Abstract
During development, cells may adjust their size to balance between the tissue metabolic demand and the oxygen and resource supply: Small cells may effectively absorb oxygen and nutrients, but the relatively large area of the plasma membrane requires costly maintenance. Consequently, warm and hypoxic environments should favor ectotherms with small cells to meet increased metabolic demand by oxygen supply. To test these predictions, we compared cell size (hindgut epithelium, hepatopancreas B cells, ommatidia) in common rough woodlice (Porcellio scaber) that were developed under four developmental conditions designated by two temperatures (15 or 22°C) and two air O2 concentrations (10% or 22%). To test whether small‐cell woodlice cope better under increased metabolic demand, the CO2 production of each woodlouse was measured under cold, normoxic conditions and under warm, hypoxic conditions, and the magnitude of metabolic increase (MMI) was calculated. Cell sizes were highly intercorrelated, indicative of organism‐wide mechanisms of cell cycle control. Cell size differences among woodlice were largely linked with body size changes (larger cells in larger woodlice) and to a lesser degree with oxygen conditions (development of smaller cells under hypoxia), but not with temperature. Developmental conditions did not affect MMI, and contrary to predictions, large woodlice with large cells showed higher MMI than small woodlice with small cells. We also observed complex patterns of sexual difference in the size of hepatopancreatic cells and the size and number of ommatidia, which are indicative of sex differences in reproductive biology. We conclude that existing theories about the adaptiveness of cell size do not satisfactorily explain the patterns in cell size and metabolic performance observed here in P. scaber. Thus, future studies addressing physiological effects of cell size variance should simultaneously consider different organismal elements that can be involved in sustaining the metabolic demands of tissue, such as the characteristics of gas‐exchange organs and O2‐binding proteins.
Highlights
Oxygen supply is typically considered a potential limiting factor for aquatic organisms (Bonvillain, Rutherford, & Kelso, 2015; Czarnoleski, Ejsmont-Karabin, Angilletta, & Kozlowski, 2015; Hoefnagel & Verberk, 2015; Kiełbasa, Walczyńska, Fiałkowska, Pajdak-Stós, & Kozłowski, 2014; Verberk et al, 2016; Walczyńska, Labecka, Sobczyk, Czarnoleski, & Kozłowski, 2015; Woods, 1999)
The results of the general linear models (GLMs) for ommatidia number (Table 3, Figure 5) showed that the number of ommatidia in the eye increased with woodlouse body mass (p = .01), animals reared in warm conditions had more ommatidia than animals reared in cold conditions (p < .001), females tended to have more ommatidia than males (p = .09), and animals reared in hypoxia tended to have more ommatidia than animals reared in normoxia (p = .06)
For P. scaber studied here, we found that the number of ommatidia increased in the eyes of larger woodlice, indicating that changes in cell number together with cell size contributed to changes in the size of eyes and possibly in the body size of woodlice
Summary
Oxygen supply is typically considered a potential limiting factor for aquatic organisms (Bonvillain, Rutherford, & Kelso, 2015; Czarnoleski, Ejsmont-Karabin, Angilletta, & Kozlowski, 2015; Hoefnagel & Verberk, 2015; Kiełbasa, Walczyńska, Fiałkowska, Pajdak-Stós, & Kozłowski, 2014; Verberk et al, 2016; Walczyńska, Labecka, Sobczyk, Czarnoleski, & Kozłowski, 2015; Woods, 1999). Following TOCS, we predicted that the cell size of woodlice would generally decrease in response to either elevated metabolic demands (warm) or lowered oxygen supply (hypoxia), and we expected that this effect would be more pronounced under combined warm and hypoxic conditions (hypothesis 1). Before we sampled tissues for the determination of cell size, we assessed the capacity of each animal to meet increased metabolic demand under poor oxygen supply For this purpose, we measured the magnitude of a metabolic increase, following a transfer of each woodlouse from cool and normoxic conditions to warm and hypoxic conditions. One could expect cell size differences among different cell types, addressing this possibility among the studied tissues was beyond the scope of our study, since differences in cell physiology among tissues could be largely attributed to function-related properties of cells, such as their shape (neurons vs. epithelial cells) or organellular content
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