Think of a trait, any trait. A bird beak, a butterfly wing, a fish fin. Highly coordinated gene expression networks ultimately produce all traits. Hence, any variation you see in these traits must be due to shifts in gene expression, whether that shift is determined genetically or by some external cue.
Evolutionary developmental biologists want to understand how adaptive traits vary within and between species, which means that they need to show how a combination of genetic and environmental factors influence a trait’s development. The field has moved far beyond the tired old question about whether nature or nurture is responsible for a phenotype. Decades of evidence show us that most traits are shaped by both. The interesting question now is whether we can untangle genetic and environmental sources of trait variation to better understand processes driving species diversification. This is exactly what Yinan Hu and Craig Albertson set out to accomplish in their paper “Baby fish working out: an epigenetic source of adaptive variation in the cichlid jaw.”
The authors studied Lake Malawi Cichlids, known for their exceptional diversity in jaw shapes that are adapted to various diets and ecological niches. Two of these species are at opposite extremes of a jaw shape spectrum. Labeotropheus fuelleborni has short jaws evolved to scrape algae off hard surfaces, while Maylandia zebra has relatively longer jaws built for suction feeding to catch prey in the water column. While suction feeding is a common feeding strategy for cichlids in Lake Malawi, the scraper jaws are an evolutionary novelty. These two species also differ in the size of their retroarticular process (RA), a lower jaw bone. The RA of the scraper species is relatively enlarged, allowing for a stronger bite force, and is smaller in the suction feeder to enable faster jaw opening.
Lake Malawi Cichlids studied in Hu and Albertson 2017 (Images modified from Wikimedia Commons). These species look similar except for drastic differences in jaw morphology.
Hu and Albertson noticed that both species repeatedly open and close their mouths as larvae right around the time that the lower jaw begins to form. They called this gaping behavior. While both species look very similar at this young age, they differed in how often they gaped. It seemed like the scraper species was working out harder than the suction feeder species. In other words, the species with the larger RA opened its mouth more frequently.
To understand how gaping behavior might affect bone size, it’s important to know that all vertebrates have special bone forming cells that act as mechanosensors. When they sense force, let’s say from jaws opening and closing over and over, these mechanosensors can activate genes that increase bone deposition. The authors predicted that some of the variation in the size of the RA bone between species was due to how often they opened and closed their mouths during this critical stage of development.
To test this prediction, Hu and Albertson did two experiments. First, they performed tiny surgeries. They cut a ligament attached to the RA that normally pulls at the tip of the RA when a fish opens its mouth. This snipping reduced mechanical stress on the RA during the gaping behavior stage of development. In a second set of experiments, they let baby fishes develop in a limited amount of water. They had previously shown that limiting water in this way led to higher gaping frequencies in both fish species.
Both of these experiments had a significant effect on RA length. Fishes that underwent surgery had tiny RAs, and fishes forced to have higher gaping frequencies had larger RAs. When the suction feeder species were forced to gape more frequently, they developed RAs that were 14% longer than controls. Incredibly, this simple experiment to increase gaping frequency made suction feeders look more like scraper species!
Diagrams show lower dentary and retroarticular bones (near black lines) that are characteristic of a) Labeotropheus fuelleborni and b) Maylandia zebra (Image modified from Hu and Albertson 2017).
Previous studies showed that the scraper species have larger RAs in part thanks to the gene ptch1. Scraper species and suction feeder species have alternate alleles near this gene that are associated with higher expression of ptch1 around the RA in scrapers and lower expression in suction feeders. Interestingly, these expression differences account for a similar amount of RA variation as gaping frequency (about 11%). Hu and Albertson measured ptch1 expression in the suction feeder group that was forced to have a higher gaping frequency and saw that the gene expression was almost twice as high as in controls.
When you put all of this together, you get a fascinating story. Two different sources of variation – divergent ptch1 alleles and gaping behavior – are affecting the expression of the same gene, ultimately affecting the same trait! This work shows that the evolution of a novel trait, like algae scraping jaws, can result from genetic and environmental factors acting together to regulate the same gene networks.
Contributed by Joe McGirr – PhD candidate in the @fishspeciation lab at the University of North Carolina Chapel Hill. @mcgirr_joe
Find Hu and Albertson’s paper here: Yinan Hu, R. Craig Albertson. 2017. Baby fish working out: an epigenetic source of adaptive variation in the cichlid jaw. Proc Biol Sci. 284(1860).