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In multicellular organisms, cell size may have crucial consequences for basic parameters, such as body size and whole-body metabolic rate (MR). The hypothesis predicts that animals composed of smaller cells (a higher membrane surface–to–cell volume ratio) should have a higher mass-specific MR because a large part of their energy is used to maintain...
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Comparison of reproductive parameters in several Cobitis forms with different ploidy shows that the maximum fertility is found in diploid Cobitis, the triploids are less fertile and the tetraploids even less fecund. The latter reach maximum values of size and weight indicators but minimum number of eggs, the smallest size of the ovaries but the big...
Induced polyploidy has been identified for yellow croaker P. crocea at various deve lopmental stages and with various t issues during 2001~ 2004. Ploidy levels from eyed embryos were determined by chromosome counts. Ploidy analyses of fish juveniles and adults were implemented using flowcytometry. The results indicated that chromosomal number of di...
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... A negative correlation between genome size and BMR has been observed across all of Lissamphibia, but not when Anura and Caudata are considered independently (Gregory, 2003). In addition, AMR and genome size are negatively correlated in some salamanders, but only at stress-inducing temperatures (Licht & Lowcock, 1991), and ploidy level and AMR are negatively correlated in tadpoles but not froglets of the hybridogenetic frog Pelophylax esculentus (Hermaniuk et al., 2017). Finally, genome size does not appear to be associated with evolutionary saltations in BMR across extant vertebrates (Gardner et al., 2020), although there are exceptions in certain mammalian lineages (Uyeda et al., 2017). ...
Adaptive and neutral processes have produced a spectrum of genome sizes across organisms. Amphibians in particular possess a wide range in C-values, from <1 to over 125 pg. However, the genome size of most amphibians is unknown, and no single family has been comprehensively assessed. We provide new estimates for 32 poison frog species representing the major lineages within Dendrobatidae using Feulgen staining of museum specimens and flow cytometry of fresh tissue. We show that genome size in Dendrobatidae has likely evolved gradually, with potential evolutionary rate shifts in the genera Phyllobates and Hyloxalus, which respectively possess species with the largest (13.0 pg) and second smallest (2.6 pg) genomes in the family. Phylogenetically controlled regression analyses indicate that genome size is positively correlated with snout-vent-length, oocyte number, and clutch size, but negatively correlated with active metabolic rate and metabolic scope. While body size and metabolic rate are also correlates of toxicity, we found no relationship between genome size and evolution of chemical defense within Dendrobatidae. Genome size evolution in Dendrobatidae provides insight into the processes shaping genome size evolution over short timescales and establishes a novel system in which to study the mechanistic links between genome size and organismal physiology.
... Mean cell size varies within and among species (Arendt, 2007;Chown et al., 2007;Czarnoleski et al., 2017;Czarnoleski et al., 2018;Glazier et al., 2013;Kierat et al., 2017;Schramm et al., 2021;Stevenson et al., 1995;Walczyńska and Sobczyk, 2017), but the relationship between the sizes of an organism's cells and its performance across different environments has been understudied (but see: Szlachcic and Czarnoleski, 2021;Verberk et al., 2022;Walczyńska et al., 2015). According to the theory of optimal cell size (TOCS), the cellular composition of an organism is not a functionally neutral characteristic; rather, the size of a cell affects physiological costs and benefits that depend on energy supply and demand (Atkinson et al., 2006;Czarnoleski et al., 2013;Davison, 1956;Hermaniuk et al., 2017;Kozłowski et al., 2003;Kozłowski et al., 2020;Miettinen et al., 2017;Szarski, 1983;Verberk et al., 2022;Woods, 1999). Whether an organism is ectothermic or endothermic, its metabolic demands and resource supply strongly depend on temperature, oxygen, food and water, as well as metabolically demanding activities, such as flight or growth. ...
