Abstract
BackgroundRana pirica tadpoles show morphological changes in response to a predation threat: larvae of the dragonfly Aeshna nigroflava induce heightened tail depth, whereas larval salamander Hynobius retardatus induce a bulgy morphology with heightened tail depth. Although both predators induce similar tail morphologies, it is possible that there are functional differences between these tail morphs.ResultsHere, we performed a discriminant microarray analysis using Xenopus laevis genome arrays to compare tail tissues of control and predator-exposed tadpoles. We identified 9 genes showing large-scale changes in their expression profile: ELAV-like1, methyltransferase like 7A, dolichyl-phosphate mannosyltransferase, laminin subunit beta-1, gremlin 1, BCL6 corepressor-like 1, and three genes of unknown identity. A further 80 genes showed greater than 5 fold differences in expression after exposure to dragonfly larvae and 81 genes showed altered expression after exposure to larval salamanders. Predation-threat responsive genes were identified by selecting genes that reverted to control levels of expression following removal of the predator. Thirteen genes were induced specifically by dragonfly larvae, nine others were salamander-specific, and sixteen were induced by both. Functional analyses indicated that some of the genes induced by dragonfly larvae caused an increase in laminins necessary for cell adhesion in the extracellular matrix. The higher expression of gremlin 1 and HIF1a genes after exposure to dragonfly larvae indicated an in vivo hypoxic reaction, while down-regulation of syndecan-2 may indicate impairment of angiogenesis. Exposure to larval salamanders caused down-regulation of XCIRP-1, which is known to inhibit expression of adhesion molecules; the tadpoles showed reduced expression of cα(E)-catenin, small muscle protein, dystrophin, and myosin light chain genes.ConclusionThe connective tissue of tadpoles exposed to larval salamanders may be looser. The differences in gene expression profiles induced by the two predators suggest that there are functional differences between the altered tail tissues of the two groups of tadpoles.Electronic supplementary materialThe online version of this article (doi:10.1186/s12864-015-1389-4) contains supplementary material, which is available to authorized users.
Highlights
Rana pirica tadpoles show morphological changes in response to a predation threat: larvae of the dragonfly Aeshna nigroflava induce heightened tail depth, whereas larval salamander Hynobius retardatus induce a bulgy morphology with heightened tail depth
Tadpoles with the dragonfly-induced higher tail morphology are less vulnerable to predation by larval salamanders than non-induced tadpoles, indicating that the higher tail phenotype has adaptive advantages compared to other phenotypes under conditions of salamander and dragonfly predation [17]
A larger functional species-specific microarray (3 k array) was prepared in the previous study [29] and used in induction-reversion experiments to analyze mRNAs extracted from the facial tissues of tadpoles. These analyses identified a novel uromodulin-like gene, pirica, that was increasingly up-regulated as the period of exposure to larval salamanders lengthened
Summary
Rana pirica tadpoles show morphological changes in response to a predation threat: larvae of the dragonfly Aeshna nigroflava induce heightened tail depth, whereas larval salamander Hynobius retardatus induce a bulgy morphology with heightened tail depth. Both predators induce similar tail morphologies, it is possible that there are functional differences between these tail morphs. R. pirica presumably evolved phenotypic plasticity in tadpoles as a defense against specific predators: the inducible bulgy body with heightened tail against larval salamanders and the heightened tail morph against the larvae of the dragonfly Aeshna nigroflava. In the presence of dragonfly risk cues, tadpoles with a bulgy morph and heightened tail induced by an earlier exposure to a salamander reduce only the bulgy body but retain the heightened tail [23]
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