Antipredator defenses predict diversification rates

Abstract

The "escape-and-radiate" hypothesis predicts that antipredator defenses facilitate adaptive radiations by enabling escape from constraints of predation, diversified habitat use, and subsequently speciation. Animals have evolved diverse strategies to reduce the direct costs of predation, including cryptic coloration and behavior, chemical defenses, mimicry, and advertisement of unprofitability (conspicuous warning coloration). Whereas the survival consequences of these alternative defenses for individuals are wellstudied, little attention has been given to the macroevolutionary consequences of alternative forms of defense. Here we show, using amphibians as the first, to our knowledge, large-scale empirical test in animals, that there are important macroevolutionary consequences of alternative defenses. However, the escape-andradiate hypothesis does not adequately describe them, due to its exclusive focus on speciation. We examined how rates of speciation and extinction vary across defensive traits throughout amphibians. Lineages that use chemical defenses show higher rates of speciation as predicted by escape-and-radiate but also show higher rates of extinction compared with those without chemical defense. The effect of chemical defense is a net reduction in diversification compared with lineages without chemical defense. In contrast, acquisition of conspicuous coloration (often used as warning signals or in mimicry) is associated with heightened speciation rates but unchanged extinction rates. We conclude that predictions based on the escape-and-radiate hypothesis must incorporate the effect of traits on both speciation and extinction, which is rarely considered in such studies. Our results also suggest that knowledge of defensive traits could have a bearing on the predictability of extinction, perhaps especially important in globally threatened taxa such as amphibians.escape-and-radiate | coevolution | speciation | extinction | amphibians T he idea that defensive traits determine macroevolutionary patterns was originally suggested in the plant literature (1) to explain heightened diversity. In this hypothesis, the presence of repellent chemical defenses was proposed to open up an "adaptive zone" of diverse ecological opportunities and hence promote speciation by adaptive radiation. This became known as the "escape-and-radiate" hypothesis (2). Similarly, it has been suggested that bright coloration can reduce the constraints of hiding, enabling niche expansion and promoting diversification in animal prey (3, 4). The escape-and-radiate hypothesis is influential in the adaptive radiation literature (2, 5, 6) but has been tested surprisingly rarely (6-8). The very few macroevolutionary studies on animal defenses focus only on coloration, are small-scale, and often only consider net diversification or comparisons of species richness in relation to the defensive trait of interest (5, 9, 10). For instance, one recent study on poison dart frogs included defense-based diversification analyses as part of an examination o...

Chemical antipredator defence is linked to higher extinction risk

“…Using a large-scale dataset of amphibians (a taxon of global conservation concern), I demonstrate that chemically defended species are more likely to be threatened and are often younger than non-chemically defended species. Such results are in line with predictions made from a recent study of background extinction rates in amphibians [30] and therefore suggest that such diversification rate estimates can potentially inform estimates of current extinction risk based on species' traits.…”

“…Data on the presence or absence of chemical defence in 857 amphibian species were extracted from reference [30]. Briefly, this dataset was assembled from literature searches, using a conservative approach in which data were only recorded for each species if it had been investigated and found to either possess or lack a chemical defence.…”

“…If information was not available for that given species no data were recorded and, consequently, species included in this study are known to either possess or lack a chemical antipredator defence. Further details on the collation of this dataset are available in the original paper [30]. …”

“…These simulations were performed using T ree S im [42] and represent predictions at regular time points of the fate of a lineage into the future. The birth and death rates were carried out first, using the estimated parameters for non-chemically defended species, and then repeated with the estimates for chemically defended species from reference [30]. At the end of each run, the proportion of the 1000 simulations in which the entire lineage had gone extinct for each time point was recorded.…”

“…I have previously suggested three main possibilities to explain higher background extinction rates in chemically defended amphibians [30]: (i) chemical defence is energetically costly, (ii) chemical defence allows shifts to ‘marginal’ (low carrying capacity) habitats, which are intrinsically more vulnerable and (iii) chemical defence is associated with slow life histories, which damages the recovery potential of populations after declines. To these could be added the possibility that well-defended species face particularly strong predation pressure and that this could then lead to higher extinction rates.…”