Environmental gradients cause evolutionary and developmental changes in the cellular composition of organisms, but the physiological consequences of these effects are not well understood. Here, we studied experimental populations of Drosophila melanogaster that had evolved in one of three selective regimes: constant 16 °C, constant 25 °C, or intergenerational shifts between 16 °C and 25 °C. Genotypes from each population were reared at three developmental temperatures (16 °C, 20.5 °C, and 25 °C). As adults, we measured thorax length and cell sizes in the Malpighian tubules and wing epithelia of flies from each combination of evolutionary and developmental temperatures. We also exposed flies from these treatments to a short period of nearly complete oxygen deprivation to measure hypoxia tolerance. For genotypes from any selective regime, development at a higher temperature resulted in smaller flies with smaller cells, regardless of the tissue. At every developmental temperature, genotypes from the warm selective regime had smaller bodies and smaller wing cells but had larger tubule cells than did genotypes from the cold selective regime. Genotypes from the fluctuating selective regime were similar in size to those from the cold selective regime, but their cells of either tissue were the smallest among the three regimes. Evolutionary and developmental treatments interactively affected a fly’s sensitivity to short-term paralyzing hypoxia. Genotypes from the cold selective regime were less sensitive to hypoxia after developing at a higher temperature. Genotypes from the other selective regimes were more sensitive to hypoxia after developing at a higher temperature. Our results show that thermal conditions can trigger evolutionary and developmental shifts in cell size, coupled with changes in body size and hypoxia tolerance. These patterns suggest links between the cellular composition of the body, levels of hypoxia within cells, and the energetic cost of tissue maintenance. However, the patterns can be only partially explained by existing theories about the role of cell size in tissue oxygenation and metabolic performance.
... В ходе проведенных исследований отмечены гистотопографические особенности в организации печеночной ткани, которые оказывают влияние на функционирование печени амфибий вида Rana terrestris как организма с эктотермной терморегуляцией, функционирующего в условиях пониженного парциального давления O 2 в крови, со сформированными в ходе эво-люции адаптациями к быстрой реоксигенации, а также большим размером генома. Концентрация O 2 может быть ограничивающим фактором для клеток большого размера, таких, например, как гепатоциты у организмов с водной средой обитания по сравнению с организмами с наземной средой обитания [49]. Учитывая, что метаболическая активность является важным фактором успешности адаптации позвоночных к среде обитания, такая естественная физиологическая адаптация, когда гипоксическое состояние резко сменяется гипероксическим вследствие реоксигенации [50,51], поддерживается за счет катаболизма липидов в качестве источников энергии. ...
The liver plays an essential role in the metabolism of animals, acting as a central hub for metabolic reactions. It serves as a “peripheral integrator” and balances the body’s energy needs. Its regenerative capacity is remarkably high and is maintained by the proliferation of hepatocytes, as well as hematopoietic and regional liver progenitor cells (LPC). This study investigated LPC-driven liver regeneration during postembryonic development in Rana terrestris under normal physiological conditions. The analysis of intrahepatic and hematopoietic markers by immunohistochemistry and flow cytometry revealed that progenitor cells with the immunophenotypes of CK19+ (intrahepatic progenitor cells), CD34+CD45+ (hematopoietic progenitor cell population), and CD34+CD45– (hemangioblast population) equally promote liver regeneration during the first year of postembryonic development. However, in the second and third years of postembryonic development, liver regeneration was found to be primarily associated with CK19+-positive cells, with a smaller contribution from CD34+CD45– cells. The results obtained were largely determined by the habitat of the amphibians, thermoregulation, and the completion of morphogenetic processes in the third year of postembryonic development. It is also noteworthy that the liver of the examined specimens remained the major hematopoietic organ throughout all observed stages of postembryonic development.
... Several studies have shown the relationship between ploidy, cell size, and cellular metabolic rate [88][89][90]. Studies of artificially induced polyploid animals such as frogs and fish also have shown that the whole-body metabolic rate is lower in both larvae and adults [91,92]. Recently, a study using Xenopus embryos and tadpoles with different ploidy showed that ploidy affects metabolism by altering the cell surface area to volume ratio when cell size correlates with genome size [89]. ...
