Prey species evolve a variety of ways to avoid their predators, including chemical toxins, camouflage, and conspicuous colouration. But what are the potential costs associated with anti-predator defences? According to a study of amphibians published today in the journal, Proceedings of the National Academy of Sciences, chemical defence and conspicuous colouration enhance speciation rates in prey species, as predicted. But unexpectedly, evolution of chemical defences also increases extinction rates -- even above the rate of speciation. As a result, developing chemical defences against predators increases the overall risk of extinction for prey species.
The predator-prey “evolutionary arms race”
Community ecology is the scientific study of patterns resulting from reciprocal interactions between particular groups of organisms, such as those between predators and prey. Predator-prey relationships can give rise to an “evolutionary arms race” where prey species develop a variety of defences that protect them from their predators. Evolution of such defences can lead to increased speciation rates due to relaxed selection pressures by predators, particularly when new niches open up that provide access to available resources (or new challenges). This process is known as adaptive radiation.
One fundamental hypothesis, which later came to be known as “escape-and-radiate coevolution”, was originally proposed in 1964 to explain the “evolutionary arms race” between butterfly larvae and their food plants (doi:10.2307/2406212). In that paper, authors Paul Ehrlich and Peter Raven proposed that organisms that are constrained by other organisms, such as prey species, will develop novel defences to escape those constraints, and this “escape” then allows them to “radiate” into new species.
“A good example is camouflage”, said the lead author of the study, evolutionary biologist and herpetologist Kevin Arbuckle, a research scientist at the University of Liverpool.
“Camouflage patterns work very well when the prey sits still (and on an appropriate background), but as soon as it moves, it breaks its camouflage and the prey is therefore restricted in its movements to times when (perhaps) predation pressure is reduced”, explained Dr Arbuckle in email.
“[T]he key thing here is that although escape-and-radiate was first suggested in the plant literature, it is a general idea that relates broadly to the response of organisms to their natural enemies”, said Dr Arbuckle.
Although the escape-and-radiate hypothesis is 50 years old, it has not yet been rigorously tested in animals.
“There is nothing particularly special about plant-herbivore interactions in relation to escape-and-radiate theory that precludes its application to other scenarios such as predator-prey”, said Dr Arbuckle in email. “[I]n fact, in the literature, the two types of interaction are often considered [to be] the same thing (herbivores are simply predators of plants).”
Thus, although amphibians are obviously not plants, they do have a number of qualities that make them a good system for testing the escape-and-radiate hypothesis in animals: First, amphibians are well-known. Second, amphibians are prey animals. And third, amphibians tend to evolve chemical defences for protection.
Amphibians are more likely to evolve toxic defences than to lose them
To test the escape-and-radiate hypothesis, and to better understand the relationship between evolution, chemical defence and conspicuousness in amphibians, Dr Arbuckle and his co-author, Dr Michael Speed, a Reader in Evolutionary Biology at the University of Liverpool, investigated searchable and hard-copy literature for information about chemical anti-predator defences for all amphibian species for which they had phylogenetic data (approximately 40 percent). Of the 857 amphibian species they examined, 35 percent did not possess chemical anti-predator defences whereas 65 percent did. Dr Arbuckle and Dr Speed analysed these data by fitting them to a model that estimates how particular traits affect speciation and extinction rates.
The researchers first tested the effects of chemical defence in amphibians upon speciation and extinction rates (note that these rates are on the x-axis) (Figure 1):
These analyses revealed that chemically defended amphibian lineages (red bump; Figure 1) have twice the rate of speciation (Figure 1A) as non-toxic lineages (blue bump; Figure 1), a finding that supports a major prediction by the escape-and-radiate hypothesis. But the researchers were surprised to learn that extinction rates are three times higher in amphibian lineages with chemical defences (Figure 1B). On one hand, the overall diversification rate is higher for chemically-defended amphibians (note that the red bump is to the left of the blue bump in Figure 1D), which indicates that everything -- speciation and extinction -- is happening faster in chemically-defended lineages. But on the other hand, these data reveal that toxic amphibians are going extinct faster than they are speciating. Further, the researchers found that the transition rate (gain or loss of toxicity) was high for non-toxic lineages (blue bump; Figure 1C) but very low for chemically defended lineages (red bump; Figure 1C).
“Amphibians are much more likely to evolve toxic defences than they are to lose them”, explained Dr Arbuckle. “[A]nd once they have, two things happen to the species. Firstly, they are more likely to radiate out into more species, but secondly, they are even more likely to go extinct.”
Amphibians with conspicuous colours speciate faster
As we know from the iconic poison dart frogs, amphibians also appear to evolve conspicuous colours. But what effects do conspicuous colours have on amphibian diversification?
