Diversity, phylogenetic distribution, and origins of venomous catfishes

Abstract

Background: The study of venomous fishes is in a state of relative infancy when compared to that of other groups of venomous organisms. Catfishes (Order Siluriformes) are a diverse group of bony fishes that have long been known to include venomous taxa, but the extent and phylogenetic distribution of this venomous species diversity has never been documented, while the nature of the venoms themselves also remains poorly understood. In this study, I used histological preparations from over 100 catfish genera, basic biochemical and toxicological analyses of fin spine extracts from several species, and previous systematic studies of catfishes to examine the distribution of venom glands in this group. These results also offer preliminary insights into the evolutionary history of venom glands in the Siluriformes.

Results: Histological examinations of 158 catfish species indicate that approximately 1250-1625+ catfish species should be presumed to be venomous, when viewed in conjunction with several hypotheses of siluriform phylogeny. Maximum parsimony character optimization analyses indicate two to three independent derivations of venom glands within the Siluriformes. A number of putative toxic peptides were identified in the venoms of catfish species from many of the families determined to contain venomous representatives. These peptides elicit a wide array of physiological effects in other fishes, though any one species examined produced no more than three distinct putative toxins in its venom. The molecular weights and effects produced by these putative toxic peptides show strong similarities to previously characterized toxins found in catfish epidermal secretions.

Conclusion: Venom glands have evolved multiple times in catfishes (Order Siluriformes), and venomous catfishes may outnumber the combined diversity of all other venomous vertebrates. The toxic peptides found in catfish venoms may be derived from epidermal secretions that have been demonstrated to accelerate the healing of wounds, rather than defensive crinotoxins.

Figure 1

The Venom Delivery System of Catfishes. (A) Northern madtom (Noturus stigmosus) with dorsal and pectoral fin spines indicated by red arrows. (B) Pectoral girdle of Noturus stigmosus with articulated pectoral fin spines. Abbreviations: ps = pectoral fin spine, cle = cleithrum, cor = coracoid, cor-pp = posterior process of coracoid. (C) Cross section of the pectoral-fin spine of Noturus stigmosus showing the association of venom gland cells with the fin spine. Abbreviations: ps = pectoral spine, vgc = venom gland cells.

Figure 2

Histological preparations of fin spines from several venomous catfish species. (A) Acrochordonichthys rugosus (Akysidae), (B) Liobagrus reini (Amblycipitidae), (C) Dianema longibarbis (Callichthyidae), (D) Chaca chaca (Chacidae), (E) Lophiobagrus cyclurus (Claroteidae), (F) Lithodoras dorsalis (Doradidae). Abbreviations: ps = pectoral fin spine, vgc = venom gland cells. Scale bars, 0.5 mm.

Figure 3

Additional histological preparations of fin spines from venomous catfish species. (A) Pimelodella mucosa (Heptapteridae), (B) Chiloglanis productus (Mochokidae), (C) Pseudolais pleurotaenia (Pangasiidae), (D) Plotosus canius (Plotosidae), (E) Schilbe mystus (Schilbidae), (F) Horabagrus brachysoma (incertae sedis). Abbreviations: ps = pectoral fin spine, vgc = venom gland cells. Scale bars, 0.5 mm.

Figure 4

Venom glands have evolved multiple times in catfishes. The results of a character optimization analysis of a siluriform phylogeny generated from 440 morphological characters indicate the independent evolution of venom glands within the Loricarioidei as well as within the Siluroidei, leading to the majority of venomous catfish diversity. Phylogeny redrawn from Diogo [26]. Red branches indicate venomous lineages, black branches indicate non venomous lineages, yellow branches indicate lineages not examined in this study.

Figure 5

Results of character optimization analysis using an alternative morphology-based phylogeny. Phylogeny redrawn from Mo [30], based on 126 morphological characters. Red branches indicate venomous lineages, black branches indicate non venomous lineages, and yellow branches indicate groups not examined in this study. As in Figs. 4 and 6, the independent evolution of venom glands is indicated in the Loricarioidei (sensu [26] and [28]), in the family Callichthyidae. Patterns of venom gland evolution in the Siluroidei are obscured, due to the poor resolution of basal relationships. Given the broad range of siluroid families in which venom glands are found and similarities in venom composition between these families, a single, relatively basal development of venom glands seems the most parsimonious and likely scenario.

Figure 6

Results of character optimization analysis using a recent molecular siluriform phylogeny. Phylogeny redrawn from Sullivan et al. [28], based on RAG 1 and RAG 2 nuclear data. Red branches indicate venomous lineages, black branches indicate non venomous lineages. Again, the independent evolution of venom glands is found in the Loricarioidei, in the family Callichthyidae. Independent evolution of venom glands must also be ascribed to the family Doradidae, due to its nesting within a clade containing the non-venomous Aspredinidae and Auchenipteridae. Similarly to Fig. 5, the evolution of venom glands at the base of the Siluroidei are obscured, due to poor resolution of basal relationships.

Figure 7

SDS-PAGE analyses of venom extracts from several catfish species. Left lanes represent venom extracts, right lanes represent extracts prepared from fin tissue. Arrows indicate positions of unique venom protein bands or proteins found in greater concentrations in venom extracts than in fin tissue extracts. (?) represents ambiguity between smearing and an additional, unique venom peptide band. Large quantities of a 110 kDa peptide are found in the venom extracts of nearly all species shown, with the exception of Pimelodus. The presence and variation of venom peptides in the size range of 10-20 kDa is also clearly visible. Samples from non-venomous Ameiurus melas are shown for comparison.

Figure 8

The distinctive venom delivery apparatus of a doradid catfish. Rather than forming longitudinal bundles along the spine, as in other siluroid catfishes, the glandular tissue in doradids is found in macroscopically visible aggregations between the posterior serrae of the fin spine. Abbreviations: s = pectoral spine, ps = posterior serrae, gt = glandular tissue.