Department of Biology

As animals grow and differentiate from egg to adult, the development of their parts is often influenced profoundly by a wide range of internal and external factors. With the help of a new award from the National Science Foundation, Armin Moczek, Class of 1955 Professor in the College of Arts and Sciences' Department of Biology at Indiana University Bloomington, and members of his research team will explore the mechanisms underlying such condition-dependent development and its evolution, using horned beetles as study organisms.

"When you look at differences between organisms within a species of animal and ask why individuals may differ from each other, among the two most important sources of variation are sex and nutrition," says Moczek. "The same trait may look quite different if it develops in a male rather than in a female—or whether a given individual experienced good or bad nutrition during its growth. At the same time, not all traits within the same individual are equally affected by sex or nutrition: instead organisms are really mosaics of parts that differ in how much they are shaped by nutrition or sex."

"And, as if this isn't complicated enough," Moczek adds, "Sex and nutrition interact to influence traits. For instance, secondary sexual traits such as horns and antlers are most elaborated in those males that also experienced the highest nutrition during their growth stages."

Because almost all cells within an individual organism possess the same genome, such context-responsive development must arise through the differential activation and suppression of different sets of genes, a process called gene regulation. Many key regulators of sex- and nutrition-responsive development are already known. Yet, how their differential activation itself is initiated and how subsequent development interprets these differences and adjusts itself accordingly remain poorly understood. The National Science Foundation's Evolution of Developmental Mechanisms Program has granted Moczek and his colleagues $950,000 for three years to explore the mystery.

Together with Phil Davidson, a postdoctoral researcher, and Erica Nadolski, a fourth-year graduate student in IU's Genome, Cell, and Developmental Biology Ph.D. program, Moczek will use horned beetles as a focal study system. Horned beetles possess highly diverse forms of context-responsive development that are amenable to comparative and experimental study.

Building on extensive preliminary data and approaches developed by Davidson and Nadolski, the researchers will characterize the regulatory networks that shape the development of diverse traits in both males and females experiencing a range of nutritional conditions. Traits include horns (which in many species are very sensitive to both nutrition and sex such that only well-nourished males produce them), genitalia (which develop very differently in both sexes but show little responsiveness to nutrition), and wings (which are affected by nutrition, but equally so in both males and females).

In all this, the team will pay particular attention to the dynamic nature of chromatin remodeling; that is, the often rapid unfolding and re-folding of DNA around histone proteins, which determines whether certain DNA regions can be accessed or not by a given cell's transcriptional machinery. Chromatin remodeling has emerged as important mechanisms of gene regulation broadly, but its role in condition-responsive development as studied by Davidson, Nadolski, and Moczek is virtually unknown.

A second major goal of the study is to investigate not just the mechanisms underlying context-responsive development, but also their evolution. Sex- and nutrition-dependent development are not only ubiquitous in animals, they also diversify extraordinarily rapidly.

"When you look across species of birds at sex-specific plumage coloration, the relative size and shape of horns in horned beetles, and examples in countless other organisms—you find that how sexes differ from each other itself differs dramatically from one species to the next; that is, sex-differences evolve really, really fast," says Moczek.

To explore the means by which the underlying regulatory mechanisms diversify, the team will investigate three species of horned beetles which—despite being closely related to each other—show marked differences in how the same traits are affected by nutrition and sex. For instance, in one species horns form in males only where they are moderately affected by nutrition. The effects of both sex and nutrition are far amplified in the second species, yielding extreme variation both between males and females as well as between small and large males. Yet in the third species, males have mostly lost the ability to make horns, which now instead grow prominently in females.

Through the lens of horned-beetle biology, Moczek and his team hope this work will transform our understanding of the developmental mechanisms that integrate genotype and environment in the genesis of organismal form and function during development as well as how changes in this integration shape organismal diversity both within and among species.