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Giants, dwarfs and the environment - metamorphic trait plasticity in the common frog.

ABSTRACT: In order to understand adaptation processes and population dynamics, it is central to know how environmental parameters influence performance of organisms within populations, including their phenotypes. The impact of single or few particular parameters in concert was often assessed in laboratory and mesocosm experiments. However, under natural conditions, with many biotic and abiotic factors potentially interacting, outcomes on phenotypic changes may be different. To study the potential environmental impact on realized phenotypic plasticity within a natural population, we assessed metamorphic traits (developmental time, size and body mass) in an amphibian species, the European common frog Rana temporaria, since a) larval amphibians are known to exhibit high levels of phenotypic plasticity of these traits in response to habitat parameters and, b) the traits' features may strongly influence individuals' future performance and fitness. In 2007 we studied these metamorphic traits in 18 ponds spread over an area of 28 km2. A subset of six ponds was reinvestigated in 2009 and 2010. This study revealed locally high variances in metamorphic traits in this presumed generalist species. We detected profound differences between metamorphing froglets (up to factor ten); both between and within ponds, on a very small geographic scale. Parameters such as predation and competition as well as many other pond characteristics, generally expected to have high impact on development, could not be related to the trait differences. We observed high divergence of patterns of mass at metamorphosis between ponds, but no detectable pattern when metamorphic traits were compared between ponds and years. Our results indicate that environment alone, i.e. as experienced by tadpoles sharing the same breeding pond, can only partly explain the variability of metamorphic traits observed. This emphasizes the importance to assess variability of reaction norms on the individual level to explain within-population variability.

SUBMITTER: Grozinger F

PROVIDER: S-EPMC3943853 | biostudies-literature | 2014

REPOSITORIES: biostudies-literature

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Giants, dwarfs and the environment - metamorphic trait plasticity in the common frog.

Grözinger Franziska F Thein Jürgen J Feldhaar Heike H Rödel Mark-Oliver MO

PloS one 20140305 3

In order to understand adaptation processes and population dynamics, it is central to know how environmental parameters influence performance of organisms within populations, including their phenotypes. The impact of single or few particular parameters in concert was often assessed in laboratory and mesocosm experiments. However, under natural conditions, with many biotic and abiotic factors potentially interacting, outcomes on phenotypic changes may be different. To study the potential environm ...[more]

PMID: 24599256

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Project description:Gigantism and dwarfism evolve in vertebrates restricted to islands. We describe four new species in the Rhinolophus hildebrandtii species-complex of horseshoe bats, whose evolution has entailed adaptive shifts in body size. We postulate that vicissitudes of palaeoenvironments resulted in gigantism and dwarfism in habitat islands fragmented across eastern and southern Africa. Mitochondrial and nuclear DNA sequences recovered two clades of R. hildebrandtii senso lato which are paraphyletic with respect to a third lineage (R. eloquens). Lineages differ by 7.7 to 9.0% in cytochrome b sequences. Clade 1 includes R. hildebrandtii sensu stricto from the east African highlands and three additional vicariants that speciated across an Afromontane archipelago through the Plio-Pleistocene, extending from the Kenyan Highlands through the Eastern Arc, northern Mozambique and the Zambezi Escarpment to the eastern Great Escarpment of South Africa. Clade 2 comprises one species confined to lowland savanna habitats (Mozambique and Zimbabwe). A third clade comprises R. eloquens from East Africa. Speciation within Clade 1 is associated with fixed differences in echolocation call frequency, and cranial shape and size in populations isolated since the late Pliocene (ca 3.74 Mya). Relative to the intermediate-sized savanna population (Clade 2), these island-populations within Clade 1 are characterised by either gigantism (South African eastern Great Escarpment and Mts Mabu and Inago in Mozambique) or dwarfism (Lutope-Ngolangola Gorge, Zimbabwe and Soutpansberg Mountains, South Africa). Sympatry between divergent clades (Clade 1 and Clade 2) at Lutope-Ngolangola Gorge (NW Zimbabwe) is attributed to recent range expansions. We propose an "Allometric Speciation Hypothesis", which attributes the evolution of this species complex of bats to divergence in constant frequency (CF) sonar calls. The origin of species-specific peak frequencies (overall range = 32 to 46 kHz) represents the allometric effect of adaptive divergence in skull size, represented in the evolution of gigantism and dwarfism in habitat islands.

Project description:BackgroundMetamorphic climax is the crucial stage of amphibian metamorphosis responsible for the morphological and functional changes necessary for transition to a terrestrial habitat. This developmental period is sensitive to environmental changes and pollution. Understanding its metabolic basis and requirements is significant for ecological and toxicological research. Rana omeimontis tadpoles are a useful model for investigating this stage as their liver is involved in both metabolic regulation and fat storage.ResultsWe used a combined approach of transcriptomics and metabolomics to study the metabolic reorganization during natural and T3-driven metamorphic climax in the liver and tail of Rana omeimontis tadpoles. The metabolic flux from the apoptotic tail replaced hepatic fat storage as metabolic fuel, resulting in increased hepatic amino acid and fat levels. In the liver, amino acid catabolism (transamination and urea cycle) was upregulated along with energy metabolism (TCA cycle and oxidative phosphorylation), while the carbohydrate and lipid catabolism (glycolysis, pentose phosphate pathway (PPP), and β-oxidation) decreased. The hepatic glycogen phosphorylation and gluconeogenesis were upregulated, and the carbohydrate flux was used for synthesis of glycan units (e.g., UDP-glucuronate). In the tail, glycolysis, β-oxidation, and transamination were all downregulated, accompanied by synchronous downregulation of energy production and consumption. Glycogenolysis was maintained in the tail, and the carbohydrate flux likely flowed into both PPP and the synthesis of glycan units (e.g., UDP-glucuronate and UDP-glucosamine). Fatty acid elongation and desaturation, as well as the synthesis of bioactive lipid (e.g., prostaglandins) were encouraged in the tail during metamorphic climax. Protein synthesis was downregulated in both the liver and tail. The significance of these metabolic adjustments and their potential regulation mechanism are discussed.ConclusionThe energic strategy and anabolic requirements during metamorphic climax were revealed at the molecular level. Amino acid made an increased contribution to energy metabolism during metamorphic climax. Carbohydrate anabolism was essential for the body construction of the froglets. The tail was critical in anabolism including synthesizing bioactive metabolites. These findings increase our understanding of amphibian metamorphosis and provide background information for ecological, evolutionary, conservation, and developmental studies of amphibians.

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Giants, dwarfs and the environment - metamorphic trait plasticity in the common frog.

Publications

Giants, dwarfs and the environment - metamorphic trait plasticity in the common frog.

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