Cells with an abnormal number of chromosomes have been found in more than 90% of solid tumors, and among these, polyploidy accounts for about 40%. Polyploidized cells most often have duplicate centrosomes as well as genomes, and thus their mitosis tends to promote merotelic spindle attachments and chromosomal instability, which produces a variety of aneuploid daughter cells. Polyploid cells have been found highly resistant to various stress and anticancer therapies, such as radiation and mitogenic inhibitors. In other words, common cancer therapies kill proliferative diploid cells, which make up the majority of cancer tissues, while polyploid cells, which lurk in smaller numbers, may survive. The surviving polyploid cells, prompted by acute environmental changes, begin to mitose with chromosomal instability, leading to an explosion of genetic heterogeneity and a concomitant cell competition and adaptive evolution. The result is a recurrence of the cancer during which the tenacious cells that survived treatment express malignant traits. Although the presence of polyploid cells in cancer tissues has been observed for more than 150 years, the function and exact role of these cells in cancer progression has remained elusive. For this reason, there is currently no effective therapeutic treatment directed against polyploid cells. This is due in part to the lack of suitable experimental models, but recently several models have become available to study polyploid cells in vivo. We propose that the experimental models in Drosophila, for which genetic techniques are highly developed, could be very useful in deciphering mechanisms of polyploidy and its role in cancer progression.
... Emerging evidence reveals variance in cell size within and between species [19][20][21][22][23][24], but the association of this variance with the metabolic performance of organisms across environments is poorly studied (but see [25][26][27]). Nevertheless, the theory of optimal cell size (TOCS) [23,[27][28][29][30][31][32][33][34][35] considers that the cellular composition of an organism brings metabolic consequences with evolutionary costs and benefits, which vary along with environmental gradients in metabolic demand and supply. On the one hand, small cells in the body bring metabolic costs, as they require additional molecular substrates (elements, organic compounds) and ATP for maintaining plasma membranes (membrane composition, ionic gradients on the cell surface). ...
Understanding metabolic performance limitations is key to explaining the past, present and future of life. We investigated whether heat tolerance in actively flying Drosophila melanogaster is modified by individual differences in cell size and the amount of oxygen in the environment. We used two mutants with loss-of-function mutations in cell size control associated with the target of rapamycin (TOR)/insulin pathways, showing reduced (mutant rictorΔ2) or increased (mutant Mnt¹) cell size in different body tissues compared to controls. Flies were exposed to a steady increase in temperature under normoxia and hypoxia until they collapsed. The upper critical temperature decreased in response to each mutation type as well as under hypoxia. Females, which have larger cells than males, had lower heat tolerance than males. Altogether, mutations in cell cycle control pathways, differences in cell size and differences in oxygen availability affected heat tolerance, but existing theories on the roles of cell size and tissue oxygenation in metabolic performance can only partially explain our results. A better understanding of how the cellular composition of the body affects metabolism may depend on the development of research models that help separate various interfering physiological parameters from the exclusive influence of cell size.
This article is part of the theme issue ‘The evolutionary significance of variation in metabolic rates’.
... Therefore, the evidence that body size, cell phenotypes, and cell-cycle controllers vary in unison among organisms provides a strong argument for the adaptive nature of this covariation. Following a theoretical framework, which we refer to as the theory of optimal cell size (TOCS), a change in cell size should bring physiological costs and benefits that balance differently with shifts in the metabolic demand and supply of resources and oxygen (Antoł et al., 2020;Atkinson et al., 2006;Czarnoleski et al., 2015b;Czarnoleski et al., 2018;Davison, 1955Davison, , 1956Glazier, 2022;Hermaniuk et al., 2017;Kozlowski et al., 2020;Kozlowski et al., 2003;Liu et al., 2022;Miettinen et al., 2017;Szarski, 1983;Szlachcic and Czarnoleski, 2021;Szlachcic et al., 2023a;Verspagen et al., 2020;Walczynska et al., 2015). Smaller cells offer larger cell surface areas for transport and communication, but at the same time require more molecular work to maintain plasma membranes and electro-chemical potentials. ...
