Introduction
Large-scale ecogeographical gradients can explain variation in diverse
traits, from body size (Ashton 2002) to colour (Friedman & Remeš 2017).
Several ecogeographical patterns have been formalised into rules; yet
there is persistent debate regarding underlying causes and the taxa to
which they apply (Gaston et al. 2008; Chown & Gaston 2010). This
problem is epitomised by Gloger’s rule and Bogert’s rule, which both
describe ecogeographical patterns of melanisation. Gloger’s rule
describes the tendency for heavily pigmented (darker) forms to be found
in hotter and more humid regions (Delhey 2017, 2019). This relationship
may be driven by one or more factors including camouflage in low light
environments (Zink & Remsen Jr 1986; Cheng et al. 2018),
protection from ultraviolet light or parasites (Burtt Jr & Ichida 2004;
Chaplin 2004), or pleiotropic effects of genes regulating both climatic
adaptations and melanin-based coloration (Ducrest et al. 2008).
Bogert’s rule (also termed the thermal melanin hypothesis) describes the
tendency for darker animals to occur in colder regions because darker
colours absorb more solar radiation, thus providing thermal benefits
(Bogert 1949). Traditionally, Bogert’s rule has been applied to
ectotherms and Gloger’s rule to endotherms; however, the accumulated
evidence suggests that both rules may apply broadly to ectotherms or
endotherms (Trullas et al. 2007; Delhey 2018; Galván et
al. 2018; Delhey et al. 2019). Efforts to reconcile the
seemingly opposing effects of these rules have so far been hampered by
the difficulty of disentangling the underlying drivers.
Most of the evidence that supports either Gloger’s or Bogert’s rule
relates to visible colour (all or part of the wavelengths range from
300–700 nm); however, the spectrum of direct sunlight extends well
beyond this range. Wavelengths from 700–1400 nm (near-infrared, NIR)
include approximately 50% of solar energy (Stuart-Fox et al.2017) and can therefore strongly affect heat gain. By contrast, NIR does
not directly affect camouflage because little or no NIR light can be
seen by animals (Stuart-Fox et al. 2017). Examining
ecogeographical gradients in NIR reflectance can therefore help to
distinguish underlying drivers of ecogeographical patterns of animal
coloration (Cuthill et al. 2017; Stuart-Fox et al. 2017;
Ruxton et al. 2018). To date, ecogeographical patterns of NIR
reflectance have only been examined in Australian birds and butterflies
(Medina et al. 2018; Munro et al. 2019), which both show
thermally adaptive variation. However, Australia is a hot and dry
continent so it remains unclear whether climatic gradients in NIR
reflectance exist for other taxa or climates.
Butterflies are a model group to investigate ecogeographical patterns of
light manipulation due to their thermal biology and extraordinary
diversity in coloration. They are primarily ectothermic like many
insects and regulate their body temperature through both physical and
behavioural traits (Clench 1966). Physical properties of the thorax and
basal wings (i.e. parts of the wings that are close to thorax) directly
affect the temperature of flight muscles through heat conduction
(Heinrich 1974). The wings beyond the basal region may have less impact
on thermoregulation because there is less haemolymph circulation and
fewer vascular extensions that can carry significant quantities of heat
to the thorax (Arnold 1964; Kammer & Bracchi 1973; Wasserthal 1983;
Kingsolver 1987). However, wings can overheat quickly under direct
sunlight due to their low thermal capacity, and butterflies have evolved
sophisticated wing scale structures to control wing temperature through
radiative cooling (Tsai et al. 2020). Butterflies also regulate
their temperature through various behavioural mechanisms including
dorsal and lateral basking (opening/folding wings to expose thorax and
wing surface), ground-contact, orientating themselves in relation to the
position of the sun, and shivering (Clench 1966). The reflectance of
butterflies plays a crucial role during behavioural thermoregulation
such as dorsal (wings open) and lateral (wings closed) basking because
the efficacy of these behaviours depends on how much light their body
and wings absorb (Kingsolver 1987, 1988). The reflectance of both
(especially dorsal) regions seems to play a key role in warming up
during basking while those of ventral regions seem to be additionally
related to preventing overheating (Kingsolver 1987). Thus, thermal
pressures may act differently on dorsal and ventral surfaces which
consequently result in the evolution of reflectance differences between
dorsal and ventral surfaces. Specifically, higher dorsal-ventral
contrast is predicted to evolve in species that are found in heat-stress
environments where the benefit for high ventral reflectance for cooling
is greater. However, this prediction has yet to be formally tested.
In this study, we tested whether climate predicts the reflectance of
both dorsal and ventral regions of 343 European butterfly species using
full-spectrum photography of museum specimens. We compiled climatic
niche characteristics of each species and tested multiple hypotheses
regarding ecogeographical patterns of butterfly reflectance after
controlling for phylogeny and phylogenetic uncertainty (Schweigeret al. 2014). We specifically addressed four questions regarding
ecogeographical variation in butterfly reflectance: (1) does butterfly
reflectance follow the patterns predicted by Bogert’s rule in both
visible and near-infrared wavebands? (2) does NIR reflectance show
thermally adaptive patterns independent of visible reflectance? (3) does
butterfly reflectance follow the patterns predicted by Gloger’s rule?
(4) does climate predict ventral-dorsal contrast in butterflies?