To hatch and hatch not: similar selective trade-offs but different responses to egg predators in two closely related, syntopic treefrogs

Gómez-Mestre, Iván; Warkentin, Karen M.

doi:10.1007/s00442-007-0708-0

Cited by 41 publications

(50 citation statements)

References 59 publications

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“…This rate is far greater than the desiccation mortality reported for many other terrestrially breeding frogs (40)(41)(42)(43). In contrast, D. ebraccatus embryos are more capable of aquatic development than other terrestrial amphibian eggs, which die if submerged before hatching competence (40,42,(44)(45)(46)(47)(48) (23)]. D. ebraccatus eggs are smaller than most terrestrial anuran eggs (10), which both reduces their oxygen demand and increases their surface areato-volume ratio, thereby enhancing oxygen diffusion under water (50).…”

Section: Discussionmentioning

confidence: 99%

Reproductive mode plasticity: Aquatic and terrestrial oviposition in a treefrog

Touchon

Warkentin

2008

Proc. Natl. Acad. Sci. U.S.A.

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Diversification of reproductive mode is a major theme in animal evolution. Vertebrate reproduction began in water, and terrestrial eggs evolved multiple times in fishes and amphibians and in the amniote ancestor. Because oxygen uptake from water conflicts with water retention in air, egg adaptations to one environment typically preclude development in the other. Few animals have variable reproductive modes, and no vertebrates are known to lay eggs both in water and on land. We report phenotypic plasticity of reproduction with aquatic and terrestrial egg deposition by a frog. The treefrog Dendropsophus ebraccatus, known to lay eggs terrestrially, also lays eggs in water, both at the surface and fully submerged, and chooses its reproductive mode based on the shade above a pond. Under unshaded conditions, in a disturbed habitat and in experimental mesocosms, these frogs lay most of their egg masses aquatically. The same pairs also can lay eggs terrestrially, on vegetation over water, even during a single night. Eggs can survive in both aquatic and terrestrial environments, and variable mortality risks in each may make oviposition plasticity adaptive. Phylogenetically, D. ebraccatus branches from the basal node in a clade of terrestrially breeding species, nested within a larger lineage of aquatic-breeding frogs. Reproductive plasticity in D. ebraccatus may represent a retained ancestral state intermediate in the evolution of terrestrial reproduction.aquatic egg-laying ͉ evolution of reproductive mode ͉ Hyla ebraccata ͉ phenotypic plasticity ͉ climate change T he evolution of terrestrially developing eggs from ancestral aquatic eggs is a repeated trend in both invertebrates and vertebrates (1-10). In both groups, aquatic predators and constraints on oxygen uptake are hypothesized to select for terrestrial eggs (2, 7-11). Terrestrial eggs can improve the embryonic respiratory environment, allow oviposition over fast-moving streams where aquatic eggs might be swept away, and allow animals to colonize habitats without permanent water bodies (2, 4, 7-10). However, terrestrial eggs experience new risks from desiccation and terrestrial predators (2, 4, 7-10). Because aquatic and terrestrial environments select for different traits, eggs are usually well adapted to only one environment (2, 4). Adaptations for terrestrial oviposition have evolved independently in several groups [e.g., gastropods (8, 12), insects (9, 13), and fishes and amphibians (1, 2, 4, 10)]. In all of these organisms, the divergence in reproductive mode [oviposition site and type of egg development (1, 2, 10)] occurred long ago, and it is thus difficult to directly assess selective pressures that may have influenced such evolution. Closely related species or populations that vary in their reproductive modes [e.g., between viviparity and oviparity (14-18)] offer the best opportunity to study the selective pressures leading to reproductive mode diversification. Although some foam-nesting frogs are reported to place nests in diverse locations (10,19,20), t...

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Section: Discussionmentioning

confidence: 99%

Reproductive mode plasticity: Aquatic and terrestrial oviposition in a treefrog

Touchon

Warkentin

2008

Proc. Natl. Acad. Sci. U.S.A.

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“…Eggs of all other Agalychnis species, Cruziohyla calcarifer, and Pachymedusa dacnicolor are also laid on vegetation over water and co-occur with various species of egg-eating snakes (Duellman 2001). Some clutches are laid close enough to the water surface that natural fluctuations of water level flood clutches, killing eggs too young to hatch (Pyburn 1970, Warkentin 2000b, Gomez-Mestre and Warkentin 2007. Also, these species often co-occur with small fishes and other aquatic predators of tadpoles.…”

