Introduction:
Our contemporary understanding of the evolution of bright and
conspicuous color patterns is rooted in the work of the early pioneers
of evolutionary themes such as natural selection. Charles Darwin
developed the theory of sexual selection to explain the presence of
conspicuous ornamentation, but realised it could not account for the
presence of bright colors in non-reproductive Lepidopteran larvae
(Darwin 1871). Alfred Russel Wallace, on the other hand, was skeptical
of sexual selection and instead built on the work of John Jenner Weir
and Henry Walter Bates, to outline a theory of aposematic warning
signals, that was later developed further by Edward Bagnall Poulton
(Caro 2017; Caro and Ruxton 2019; Marchant 1916; Poulton 1890).
Aposematic and sexually selected color patterns are highly diverse, but
such signals are often characterised by high visual contrast both
between pattern components within an organism, and to the background
against which the organism is viewed (Andersson 1994; Ruxton et al.
2019; Stevens and Ruxton 2012). Brighter and more conspicuous signals
are commonly associated with more potent defences and greater
reproductive fitness, such that predators are more easily deterred
(Aronsson and Gamberale-Stille 2008; Forsman and Herrström 2004; Forsman
and Merilaita 1999; Halpin et al. 2020; Prudic et al. 2006; Stevens et
al. 2010), rivals are more wary, and potential mates more interested
when signals are highly contrasting (Andersson 1994; Endler 1983; Ryan
and Keddy-Hector 1992; Svensson and Wong 2011).
High signal contrast can be achieved via two interconnected visual
pathways: achromatic contrast (luminance/brightness) and chromatic
contrast (hue/saturation). In vertebrates, achromatic contrast is
measured as a single intensity value received by longwave sensitive
photoreceptors, whereas hue is perceived through opponent processing by
two or more photoreceptors that differ in their peak wavelength
sensitivity (Kelber and Osorio 2010; Vorobyev and Osorio 1998).
Consequently, different colors contribute to phenotypic contrast in
different ways: longwave colors (e.g., red, orange, and yellow)
contribute to both achromatic and chromatic contrast, whereas shortwave
colors (e.g., blue and ultraviolet (UV)) only significantly affect
chromatic contrast (Stevens and Ruxton 2012; Umbers 2013).
For this reason, conspicuous signals frequently generate high visual
contrast by combining bright long wavelength colors with low luminance
black (Stevens and Ruxton 2012). Short wavelength colors, including UV,
can also create high contrast and are occasionally incorporated into
seemingly conspicuous signals (Umbers 2013). However, evidence for the
efficacy of UV in aposematic signals has been mixed, with no compelling
confirmation that naturally occurring UV signals are effective at
deterring predators despite some evidence that UV signals can be learned
(Lyytinen et al. 2001; Werner et al. 2014a; Werner et al. 2014b; Werner
et al. 2012). Moreover, rather than preventing attacks UV containing
(UV+) signals can instead deflect attacks to more expendable body parts
(Olofsson et al. 2010), or they may actually increase predation risk
(Lyytinen et al. 2004). Despite the discovery of UV reflectance
attracting much attention, perhaps due to our own inability to perceive
such signals, we currently lack a complete understanding of if, or to
what extent, UV reflectance contributes to aposematic signaling.
In the Neotropics two independent, and completely unrelated, radiations
of bright conspicuous colors have drawn much scientific attention: the
heliconiian butterflies (Heliconiinae; Nymphalidae) and the poison frogs
(Dendrobatidae: Anura). Both groups are found in similar rainforest
habitats, are highly toxic, are at risk from similar predatory taxa, and
have become renowned for their high diversity of species and bright
colors (Merrill et al. 2015; Stynoski et al. 2015).
Despite many similarities in color diversity, chemical defense, the
visual environment, and the predator community, ultraviolet reflective
colors are relatively common in heliconiian butterflies but seemingly
rare in poison frogs (Briscoe et al. 2010; Bybee et al. 2012; Yeager and
Barnett 2020). Indeed, we recently described the first example of
UV-reflectance in poison frogs, from an Ecuadorian population ofOophaga sylvatica . We found that although UV shows up brightly in
photographs, it adds little to internal color pattern contrast (Yeager
and Barnett 2020). As coloring in both groups has been selected under
the influence of similar UV-sensitive predators for the purpose of
aposematism, the lack of UV reflection in frogs is perplexing. Here we
expand these previous findings to describe UV reflectance in two more
species of poison frog (Ameerega bilinguis and Epipedobates
tricolor ). We compare the contribution of UV to signal contrast between
these two dendrobatid frogs and five species of heliconiian butterflies,
and then discuss the importance of predator versus conspecific vision to
point to potential explanations for the evolution of UV reflectance in
these groups.