Discussion
We found that our sample of heliconiian butterflies and poison frogs all
reflected detectable quantities of ultraviolet light. When comparing
between VIS and UV sensitive visual models, this UV reflectance had a
negligible effect on achromatic contrast but did affect chromatic
contrast, to varying degrees. The visual signals of heliconiian
butterflies and poison frogs have both evolved under the influence of UV
sensitive predators for the purpose of mitigating predation risk via
aposematism. However, we found that UV reflectance from butterfly color
patterns had a much greater effect on enhancing chromatic contrast, both
in terms of absolute (change in JNDs) and proportional (percent increase
due to the addition of UV) change, than was recorded from the color
patterns of either of the poison frog species.
Maximizing visual contrast is not necessarily the goal of aposematic
signals, and two patterns can be visually distinct (e.g., different
combinations of colors) while being equally contrasting. However, by
quantifying the contribution of UV to achromatic and chromatic contrast,
our approach allows us to estimate the relative importance of these
wavelengths to signal design. That said, it is important to note that
the presence of UV reflectance within a color pattern does not equate to
UV serving an explicit function; and depending on context UV reflectance
could act as aposematism, camouflage, sexual signaling,
thermoregulation, or protection from solar radiation (Umbers 2013).
Moreover, pigments and structural colors will interact with light beyond
the wavelengths visible to observers, and reflectance characteristics
outside of the visible range may evolve without direct selection. For
example, selection for very high reflectance across 400-700 nm would
very plausibly, as a byproduct, also produce significant reflectance in
the near ultraviolet (350-400 nm) and perhaps near infrared (700-750
nm).
We cannot, therefore, definitively state a function for ultraviolet
reflectance in poison frogs, if indeed there is a function. However, by
directly comparing the characteristics of frog coloring to the
well-known UV signals of heliconiian butterflies we can provide guidance
for future investigations.
Many heliconiian butterflies have evolved highly contrasting signals
that contain a significant amount of UV light. However, despite high
contrast, and likely being visible to potential predators, UV
reflectance does not appear to play an important role in predator
aversion (Dell’Aglio et al. 2018; Finkbeiner et al. 2017). The most
compelling selection-based explanation for the evolution of UV+ signals
comes from their potential use(s) for sexual selection in the genusHeliconius, where UV+ 3-hydroxy-DL-kynurenine (3-OHK) yellow
pigments coincide with the duplication of UVS opsin genes (Briscoe et
al. 2010). These signals have, therefore, co-evolved with complex UV
sensitive visual systems that allow heliconiian butterflies to tune into
UV reflectance for both mate choice and species recognition (Briscoe et
al. 2010; Bybee et al. 2012; Finkbeiner et al. 2014; Finkbeiner et al.
2017). Visual discrimination that potentially plays an important role in
preventing intergeneric hybridization between mimetic Heliconiusand Eueides butterflies (Finkbeiner et al. 2017). Whereas allHeliconius species have duplicated UV coding opsin genes, it is
only likely truly influencing vision in certain clades ofHeliconius (such as H. erato, UV contrast shown in Figure
1E), yet even in these clades, expression is sex-specific and benefits
apparently restricted to females (Finkbeiner and Briscoe 2020; McCulloch
et al. 2016).
In comparison, UV reflectance in poison frogs appears to only have a
small effect on pattern contrast, and its utility, if any, remains
unknown (Yeager and Barnett 2020). Preliminary findings do not suggest
UV in A. bilinguis inguinal flash marks enhances detection with
model human predators (McEwan personal communication ). Although
color can be an important intra-specific signal for poison frogs (Maan
and Cummings 2009; Yang et al. 2019) the lack of UV sensitive
photoreceptors in the dendrobatid visual system means that it is
unlikely that ultraviolet reflectance has evolved in response to mating
preferences or intraspecific recognition. Importantly, however, visual
perception has only be characterized for O. pumilio (Siddiqi et
al. 2004), a species that lacks UV reflectance (Chaves-Acuña et al.
2020; Maan and Cummings 2009; Siddiqi et al. 2004; Summers et al. 1999).
Therefore, although it may be unlikely, we cannot conclusively rule out
the presence of UV sensitive vision in other dendrobatid species.
Moreover, as strong UV reflectance does not appear to affect predation
risk in artificial targets (Lyytinen et al. 2001) or heliconiian
butterflies (Finkbeiner et al. 2017), it also seems improbable that the
comparatively weak UV reflectance observed in poison frogs would be an
important contribution to aposematic signals. Indeed, where UV
reflectance has been reported in poison frogs other color pattern
combinations that lack UV have actually been found to result in greater
visual contrast (Yeager and Barnett 2020), and are more likely to be
avoided by avian predators (Lawrence and Noonan 2018).
To fully understand UV coloring in poison frogs we believe further study
is required. Firstly, we believe that it is important to characterize
the visual systems of a greater diversity of dendrobatid species
considering the impressive diversity of intra- and inter-specific color
patterns, where some species reflect UV and many well-studied species
apparently do not. Secondly, behavioral trials both with potential
predators and conspecifics are needed to examine whether observers
respond differently to UV+ and UV- signals under natural lighting
conditions. More widely, we believe that the role of UV reflectance in
aposematic signaling deserves more attention, or perhaps publication
bias against non-significant findings needs to be addressed. Finally, we
caution about the over interpretation of function in animal coloration,
such as in UV signals, and specifically suggest that neutral
evolutionary processes may be more common in shaping animal color
patterns than currently acknowledged.
Here we investigated the degree to which UV reflectance affected the
visual contrast of conspicuous signals. UV is known to play an important
role in intra-specific communication in heliconiian butterflies, and we
found that UV had a correspondingly large effect on increasing the
chromatic contrast of butterfly coloration. Conversely, poison frogs are
not known to perceive UV light, and UV reflectance had a comparatively
small effect on signal contrast. These data support the notion that UV
reflectance does not necessarily have a special role in aposematic
signal design and has likely evolved neutrally in many poison frogs
(Yeager and Barnett 2020), however, much remains unknown.