Not all cells are equal: effects of temperature and sex on the size of different cell types in the Madagascar ground gecko Paroedura picta.

Marcin Czarnoleski,Anna Maria Labecka,Jan Kozlowski,Lukáš Kratochvíl,Elżbieta Bonda-Ostaszewska,Katarzyna Woch,Anna Sikorska,Zuzana Starostová,Lukáš Kubička

doi:10.1242/bio.025817

Marcin Czarnoleski, Anna Maria Labecka + Show 7 more

Open Access

https://doi.org/10.1242/bio.025817

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Abstract

ABSTRACTCell size plays a role in evolutionary and phenotypically plastic changes in body size. To examine this role, we measured the sizes of seven cell types of geckos (Paroedura picta) reared at three constant temperatures (24, 27, and 30°C). Our results show that the cell size varies according to the body size, sex and developmental temperature, but the pattern of this variance depends on the cell type. We identified three groups of cell types, and the cell sizes changed in a coordinated manner within each group. Larger geckos had larger erythrocytes, striated muscle cells and hepatocytes (our first cell group), but their renal proximal tubule cells and duodenal enterocytes (our second cell group), as well as tracheal chondrocytes and epithelial skin cells (our third cell group), were largely unrelated to the body size. For six cell types, we also measured the nuclei and found that larger cells had larger nuclei. The relative sizes of the nuclei were not invariant but varied in a complex manner with temperature and sex. In conclusion, we provide evidence suggesting that changes in cell size might be commonly involved in the origin of thermal and sexual differences in adult size. A recent theory predicts that smaller cells speed up metabolism but demand more energy for their maintenance; consequently, the cell size matches the metabolic demand and supply, which in ectotherms, largely depends on the thermal conditions. The complex thermal dependency of cell size in geckos suggests that further advancements in understanding the adaptive value of cell size requires the consideration of tissue-specific demand/supply conditions.

Highlights

The body size achieved at maturation has fundamental effects on the evolutionary fitness of an organism (Ejsmond et al, 2015; Kozlowski, 1992, 2006; Stearns, 1992)
Table S1 reports the means of raw values of body size, cell size and nuclei size in each group of geckos
The cell size within a given cell type varied considerably among individual geckos. Integrating this variance with data on body size, our factor analysis extracted three components, which together accounted for the 68% of the variance in the data (Table 1), showing that cell types clustered into three groups

Summary

INTRODUCTION

The body size achieved at maturation has fundamental effects on the evolutionary fitness of an organism (Ejsmond et al, 2015; Kozlowski, 1992, 2006; Stearns, 1992). As suggested by the theory of optimal cell size (TOCS), changes in cell number and cell size may not have equal fitness consequences, and the ultimate size of cells in organs results from a compromise between costs and benefits (Czarnoleski et al, 2015b; Davison, 1956; Kozlowski et al, 2003; Szarski, 1983) Following this theory, a body composed of many small cells is rich in cell membranes because with the decreasing volume of single cells, the total surface area of cells increases. Following Maciak et al (2014), we expected invariance in the relative sizes of nuclei in cell types with high levels of anabolic activity but not in other cell types

RESULTS

DISCUSSION

MATERIALS AND METHODS