Snake Mimicry Research Articles

Foraging predicts the evolution of warning coloration and mimicry in snakes

Warning coloration and Batesian mimicry are classic examples of Darwinian evolution, but empirical evolutionary patterns are often paradoxical. We test whether foraging costs predict the evolution of striking coloration by integrating genetic and ecological data for aposematic and mimetic snakes (Elapidae and Dipsadidae). Our phylogenetic comparison on a total of 432 species demonstrated that dramatic changes in coloration were well predicted by foraging strategy. Multiple tests consistently indicated that warning coloration and conspicuous mimicry were more likely to evolve in species where foraging costs of conspicuous appearance were relaxed by poor vision of their prey, concealed habitat, or nocturnal activity. Reversion to crypsis was also well predicted by ecology for elapids but not for dipsadids. In contrast to a theoretical prediction and general trends, snakes' conspicuous coloration was correlated with secretive ecology, suggesting that a selection regime underlies evolutionary patterns. We also found evidence that mimicry of inconspicuous models (pitvipers) may have evolved in association with foraging demand for crypsis. These findings demonstrate that foraging is an important factor necessary to understand the evolution, persistence, and diversity of warning coloration and mimicry of snakes, highlighting the significance of additional selective factors in solving the warning coloration paradox.

The banded colour patterns of sea snakes discourage attack by predatory fishes, enabling Batesian mimicry by harmless species.

The evolution of bright 'warning' colours in nontoxic animals often is attributed to mimicry of toxic species, but empirical tests of that hypothesis must overcome the logistical challenge of quantifying differential rates of predation in nature. Populations of a harmless sea snake species (Emydocephalus annulatus) in New Caledonia exhibit colour polymorphism, with around 20% of individuals banded rather than melanic. Stability in that proportion over 20 years has been attributed to Batesian mimicry of deadly snake species by banded morphs of the harmless taxon. This hypothesis requires that banded colours reduce a snake's vulnerability to predation. We tested that idea by pulling flexible snake-shaped models through the water and recording responses by predatory fish. Black and banded lures attracted similar numbers of following fish, but attacks were directed almost exclusively to black lures. Our methods overcome several ambiguities associated with experimental studies on mimicry in terrestrial snakes and support the hypothesis that banded colour patterns reduce a non-venomous marine snake's vulnerability to predation.

Correction to: Predator‑based selection and the impact of edge sympatry on components of coral snake mimicry

Correction to: Predator‑based selection and the impact of edge sympatry on components of coral snake mimicry

Concepts and contentions of coral snake resemblance: Batesian mimicry and its alternatives

Abstract Venomous coral snakes and non-venomous coral snake lookalikes are often regarded as a classic example of Batesian mimicry, whereby a harmless or palatable organism imitates a harmful or less palatable organism. However, the validity of this claim is questionable. The existing literature regarding coral snake mimicry presents a divisive stance on whether Batesian mimicry is occurring or whether the similarity between snakes is attributable to alternative factors. Here, we compile available literature on coral snake mimicry and assess the support for Batesian mimicry. We find that most of the recent relevant literature (after approximately 2000) supports the Batesian mimicry hypothesis. However, this is not strongly supported by empirical evidence. Potential considerations addressed here for both the Batesian and alternative hypotheses include the function of the colour pattern, predatory learning and the biogeographical distribution of similar snakes. The analyses performed previously by mimicry researchers show that the interpretation of the conditions for mimicry is not consistent throughout the scientific community when applied to coral snake systems. This review focuses on this division and stresses the need to reach an agreement about the adaptive significance of New World coral snakes and their lookalikes.

