From cells to colonies: at what levels of body organization does the ‘temperature‐size rule’ apply?

Abstract

An inverse relationship between temperature during ontogeny and final body size is widespread in ectotherms, but poorly understood. Evidence suggests that within organs, this "temperature-size rule" (TSR) may also apply to cell size with no change in numbers. So how closely do reductions in size and number of cells and other repeated structures correlate with size reduction at higher levels of organization? We examine this in the context of a proposal that size and/or number changes at various organizational levels are adaptive responses to temperature- and size-dependent oxygen supply. We subjected two clones of the modular colonial bryozoan, Celleporella hyalina, to orthogonal combinations of two temperatures and two oxygen concentrations during ontogeny, observing effects on sizes of colonies and larvae, and sizes and numbers of cells, tentacles, and modules (autozooids). We found that the size:number responses varied among cell types and among structures at different levels of organization, with the inverse temperature-size relationship applying only to larval parenchymal cells and colony modules. Using our findings and other evidence we propose a unifying adaptive hypothesis that predicts how temperature affects the sizes of mitochondria, cells, organs, modules and organisms, and their relationships with processes that determine the functional capacity of aerobic metabolism.

The underestimated role of temperature–oxygen relationship in large‐scale studies on size‐to‐temperature response

“…One of the most promising suggestions states that the TSR evolved to optimize the temperature‐dependent oxygen demand and supply. This idea was conceptualized in two hypotheses, the MASROS (Maintaining Aerobic Scope by Regulating Oxygen Supply; Atkinson, Morley, & Hughes, 2006) and OCLTT (Oxygen‐ and Capacity‐Limited Thermal Tolerance; Poertner, 2010). According to both hypotheses, the steeper increase of oxygen demands than of oxygen supply with increasing temperature reduces the range of possible aerobic metabolism (=aerobic scope).…”

“…The ectotherms apply certain performance to prevent this damaging process. The MASROS hypothesis refers directly to temperature‐dependent size response to such oxygen limitations; the reduction in size increases the diffusive surface relative to size and, in consequence, improves the oxygen consumption (Atkinson et al., 2006). …”

Flies evolved small bodies and cells at high or fluctuating temperatures

“…An emerging theory holds that cell size evolves according to a trade‐off between the capacity for and the efficiency of metabolism (Atkinson, Morley, & Hughes, 2006; Czarnoleski, Dragosz‐Kluska, & Angilletta, 2015; Czarnoleski et al., 2013; Kozłowski, Konarzewski, & Gawelczyk, 2003; Szarski, 1983). The optimal size balances the benefit of acquiring resources quickly against the cost of keeping membranes operational.…”

Equal temperature–size responses of the sexes are widespread within arthropod species

“…This intra-specific phenotypically plastic response commonly leads to a reduction in size-atstage with warming and has been called the temperature-size rule (TSR) [20]. Given the ubiquity of the TSR in taxonomic groups as diverse as bacteria, protists and metazoans [22,24,25], the proximate and ultimate causes have been explored in some detail [22,[25][26][27][28][29]. The temperature-body size (T-S) response has been shown to vary in magnitude in relation to species body size, voltinism and taxonomic group, and between aquatic and terrestrial-living species [22,23].…”