Host egg pigmentation protects developing parasitoids from ultraviolet radiation

Abstract

Parasites rely on their hosts not only for nutrition and reproduction, but also for protection against natural enemies and adverse climatic conditions. In host-parasite interactions, protective characteristics of both players are important to consider regarding damaging effects of environmental hazards. While ultraviolet radiation (UVR) is pervasive and harmful to organisms in general, its impact on parasite fitness remains understudied. Moreover, studies that do examine the effects of UV exposure on parasitic organisms tend to neglect host traits, which may vary inter-or intra-specifically and thus confer different levels of environmental protection. We examined in the laboratory whether the UV-protective value of host egg pigmentation could also benefit parasitoids, using the egg parasitoid Telenomus podisi and the predatory stink bug Podisus maculiventris. This host species lays eggs of variable pigmentation levels from light to dark grey, an adaptation protecting its own embryos from UVR. We showed that higher levels of host egg pigmentation protect parasitoids subjected to a developmental exposure to UVR, increasing emergence rates by up to 86% and reducing development time by up to 4%. This protective effect of host pigmentation was context-dependent, being less pronounced at low UVR intensity and towards the end of parasitoid development. Parasitoids that emerged from darker-coloured eggs exposed to UVR were of slightly larger size than those developing in light-coloured eggs, but other fitness-related traits (fecundity, longevity, sex ratio) were unaffected. This study provides the first experimental evidence that host pigmentation can increase host suitability for parasitic organisms, and emphasizes the importance of considering trait variation in interacting species when investigating the susceptibility of ecological communities to important abiotic environmental factors.

Latitudinal variation in biophysical characteristics of avian eggshells to cope with differential effects of solar radiation

“…In ground-nesting birds, darker eggs can sometimes have better camouflage than lighter eggs (Gómez et al, 2016;Troscianko et al, 2016), which suggests that ground-nesting birds may face trade-offs between the level of egg camouflage and dealing with high levels of solar radiation (Gómez et al, 2016;Wilson-Aggarwal et al, 2016). However, in sites where solar radiation is very high (>0.8 kW/m 2 ), lighter colors may not be advantageous because of the higher transmittance of light-colored eggshells, assuming no variation in eggshell thickness, as this increases the risk of UV radiation reaching the embryo (Abram et al, 2015;Brulez et al, 2015;Gaudreau et al, 2017;Lahti & Ardia, 2016;Maurer et al, 2015). Such high UV radiation levels are found at low latitudes, and this may be a reason for the occurrence of eggs of dark coloration at such latitudes in spite of high levels of solar radiation.…”

“…Because the eggs contain the DNA, harmful mutations could be inherited by the next generation (e.g., Flenley, 2011). Darker colors reduce light transmittance through eggshells, thus protecting the embryo from UV radiation (Abram et al, 2015;Brulez, Pike, & Reynolds, 2015;Gaudreau, Abram, & Brodeur, 2017;Lahti & Ardia, 2016;Maurer et al, 2015;Shafey, Ghannam, Al-Batshan, & Al-Ayed, 2004). Because the absorptance by darker colors is higher than that of lighter colors, this may result in a trade-off between the risk of egg overheating and the risk of UV radiation on embryos if ambient temperature and solar radiation are positively related (Lahti & Ardia, 2016): Darker eggshells would protect the embryo from UV radiation, but in turn would increase the risk of overheating.…”

Resisting the Pied Piper: Colorful Defense Mechanisms in Insect Eggs, with a Focus on Stink Bugs (Heteroptera: Pentatomidae)

“…The fact that the black markings absorb UV radiation while the white markings reflect it suggests that the embryos are probably protected against ionizing radiation. Podisus maculiventris (Say 1832), another stink bug, is known to have evolved selective egg pigmentation as a way to cope with UV radiation (Abram et al, 2015b) and predation (Torres-Campos et al, 2016), a trait that is recycled by its egg parasitoids (Gaudreau et al, 2017). Farnesi et al (2017) have also shown that higher levels of melanisation in mosquito eggs are inversely correlated to egg desiccation; such a function could also be served by the pigment in the Harlequin bug eggs.…”

“…Excess exposure to water can however be just as deadly, as is the case for rainfall-related mortality in mosquito eggs (Frank and Curtis, 1977). Yet, the abiotic stressor that probably has the highest impact on egg survival is solar radiation, as prolonged exposure to sunlight can cause overheating (Hinton, 1981) and ultraviolet irradiation (Abram et al, 2015b;Gaudreau et al, 2017).…”

“…Abram et al (2015b) sought to test that hypothesis and found that darker eggs had a higher probability of surviving prolonged exposure to UV radiation than pale eggs, especially at higher intensities. As a case of extended phenotype, parasitoid wasps attacking P. maculiventris eggs also benefit from the photoprotective pigment in question (Gaudreau et al, 2017), which surprisingly is not melanin and has yet to be identified (Abram et al, 2015b).…”