Origin of the mechanism of phenotypic plasticity in satyrid butterfly eyespots

Elife. 2020 Feb 11;9:e49544. doi: 10.7554/eLife.49544.

Abstract

Plasticity is often regarded as a derived adaptation to help organisms survive in variable but predictable environments, however, we currently lack a rigorous, mechanistic examination of how plasticity evolves in a large comparative framework. Here, we show that phenotypic plasticity in eyespot size in response to environmental temperature observed in Bicyclus anynana satyrid butterflies is a complex derived adaptation of this lineage. By reconstructing the evolution of known physiological and molecular components of eyespot size plasticity in a comparative framework, we showed that 20E titer plasticity in response to temperature is a pre-adaptation shared by all butterfly species examined, whereas expression of EcR in eyespot centers, and eyespot sensitivity to 20E, are both derived traits found only in a subset of species with eyespots.

Keywords: 20E; developmental biology; ecdysone; evolutionary biology; eyespot size; lepidoptera; phenotypic plasticity; seasonal polyphenism.

Plain Language Summary

A well-known family of butterflies have circular patterns on their wings that look like eyes. These eye-like markings help deflect predators away from the butterfly’s body so they attack the outer edges of their wings. However, in certain seasons, such as the dry season in Africa, the best way for this family to survive is by not drawing any attention to their bodies. Thus, butterflies born during this season shrink the size of their eyespots so they can hide among the dry leaves. How this family of butterflies are able to change the size of these eye-like spots has only been studied in the species Bicyclus anynana. During development low temperatures, which signify the beginning of the dry season, reduce the amount of a hormone called 20E circulating in the blood of this species. This changes the behavior of hormone-sensitive cells in the eyespots making them smaller in size. But it remains unclear how B. anynana evolved this remarkable tactic and whether its relatives have similar abilities. Now, Bhardwaj et al. show that B. anynana is the only one of its relatives that can amend the size of its eyespots in response to temperature changes. In the experiments, 13 different species of butterflies, mostly from the family that has eyespots, were developed under two different temperatures. Low temperatures caused 20E hormone levels to decrease in all 13 species. However, most of these species did not develop smaller eyespots in response to this temperature change. This includes species that are known to have larger and smaller eyespots depending on the season. Like B. anynana, four of the species studied have receptors for the 20E hormone at the center of their eyespots. However, changing 20E hormone levels in these species did not reduce eyespot size. These results show that although temperature changes alter hormone levels in a number of species, only B. anynana have taken advantage of this mechanism to regulate eyespot size. In addition, Bhardwaj et al. found that this unique mechanism evolved from several genetic changes over millions of years. Other species likely use other environmental cues to trigger seasonal changes in the size of their eyespots.

Publication types

  • Comparative Study
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adaptation, Physiological / genetics*
  • Animals
  • Biological Evolution*
  • Butterflies / genetics*
  • Butterflies / metabolism
  • Ecdysterone / metabolism
  • Female
  • Pigmentation / genetics
  • Receptors, Steroid / metabolism
  • Seasons
  • Temperature

Substances

  • Receptors, Steroid
  • ecdysone receptor
  • Ecdysterone