A scenario for the evolution of selective egg coloration: the roles of enemy-free space, camouflage, thermoregulation and pigment limitation

Abstract

Behavioural plasticity can drive the evolution of new traits in animals. In oviparous species, plasticity in oviposition behaviour could promote the evolution of new egg traits by exposing them to different selective pressures in novel oviposition sites. Individual females of the predatory stink bug Podisus maculiventris are able to selectively colour their eggs depending on leaf side, laying lightly pigmented eggs on leaf undersides and more pigmented eggs, which are more resistant to ultraviolet (UV) radiation damage, on leaf tops. Here, we propose an evolutionary scenario for P. maculiventris egg pigmentation and its selective application. We experimentally tested the influence of several ecological factors that: (i) could have favoured a behavioural shift towards laying eggs on leaf tops and thus the evolution of a UV-protective egg pigment (i.e. exploitation of enemy-reduced space or a thermoregulatory benefit) and (ii) could have subsequently led to the evolution of selective pigment application (i.e. camouflage or costly pigment production). We found evidence that a higher predation pressure on leaf undersides could have caused a shift in oviposition effort towards leaf tops. We also found the first evidence of an insect egg pigment providing a thermoregulatory advantage. Our study contributes to an understanding of how plasticity in oviposition behaviour could shape the responses of organisms to ecological factors affecting their reproductive success, spurring the evolution of new morphological traits.

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

“…Populations of African village weaverbirds Ploceus cucullatus changed in egg appearance after being introduced in sites where they experienced different levels of solar radiation compared to those in their original sites (Lahti, ). However, the variation described in these studies can also be interpreted either as local adaptation (evolution), or environmental constraints affecting egg coloration by modifying the state (nutritional status/stress level) of the female bird, and it remains to be demonstrated whether birds plastically adjust egg coloration to match environmental conditions, as it has been shown in insects (Abram et al., ; Torres‐Campos, Abram, Guerra‐Grenier, Boivin, & Brodeur, ). Individual phenotypic plasticity may be adaptive, as there may be differences in the effects of solar radiation throughout the long nesting season of the Kentish plover (individual females may lay up to four clutches in a season [Fraga & Amat, ]), as well as between sites at which individual plovers may breed during successive nesting attempts.…”

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.…”

“…Although this paper looked at the three likely derived egg-laying strategies (PT, NT and PB) as evolving simultaneously, this may not have been the case in nature. Indeed, -Campos et al (2016) suggested that selective egg pigmentation evolved after the selective oviposition site choice, implying that NT disappeared at some point in favor of PT and PB, only to eventually reappear and replace PB. In such a scenario, the cost of pigmentation may have been the key selective pressure in the evolution of color polymorphism.…”

“…Although the hypotheses put forward by Torres-Campos et al (2016) to explain the evolution of selective egg coloration in P. maculiventris are valid, they cannot fully explain the maintenance of the dual oviposition strategies: pigmented eggs on top (PT) and non-pigmented eggs on the bottom (NB). Indeed, the data from one of the experiments carried out on soybean plants by Abram et al (2015b) show that both strategies are employed by females at relatively equal frequencies (i.e.…”

“…(2013), adapted to the Podisus system and parametized with experimental data (Abram et al, 2015b;Torres-Campos et al, 2016). We considered leaf sides to be instrumental in distinguishing prey types targeted by predators.…”