Being composed of small cells may carry energetic costs related to maintaining ionic gradients across cell membranes as well as benefits related to diffusive oxygen uptake. Here we test the hypothesis that these costs and benefits of cell size in ectotherms are temperature dependent. To study the consequences of cell size for whole-organism metabolic rate we compared diploid and triploid zebrafish larvae differing in cell size. A fully factorial design was applied combining three different rearing and test temperatures that allowed us to distinguish acute from acclimated thermal effects. Individual oxygen consumption rates of diploid and triploid larvae across declining levels of oxygen availability were measured. We found that both acute and acclimated thermal effects affected the metabolic response. In comparison to triploids, diploids responded more strongly to acute temperatures, especially when reared at the highest temperature. These observations support the hypothesis that animals composed of smaller cells (i.e. diploids) are less vulnerable to oxygen limitation in warm aquatic habitats. Furthermore, we found slightly improved hypoxia tolerance in diploids. By contrast, warm-reared triploids had higher metabolic rates when they were tested at acute cold temperature, suggesting that being composed of larger cells may provide metabolic advantages in the cold. We offer two mechanisms as a potential explanation of this result, related to homeoviscous adaptation of membrane function and the mitigation of developmental noise. Our results suggest that being composed of larger cells provides metabolic advantages in cold water, while being composed of smaller cells provides metabolic advantages in warm water.

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.

Previous studies reported that low temperatures result in increases in both cell size and body size in ectotherms that may explain patterns of geographic variation of their body size across latitudinal ranges. Also, polyploidy showed the same effect on body size in invertebrates. In vertebrates, despite their having larger cells, no clear effect of polyploidy on body size has been found. This article presents the relationship between temperature, cell size, growth rate, and body size in diploid and polyploid hybridogenetic frog Pelophylax esculentus reared as tadpoles at 19° and 24°C. The size of cells was larger in both diploid and triploid tadpoles at 19°C, and triploids had larger cells at both temperatures. In diploid and triploid froglets, the temperature in which they developed as tadpoles did not affect the size of their cells, but triploids still had larger cells. Triploid tadpoles grew faster than diploids at 19°C and had larger body mass; there was no clear difference between ploidies in growth rate at 24°C. This indicates better adaptation of triploid tadpoles to cold environment. This is the first report on the increase of body mass of a polyploid vertebrate caused by low temperature, and we showed relationship between increase in cell size and increased body mass. The large body mass of triploids may provide a selective advantage, especially in colder environments, and this may explain the prevalence of triploids in the northern parts of the geographic range of P. esculentus.

No abstract

No abstract