September’s issue image depicts the work of Monteiro et al, which presents a molecular mechanism for the control of phenotypic plasticity in butterfly wing patterns.
Shivam Bhardwaj is a PhD candidate working on a thesis on mechanisms of eyespot plasticity. Antónia Monteiro is Associate Professor at the National University of Singapore and Yale-NUS-College, where her research investigates the evolution and development of butterfly wing patterns. More information about the authors of this blog, and their research, can be found here.
Competing interests: Shivam Bhardwaj and Antónia Monteiro are authors of the article discussed in this post.
Adaptations and Phenotypic Plasticity
In nature, animals have devised different strategies to survive in different environments. These include the ability to develop large decoy patterns on their bodies, allowing them to deflect attacks from predators, or alternatively develop camouflage patterns, which make them inconspicuous to predators. Some animals, however, instead of adopting the same strategy all year round, have evolved the ability to adjust strategies to maximize their survival in changing environments. This type of adaptation is called phenotypic plasticity and often evolves in species that experience recurrent and predictable changes in their environments. Some prominent examples from nature include variations in horn sizes in male dung beetles, coloration in grasshoppers, and color patterns in butterflies.
This month’s PLOS Genetics Issue Image shows a mating pair of Bicyclus anynana butterflies. These tropical African butterflies experience two major seasons (Dry and Wet) in their natural habitats. They encounter different predators in each season and hence they have evolved to develop two very different-looking phenotypic forms, each highly adapted to the specific season. The Wet Season (WS) form has big and bright concentric circular patterns on the wings (bottom butterfly in above image); the ‘eyespots’ help deflect invertebrate predator attacks to wing margins, allowing the butterfly to escape unharmed. The Dry Season (DS) form has dull wing color and cryptic eyespots (top butterfly in above image), improving its camouflage against the dry leaf litter, and hiding it from the sight of the more common vertebrate predators of this season.
Our work shows that not all eyespots undergo the same change in strategy. The eyespots found on the hindwings, which are primarily visible to predators, are more likely to undergo change than their forewing counterparts. Large forewing eyespots are often hidden in the natural resting position of the butterfly and are displayed only conditionally – as a last resort to deflect predation or perhaps to attract mates at close distance. These forewing eyespots remain large and bright across both seasonal forms.
Both WS and DS butterflies share the same genotype yet have different phenotypic appearances. Each form can be induced under laboratory conditions by changes in developmental rearing temperature, which acts as a cue to indicate which season the adults will be born in. Our research, published in PLOS Genetics, identifies the molecular mechanisms that allow these butterflies to regulate the size and brightness of their hindwing eyespots, in response to developmental rearing temperature while keeping other eyespots unaltered and insensitive to rearing temperature.
20E and its receptor control plasticity
We have shown that temperature experienced during the larval wandering stage of development alters the amounts of the hormone 20-hydroxyecdysone (20E), present in the blood of the different seasonal forms. Higher amounts of 20E are produced in WS forms, whereas lower amounts are produced in DS forms. In addition, cells responsible for differentiating the eyespot patterns on the wing express the receptor that permits sensitivity to this hormone. Interestingly, cells at the center of the forewing eyespots – those that don’t change as much in size or brightness across seasonal forms – did not express the hormone receptor at this critical period in development. These cells momentarily turned this gene off, making the eyespots insensitive to the fluctuating hormone. Functional analyses using experimentally manipulated hormone amounts, or hormone receptor inhibitors, showed a reversal of phenotype in the temperature-sensitive hindwing eyespots, but not in the insensitive eyespots. For instance, injections of additional 20E into DS form larvae produced WS form adult wing patterns. Conversely, injecting a hormone receptor inhibitor in WS form larvae produced DS form adults.
Implications of findings
We’ve presented a novel mechanistic explanation for the evolution of different levels of phenotypic plasticity for traits that use the same genetic network – wing eyespots. Though it was previously believed that hormones mediated this flexible response, we show that the control of these responses lies both in the levels of hormones as well as in the availability of hormone receptors in specific groups of cells at critical moments of trait development. Further work is required to establish how temperature leads to variation in levels of 20E in the blood of these insects, and how active or inactive 20E signaling in the eyespot centers regulates eyespot size and brightness. Future studies using comparisons across different species should identify when the physiological and molecular components of this plastic response originated on the phylogenetic tree of butterflies. This will help us determine whether a complex trait such as eyespot phenotypic plasticity is ancestral and common across all butterflies with eyespots, or is derived and present in only one or a few butterfly lineages.
Monteiro A, Tong X, Bear A, Liew SF, Bhardwaj S, Wasik BR, et al. (2015) Differential Expression of Ecdysone Receptor Leads to Variation in Phenotypic Plasticity across Serial Homologs. PLoS Genet 11(9): e1005529. doi:10.1371/journal.pgen.1005529