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You are what you eat!

Indiana University biologists have mapped genetic pathways in dung beetles to find how maternal nutrition affects developing larva.

Biologists at Indiana University (IU) have been observing how gene pathways control different physical traits in horned beetles — genus Onthophagus. They found that variation in physical traits within the same species can depend solely on nutritional changes during fetal development.

In many animals, nutrition — not genetic differences — controls the appearance of certain physical traits. Ants and bees, for example, grow into workers or queens based upon the food they are fed as larvae.

But the exact genetic mechanisms connecting developmental fate to nutritional conditions were poorly understood. Now, IU biologists Armin Moczek and Teiya Kijimoto, his former postdoctoral research associate and lead author on the paper, have pinpointed genetic pathways controlling some decisions.

Their work is published in the May 4th issue of the Proceedings of the National Academy of Sciences.

"For the first time, we've found a set of mechanisms that actively inhibit or promote the production of specific traits in the same species during development based upon precise nutritional conditions."

Armin Moczek PhD, Professor, Department of Biology, Indiana University, Bloomington, Indiana, USA

The genes reported on in the study are part of the hedgehog signaling pathway, best known to biologists for playing a role in specifying front and back location for body structures — such as a leg or wing. In horned beetles, Kijimoto and Moczek identified that this pathway inhibits the growth of structures when an insect experiences low nutrition during development.

Previously, Moczek found a separate signaling pathway, the "sex determination pathway," possessed a complimentary function, promoting growth only under high nutritional conditions.

"If you put these two pathways together, the result is ... a nutrition-dependent developmental threshold, a phenomenon that biologists have been trying to explain for a very long time."

Armin Moczek PhD

Specific genes in the hedgehog signaling pathway are called "hedgehog," "patched" and "smoothened." Together, they form a "relay" system transmitting information from outside the nucleus, such as levels of nutrition, to influence which genes get turned on or off (expressed) inside the nucleus.

Biologists are interested in "developmental thresholds" as they allow members of the same species to adapt in response to changing levels of nutrition. In tunneling dung beetles (Onthophagus taurus), high nutrition initiates males to develop horns and become aggressive fighters, jousting for access to females. However, low nutrition stops male beetles from developing horns forcing them to mate by stealth — sneaking between a rival and his willing mate, to copulate and run away before attack. Tunneling dung beetle males only turn into horned fighters if larva receive enough nutrition to reach over 5 millimeters in size as adults.

Thresholds also evolve and shift. Over the last 50 years, horn size in Onthophagus taurus males in the United States has lowered for lack of competition from other males. But in Western Australia, male on male competition is so intense — only the largest males succeed as fighters and thus mate more frequently.

Other than nutrition, many organisms react to external cues to reach similar developmental thresholds. Temperature seasonally cues butterflies to appear different in the spring and fall; cues the winged and wingless stages of aphids; and the winter and summer fur coats of arctic foxes. Underlying thresholds allow organisms to generate alternative versions of themselves, despite sharing a single genome between them.

Looking forward, Moczek plans to investigate:
(1) how hedgehog and sex-determination cellular pathways detect nutrition
(2) how nutrition thresholds affect sex, producing differences in body plan
(3) how pathways affect each other, such as the insulin-signaling pathway.

"Now that we understand how these pathways communicate with the outside world, we want to start listening in on the [internal] conversation."

Armin Moczek PhD

Complex, nongradual responses to environmental conditions are commonplace in nature and perhaps most extreme in polyphenic insects where continuous variation in nutrition experienced in early development gives rise to discrete alternative castes or morphs. This research shows that the hedgehog (Hh) pathway has acquired a novel and highly unusual role in the nutrition-dependent regulation of polyphenic development of a beetle. Experimental repression of Hh signaling returns a highly discontinuous response to nutrition to its presumed ancestral, gradual state. Our results suggest that recruitment of the Hh signaling pathway may have been a key step in the evolution of trait thresholds and the corresponding origin of alternative phenotypes and complex allometries.

The recruitment of modular developmental genetic components into new developmental contexts has been proposed as a central mechanism enabling the origin of novel traits and trait functions without necessitating the origin of novel pathways. Here, we investigate the function of the hedgehog (Hh) signaling pathway, a highly conserved pathway best understood for its role in patterning anterior/posterior (A/P) polarity of diverse traits, in the developmental evolution of beetle horns, an evolutionary novelty, and horn polyphenisms, a highly derived form of environment-responsive trait induction. We show that interactions among pathway members are conserved during development of Onthophagus horned beetles and have retained the ability to regulate A/P polarity in traditional appendages, such as legs. At the same time, the Hh signaling pathway has acquired a novel and highly unusual role in the nutrition-dependent regulation of horn polyphenisms by actively suppressing horn formation in low-nutrition males. Down-regulation of Hh signaling lifts this inhibition and returns a highly derived sigmoid horn body size allometry to its presumed ancestral, linear state. Our results suggest that recruitment of the Hh signaling pathway may have been a key step in the evolution of trait thresholds, such as those involved in horn polyphenisms and the corresponding origin of alternative phenotypes and complex allometries.

This research was funded in part by the National Science Foundation. Kijimoto is currently on faculty at West Virginia University.
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May 13, 2016   Fetal Timeline   Maternal Timeline   News   News Archive   

Two horned beetles — genus Onthophagus. Despite having the same genome, these beetles
develop horns (RIGHT) or no horns (LEFT) based on what they ate when they were larvae.
Image Credit: Alex Wild





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