Dr Arbuckle and Dr Speed’s analysis showed that conspicuous colours and patterns did increase speciation rates in amphibians, but without a corresponding increase in extinction rates (Figure 2):
The analysis revealed that the speciation rate (Figure 2A & C) for conspicuously coloured amphibians (red bump; Figure 2) is two to three times higher than that for species with cryptic coloration (blue bump; Figure 2) or polymorphic colouration (possessing several colour variants) (yellow bump; Figure 2). Further, the analysis showed that extinction rates were equal across all colouration strategies -- conspicuous, cryptic and polymorphic -- so the net diversification rate was higher overall for conspicuous amphibian species (Figure 2C).
These results strongly support the escape-and-radiate hypothesis prediction that conspicuous colouration increases speciation and net diversification rates compared with camouflage and other forms of protective coloration.
“Amphibians with bright, conspicuous colour patterns are more likely to radiate out into lots of different species ... and because the colour patterns don’t influence their chances of going extinct, the amphibians are free to expand in this way”, said Dr Arbuckle in email.
The evolutionary benefits of conspicuousness contrast sharply with the team’s findings for the evolve chemical defences. And indeed, it appears that chemically defended amphibians that later develop conspicuous colours may enjoy some benefits on an evolutionary timescale.
“Warning colours paired with toxins may also allow species to move into new ecological niches, and even evolve complex behaviours”, said evolutionary ecologist Hannah Rowland, a Lecturer at the University of Cambridge and a Research Fellow at the Zoological Society of London, who was not part of the study.
“Dendrobatid (poison) frogs, for example, have complex behaviours like parental care and sexual conflict”, added Dr Rowland.
Frogs: “It’s not easy being mean”
“This is a fascinating analysis that derives general macroevolutionary patterns from a study of diversification and extinction rates in amphibians”, said herpetologist Wolfgang Wüster, a Senior Lecturer in the Department of Biological Sciences at Bangor University, who was not part of the study.
“The most novel and perhaps most surprising finding is that chemical anti-predator defences are a double-edged sword: they trigger higher diversification rates but even greater extinction rates, and since reversals are rare, they are essentially evolutionary dead ends”, explained Dr Wüster in email.
Since chemical defences protect amphibians from predators, it seems counter-intuitive that evolving this trait speeds extinction of the lineage.
“What’s most fascinating about Arbuckle and Speed’s research is that these costs play out on a macroevolutionary scale, in that chemically defended prey are three times more likely to go extinct than those lineages without chemical defences”, said Dr Rowland.
Additionally, conspicuousness would seem to increase an amphibian’s risk of predation, but evolving this trait actually protects the lineage from extinction.
“In contrast, it turns out that conspicuous coloration increases speciation rates without increasing extinction rates”, said Dr Wüster.
Further, the speciation effects of chemical defence and of conspicuous coloration are independent from each other, so when a toxic species then evolves conspicuous colouration, the increased diversification rate that accompanies colouration may offset the reduced diversification rate conferred by chemical defence.
Conspicuousness is not permanent in amphibians.
“[C]onspicuous coloration appears to be a labile character that frequently reverts to inconspicuous coloration, so that conspicuous lineages are not trapped in an evolutionary dead-end if the conditions that favoured the evolution of conspicuousness disappear”, Dr Wüster pointed out.
Although people are most familiar with the brilliantly coloured poison dart frogs, and for that reason, might assume that most frog species are colourful, in reality, conspicuousness is not a very common trait in amphibians.
“If I leaf through some of my field guides, it always strikes me how comparatively rare conspicuous colouration is”, said Dr Rowland. “One other finding by Arbuckle and Speed might explain why: conspicuous colouration is a short-lived tactic, with animals either going extinct or reverting to crypsis frequently.”
In addition to offsetting the evolutionary costs of toxicity, conspicuousness provides other benefits to amphibians.
“We know that pairing a bright colour with a chemical defence (warning colouration) is a good idea because it teaches predators not to attack”, said Dr Rowland.
“Birds are more wary of brightly coloured prey, and remember to avoid attacking them for a relatively long time”, explained Dr Rowland in email.
“Chemical defences, like poisons, are great for defending yourself against predators, but there may be unforeseen consequences that make you much more likely to go extinct”, explained Dr Arbuckle.
“To paraphrase a popular champion of amphibian rights, it’s really not easy being mean!”
Kevin Arbuckle and Michael P. Speed (2015). Antipredator defenses predict diversification rates, Proceedings of the National Academy of Sciences, published online on 19 October 2015 ahead of print | doi:pnas.1509811112
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