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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.
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Phenotypic differentiation in populations of a gladiator tree frog: environment, genetic drift and sexual selection
Abstract Phenotypic differentiation among animal populations is common, yet few studies have simultaneously examined the adaptive and neutral mechanisms behind it. Such evolutionary processes become more relevant in species with complex behaviours that undergo global and local selective pressures throughout their geographical range. Here we measured and compared morphological and acoustic variation across the distribution range of a Neotropical gladiator tree frog that shows elaborate reproduction (territoriality, complex courtship and female choice). We then incorporated molecular and landscape data to examine the roles of sexual selection, genetic drift and acoustic adaptation to the environment in call differentiation, i.e. the acoustic adaptation hypothesis (AAH). We found that calls varied more than morphology among populations, but differences in calls or morphological traits were not explained by genetic differentiation. We found no evidence for the AAH, but a significant relationship in the opposite direction regarding call frequencies suggests an indirect role of sexual selection. Differentiation on call traits that are associated with individual discrimination and/or female attraction also corroborated an important role of sexual selection. We show that multitrait and multimechanism approaches can elucidate intricate processes leading to phenotypic variation among individuals and populations. We emphasize that studies of species with complex reproductive behaviours across their range may provide insights into different selective pressures leading to phenotypic differentiation.
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- Award ID(s):
- 2151540
- PAR ID:
- 10429118
- Date Published:
- Journal Name:
- Biological Journal of the Linnean Society
- Volume:
- 139
- Issue:
- 3
- ISSN:
- 0024-4066
- Page Range / eLocation ID:
- 243 to 256
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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- Free Publicly Accessible Full Text
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1093/biolinnean/blad028
