Charles Darwin’s view of evolution by natural selection envisioned one species changing gradually into another by means of many, small genetic mutations over a very long time. As Darwin wrote in his seminal work, On the Origin of Species by Natural Selection, “We see nothing of these slow changes in progress, until the hand of time has marked the long lapse of ages.”
Not all evolutionary biologists agree with this view of genetic change, however. Although it may explain the way in which species adapt to changing conditions over time, there are many instances where sudden, large morphological alterations occur within relatively short geologic timespans. Such changes are thought to be due to instances of significant genetic mutation, rather than to micro-mutations that accumulate over time. In this case, biologists would view evolution as involving sudden punctuations, or steps, during which genetic changes give rise to radical new morphologies.
Professor Scott Hodges in the UC Santa Barbara Department of Ecology, Evolution, and Marine Biology, along with doctoral student Zachary Cabin and their colleagues, have just identified an example of a sudden evolutionary change. They have found a population of mutant Colorado blue columbine plants (Aquilegia coerulea) that produce flowers with no petals. Columbine flowers usually have small, white petals, each with an elongated spur that contains nectar and attracts pollinating insects. The mutants have lost their petals and nectar-filled spurs entirely, and these have been replaced by an extra set of sepals.
It seems that this type of mutation in A. coerulea has been seen before; in 1897, a mutant where the petals were replaced by sepals was described in the Proceedings of the California Academy of Sciences. And a 100 years later, mutant plants were found to be abundant in an area about 24 km south of the original locality in central Colorado. This implies that the mutation involving petal loss was not a disadvantage to the plants – they have continued to survive and reproduce without being able to attract pollinators to their nectar-filled spurs.
The plants are usually pollinated bumblebees and hawkmoths, that would normally be attracted to the petals with spurs because of the nectar reward they contain. It is highly unusual to find that a mutation persists in a population when this makes the plant less attractive to its pollinating agents.
This is why Hodges and the team decided to investigate this population (in Reynolds Park Open Space) more closely. Over the span of three flowering seasons (between 2014 and 2016), they mapped the position of every flowering plant in one portion of Reynolds Park and recorded the morphology, number of flowers produced, signs of herbivory on the flowers, and whether the fruits matured. They also made extensive video recordings of the insect pollinators that visited flowers, and collected tissue samples for genetic analysis.
The researchers found that at least 25 percent of the plants in the area were of the mutant variety and had no petals or spurs. When they searched the DNA for the source of this unexpected change in morphology, they found the culprit to be a mutation in a single gene, APETALA3-3, which is known to affect spur development. This type of gene is a homeotic gene because it controls the development of an entire organ. It codes for a transcription factor that influences many other genes involved in building the whole organ.
“The gene is either on or off, so it’s about as simple of a change you can get,” said lead author Zachary Cabin. “But that simple difference causes a radical change in morphology.” The finding adds weight to the idea that adaptation can occur in large jumps, rather than by merely plodding along over extended timespans.
Geneticists who have managed to introduce experimental mutations in the homeotic genes of fruit flies, have produced flies with entire organs in the wrong place in the body. For example, antennae grow out of the abdomen of the fly, or legs grow where there should be wings. These extreme changes are likely to affect survival in most instances.
“Most of the mutations of this nature are going to be like that, just awful,” Hodges said. “The animal won’t have any chance of surviving.”
But every once in a very long while, a macromutation can be neutral, or even confer an advantage to an individual in a particular environment. This individual could, according to Richard Goldschmidt – a prominent US geneticist – be seen as a ‘hopeful monster’. Such an individual would be the product of a fortuitous radical genetic mutation that would enable it to adopt a new mode of life.
Hopeful monsters are not usually found in the fossil record because changes take place rapidly, but if biologists could spot a hopeful monster in the early stages of its evolution, it would show that evolution can indeed proceed in single, large jumps.
Could it be that this recent research study on columbines, published today in the journal Current Biology, has unearthed a hopeful monster?
“We did not have a good example of a hopeful monster due to a single genetic change,” said Hodges, “until now.” Researchers have to catch these abrupt changes as they’re happening, otherwise they disappear into an organism’s genome. The fact that it is actively happening in the Colorado blue columbine enabled the team to confirm this plant’s status as a hopeful monster.
“There’s definitely some luck involved with us being around at the right time to capture this,” Cabin said.
The team discovered five versions, or alleles, of APETALA3-3, only one of which codes for a petal with a functional nectar spur. The other four were ‘broken’, as Hodges put it. They also determined that spurlessness is a recessive trait. The flower will develop normally as long as the plant has one copy of the functional allele. But any two of the mutant alleles together will prevent this.
Since about a quarter of Colorado blue columbines in the study area displayed the recessive trait of spurlessness, it appeared that this mutation was advantageous to the plants in some way.
“To get that many of this mutant type really suggests that there’s selection favoring it somehow,” Hodges said, which proved perplexing as the spurs produce nectar that attracts the plant’s pollinators. “So, how the heck can you lose your spurs and still be favored?” he asked.
Analyzing the data that they had collected in the field, the researchers identified that flowers with spurs attracted more herbivores in the form of aphids and deer. These animals seemed to prefer eating the flowers with the nectar-filled spurs, and it was this pressure that was likely driving the selection for flowers with no spurs.
“The first time we really realized the pattern was at the airport on the way home,” Cabin recalled. He was reading off data as Hodges entered it into the computer. “Scott could see the pattern developing, because he had all the data in front of him, and was getting more and more excited.”
Shifts in floral morphology are usually driven by pollinators, but spurlessness seems to be driven by herbivory. “Natural selection can come from very surprising sources,” Hodges said. “It’s not always what you’d expect it to be.”
The researchers now want to track how spurlessness is spreading through the columbine population. They also suspect that, thanks to this genetic mutation, the Colorado blue columbine may be diverging into separate species. “That splitting process would be slow,” Cabin said, “but there is evidence that it could be on its way.”