Predator-based selection and the impact of edge sympatry on components of coral snake mimicry

Mimicry is a vivid example of how predator-driven selection can impact phenotypic diversity, which itself can be influenced by the presence (sympatry) or absence (allopatry) of a dangerous model. However, the impact of sympatry and allopatry on predation on mimicry systems at fine spatial scales (e.g., edge sympatry, allopatry) is not well understood. We studied mimicry in a montane tropical site in Honduras with an abrupt elevational gradient where coral snakes and mimics exist in close sympatry and allopatry. Specifically, we used clay replicas to test the impact of edge sympatry on (1) overall attack rates, (2) the fitness benefit of mimetic coloration, and (3) predation on specific mimetic signal components. Unlike previous research, we found that mimetic phenotypes received significantly more attacks than cryptic replicas in edge sympatry, suggesting that mimetic phenotypes might not confer a fitness benefit in areas of edge sympatry. Additionally, we documented temporal variation in predator-based selection, as the impacts of allopatry on predatory attacks varied among years. Our results imply that the effect of sympatry and allopatry on predator-based selection in mimicry systems may be more complex than previously thought for species-rich assemblies of coral snakes and their mimics in the montane tropics.

Convergence and divergence in anti-predator displays: a novel approach to quantitative behavioural comparison in snakes

AbstractAnimals in nature use many strategies to evade or deter their predators. Within venomous snake mimicry, stereotyped anti-predator behaviours are hypothesized to be effective warning signals under strong selection for independent convergence across species. However, no studies have systematically quantified snake anti-predator displays across taxonomically broad clades to examine how these behaviours evolve within a comparative methods framework. Here we describe a new high-throughput approach for collecting and quantifying anti-predator displays in snakes that demonstrates both low observer bias and infinite extension. Then, we show this method’s utility by comparing 20 species spanning six taxonomic families from Peru. We found that a simple experimental set-up varying simulated predator cues was successful in eliciting displays across species and that high-speed videography captured a great diversity of anti-predator responses. Although display components show complicated patterns of covariance, we found support for behavioural convergence in anti-predator displays among elapid coral snakes and their distantly related mimics. Our approach provides new analytical opportunities for both behaviour and kinematics, especially macroevolutionary analyses across clades with similar difficulty in observing or comparing trait diversity.

Behavioral snake mimicry in breeding tits.

Many animals mimic the behavior or the appearance of venomous snakes. When humans or other potential predators place their hand near the nest of tits belonging to the family Paridae (and a few other species), the incubating female performs a hissing display that mimics the inhalation hiss of a viper or another snake. They hiss vigorously while lunging their head forward and shaking their wings and tail, repeating this behavior several times. The structure of the hiss in tits is similar to that of the inhalation hiss of a snake, providing evidence of significant convergence of the mimic toward the model. The behavior of individual females is repeatable among trials. Individuals that flew away from their nest box only performed the hissing display on 6% of later trials, when present at their box, whereas individuals that did not fly away hissed on 28% of occasions, consistent with great tits Parus major either cautiously flying away or staying put on their nest while actively defending it. Individuals that flew away produced fewer chicks than individuals that stayed and hissed. The hissing display was more common when snakes were more abundant: 1) When breeding late during the season; 2) when breeding at sites with more snakes; and 3) when breeding in subtropical and tropical China with a higher abundance of snakes than in Denmark with a lower abundance. The frequency of nest predation was higher in sites with no snakes, and the frequency of predation increased with decreasing frequency of hissing display. These findings are consistent with expectations for frequency-dependent selection acting on snake mimicry.

Multiple models generate a geographical mosaic of resemblance in a Batesian mimicry complex.

Batesian mimics-benign species that receive protection from predation by resembling a dangerous species-often occur with multiple model species. Here, we examine whether geographical variation in the number of local models generates geographical variation in mimic-model resemblance. In areas with multiple models, selection might be relaxed or even favour imprecise mimicry relative to areas with only one model. We test the prediction that model-mimic match should vary with the number of other model species in a broadly distributed snake mimicry complex where a mimic and a model co-occur both with and without other model species. We found that the mimic resembled its model more closely when they were exclusively sympatric than when they were sympatric with other model species. Moreover, in regions with multiple models, mimic-model resemblance was positively correlated with the resemblance between the model and other model species. However, contrary to predictions, free-ranging natural predators did not attack artificial replicas of imprecise mimics more often when only a single model was present. Taken together, our results suggest that multiple models might generate a geographical mosaic in the degree of phenotype matching between Batesian mimics and their models.

