School of Biology

Catching Evolution Red-Handed
(Nathan Bailey 9/3/2012)

Hermaphroditic worms. Human intelligence. Insect societies. Carnivorous plants. Evolutionary biologists are obsessed with understanding why there is such a bewildering diversity of species, forms and behaviours in the natural world.

One of the challenges we face is that evolution tends to proceed at a glacially slow pace. Changes in the genetic code that affect an organism's appearance or behaviour are not everyday events, and when they do happen they usually only cause subtle variations that are difficult to detect and might not persist across generations. So even though evolution continually putters along right under our noses, we are unlikely to witness in our lifetimes the types of dramatic transitions that generate new forms or species in the wild.

However, an unassuming field cricket from Hawaii recently defied all the odds.

Biologists at St. Andrews are studying the genetics of a wild population of the cricket Teleogryllus oceanicus that recently experienced an extraordinary evolutionary event. Male crickets chirp to attract females, but over the course of about 20-30 generations a mutant variety of silent male crickets has arisen and spread in a population on Hawaii. Being silent protects them from attack by deadly parasitoid flies that are attracted to their song. The shift from singing to silent male crickets on Hawaii represents one of the fastest rates of evolution ever documented in the wild, but the genetic mutation responsible for this rapid change remains elusive.

Why is it important to understand what genetic changes alter the appearance or behavior of animals?

When a mutation does become established in a population, it can trigger a cascade of changes that affect how genes are regulated, how the physical features of an organism develop, and how individuals behave. Understanding what parts of the genome those mutations occur in and how they propagate gives us a clearer picture of how evolution by natural selection changes the way organisms develop, look and behave, and ultimately how new biological diversity is generated.

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Audio: listen to male crickets calling

Scientific Background

The Pacific field cricket Teleogryllus oceanicus is a typical field cricket: small, brown and retiring. Most cricket species look similarly bland and unobtrusive. But crickets own the night: at dusk, males transform into tiny caterwauling troubadours as they sing to lure females to mate with them. They sing by raising their front wings and rubbing them together. The movement of the wings against one another vibrates specialised structures on the surfaces that act as resonating membranes in a manner analogous to striking the surface of a drum. The vibrating membranes produce the chirruping sounds that we enjoy on summer evenings. Each species of cricket has its own special song, and females are fine-tuned to be able to pick out attractive males of their own species to mate with.

However, male Pacific field crickets that live in Hawaii have a major problem. They share their tropical paradise with an introduced parasitoid fly which attacks them when they sing. Female flies listen for singing males and manoeuvre very carefully and very quickly towards the sound of their call, and once they reach a male, they spew larvae on and around his body. The larvae drill through his exoskeleton, and then squirm into his body and devour him from the inside out over a period of about a week. They eat his fatty tissues and some muscles, but leave enough of him intact so that he stays alive, stumbling around like a zombie cricket, until the larvae are ready to pop out of the side of his abdomen and pupate. Once they've done that, the male has become little more than a hollow husk of his former self, and he staggers around briefly before finally dropping dead.

How do males survive and reproduce in the face of this threat? About 10 years ago, a new, mutant form of male cricket arose on the Hawaiian island of Kauai and was discovered by a graduate student in California. The story can be found here. Mutant males cannot sing, because the specialised structures on their wings are almost completely gone, but this protects them from the fly.

In fact, mutant male wings more closely resemble female cricket wings, which do not have sound-producing membranes. This mutation is called flatwing, and males inherit it as a single-locus, sex-linked trait. Silent males appear to adopt an alternative mating strategy by lurking nearby any remaining singing males in the population, and then intercepting females who are coming in to mate.

Normal (left) and 'Flatwing' (right) crickets

One reason for wanting to understand the genetic basis of the wing mutation is that this single mutation has effects that extend beyond just altering the structure of male wings. For example, males and females in Hawaii are now developing in relative silence because most of the males cannot sing. This change in the acoustic environment that developing nymphs experience has knock-on effects on how males and females behave. For example, males developing in silence are more likely to hang around other singing males to sneak matings with unsuspecting females, whereas females developing in silence are less picky about who they mate with, probably because they perceive the field of potential suitors to be fairly slim pickings.

A major debate in evolutionary biology concerns exactly what kinds of genetic mutations are most likely to lead to rapid evolutionary change. Most DNA doesn't code for proteins. In fact, large chunks of sequence can function to regulate the expression of a small number of protein-coding genes. So where are mutations that cause adaptive changes more likely to reside? Are mutations in regulatory regions more likely to cause variation in the wild than mutations in coding sequence? And are certain regions of the genome evolutionary 'hotspots', in other words, are mutations more likely to accumulate on some chromosome locations than others?

The cricket wing mutation allows us to answer questions like these in a population that is evolving right now and can be tracked on an almost month-to-month basis. Evolution has already been caught red-handed... the trick now is to understand exactly what it's getting away with.

Finding out more

Contact details:

There is more information on this and other projects on the lab website at: www.flexiblephenotype.org