Non-coding DNA drives the evolution of avian beak morphology

“Living things do not inherit skulls, backbones, or cell layers from their ancestors—they inherit the processes to build them.”

– Neil Shubin (Some Assembly Required)

A few days ago, I finished the book “Some Assembly Required” by Neil Shubin. It is a great read about the big changes during evolution. Combining insights from paleontology, genomics and development biology, Shubin explains how major evolutionary transitions took place. One key idea that I took away from this book is illustrated by the quote above: if we want to reconstruct the evolution of complex traits, we need to understand how they are build. In other words, we have to unravel the genetic and developmental underpinnings of these traits.

One of the most important traits in avian evolution is the shape of the bill. Variations in bill morphology – from the sharp beaks of predators to the long bills of avocets – have allowed birds to exploit a myriad of ecological niches and diversify into the many species we see today. Surprisingly, little is known about the genetic and developmental processes underlying this variation. A recent study in the journal Genome Research took a macroevolutionary perspective on the avian beak.

The diversity of bird beaks – Adapted from L. Shyamal | Wikimedia Commons

 

Candidate Genes

To be honest, we do know quite a bit about the genetics of beak morphology. Studies on particular species have uncovered several candidate genes. For example, the beak shapes of Darwin’s finches are determined by, among others, the genes BMP4 (depth and width) and CALM1 (beak length). Recent genomic work suggested additional roles for ALX1 (craniofacial development) and HGMA2 (beak size). Interestingly, in great tits (Parus major) another gene – COL4A5 – was linked to variation in beak morphology. These examples indicate that beak shape is probably influenced by many genes and that different genes are under selection in different bird groups.

Leeban Yusuf and his colleagues compared the genomes of 72 bird species to see whether there is a common genetic mechanism underlying the evolution of beak morphology. They divided the species into separate bins based on the rates of beak shape evolution. Next, they estimated the rate at which different protein-coding genes evolved (using the dN/dS approach). If certain protein-coding genes are involved in the evolution of beak morphology, you expect a positive correlation between the bird-bins and the rate of molecular evolution. This analysis uncovered 1434 candidate genes of which several are part of developmental pathways that are involved in beak morphology (namely the Wnt signalling pathway and the ESC pluripotency pathways). There was, however, no positive correlation between the rates of beak shape change and molecular evolution. This result shows that the evolution of beak morphology is more complicated than a few mutations in protein-coding genes.

An example of how rates of beak morphology change are divided into different bins (six in this case) from slowest to fastest. From: Yusuf et al. (2020) Genome Research.

 

Non-coding DNA

Next, the researchers turned to non-coding genomic regions, which make up the majority of the genome. Neil Shubin formulated it nicely in his book: “Gene sequences that code for proteins compose less than 2 percent of the human genome. That leaves some 98 percent with no genes at all in it. Genes are but islands in a sea of DNA.” These non-coding regions were initially seen as “junk DNA” without a function, but we now know that some of these regions play crucial roles in regulating gene expression. The search for significant non-coding regions involved in beak morphology evolution resulted in no less than 39,806 of these genetic elements. But which genes were they regulating?

These regulatory regions come in two main types: cis-regulatory elements that are linked to nearby genes and trans-regulatory elements that affect distant genes (millions of DNA-letters apart). Analyses focused on cis-regulatory elements pointed to 884 genes of which most are involved in early craniofacial development, as shown in mice (including the the ESC pluripotency pathways that were also found for the protein-coding genes). Similarly, detailed analyses of trans-regulatory elements identified genes associated with the development of beak morphology.

The difference between cis- and trans-regulatory elements. Cis-regulatory elements affect nearby genes, while trans-regulatory elements code for proteins (e.g., transcription factors) that influence distant genes. Adapted from: Signor & Nuzhdin (2018) Trends in Ecology & Evolution.

 

Endless Forms

These findings highlight that fundamental developmental pathways underlie the evolutionary changes in beak morphology. Mutations in the non-coding elements that regulate these pathways can result in novel beak phenotypes, providing the raw material for natural selection. In addition, changes in protein-coding genes – which seem to be specific to particular bird lineages – add more variation to this pool of possibilities. Together, coding and non-coding genomic regions drive the spectacular diversification of avian beaks. To end with a famous quote from Charles Darwin, who would have been delighted by these findings: “From so simple a beginning endless forms most beautiful and most wonderful have been, and are being, evolved.”

 

References

Yusuf, L., Heatley, M. C., Palmer, J. P., Barton, H. J., Cooney, C. R., & Gossmann, T. I. (2020). Noncoding regions underpin avian bill shape diversification at macroevolutionary scales. Genome research, 30(4), 553-565.