Are acute and acclimated thermal effects on metabolic rate modulated by cell size? a comparison between diploid and triploid zebrafish larvae

Abstract

Being composed of small cells may carry energetic costs related to maintaining ionic gradients across cell membranes as well as benefits related to diffusive oxygen uptake. Here we test the hypothesis that these costs and benefits of cell size in ectotherms are temperature dependent. To study the consequences of cell size for whole-organism metabolic rate we compared diploid and triploid zebrafish larvae differing in cell size. A fully factorial design was applied combining three different rearing and test temperatures that allowed us to distinguish acute from acclimated thermal effects. Individual oxygen consumption rates of diploid and triploid larvae across declining levels of oxygen availability were measured. We found that both acute and acclimated thermal effects affected the metabolic response. In comparison to triploids, diploids responded more strongly to acute temperatures, especially when reared at the highest temperature. These observations support the hypothesis that animals composed of smaller cells (i.e. diploids) are less vulnerable to oxygen limitation in warm aquatic habitats. Furthermore, we found slightly improved hypoxia tolerance in diploids. By contrast, warm-reared triploids had higher metabolic rates when they were tested at acute cold temperature, suggesting that being composed of larger cells may provide metabolic advantages in the cold. We offer two mechanisms as a potential explanation of this result, related to homeoviscous adaptation of membrane function and the mitigation of developmental noise. Our results suggest that being composed of larger cells provides metabolic advantages in cold water, while being composed of smaller cells provides metabolic advantages in warm water.

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

“…As predicted, interspecific analyses often show that mass-specific metabolic rate is negatively related to genome size [ 8 , 118 , 205 , 238 , 253 , 256 , 257 , 320 , 325 , 326 , 327 , 328 , 329 ] (but see [ 330 ]). However, intraspecific tests in animals comparing polyploids with diploids have shown that increasing ploidy more often has no effect on metabolic rate than negative effects, and sometimes positive effects have even been observed (reviewed in [ 331 , 332 , 333 , 334 ]; also see [ 335 , 336 ]), as also seen for rates of photosynthesis in plants (e.g., [ 195 , 201 , 293 , 333 ]). Differences in metabolic rate between polypoid and diploid animals may be temperature-dependent [ 334 , 335 , 336 ].…”

“…However, intraspecific tests in animals comparing polyploids with diploids have shown that increasing ploidy more often has no effect on metabolic rate than negative effects, and sometimes positive effects have even been observed (reviewed in [ 331 , 332 , 333 , 334 ]; also see [ 335 , 336 ]), as also seen for rates of photosynthesis in plants (e.g., [ 195 , 201 , 293 , 333 ]). Differences in metabolic rate between polypoid and diploid animals may be temperature-dependent [ 334 , 335 , 336 ]. In addition, some studies have shown that, although metabolic rate and its scaling with body mass relate to variation in cell size, they do not relate to variation in genome size [ 337 , 338 ].…”

“…For example, in resource-poor and other kinds of stressful environments, increased sizes of cells and propagules and lower rates of growth, development and metabolism may all be advantageous responses (see, e.g., [ 101 , 253 , 300 , 309 , 357 ]). Perhaps this is why organisms with large genome sizes (including polyploids) often occur in stressful environments (e.g., [ 103 , 193 , 194 , 195 , 287 , 293 , 336 , 358 , 359 ]).…”

Thermal and Oxygen Flight Sensitivity in Ageing Drosophila melanogaster Flies: Links to Rapamycin-Induced Cell Size Changes

“…Here, we hypothesize that the cellular architecture of tissue and organs can help ectotherms meet their metabolic demands via the oxygen supply in response to environmental conditions and organismal activity. Following Antoł et al [ 29 ], our study uses a conceptual framework integrating earlier hypotheses about fitness costs and benefits associated with cell size differences among organisms that we refer to as the theory of optimal cell size (TOCS) ([ 30 , 31 , 32 , 33 , 34 , 35 , 36 , 37 , 38 , 39 , 40 , 41 , 42 ]; see also a recent review by Kozłowski et al [ 43 ]). According to TOCS, the life history strategies of organisms involve different developmental cellular mechanisms that ultimately decide whether a body consists of many small cells or fewer large cells, which should have vital effects on physiology.…”

Early, nonlethal ploidy and genome size quantification using confocal microscopy in zebrafish embryos

“…Such studies have shown that triploid fish are less able to tolerate environmental conditions that impose physiological challenges on conspecific diploids (e.g., Hyndman et al, 2003; Ojolick et al, 1995; Verhille et al, 2013), which has prevented the wide‐scale adoption of this technology. However, there has been a resurgence of interest in assessing triploid salmonid fishes for use in aquaculture due to improvements in our understanding of their thermal (Riseth et al, 2020; Sambraus et al, 2018; Verhille et al, 2013) and hypoxia tolerance (Benfey & Devlin, 2018; Hansen et al, 2015; Hermaniuk et al, 2021; Sambraus et al, 2017; Scott et al, 2014), and dietary requirements (Sambraus et al, 2020). Despite these advances in understanding the biology of triploid salmonids, they are slow‐growing, cold‐water fish with a long generation time (~3 years) making them a rather impractical model organism.…”