Diverse Evidence for the Decline of an Adaptation in a Coral Snake Mimic

Losses of adaptations in response to changed selective pressures are evolutionarily important phenomena but relatively few empirical examples have been investigated in detail. To help fill this gap, we took advantage of a natural experiment in which coral snake mimics occur on two nearby tropical islands, one that has coral snake models (Trinidad) and one that lacks them (Tobago). On Tobago, an endemic coral snake mimic (Erythrolamprus ocellatus) exists but has a relatively poor resemblance to coral snakes. Quantitative image analysis of museum specimens confirmed that E. ocellatus is a poor mimic of coral snakes. To address questions related to the functional importance of this phenotype, we conducted a field experiment on both islands with snake replicas made of clay. These results clearly indicated a strong inter-island difference in predator attack rates where snake replicas that resembled coral snakes received protection in Trinidad but not in Tobago. Further, a molecular phylogenetic analysis of the ancestry of E. ocellatus revealed that this poor coral snake mimic is deeply nested in a clade of good coral snake mimics. These data suggest that the lack of coral snakes on Tobago altered the selective environment such that the coral snake mimicry adaptation was no longer advantageous. The failure to maintain this ancestral feature in allopatry provides a compelling example of how losses of complex adaptations can occur.

Coral snakes predict the evolution of mimicry across New World snakes.

Batesian mimicry, in which harmless species (mimics) deter predators by deceitfully imitating the warning signals of noxious species (models), generates striking cases of phenotypic convergence that are classic examples of evolution by natural selection. However, mimicry of venomous coral snakes has remained controversial because of unresolved conflict between the predictions of mimicry theory and empirical patterns in the distribution and abundance of snakes. Here we integrate distributional, phenotypic and phylogenetic data across all New World snake species to demonstrate that shifts to mimetic coloration in nonvenomous snakes are highly correlated with coral snakes in both space and time, providing overwhelming support for Batesian mimicry. We also find that bidirectional transitions between mimetic and cryptic coloration are unexpectedly frequent over both long- and short-time scales, challenging traditional views of mimicry as a stable evolutionary ‘end point' and suggesting that insect and snake mimicry may have different evolutionary dynamics.

Unlinked Mendelian inheritance of red and black pigmentation in snakes: Implications for Batesian mimicry

Identifying the genetic basis of mimetic signals is critical to understanding both the origin and dynamics of mimicry over time. For species not amenable to large laboratory breeding studies, widespread color polymorphism across natural populations offers a powerful way to assess the relative likelihood of different genetic systems given observed phenotypic frequencies. We classified color phenotype for 2175 ground snakes (Sonora semiannulata) across the continental United States to analyze morph ratios and test among competing hypotheses about the genetic architecture underlying red and black coloration in coral snake mimics. We found strong support for a two-locus model under simple Mendelian inheritance, with red and black pigmentation being controlled by separate loci. We found no evidence of either linkage disequilibrium between loci or sex linkage. In contrast to Batesian mimicry systems such as butterflies in which all color signal components are linked into a single "supergene," our results suggest that the mimetic signal in colubrid snakes can be disrupted through simple recombination and that color evolution is likely to involve discrete gains and losses of each signal component. Both outcomes are likely to contribute to the exponential increase in rates of color evolution seen in snake mimicry systems over insect systems.

Batesian mimicry promotes pre- and postmating isolation in a snake mimicry complex.

We evaluated whether Batesian mimicry promotes early-stage reproductive isolation. Many Batesian mimics occur not only in sympatry with their model (as expected), but also in allopatry. As a consequence of local adaptation within both sympatry (where mimetic traits are favored) and allopatry (where nonmimetic traits are favored), divergent, predator-mediated natural selection should disfavor immigrants between these selective environments as well as any between-environment hybrids. This selection might form the basis for both pre- and postmating isolation, respectively. We tested for such selection in a snake mimicry complex by placing clay replicas of sympatric, allopatric, or hybrid phenotypes in both sympatry and allopatry and measuring predation attempts. As predicted, replicas with immigrant phenotypes were disfavored in both selective environments. Replicas with hybrid phenotypes were also disfavored, but only in a region of sympatry where previous studies have detected strong selection favoring precise mimicry. By fostering immigrant inviability and ecologically dependent selection against hybrids (at least in some habitats), Batesian mimicry might therefore promote reproductive isolation. Thus, although Batesian mimicry has long been viewed as a mechanism for convergent evolution, it might play an underappreciated role in fueling divergent evolution and possibly even the evolution of reproductive isolation and speciation.

