Weak warning signals can persist in the absence of gene flow

Abstract

Aposematic organisms couple conspicuous warning signals with a secondary defense to deter predators from attacking. Novel signals of aposematic prey are expected to be selected against due to positive frequency-dependent selection. How, then, can novel phenotypes persist after they arise, and why do so many aposematic species exhibit intrapopulation signal variability? Using a polytypic poison frog (Dendrobates tinctorius), we explored the forces of selection on variable aposematic signals using 2 phenotypically distinct (white, yellow) populations. Contrary to expectations, local phenotype was not always better protected compared to novel phenotypes in either population; in the white population, the novel phenotype evoked greater avoidance in natural predators. Despite having a lower quantity of alkaloids, the skin extracts from yellow frogs provoked higher aversive reactions by birds than white frogs in the laboratory, although both populations differed from controls. Similarly, predators learned to avoid the yellow signal faster than the white signal, and generalized their learned avoidance of yellow but not white. We propose that signals that are easily learned and broadly generalized can protect rare, novel signals, and weak warning signals (i.e., signals with poor efficacy and/or poor defense) can persist when gene flow among populations, as in this case, is limited. This provides a mechanism for the persistence of intrapopulation aposematic variation, a likely precursor to polytypism and driver of speciation.

Predators’ consumption of unpalatable prey does not vary as a function of bitter taste perception

“…Disentangling the effects of taste and toxicity on predators' foraging decisions is often difficult. Stronger taste might not be always linked to a higher toxin concentration (Ruxton and Kennedy 2006;Holen 2013;Nissim et al 2017;Marples et al 2018) or vice versa (Lawrence et al 2019), and predator species may vary in what they find unpalatable (Rojas et al 2017). Our study indicates that after detecting bitter taste, birds make their foraging decisions based on the post-ingestive feedback of consuming toxins.…”

The impact of life stage and pigment source on the evolution of novel warning signal traits

“…Gregariousness could have therefore facilitated shifts in warning coloration among N. lecontei populations. Finally, we cannot exclude the possibility that predators could also generalize avoidance learning across white to yellow color variants (22), but see (10) erato color phenotypes (73,83). Consistent with this "advergence" hypothesis, early-radiating erato-clade species exhibit much more pronounced population substructure than melpomeneclade species (73).…”

“…Despite several promising study systems (e.g. (22)(23)(24)), this level of integration remains rare with one notable exception: Müllerian mimics in the genus Heliconius (e.g. (25,26)).…”

“…Heliconius species have pronounced population genetic structure indicative of subdivision and drift(73). Color-associated population structure has also been detected in other aposematic species, such as the strawberry poison frog, Dendrobates pumilio(74) and the polytypic dyeing dart poison frog (Dendrobates tinctorius)(22). One important difference between N. lecontei and many other aposematic study systems is the role of warning coloration in mate choice.…”

Biased predation could promote convergence yet maintain diversity within Müllerian mimicry rings of Oreina leaf beetles

“…Asymmetric generalization has been found among different coloured seed bugs (Lygaeidae; Gamberale-stille & Tullberg, 1999) and firebugs (Pyrrhocoridae; Svádová et al, 2009), in shiny versus dull O. cacaliae (Waldron et al, 2017), and in poison frogs (Lawrence et al, 2019). Why it occurs is not entirely clear.…”