Department of Biology

Indiana University biologist Armin Moczek is a co-author of a new study published in Nature Ecology & Evolution. Moczek, professor and chair of the Department of Biology in the IU College of Arts and Sciences, contributed to the paper, “Rewiring of two conserved signaling hubs into one axis underlies convergent female-specific wing regression in insects.”

Differences between males and females of the same species, or sexual dimorphism, are ubiquitous in nature. How they evolve and diversify over evolutionary time scales, and how they develop as organism differentiate from egg to adult, are the research foci of diverse biological disciplines. Because males and females within a species share almost all the same genes, sexual dimorphism arises because the different sexes use the same genes in different ways and combinations.  An additional complication is that not all traits that make up an organism are equally sexually dimorphic: instead organisms need to be viewed as mosaics of traits that differ in the degree to which they diverge among the sexes.  

In this study, several research teams combined to examine the regulation and evolution of sexual dimorphism in wing development, a widespread feature in many groups of insects. Typically, males form fully developed and functional wings, allowing them to disperse and find mates, while females halt wing formation prematurely, produce rudimentary wings, adopt a cryptic lifestyle and invest energy instead into reproduction.

Surveying this type of dimorphism, named "female specific wing regression" or FSWR across the insects, the team first documented that it appeared to have evolved numerous times within many different groups of insects, including the Orthoptera (grasshoppers, katydids, crickets, etc.), Blattodea (roaches and termites), Mantodea (mantis) as well as others. Focusing on roaches and crickets, the team then made two additional, major discoveries:

First, they zeroed in on two well-known genes, both encoding transcription factors. In regular insects - and independent of each other - these two factors regulate male and female specific development on one side, and the transition from immature to adult stages on the other. Fully formed wings are present only in adult insects. The team was able to show that in FSWR species only, both of these regulators interact in ways that ultimately promote wings in males but inhibit them in females. Specifically, one of these regulators named doublesex produces two so-called isoforms, resulting in a male-specific and a female-specific protein. In males of FSWR species, the male-specific protein binds near the coding region of the other regulator, named E93, and quickly activates its expression, promoting proper wing development in the process. In females, the female-specific doublesex protein inhibits E93 expression, yielding rudimentary wings instead. Such doublesex-isoform specific activation and repression had been shown previously, however what came next really surprised the team.

When surveying the corresponding DNA binding sites that enabled the interactions between doublesex and E93 in FSWR species, they found that these binding sites seemed to exist in every species surveyed, FSWR or regular. What made the difference was whether these binding sites were accessible, that is whether at this specific stage in development and location - i.e. in wing primordia - this particular DNA region was condensed and wrapped around proteins called histones and thus inaccessible to binding by transcription factors (most DNA most of the time is in this stage), or open, unwound, and thus accessible to binding. Such dynamic changes in DNA accessibility are commonplace, but their role in the evolution of complex developmental phenomena like FSWR is poorly understood.

This paper is important for two major reasons. First, the study helps us understand how a complex developmental phenomenon – like FSWR – can evolve in the first place, and then repeatedly over and over again. The origin of FSWR was made possible because even though regulators such as doublesex and E93 are evolutionarily ancient and deeply conserved across different groups of organisms, by combining them into one module roaches, crickets, and likely many other insects were able to evolve a novel form of sexual dimorphism. Doing so many times over and over was then made possible not by the repeated evolution of novel binding sites, but by simple changes in whether the same already existing binding sites are made accessible to binding or not.

Second, the study highlights a way in which the regulation of development may evolve that is both powerful and also very fast. Evolving new genes is expected to take a long time. Evolving new binding sites is expected to be faster, but still requires DNA sequence evolution. Evolving a change in whether an already existing binding site is accessible at a given time and location in development is likely much easier and faster, yet it is a mode of regulatory change relatively few studies have so far examined in the context of the evolution of development.

Moczek said, “This study exemplifies the power and impact of scientific collaborations, including international collaborations, and the new discoveries that are possible when scientists with partly overlapping expertise work together, and are able to make connections and gather insights individual members would miss.” He adds: “They are also a gift that keeps on giving. I learned a lot in the process, and the study introduced me to experimental approaches I was not yet familiar with, which I am now considering including in my research here at IU.”