Evolution of Dietary Specialization and Chemical Defense in Poison Frogs (Dendrobatidae): A Comparative Analysis

Abstract

Defensive mechanisms, including noxious or toxic substances, are favored by predation-driven natural selection. The acquisition of noxious/toxic substances can be either endogenous, in which the substances are produced by the organism, or exogenous, in which the substances are produced by another organism and are sequestered. Evidence indicates that the defensive skin alkaloids of Neotropical poison frogs (Dendrobatidae) have an exogenous source: a diet of ants and other small alkaloid-containing arthropods, which we term the diet-toxicity hypothesis. A critical prediction of the diet-toxicity hypothesis is that independent origins of dietary specialization will be found to be correlated with independent origins of skin alkaloids. We tested this prediction in an integrated framework using comparative methods with new and published data on feeding ecology and chemical defense for 15 species of dendrobatids in five genera. We found a significant correlation between alkaloid profiles and degree of dietary specialization. This reveals a recurring association of dietary specialization and alkaloid sequestration in dendrobatids, which suggests parallel evolutionary trends in the origins of defensive mechanisms.

Indolizidine 239Q and quinolizidine 275I. Major alkaloids in two Argentinian bufonid toads (Melanophryniscus)

“…It now appears that all the skin alkaloids of the dendrobatid, mantellid and bufonid anurans are sequestered from dietary alkaloid-containing arthropods (Daly et al , 2002; Jones et al , 1999; Saporito et al , 2004, 2006, 2007a, b; Takada et al , 2005), while the skin pseudophrynamines of the myobatrachid frogs ( Pseudophryne ) are produced by the frogs (Smith et al , 2002). Both dietary specialization and microphagy have been proposed as significant components in the ecology and evolution of sequestered defenses in poison frogs, and in dendrobatid poison frogs, multiple origins of dietary specialization have been proposed (see Toft, 1995; Caldwell, 1996; Vences et al, 1998; Santos et al, 2003; Darst et al, 2005). Recently, the over 800 alkaloids detected in amphibian skin extracts were summarized along with their occurrence in the four above-mentioned anuran families and, for some, the discovery of putative dietary arthropod sources (Daly et al , 2005).…”

Lenomyrmex hoelldobleri: a new ant species discovered in the stomach of the dendrobatid poison frog, Oophaga sylvatica (Funkhouser)

“…In addition to systematic leaf litter sampling and hand collecting, the examination of stomach contents of leaf-litter foraging amphibians is a valuable source of cryptic and rarely collected ant species (Weber 1938, Delsinne and Fernández 2012, Sosa-Calvo 2015). Many species of amphibians and non-avian reptiles specialize on ant feeding and some species are predominantly myrmecophagous (Solé et al 2002, Darst et al 2005, Esteves et al 2008). In the Neotropical poison frog family Dendrobatidae, myrmecophagy evolved at least twice, possibly three times independently (Santos et al 2003, Darst et al 2005), and the frogs sequester the skin alkaloids mostly from their ant and mite diet (McGugan et al 2016).…”

“…Many species of amphibians and non-avian reptiles specialize on ant feeding and some species are predominantly myrmecophagous (Solé et al 2002, Darst et al 2005, Esteves et al 2008). In the Neotropical poison frog family Dendrobatidae, myrmecophagy evolved at least twice, possibly three times independently (Santos et al 2003, Darst et al 2005), and the frogs sequester the skin alkaloids mostly from their ant and mite diet (McGugan et al 2016). In addition to ants and mites, other arthropods, such as beetles and millipedes, are considered alkaloid sources for poison frogs (Dumbacher et al 2004, Saporito et al 2003, 2004, 2007).…”

“…4). Many amphibians, including species of the aposematic poison frogs in the family Dendrobatidae, and non-avian reptiles are known to be specialized predators of ants (Weber 1938, Darst et al 2005, Esteves et al 2008, Sosa-Calvo 2015), and therefore they provide interesting sources of rarely collected and new arthropod species. Dendrobatid poison frogs sequester alkaloids that are found in their skin toxins from their diet (Daly et al 2000, Saporito et al 2004, 2007, Darst et al 2005, McGugan et al 2016), and therefore we briefly discuss the ecology of the specialized ant feeding behavior, or myrmecophagy, of dendrobatid frogs.…”

Autophagy Therapeutic Potential of Garlic in Human Cancer Therapy

“…Many natural components have incredible potential to cure diseases without any adverse side effects, such as the collagenase isolated from the King crab ( Paralithodes camtschatica ) as a the strongest antibiotic,[1] the alkaloids from the skin of poison dart frogs (Dendrobatidae) toward the development of chemical defense. [2]…”