When three steps forward is one step back
4 July 2001 17:00 GMT

by Henry Nicholls, BioMedNet News

© Smudge/Neil Smith
Research published tomorrow further enhances Lewis Carroll's reputation as a closet evolutionary biologist by revealing, in an exceptional analysis according to some specialists, how genetic evolution can fail to keep up with a changing environment. Such "cryptic evolution", so called because the evolving genotype is masked by an apparently unresponsive phenotype, could be widespread in nature, says the Finnish researcher who led the work.

The analysis focuses on a 20-year study of an isolated bird population, reports Juha Merilä, senior researcher in the department of ecology and systematics at the University of Helsinki. Collared flycatchers, Ficedula albicollis, on the Swedish island of Gotland have evolved genes to increase their body mass as the birds' environment has deteriorated, but they are losing weight.

"Quantitative genetic theory predicts that the relative body mass of flycatcher offspring, which is a heritable trait under positive directional selection, should increase over time, but the relative mass at fledging has actually decreased," Merilä told BioMedNet News.

"Our results suggest that if today's flycatcher chicks were to experience a similar environment as the ones that lived in the early 1980s, they would be much fatter than they are today," he said.

"I would not be surprised if this [cryptic evolution] turned out to be common," he added. "We should realize ... that similarity in character state in time or space does not mean that evolution has not occurred. A lot of evolution might be of this cryptic nature and we will keep on overlooking it unless we focus more on similarities, rather than exclusively on dissimilarities in character state," warned Merilä.

"To my knowledge, this is the first time we have managed to demonstrate occurrence of cryptic genetic evolution over a relatively short period of time in the wild," he said.

The work impresses Peter Boag, professor of biology at Queen's University in Ontario. "The really unique feature of this study is that rarely has anyone collected sufficient data from a real world, wild vertebrate population to allow a believable dissection of this complex web of interactions," noted Boag.

Merilä readily drew a parallel between his findings and the Red Queen Hypothesis, which originates from Carroll's Through the Looking Glass. "To my mind, the Red Queen metaphor is a fascinating and an intuitive way of thinking about evolution," he acknowledged.

Leigh Van Valen, now professor of ecology and evolution at the University of Chicago, famously drew on Carroll's fantasy tale, and in particular the Red Queen's advice to Alice that "it takes all the running you can do to keep in the same place", as a metaphor for evolution. In 1973, he proposed that in a changing environment, organisms must evolve just to maintain their fitness.

The hypothesis is most commonly cast in terms of two organisms, such as the co-evolution between a parasite and its host. As the parasite evolves novel ways of exploiting its host, selection favours the host that evolves novel ways of defending itself against the parasite. Over an evolutionary timescale, both parasite and host will have evolved and yet their relationship might not have changed - neither will appear to be any more successful at outwitting the other.

However, in an interview with BioMedNet News, Van Valen pointed out that "the Red Queen's Hypothesis can easily apply to abiotically caused deterioration, which isn't usually realized," and he agreed that Merilš's flycatchers seem to be subject to the paradox of the Red Queen.

"The [flycatchers'] response to selection isn't enough to prevent the population from deteriorating," he noted. "All the running [the flycatchers] can do isn't enough to keep [them] in the same place... It's pretty persuasive and fascinating [research]," he said.

Merilä speculates that a large-scale climatic trend could underlie the worsening environment that the flycatchers are experiencing. "Increased spring temperatures have led to increasingly poor synchronization between the hatching date of caterpillars and the date of bud-burst of the oak trees on which they feed," he writes in this week's issue of Nature, published tomorrow.

This is bad news for the flycatchers, notes Merilä, because caterpillars are the main source of food for growing nestlings. And it raises the evolutionarily interesting question of "how far can [the flycatchers] lag behind before they have to give up the race?"

Merilä concluded: "This strengthens my belief that long-term population studies can be immensely valuable for both evolutionary and environmental biologists, especially now that we seem to be entering into an era of rapid environmental changes caused by anthropogenic activities... These studies can be a valuable resource in the future."

Send us your feedback.