Rapid evolution of mimicry following local model extinction

Batesian mimicry evolves when individuals of a palatable species gain the selective advantage of reduced predation because they resemble a toxic species that predators avoid. Here, we evaluated whether-and in which direction-Batesian mimicry has evolved in a natural population of mimics following extirpation of their model. We specifically asked whether the precision of coral snake mimicry has evolved among kingsnakes from a region where coral snakes recently (1960) went locally extinct. We found that these kingsnakes have evolved more precise mimicry; by contrast, no such change occurred in a sympatric non-mimetic species or in conspecifics from a region where coral snakes remain abundant. Presumably, more precise mimicry has continued to evolve after model extirpation, because relatively few predator generations have passed, and the fitness costs incurred by predators that mistook a deadly coral snake for a kingsnake were historically much greater than those incurred by predators that mistook a kingsnake for a coral snake. Indeed, these results are consistent with prior theoretical and empirical studies, which revealed that only the most precise mimics are favoured as their model becomes increasingly rare. Thus, highly noxious models can generate an 'evolutionary momentum' that drives the further evolution of more precise mimicry-even after models go extinct.

Mimicry's palette: widespread use of conserved pigments in the aposematic signals of snakes

Mimicry, where one species resembles another species because of the selective benefits of sharing a common signal, is especially common in snakes. Snakes might be particularly prone to evolving mimicry if all species share some of the same proximate mechanisms that can be used to produce aposematic/mimetic signals. We evaluated this possibility by examining color pigments in 11 species of snakes from four different families, three species of which participate in a coral snake mimicry complex involving convergence in coloration. We found that all 11 species used combinations of two pteridine pigments and melanin in their coloration, regardless of whether or not they were mimics. Furthermore, the presence or absence of red pteridines was strongly correlated with the relative excitation of medium- and long-wavelength photoreceptors in birds, thereby linking shared pigmentation to perception of those pigments by likely agents of selection. Thus, precise color mimicry might be relatively easy to evolve among snakes owing to symplesiomorphies in pigmentation.

Facultative pheromonal mimicry in snakes: “she-males” attract courtship only when it is useful

Males of many animal species mimic females, and thereby deceive rival males. Facultative shifts in posture, color, or movement allow a male using visually-based mimicry to adopt and terminate mimicry rapidly. Pheromonal mimicry is rare in vertebrates perhaps because it is difficult to redeploy pheromones rapidly enough to adjust male tactics to local conditions. In Manitoba garter snakes (Thamnophis sirtalis parietalis), female mimicry benefits males immediately after they have emerged from hibernation. While the snakes are cold and slow, courtship warms them and protects them against predatory crows. This benefit disappears as soon as the snakes are warm. We show that (unlike females) she-male garter snakes attract courting males only when they are cold. Low temperatures may suppress volatility of “less attractive” components of the pheromones (saturated methyl ketones) that she-males use to attract courtship, allowing male snakes to function as transvestites only when this tactic is beneficial.

Body size as a primary determinant of ecomorphological diversification and the evolution of mimicry in the lampropeltinine snakes (Serpentes: Colubridae)

