skip to main content


This content will become publicly available on June 2, 2024

Title: Phenotypic outcomes of predator–prey coevolution are predicted by landscape variation in climate and community composition
Abstract

Landscape patterns of phenotypic coevolution are determined by variation in the outcome of predator–prey interactions. These outcomes may depend not only on the functional phenotypes that mediate species interactions, but also on aspects of the environment that enable encounters between coevolutionary partners.

Exploring the relationship between coevolutionary traits and the environment requires extensive sampling across the range of the interaction to determine the relationship between local ecological variation and coevolution.

In this study, we synthesized >30 years of data on predator–prey interactions between toxic newts (Taricha granulosa) and their snake predators (Thamnophis sirtalis) to explore the environmental predictors of arms race escalation.

We found that geographic variation in phenotypes at the interface of coevolution was best predicted by a combination of community and climatic variation. Coevolutionary phenotypes were greatest in environments with climate favourable for newt–snake overlap. We found prey toxicity was elevated in regions with more predator species, and predator resistance was higher in regions with more prey species.

Our results suggest specific environmental conditions reinforce the process of coevolution, signifying the phenotypic outcomes of coevolutionary arms races are sensitive to local ecological contexts that vary across the landscape.

Read the freePlain Language Summaryfor this article on the Journal blog.

 
more » « less
NSF-PAR ID:
10419854
Author(s) / Creator(s):
 ;  ;  ;  ;  ;  ;  ;  
Publisher / Repository:
Wiley-Blackwell
Date Published:
Journal Name:
Functional Ecology
Volume:
37
Issue:
8
ISSN:
0269-8463
Page Range / eLocation ID:
p. 2170-2180
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Abstract

    The Geographic Mosaic Theory of Coevolution predicts that coevolutionary arms races will vary over time and space because of the diverse ecological settings and population histories of interacting species across the landscape. Thus, understanding coevolution may require investigating broad sets of populations sampled across the range of the interaction. In addition, comparing coevolutionary dynamics between similar systems may reveal the importance of specific factors that structure coevolution.

    Here, we examine geographic patterns of prey traits and predator traits in the relatively unstudied interaction between the Sierra garter snake (Thamnophis couchii) and sympatric prey, the rough‐skinned newt (Taricha granulosa), Sierra newt (Ta. sierrae) and California newt (Ta. torosa). This system parallels, in space and phenotypes, a classic example of coevolution between predatory common garter snakes (Th. sirtalis) and their toxic newt prey exhibiting hotspots of newt tetrodotoxin (TTX) levels and matching snake TTX resistance.

    We quantified prey and predator traits from hundreds of individuals across their distributions, and functional trait matching at sympatric sites.

    We show strong regional patterns of trait covariation across the shared ranges ofTh. couchiiand newt prey. Traits differ significantly among localities, with lower newt TTX levels and snake TTX resistance at the northern latitudes, and higher TTX levels and snake resistance at southern latitudes. Newts and snakes in northern populations show the highest degree of functional trait matching despite possessing the least extreme traits. Conversely, newts and snakes in southern populations show the greatest mismatch despite possessing exaggerated traits, with some snakes so resistant to TTX they would be unaffected by any sympatric newt. Nevertheless, individual variation was substantial, and appears to offer the opportunity for continued reciprocal selection in most populations.

    Overall, the three species of newts appear to be engaged in a TTX‐mediated arms race withTh. couchii. These patterns are congruent with those seen between newts andTh. sirtalis, including the same latitudinal gradient in trait covariation, and the potential ‘escape’ from the arms race by snake predators. Such concordance in broad scale patterns across two distinct systems suggests common phenomena might structure geographic mosaics in similar ways.

     
    more » « less
  2. Abstract

    Antagonistic coevolution between natural enemies can produce highly exaggerated traits, such as prey toxins and predator resistance. This reciprocal process of adaptation and counter‐adaptation may also open doors to other evolutionary novelties not directly involved in the phenotypic interface of coevolution. We tested the hypothesis that predator–prey coevolution coincided with the evolution of conspicuous coloration on resistant predators that retain prey toxins. In western North America, common garter snakes (Thamnophis sirtalis) have evolved extreme resistance to tetrodotoxin (TTX) in the coevolutionary arms race with their deadly prey, Pacific newts (Tarichaspp.). TTX‐resistant snakes can retain large amounts of ingested TTX, which could serve as a deterrent against the snakes' own predators if TTX toxicity and resistance are coupled with a conspicuous warning signal. We evaluated whether arms race escalation covaries with bright red coloration in snake populations across the geographic mosaic of coevolution. Snake colour variation departs from the neutral expectations of population genetic structure and covaries with escalating clines of newt TTX and snake resistance at two coevolutionary hotspots. In the Pacific Northwest, bright red coloration fits an expected pattern of an aposematic warning to avian predators: TTX‐resistant snakes that consume highly toxic newts also have relatively large, reddish‐orange dorsal blotches. Snake coloration also seems to have evolved with the arms race in California, but overall patterns are less intuitively consistent with aposematism. These results suggest that interactions with additional trophic levels can generate novel traits as a cascading consequence of arms race coevolution across the geographic mosaic.