Spatio-temporal gradients in thermal and oxygen conditions trigger evolutionary and developmental responses in ectotherms' body size and cell size, which are commonly interpreted as adaptive. However, the evidence for cell-size responses is fragmentary, as cell size is typically assessed in single tissues. In a laboratory experiment, we raised genotypes of Drosophila melanogaster at all combinations of two temperatures (16 °C or 25 °C) and two oxygen levels (10 % or 22%) and measured body size and the sizes of cells in different tissues. For each sex, we measured epidermal cells in a wing and a leg and ommatidial cells of an eye. For males, we also measured epithelial cells of a Malpighian tubule and muscle cells of a flight muscle. On average, females emerged at a larger body size than did males, having larger cells in all tissues. Flies of either sex emerged at a smaller body size when raised under warm or hypoxic conditions. Development at 25°C resulted in smaller cells in most tissues. Development under hypoxia resulted in smaller cells in some tissues, especially among females. Altogether, our results show thermal and oxygen conditions trigger shifts in adult size, coupled with the systemic orchestration of cell sizes throughout the body of a fly. The nature of these patterns supports a model in which an ectotherm adjusts its life-history traits and cellular composition to prevent severe hypoxia at the cellular level. However, our results revealed some inconsistencies linked to sex, cell type, and environmental parameters, which suggest caution in translating information obtained for single type of cells to the organism as a whole.
... A negative correlation between genome size and basal metabolic rate (BMR) has been observed multiple times in birds and mammals (Vinogradov 1995;Gregory 2002;Kozłowski et al. 2003), and a negative correlation between genome size and BMR has been observed across all of Lissamphibia, but not when Anura and Caudata are considered independently (Gregory 2003). In addition, AMR and genome size are negatively correlated in salamanders, but only at stress-inducing temperatures (Licht and Lowcock 1991) and ploidy level and AMR are negatively correlated in tadpoles but not froglets of the hybridogenetic frog Pelophylax esculentus (Hermaniuk et al. 2017). Finally, genome size does not appear to be associated with evolutionary saltations in BMR across extant vertebrates (Gardner et al. 2020), although there are exceptions in certain mammalian lineages (Uyeda et al. 2017). ...
Adaptive and neutral processes have produced a spectrum of genome sizes across organisms. Amphibians in particular possess a wide range in C-values, from <1 to over 125 pg. However, the genome size of most amphibians is unknown, and no single family has been comprehensively assessed. We provide new estimates for 32 poison frog species representing the major lineages within Dendrobatidae using Feulgen staining of museum specimens and flow cytometry of fresh tissue. We show that genome size in Dendrobatidae has likely evolved gradually, with potential evolutionary rate shifts in the genera Phyllobates and Hyloxalus , which respectively possess species with the largest (13.0 pg) and second smallest (2.6 pg) genomes in the family. Phylogenetically controlled regression analyses indicate that genome size is positively correlated with snout-vent-length, oocyte number, and clutch size, but negatively correlated with active metabolic rate and metabolic scope. While body size and metabolic rate are also correlates of toxicity, we found no relationship between genome size and evolution of chemical defense within Dendrobatidae. Genome size evolution in Dendrobatidae provides insight into the processes shaping genome size evolution over short timescales and establishes a novel system in which to study the mechanistic links between genome size and organismal physiology.
... Like interspecific comparisons, intraspecific comparisons of R/M with cell size often show significant negative relationships [33,39,55,[58][59][60][61][62][63], but contrary to cell SA theory, nonsignificant [39,61,[64][65][66][67] and even positive [42,56,59,60,63,68] relationships have also been frequently reported. Why intraspecific relationships vary so much is little understood, but differences in temperature [28,54,59,61,63], fasting duration [68], developmental stage [39], tissue type [40,60], and duration of laboratory acclimation [61,63] or evolutionary adaptation [54,56,69] may be at least partially involved. ...
... Like interspecific comparisons, intraspecific comparisons of R/M with cell size often show significant negative relationships [33,39,55,[58][59][60][61][62][63], but contrary to cell SA theory, nonsignificant [39,61,[64][65][66][67] and even positive [42,56,59,60,63,68] relationships have also been frequently reported. Why intraspecific relationships vary so much is little understood, but differences in temperature [28,54,59,61,63], fasting duration [68], developmental stage [39], tissue type [40,60], and duration of laboratory acclimation [61,63] or evolutionary adaptation [54,56,69] may be at least partially involved. ...