Section: Introductionmentioning

confidence: 99%

“…Vibrations cue hatching during snake attacks, whereas hypoxic stress stimulates hatching of submerged clutches (Warkentin 2002(Warkentin , 2005. These risks occur at different frequencies, with snake predation substantially more common than underwater submergence in nature (Warkentin 1995, 2000b, Gomez-Mestre and Warkentin 2007. Eggs of all other Agalychnis species, Cruziohyla calcarifer, and Pachymedusa dacnicolor are also laid on vegetation over water and co-occur with various species of egg-eating snakes (Duellman 2001).…”

Section: Introductionmentioning

confidence: 99%

Evolution of Adaptive Plasticity: Risk‐sensitive Hatching in Neotropical Leaf‐breeding Treefrogs

Gómez-Mestre

Wiens

Warkentin

2008

Ecological Monographs

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119

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Abstract. Adaptive plasticity at switch points in complex life cycles (e.g., hatching, metamorphosis) is well known, but the evolutionary history of such plasticity is not. Particularly unclear is how a single plastic response (e.g., shifts in hatching timing) evolves to respond to different threats and cues (e.g., abiotic and biotic). We conducted a comparative phylogenetic study of hatching plasticity in a group of frogs with arboreal embryos to determine when risk-accelerated hatching evolved in the clade, whether responses to two common egg-stage risks (snake predation and flooding) evolved independently, and whether the overall capacity for hatching plasticity was evolutionarily more conservative than responses to specific cues. Red-eyed treefrogs (Agalychnis callidryas) hatch early to escape from several egg-stage risks but otherwise hatch later, improving larval survival with predators. We reconstructed a phylogeny for Agalychnis and related genera based on three mitochondrial and four nuclear genes. We quantified onset of hatching competence, spontaneous hatching timing, responses to egg-stage risks, and costs of premature hatching in Agalychnis and Pachymedusa. We also assessed hatching plasticity in a basal phyllomedusine, Cruziohyla calcarifer. The capacity to hatch ;30% before the spontaneous hatching age appears ancestral for phyllomedusines, with little change over ;34-50 million years among the species examined. A strong hatching response to flooding, with no mortality of hatching-competent eggs, is similarly ancient and conserved. Premature hatchlings of Agalychnis and Pachymedusa are more vulnerable to fish predation than are full-term hatchlings, indicating a conserved risk trade-off across hatching that would make plasticity advantageous. In contrast, the hatching response to snake attack has undergone major changes at least twice in the Agalychnis-Pachymedusa clade, with two species showing substantially lower escape success than the others. Responses to different threats have thus evolved independently. The capacity for switch point plasticity may be evolutionarily more stable than the response to individual stage-specific threats.

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“…Taken together, these studies suggest that the expression of genetic variation in a trait is not only trait-dependent but can also be reliant on the stressor. To add an additional level of complexity, the amount of genetic variation in a trait can also vary among populations, due to genetic drift and/or local adaptation (Einum and Fleming 2000;Gomez-Mestre and Warkentin 2007). Indeed, in the case of salmonids, life histories are typically finely tuned to local environmental conditions (Crozier et al 2008).…”

Section: Introductionmentioning

confidence: 99%

Pathogen-induced hatching and population-specific life-history response to waterborne cues in brown trout (Salmo trutta)

Pompini

Clark

Wedekind

2013

Behav Ecol Sociobiol

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Hatching is an important niche shift, and embryos in a wide range of taxa can either accelerate or delay this life-history switch in order to avoid stage-specific risks. Such behavior can occur in response to stress itself and to chemical cues that allow anticipation of stress. We studied the genetic organization of this phenotypic plasticity and tested whether there are differences among populations and across environments in order to learn more about the evolutionary potential of stress-induced hatching. As a study species, we chose the brown trout (Salmo trutta; Salmonidae). Gametes were collected from five natural populations (within one river network) and used for full-factorial in vitro fertilizations. The resulting embryos were either directly infected with Pseudomonas fluorescens or were exposed to waterborne cues from P. fluorescens-infected conspecifics. We found that direct inoculation with P. fluorescens increased embryonic mortality and induced hatching in all host populations. Exposure to waterborne cues revealed population-specific responses. We found significant additive genetic variation for hatching time, and genetic variation in trait plasticity. In conclusion, hatching is induced in response to infection and can be affected by waterborne cues of infection, but populations and families differ in their reaction to the latter.

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To hatch and hatch not: similar selective trade-offs but different responses to egg predators in two closely related, syntopic treefrogs

Cited by 41 publications

References 59 publications

Reproductive mode plasticity: Aquatic and terrestrial oviposition in a treefrog

Reproductive mode plasticity: Aquatic and terrestrial oviposition in a treefrog

Evolution of Adaptive Plasticity: Risk‐sensitive Hatching in Neotropical Leaf‐breeding Treefrogs

Pathogen-induced hatching and population-specific life-history response to waterborne cues in brown trout (Salmo trutta)

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