     
    more » « less
  3. Abstract

    Reciprocal adaptation is the hallmark of arms race coevolution. Local coadaptation between natural enemies should generate a geographic mosaic pattern where both species have roughly matched abilities across their shared range. However, mosaic variation in ecologically relevant traits can also arise from processes unrelated to reciprocal selection, such as population structure or local environmental conditions. We tested whether these alternative processes can account for trait variation in the geographic mosaic of arms race coevolution between resistant garter snakes (Thamnophis sirtalis) and toxic newts (Taricha granulosa). We found that predator resistance and prey toxin levels are functionally matched in co-occurring populations, suggesting that mosaic variation in the armaments of both species results from the local pressures of reciprocal selection. By the same token, phenotypic and genetic variation in snake resistance deviates from neutral expectations of population genetic differentiation, showing a clear signature of adaptation to local toxin levels in newts. Contrastingly, newt toxin levels are best predicted by genetic differentiation among newt populations, and to a lesser extent, by the local environment and snake resistance. Exaggerated armaments suggest that coevolution occurs in certain hotspots, but prey population structure seems to be of particular influence on local phenotypic variation in both species throughout the geographic mosaic. Our results imply that processes other than reciprocal selection, like historical biogeography and environmental pressures, represent an important source of variation in the geographic mosaic of coevolution. Such a pattern supports the role of “trait remixing” in the geographic mosaic theory, the process by which non-adaptive forces dictate spatial variation in the interactions among species.

     
    more » « less
  4. Abstract

    In the evolutionary arms race between predators and their prey, prey often evolve to be as cryptic as they can, while predators in turn hone their sensory strategies to detect prey. Examinations of the sensory strategies implemented by predators to detect their prey, as well as the ecological consequences of these interactions, are at the crux of understanding and predicting predator–prey dynamics.

    We review the sensory strategies used by predators that rely on private information (attending directly to cues and signals generated by their prey) and those that gather social information (attending to the signals and behaviours of others). We focus our enquiry on bats, an ideal group to shed light on these questions given their ecological diversity, varied foraging strategies and wide range of social behaviours.

    We discuss the costs and benefits of using private and social information for foraging. We investigate diverse strategies of information use and examine the effects different predatory strategies have on predator sensory systems.

    We provide an overview of the sensory ecology of information use in hunting in bats and, by identifying current gaps in knowledge, highlight fruitful directions for future research.

    A freePlain Language Summarycan be found within the Supporting Information of this article.

     
    more » « less
  5. Abstract

    Theory suggests that intraspecific trait variation will alter species interaction strengths through nonlinear averaging when interaction strengths are nonlinear functions of individuals' traits. This effect is expected to be widespread, yet what factors mediate its magnitude in nature and hence its potential effects on ecosystems and communities are unclear.

    We sought to quantify how nonlinear predator functional responses, variation in prey densities and counteracting variation in attack rates and handling times among predator individuals of similar body size alter their population‐level feeding rates through nonlinear averaging in a natural system, and to determine the processes influencing the net magnitude of this effect.

    We used a field caging experiment in the rocky intertidal of Oregon, USA to quantify attack‐rate variation and feeding rates of the whelkNucella ostrinaon its barnacle and mussel prey. We also used empirically parameterized simulations to examine the effects of handling‐time variation among individuals on population‐level feeding rates.

    Within cages, individual attack‐rate variation reduced population‐level whelk feeding rates. However, the magnitude of this reduction differed among prey species and cages depending on cage‐specific magnitudes of attack‐rate variation and functional‐response nonlinearity. The inferred effects of handling‐time variation among individuals were of smaller magnitude than those of attack‐rate variation, yet counteracted them to cause a net weakening of the effect of individual attack‐rate variation on population‐level feeding rates. Across cages, attack‐rate and prey‐density variation had non‐additive effects that produced greater feeding‐rate reductions at the experiment scale relative to the cage scale.

    Our results indicate that the effects of trait variation via nonlinear averaging depend critically on the features of systems that determine the magnitudes of nonlinearities and trait variation. Because of counteracting trait variation, nonlinear‐averaging effects may be quite complex, involving both the variances and covariances of all traits and environmental variables influencing the ecological process of interest.

    A freePlain Language Summarycan be found within the Supporting Information of this article.

     
    more » « less