... Like interspecific comparisons, intraspecific comparisons of R/M with cell size often show significant negative relationships [33,39,55,[58][59][60][61][62][63], but contrary to cell SA theory, nonsignificant [39,61,[64][65][66][67] and even positive [42,56,59,60,63,68] relationships have also been frequently reported. Why intraspecific relationships vary so much is little understood, but differences in temperature [28,54,59,61,63], fasting duration [68], developmental stage [39], tissue type [40,60], and duration of laboratory acclimation [61,63] or evolutionary adaptation [54,56,69] may be at least partially involved. ...
Simple Summary
The metabolic conversion of resources into living structures and processes is fundamental to all living systems. The rate of metabolism (‘fire of life’) is critical for supporting the rates of various biological processes (‘pace of life’), but why it varies considerably within and among species is little understood. Much of this variation is related to body size, but such ‘metabolic scaling’ relationships also vary extensively. Numerous explanations have been offered, but no consensus has yet been reached. Here, I critically review explanations concerning how cell size and number and their establishment by cell expansion and multiplication may affect metabolic rate and its scaling with body mass. Numerous lines of evidence suggest that cell size and growth can affect metabolic rate at any given body mass, as well as how it changes with increasing body mass during growth or evolution. Mechanisms causing negative associations between cell size and metabolic rate may involve reduced resource supply and/or demand in larger cells, but more research is needed. A cell-size perspective not only helps to explain some (but not all) variation in metabolic rate and its body-mass scaling, but may also foster the conceptual integration of studies of ontogenetic development and body-mass scaling.
Abstract
Metabolic rate and its covariation with body mass vary substantially within and among species in little understood ways. Here, I critically review explanations (and supporting data) concerning how cell size and number and their establishment by cell expansion and multiplication may affect metabolic rate and its scaling with body mass. Cell size and growth may affect size-specific metabolic rate, as well as the vertical elevation (metabolic level) and slope (exponent) of metabolic scaling relationships. Mechanistic causes of negative correlations between cell size and metabolic rate may involve reduced resource supply and/or demand in larger cells, related to decreased surface area per volume, larger intracellular resource-transport distances, lower metabolic costs of ionic regulation, slower cell multiplication and somatic growth, and larger intracellular deposits of metabolically inert materials in some tissues. A cell-size perspective helps to explain some (but not all) variation in metabolic rate and its body-mass scaling and thus should be included in any multi-mechanistic theory attempting to explain the full diversity of metabolic scaling. A cell-size approach may also help conceptually integrate studies of the biological regulation of cellular growth and metabolism with those concerning major transitions in ontogenetic development and associated shifts in metabolic scaling.
... The cumulative hypotheses about different potential fitness consequences of cell size (Atkinson et al., 2006;Czarnoleski et al., 2013Czarnoleski et al., , 2015Czarnoleski et al., , 2018Czarnoleski et al., , 2017Davison, 1956;Hermaniuk et al., 2017Hermaniuk et al., , 2021Kozlowski et al., 2003;Maciak et al., 2014;Szarski, 1983;Walczyńska et al., 2015) underpin the research framework that we refer to here as the theory of optimal cell size (TOCS), which helps us provide an ultimate (evolutionary) perspective for this comparative study. Following Szarski (1983), TOCS considers that the diversity of life strategies, and thus the variance in adult body mass among organisms, spans a frugal-wasteful physiological continuum, which is at least partially associated with cell size differences among organisms (see also review by Kozlowski et al. (2020). ...
