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

Abstract

Cell 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.

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

“…Increasing temperature tends to be associated with smaller cell sizes in a variety of organisms (reviewed in [61,62]; also see [63][64][65][66][67][68]). 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].…”

Variability in vertebral numbers does not contribute to sexual size dimorphism, interspecific variability, or phenotypic plasticity in body size in geckos (Squamata: Gekkota: Paroedura)

“…We split the eggs from a single female across each temperature in order to provide an equal genetic background. The details and other results of this complex experiment have been published elsewhere (Czarnoleski et al., ; Kubička et al., ; Starostová et al., , ; Weiser, Starostová, Kubička, & Kratochvíl, ). Briefly, we obtained eggs from 20 P. picta females maintained under common conditions and incubated them in thermal cabinets with a 12 h light:12 h dark cycle at one of three temperatures (± 0.3°C).…”

“…As the final SVL was highly correlated with the asymptotic SVL across all individuals (Pearson's correlation coefficient r = 0.98, P < 0.0001, n = 95) and the mean difference between final SVL and asymptotic SVL estimated for each individual was only 3.6%, we used final SVL throughout our analyses. When the animals reached a SVL close to their asymptotic SVL at a given temperature, they were euthanized by decapitation, their tissues were examined and stored for future studies (Czarnoleski et al., ; Starostová et al., ; Weiser et al., ) and the carcasses were frozen. Temperature strongly affected the final/asymptotic body size and SSD.…”

“…Final/asymptotic body size is affected by incubation or rearing temperatures in both sexes, but males exhibited larger temperature‐induced phenotypic plasticity in size than females (Starostová et al., ). Previously, we documented in geckos, including P. picta , that both interspecific and intraspecific changes in body size, including SSD, are connected with correlated changes of cell size in some, but not all cell types (Czarnoleski et al., ; Starostová, Kratochvíl, & Frynta, ; Starostová, Kozlowski, Konarzewski, & Kratochvíl, ). These results mean that alterations in body size are correlated with changes of both size and number of at least some basic organismal units.…”

“…We split the eggs from a single female across each temperature in order to provide an equal genetic background. The details and other results of this complex experiment have been published elsewhere (Czarnoleski et al, 2017;Kubička et al, 2012;Starostová et al, 2010Starostová et al, , 2012Weiser, Starostová, Kubička, & Kratochvíl, 2012).…”