How does animal behavior evolve?
How have genes and neural circuits evolved to generate behavioral diversity?
This is an extraordinary time to study evolutionary biology. Many deep and old evolutionary questions are being solved by the application of new technologies. For example, new genomic methods provide unprecedented insight into the evolution of genomes. But these discoveries are often disconnected from the consequences of genomic changes. How, precisely, do changes in the genome cause the evolution of new behaviors?
The Stern lab develops new approaches and new tools to ask how molecular changes cause the evolution of behavior. We study both the genome and neurons to reveal how evolution really happens.
We want to know, for example, precisely how changes in the genome ramify through cell biology to generate behavioral evolution. We want to know how the nervous system evolves to generate conserved and divergent behaviors.
We focus on behaviors performed by fruit flies of the genus Drosophila. There are more than 1500 Drosophila species on Earth, each displaying a unique suite of behaviors that allows them to find food, avoid predators, and mate. Some of these behaviors, like courtship and olfaction, evolve quickly between species and can be studied conveniently in the laboratory. We have developed new quantitative methods to study these behaviors and new genomic and genetic technologies to probe the molecular causes of behavior evolution. Now, we are developing new tools in many Drosophila species to study directly how neural circuits have evolved to generate new behaviors.
Over the past two decades, we have focused on studying interesting evolving phenotypes that we can quantify with reasonable throughput. This means that we usually study relatively simple evolutionary transitions. Studying evolution can be very challenging, and there are enormous experimental advantages to studying relatively simple phenotypic changes.
Evolution of Behavior
We aim to identify the genetic and neural basis for the evolution of behavior, because we believe that there may be general principles to behavior evolution, similar to the principles that have been revealed for morphological evolution (Stern & Orgogozo, 2009; Stern 2010).
Current projects include the evolution of courtship song and of olfactory preferences. We have developed several tools to aid these studies, including high-throughput genotyping (Andolfatto et al. 2011) and phenotyping platforms (Arthur et al. 2013) and new transgenic reagents for all of the species we study.
We are also studying how neural circuits have evolved to generate behavioral diversity. This work includes both identifying the neural substrate for behaviors in Drosophila melanogaster (Shirangi et al. 2013) and developing tools to study the evolution of these same neurons in other species. Ultimately, we hope to identify changes in neural circuits that caused the evolution of novel behaviors.
Evolution of Morphology
For many years, the lab has studied the genetic causes for the evolution of a morphological difference between species, a change in the pattern of cuticular trichomes on larvae (Sucena & Stern 2000). In a series of papers, we have demonstrated that this seemingly trivial morphological difference resulted from the accumulation of a very large number of mutations of small effect all at a single gene, called shavenbaby (Sucena & Stern 2000, McGregor et al. 2007, Frankel et al. 2011).
These results help to explain a confusing discrepancy between many observations in evolutionary genetics -- which indicate that evolution often occurs by the accumulation of mutations of small effect -- and the results from evolutionary developmental biology -- which suggest that morphological evolution often occurs by changes at key regulatory genes. In fact, both may be true. Long-term evolutionary changes may have resulted from the accumulation of small-effect mutations at a few, special loci. We call these hot-spot genes and we suspect that the structure of developmental networks helps to explain why mutations at these hot-spot genes are preferred over mutations elsewhere in the network (Stern & Orgogozo 2008, 2009).
If some genes really are hot spots for evolutionary change, then we would expect to see these genes involved in similar evolutionary changes in other lineages. We therefore examined species of the D. virilis clade of flies, which also display a diversity of larval trichome patterns. In this group, we found that the pattern of svb expression is precisely correlated with larval trichome patterns, suggesting that svb is indeed involved in the evolution of trichome patterns in this group of species as well (Sucena et al., 2003). Recently, we have demonstrated that not only has svb evolved in the D. virilis clade, but precisely the same cis-regulatory enhancers have evolved both in the D. virilis clade and in the D. melanogaster group to generate identical morphological evolution (Frankel et al. 2011). This is a remarkable case of genetic parallelism underlying morphological convergence.
We have recently identified the specific transcription factors that bind to the evolving binding sites in these enhancers, revealing how the loss and gain of transcription factor binding sites caused functional evolution of an enhancers.
"I came to Janelia to do science with my own hands. I am an inveterate lab rat and I really appreciate the fact that I can spend all day, every day, doing experiments that enhance the lab's research. I feel incredibly lucky to be a post-doc in my own lab!"
David L. Stern, December 2014
"Throughout their careers [Thomas Hunt] Morgan and [his] students worked at the bench. The investigator must be on top of the research if he or she is to recognize unexpected findings when they occur."
Male Drosophila produce courtship songs by vibrating their wings. (Image credit: David L. Stern)
Males of some species perform a slow wing "rowing" to court females. (Image credit: Jessica Cande)
Specific thoracic neurons (labeled in green) are required for courtship song. (Image credit: Troy Shirangi)
Specific neurons in the larval brain of Drosophila are involved in perceiving aggregation pheromones. (Image credit: Joshua Mast)
Different enhancer of the shavenbaby gene drive expression in largely complementary domains of expression in the Drosophila embryo. Some of these enhancers have evolved to generate novel anatomy in closely related species. (Image credit: Ella Preger-Noon)
A male Drosophila melanogaster courts a female by "singing" to her. He extends and vibrates one wing to produce the machine-gun-like "pulse" song and the humming "sine" song.