Effects of thermal and oxygen conditions during development on cell size in the common rough woodlice Porcellio scaber

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.

Genome Size Covaries More Positively with Propagule Size than Adult Size: New Insights into an Old Problem

“…Most of these studies involve testing whether the effects of temperature on body size relate to changes in the sizes of somatic cells, reproductive propagules, or offspring. A common finding in ectothermic organisms is that decreasing temperature is associated with not only larger adult body size (following the ‘temperature-size rule’ [ 260 ]), but also significantly larger cells, propagules and (or) offspring (e.g., [ 103 , 218 , 219 , 248 , 250 , 252 , 261 , 262 , 263 , 264 , 265 , 266 , 267 , 268 , 269 , 270 , 271 , 272 , 273 , 274 , 275 , 276 , 277 , 278 , 279 , 280 , 281 , 282 , 283 , 284 , 285 , 286 , 287 , 288 , 289 ]). These studies provide further evidence that the sizes of somatic cells and reproductive propagules tend to be positively correlated (as illustrated in Figure 5 ).…”

Systemic orchestration of cell size throughout the body: influence of sex and rapamycin exposure in Drosophila melanogaster

“…Rapamycin administration to D. melanogaster larvae has been shown to delay development and lead to smaller adult flies and smaller cells [ 29 , 49 , 50 ], but it remains unclear how, if at all, modulation of TOR activity orchestrates cell sizes in different tissues and organs in the body. Additionally, such systemic control may not occur, as emerging (but still fragmentary) evidence in snails [ 51 ], geckos [ 25 ] and woodlice [ 39 ] indicates irregularities in cell-size changes in different tissues. Importantly, previous studies on the effects of rapamycin in flies have typically focused on larvae directly exposed to rapamycin and examined only single cell types (but see [ 52 , 53 ]).…”

Systemic orchestration of cell size throughout the body: Influence of sex and rapamycin exposure inDrosophila melanogaster

“…Coupling between body size and cell size has been reported by previous studies [7,24,26,28,51,59], although this evidence was largely based on the measurements of single cell types (but see [8]). Systemic coordination of cell-size changes has been suggested by some interspecies [8,12,24,38,42] and intraspecies [20,[39][40][41] comparisons, but until now, never demonstrated experimentally by manipulating the activity of cell-cycle regulatory pathways. Emerging evidence of the involvement of cell-cycle control in sex determination in D. melanogaster suggests that this control system includes autonomous regulation of cell size, which in females, but not in males, is additionally associated with a systemic signalling network via TOR/insulin pathways [43,60,61].…”

“…Rapamycin administration to D. melanogaster larvae has been shown to lead to smaller adult flies and smaller cells [29,49,50], but it remains unclear how, if at all, modulation of TOR activity orchestrates cell sizes in different tissues and organs in the body. Additionally, such systemic control may not occur, as emerging (but still fragmentary) evidence in snails [51], geckos [25] and woodlice [39] indicates irregularities in cell-size changes in different tissues. Importantly, previous studies on the effects of rapamycin in flies have typically focused on larvae directly exposed to rapamycin and examined only single cell types and only cells that lose viability after fly metamorphosis (i.e., larval epidermal cells, which are responsible for the production of exoskeleton elements in adults).…”