Alterations in cell number and size are apparently associated with the body mass differences between species and sexes, but we rarely know which of the two mechanisms underlies the observed variance in body mass. We used phylogenetically informed comparisons of males and females of 19 Carabidae beetle species to compare body mass, resting metabolic rate, and cell size in the ommatidia and Malpighian tubules. We found that the larger species or larger sex (males or females, depending on the species) consistently possessed larger cells in the two tissues, indicating organism-wide coordination of cell size changes in different tissues and the contribution of these changes to the origin of evolutionary and sex differences in body mass. The species or sex with larger cells also exhibited lower mass-specific metabolic rates, and the interspecific mass scaling of metabolism was negatively allometric, indicating that large beetles with larger cells spent relatively less energy on maintenance than small beetles. These outcomes also support existing hypotheses about the fitness consequences of cell size changes, postulating that the low surface-to-volume ratio of large cells helps decrease the energetic demand of maintaining ionic gradients across cell membranes. Analyses with and without phylogenetic information yielded similar results, indicating that the observed patterns were not biased by shared ancestry. Overall, we suggest that natural selection does not operate on each trait independently and that the linkages between concerted cell size changes in different tissues, body mass and metabolic rate should thus be viewed as outcomes of correlational selection.
... This suggests that diploid and triploid relatives within a species or a complex may be a good model for studying the link between cell size and MR and their scaling. Many previous studies have shown that triploids have a lower MR than diploids (Swarup 1959a;Maciak et al. 2011;Bowden et al. 2018;Hermaniuk et al. 2017) because the smaller relative area of exchange combined with the longer distance of diffusion in the larger cells of triploids could decrease the speed of transport and metabolic processes (Szarski 1976;Czarnoleski et al. 2014Czarnoleski et al. , 2015. It seems that triploids may have a larger b R than diploids because of the negative correlation between b R and MR, according to the MLB hypothesis (Glazier 2005(Glazier , 2010. ...
... In addition, the maintenance of the nucleocytoplasmic ratio suggests that the cells of the triploids are larger than those of the diploids (Benfey 1999). SA RBC has been observed to be larger in many triploids than in diploids (Benfey et al. 1984;Graham et al. 1985;Biron and Benfey 1994;Yamamoto and Iida 1994a, b ;Maciak et al. 2011;Hardie and Hebert 2003Hermaniuk et al. 2017. Consistent with this finding, the results of this study showed that the SA RBC of the triploid common carp was larger than that of the diploid common carp. ...
... The results also suggest that the effects of ploidy differences on RMR may vary among species. Several studies observed a lower RMR of triploid fish than that of diploid fish (Swarup 1959b;Maciak et al. 2011;Bowden et al. 2018;Hermaniuk et al. 2017), possibly because triploids have larger cell sizes (Maciak et al. 2011;Bowden et al. 2018;Hermaniuk et al. 2017), lower hemoglobin concentrations (Benfey et al. 1984;Benfey and Sutterlin 1984b;Graham et al. 1985), lower quantities of membrane oxidase (Ballarin et al. 2004) and lower plasma cortisol and concentrations of electrolytes (Perruzi et al. 2005). However, other results showed that triploids have a higher MR than diploids (Polymeropoulos et al. 2014;O'Donnell et al. 2017). ...
Ploidy level affects both the cell size and metabolic rate (MR) of organisms. The present study aimed to examine whether ploidy levels cause differences in cell surface area (SA), MR and metabolic scaling. The resting MR (RMR), red blood cell SA (SARBC), red blood cell count (RBCC), gill SA (GSA), and ventilation frequency (VF) were measured in diploid and triploid common carp with different body masses (M). The results showed that both M and ploidy level affected the RMR, GSA, VF, and SARBC, with interactions between M and ploidy level. The triploids had larger SARBC but lower RBCC than those of the diploids. The SARBC increased weakly but significantly with increasing M, by an exponent of 0.043, in the triploids but did not increase in the diploids. The RMR of the triploids and diploids scaled with M, by exponents of 0.696 and 1.007, respectively. The RMR was higher in the triploids than the diploids. The GSA scaled with M, with an exponent of 0.906 in the triploids and an exponent of 1.043 in the diploids. The VF scaled with M by an exponent of − 0.305 in the triploids but showed no correlation with M in the diploids. The larger SARBC and RMR and smaller scaling exponents of both the GSA and VF of the triploids were consistent with the finding that the bR was smaller in the triploids than in the diploids. This suggests that the ploidy-induced changes of SA and SA scaling affect the metabolic scaling of fish.
