Metabolic Rate of Diploid and Triploid Edible FrogPelophylax esculentusCorrelates Inversely with Cell Size in Tadpoles but Not in Frogs

Abstract

In multicellular organisms, cell size may have crucial consequences for basic parameters, such as body size and whole-body metabolic rate (MR). The hypothesis predicts that animals composed of smaller cells (a higher membrane surface-to-cell volume ratio) should have a higher mass-specific MR because a large part of their energy is used to maintain cell membranes and ionic gradients. In this article, we investigated the link between cell size and MR in diploid and triploid tadpoles and froglets of the hybridogenetic frog Pelophylax esculentus. In our previous study, we showed that triploids had significantly larger cells (erythrocytes, hepatocytes, and epidermal cells were measured). Therefore, we hypothesized that triploid tadpoles and froglets would have a lower standard metabolic rate (SMR). Our study demonstrated for the first time two distinct effects of polyploidy/cell size on MR within a single species developing in both aquatic and terrestrial habitats. As we hypothesized, diploid tadpoles had a higher SMR than triploids, whereas in froglets, ploidy did not affect the SMR. We also found that the water temperatures in which tadpoles were reared had no effect on the SMR of froglets after metamorphosis. Based on our results and other reports, we suggest that cell size may have more consequences for whole-body MR in aquatic habitats than in terrestrial habitats because oxygen is less available in water and its availability in relation to oxygen demand decreases with temperature.

Effects of Contingency versus Constraints on the Body-Mass Scaling of Metabolic Rate

“…Small cells (and organisms containing them) tend to have higher mass-specific metabolic rates than large cells (and organisms containing them) [26,[69][70][71][72][73][74][75][76][77]. Therefore, like the MTE, cell-size theory predicts that changing temperature should affect the elevation of metabolic scaling relationships, but not their slopes (but see Section 3.2.2), which again is contradicted by the results described in this study.…”

Rediscovering and Reviving Old Observations and Explanations of Metabolic Scaling in Living Systems

“…Since that time, many investigators have discussed the cell-size model, including providing additional theoretical formulations, conceptual justifications, and empirical tests [19,20,56,97,105,106,130,[143][144][145][146][147][148]. However, so far the model has received mixed empirical support [19,20,97,105,106,[139][140][141][142][143]145,[149][150][151][152][153][154][155].…”

“…In any case, tests of the identical predictions of the SA and RT versions of the cell-size model have produced mixed support (see Section 2.2.1). Most support comes from scaling analyses at the intraspecific (ontogenetic) level (the focal level of the RT model [130]; but see [152,155]), whereas support at the interspecific level is weaker. For example, although cell-size models correctly predict the hypometric (negatively allometric) scaling (slope~0.75) among species of insects [145], they do not for mammals.…”

Cell size control – a mechanism for maintaining fitness and function

“…This suggests that maintaining a specific cell size may be more beneficial (or at least easier) than to generate large organisms by increasing cell size. More recently, comparisons of diploid and triploid animals has revealed that especially in aquatic environments triploid animals tend to have a reduced metabolic rate, despite maintaining same organismal size [60], suggesting a potential fitness disadvantage for abnormally large cell size. These animals can be fully polyploid or may contain polyploid cells in otherwise normal diploid tissue.…”