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  • What can horned beetles tell us about the mechanisms of plasticity and their evolution?

What can horned beetles tell us about the mechanisms of plasticity and their evolution?

By: Sofía Casasa

Monday, May 18, 2020

Beetle: Digitonthophagus-gazella.
Digitonthophagus gazella large, horned male. Photo by Sofía Casasa

Editor's note: Sofía Casasa, a postdoctoral fellow in the laboratory of Assistant Professor Erik Ragsdale in the Indiana University College of Arts and Sciences Department of Biology, writes about the research she performed as a graduate student in Professor Armin Moczek's laboratory in the department. Collaborating on the project was Eduardo Zattara, who had been a postdoctoral researcher in the Moczek lab and is now an adjunct researcher at INIBIOMA-CONICET in Argentina as well as a research associate at Indiana University and at Smithsonian Institution. Their landmark research focuses on plasticity—the adaptability of an organism to changes in its environment or differences between its various habitats—and was published in Nature Ecology & Evolution.

How do organisms interact with their environments? Research on phenotypic plasticity focuses on how organisms with the same genotype can adjust their phenotypes in response to different environmental conditions. Plasticity can take many forms and can occur at any stage during development, but those changes that occur early in development are commonly irreversible and it is those changes that fall under the rubric of developmental plasticity.

An extreme case of developmental plasticity are polyphenisms, where instead of showing a gradual response to a particular environmental factor, individuals develop into distinctly different, alternative phenotypes. One of the most well-known examples of polyphenism are castes in social insects (bees, ants, etc.), in which nutritional conditions determine whether females with the same genotype develop into workers or queens, with no intermediates.

Yet, what are the mechanisms that specify development of one or the other phenotype? And, how does plasticity itself evolve? Are the genetic mechanisms underlying plasticity responsible for the different degrees of plasticity seen across species?

I have been tackling these questions for the past several years. Our recently published article in Nature Ecology & Evolution was the last chapter of my Ph.D. dissertation, and tried to answer some of these questions from a comparative transcriptomic approach. My advisor, Armin Moczek, and I decided to collaborate with Eduardo Zattara, a former postdoctoral researcher in the lab who has ample experience in analyzing transcriptomes. Despite having returned to Argentina, Eduardo was the perfect mentor to remotely guide me through all the bioinformatic tools needed for this project.

Sofia Casasa.
Sofía Casasa [hi-res]. Courtesy photo
Eduardo Zattara.
Eduardo Zattara [hi-res]. Photo by Indiana University

To address our questions, we focused on horned dung beetles from the tribe Onthophagini. In these beetles, the quality and quantity of nutrition received during larval development dictates whether males develop as large individuals with large horns or as small individuals with no horns. Large horns are used in male-male combat to gain access to females, while hornless males rely on more sneaky tactics to circumvent large males and intercept females. Importantly, like the castes of social insects horned and hornless males, too, constitute a polyphenism with very few intermediates seen in nature.

The wide diversity of horns and plastic responses found among Onthophagini allowed us to explore the mechanisms and evolution of plasticity. We focused on three species of horned beetles that show vast differences in the degree of plasticity: Onthophagus taurus, which exhibits an extreme, explosive response to nutrition; closely related Onthophagus sagittarius, which has secondarily lost horns; and distantly related Digitonthophagus gazella, which displays a modest plastic response, similar to what it is thought to be the ancestral condition for the tribe.

Small, low-nutrition males (left) and large, high-nutrition males (right) of the three species of beetle used in this study and their phylogenetic relationship.
Small, low-nutrition males (left) and large, high-nutrition males (right) of the three species of beetle used in this study and their phylogenetic relationship [figure hi-res | beetle photo hi-res]. Image courtesy of Sofía Casasa and Nature Ecology & Evolution

To collect tissues for transcriptomic analyses the first step is to get adult beetles from the field to start beetle colonies. Beetles are collected in organic cattle farms by our collaborators in North Carolina (O. taurus) and Hawaii (O. sagittarius and D. gazella), and then shipped to Bloomington, Indiana, where we keep them in separate colonies of approximately 300 beetles. Females build dung balls and lay a single egg in each ball. We collect the balls and open them to move the recently hatched larvae to be artificially reared in 12-well plates. This setup allowed us to manipulate nutrition levels by supplying dung of varying quality and pick either large, horned or small, hornless individuals of each species that were later used to dissect horn tissue and perform RNA extractions and sequencing.

We were particularly interested in understanding the relationship between gene expression changes across nutrition conditions and what we saw at the morphological level (horned vs. hornless). Are differences in gene expression between small and large individuals greater in the species showing the more dramatic morphological response? How about the species that has lost the plastic response? Using RNAseq to estimate genome-wide expression in horn tissues, we found that gene expression differences mirrored what we saw at the morphological level; more exaggerated polyphenisms correspond with an increased number of nutrition-responsive genes. While this may seem intuitive, there was no previous evidence or expectation that this would be the case (e.g., we could have seen the same number of genes but more growth promoters vs. inhibitors in extreme responses).

Finally, we explored several additional questions that remain heavily debated in the field. For example, genetic accommodation is a process proposed to explain how variation in plastic responses among individuals can fuel evolutionary diversification of plasticity among species. Our data is consistent with such a scenario: ancestral plasticity in gene expression may have contributed to the evolution of growth exaggeration as well as loss in the Onthophagini tribe. Similarly, whether the evolution of novel degrees of plasticity is made possible by new genes (so called taxon-restricted genes) or facilitated by already existing, conserved, and repurposed genes was unknown. We found evidence that a combination of both contributed to the exaggeration and loss of plasticity. As such our work advances our understanding of the evolution of developmental plasticity, a fundamental feature of most forms of life on our planet.

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