Evolutionary correlations between functionally related character suites are expected as a consequence of coadaptation due to physiological relationships between traits. However, significant correlations may also exist between putatively unrelated characters due to shared relationships between those traits and underlying variables, such as body size. Although such patterns are often dismissed as simple body size scaling, this presumption may overlook important evolutionary patterns of diversification. If body size is the primary determinant of potential diversity in multiple unrelated characters, the observed differentiation of species may be governed by variability in body size, and any biotic or abiotic constraints on the diversification thereof. Here, we demonstrate that traits related to both predatory specialization (gape and diet preference) and predatory avoidance (the development of Batesian mimicry) are phylogenetically correlated in the North American snake tribe Lampropeltini. This is apparently due to shared relationships between those traits and adult body size, suggesting that size is the primary determinant of ecomorphological differentiation in the lampropeltinines. Diversification in body size is apparently not linked to climatic or environmental factors, and may have been driven by interspecific interactions such as competition. Additionally, we find the presence of a 'key zone' for the development of both rattle- and coral snake mimicry; only small snakes feeding primarily on ectothermic prey develop mimetic colour patterns, in or near the range of venomous model species.

Not so rare snakes: a revision of theGeophis sieboldigroup (Colubridae: Dipsadinae) in lower Central America and Colombia

The Geophis sieboldi species group is composed of 16 currently recognized species distributed from Mexico to Colombia. Within this group, snakes of populations referred to the Geophis brachycephalus complex of lower Central America and Colombia display a remarkable polychromatism and the systematic status of these and other populations is problematic. The present study provides an analysis, including multivariate techniques, of variation in scalation, coloration, relative tail length and hemipenes to clarify the specific allocation of the populations belonging to this clade. Our results confirm the validity of three previously described taxa, namely G. brachycephalus, G. nigroalbus and G. talamancae, with reassignments of several populations previously referred to G. brachycephalus. In addition we recognize as a new species a suite of western Panama Geophis previously of uncertain status. We further provide a review of all other members of the G. sieboldi group in lower Central America and Colombia based on material obtained since the last revision of the group. Basic synonymies, diagnostics and known distributions are included for the treated taxa. Dietary guild, possible venomous coral snake mimicry and distributional anomalies for the group are discussed. © 2008 The Linnean Society of London, Zoological Journal of the Linnean Society, 2008, 153, 561–599.

Batesian Mimicry: Can a Leopard Change Its Spots — and Get Them Back?

Can undefended mimics survive outside the range of their noxious models? Two recent studies on Batesian mimicry suggest they can, but alternative survival strategies and morphologies are then favoured.

Population differences in predation on Batesian mimics in allopatry with their model: selection against mimics is strongest when they are common

Batesian mimicry evolves when a palatable species, the "mimic," resembles a dangerous species, the "model," because both receive protection from predation. Yet, this protection should break down where the model is absent, because predators in such areas would not be under selection to avoid the model.Here,we test this prediction in a coral snake mimicry complex. We exposed plasticine replicas of milk snakes that closely mimic coral snakes to natural predators to determine if good mimetic milk snakes are preferentially attacked in allopatry with their model. Moreover, we evaluated whether attack rates on these replicas varied among three different allopatric regions that differed in the type of mimic found locally (i.e., good mimic, poor mimic, or no mimic). When all three regions were considered together, mimics were not preferentially attacked. When regions were analyzed separately, however, attacks on mimics were significantly greater than randomness only where good mimics were found. These variable levels of predation on good mimics might reflect frequency-depen- dent (i.e., apostatic) predation. In allopatric regions where good mimics are present, predators might have learned or evolved preferences for conspicuous, palatable prey that they encounter frequently.By contrast, in allopatric regions where good mimics are absent, predators might not have learned or evolved preferences for novel phenotypes. Thus, when predation is frequency-dependent, as long as good mimics are rare, they might not experience elevated levels of predation in allopatry with their model as predicted by the Batesian mimicry hypothesis.

Benefits of female mimicry in snakes.

She-male garter snakes exploit the amorous attentions of other males to warm up. Males of several animal species mimic females either in appearance or in the chemical cues they release1,2, and this mimicry has generally been interpreted in terms of alternative mating strategies –– for example, a male that mimics a female may obtain stolen inseminations or avoid aggression from larger rivals3. Our studies of snakes suggest a different explanation, which relies on natural selection rather than sexual selection. Male garter snakes that produce female-like pheromones (she-males) may benefit simply because large 'mating balls' of amorous males form around them, transferring heat to the she-male after it emerges from hibernation and reducing its exposure to predators.