) The phylogenetic relationships of the suborder Acanthuroidei (Teleostei: Perciformes) based on molecular and morphological evidence. Mol Phylogenet Evol 11:415–425.[CrossRef][ISI][Medline]
Vetrano SJ, Lebowitz JB, Marcus S. (2002) Lionfish envenomation. J Emerg Med 23:379–382.[CrossRef][ISI][Medline]
Wheeler WC. (1996) Optimization alignment: the end of multiple sequence alignment in phylogenetics. Cladistics 12:1–9.
Wheeler WC. (1999) Fixed character states and the optimization of molecular sequence data. Cladistics 15:379–385.[CrossRef]
Wheeler WC. (2003a) Implied alignment: a synapomorphy-based multiple-sequence alignment method and its use in cladogram search. Cladistics 19:261–268.[CrossRef][ISI][Medline]
Wheeler WC. (2003b) Iterative pass optimization of sequence data. Cladistics 19:254–260.[CrossRef][ISI][Medline]
CiteULike 
Connotea 
Del.icio.us What's this?
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||