Evolution and development of Drosophila melanogaster under different thermal conditions affected cell sizes and sensitivity to paralyzing hypoxia.

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.

Concerted evolution of body mass, cell size and metabolic rate among carabid beetles.

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.

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

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.

Cell size control and gene expression homeostasis in single-cells.

Growth of a cell and its subsequent division into daughters is a fundamental aspect of all cellular living systems. During these processes, how do individual cells correct size aberrations so that they do not grow abnormally large or small? How do cells ensure that the concentration of essential gene products are maintained at desired levels, in spite of dynamic/stochastic changes in cell size during growth and division? Both these questions have fascinated researchers for over a century. We review how advances in singe-cell technologies and measurements are providing unique insights into these questions across organisms from prokaryotes to human cells. More specifically, diverse strategies based on timing of cell-cycle events, regulating growth, and number of daughters are employed to maintain cell size homeostasis. Interestingly, size homeostasis often results in size optimality - proliferation of individual cells in a population is maximized at an optimal cell size. We further discuss how size-dependent expression or gene-replication timing can buffer concentration of a gene product from cell-to-cell size variations within a population. Finally, we speculate on an intriguing hypothesis that specific size control strategies may have evolved as a consequence of gene-product concentration homeostasis.

Concerted evolution of body mass and cell size: similar patterns among species of birds (Galliformes) and mammals (Rodentia).

Cell size plays a role in body size evolution and environmental adaptations. Addressing these roles, we studied body mass and cell size in Galliformes birds and Rodentia mammals, and collected published data on their genome sizes. In birds, we measured erythrocyte nuclei and basal metabolic rates (BMRs). In birds and mammals, larger species consistently evolved larger cells for five cell types (erythrocytes, enterocytes, chondrocytes, skin epithelial cells, and kidney proximal tubule cells) and evolved smaller hepatocytes. We found no evidence that cell size differences originated through genome size changes. We conclude that the organism-wide coordination of cell size changes might be an evolutionarily conservative characteristic, and the convergent evolutionary body size and cell size changes in Galliformes and Rodentia suggest the adaptive significance of cell size. Recent theory predicts that species evolving larger cells waste less energy on tissue maintenance but have reduced capacities to deliver oxygen to mitochondria and metabolize resources. Indeed, birds with larger size of the abovementioned cell types and smaller hepatocytes have evolved lower mass-specific BMRs. We propose that the inconsistent pattern in hepatocytes derives from the efficient delivery system to hepatocytes, combined with their intense involvement in supracellular function and anabolic activity.

A Normalized Congruent Matching Area Method for the Correlation of Breech Face Impression Images.

The congruent matching cells (CMC) method was invented at the National Institute of Standards and Technology (NIST) for firearm evidence identification and error rate estimation. The CMC method divides the correlated image pairs into cells and uses four parameters to quantify topography similarity and pattern congruency of the correlated cell pairs in firearm breech face impressions on fired cartridge cases. A preliminary conservative numerical identification criterion of C = 6 CMCs was suggested for identifying images of cartridge cases fired from the same firearm. The CMC method was validated by correlations using both three-dimensional (3D) topography images and two-dimensional (2D) optical images from a set of 40 cartridge cases fired from a firearm set composed of 10 consecutively manufactured pistol slides. However, in the original CMC method, due to the difference in the effective data area of the correlated cells, final CMCs obtained from an image pair presented different data quantity (or validity level), and thus the empirical criterion C = 6 CMCs did not remain optimal for identification when the correlated cell size changed. In this study, a normalized congruent matching area (NCMA) method that considers the difference in the data area in each correlated cell pair was developed. Based on the NCMA method, an optimal range of cell sizes for breech face identification with granular characteristics was determined. A binomial model was used to fit the known nonmatching NCMA probability distribution Ψ NCMA, and a beta-binomial model was used to fit the known matching NCMA probability distribution Φ NCMA. An experimental improvement in the normalized identification criterion C of around 6 % was observed in the validation tests when the cell sizes were in the optimal range.

The thermal environment of the nest affects body and cell size in the solitary red mason bee (Osmia bicornis L.).

Many ectotherms grow larger at lower temperatures than at higher temperatures. This pattern, known as the temperature-size rule, is often accompanied by plastic changes in cell size, which can mechanistically explain the thermal dependence of body size. However, the theory predicts that thermal plasticity in cell size has adaptive value for ectotherms because there are different optimal cell-membrane-to-cell-volume ratios at different temperatures. At high temperatures, the demand for oxygen is high; therefore, a large membrane surface of small cells is beneficial because it allows high rates of oxygen transport into the cell. The metabolic costs of maintaining membranes become more important at low temperatures than at high temperatures, which favours large cells. In a field experiment, we manipulated the thermal conditions inside nests of the red mason bee, a solitary bee that does not regulate the temperature in its nests and whose larvae develop under ambient conditions. We assessed the effect of temperature on body mass and ommatidia size (our proxy of cell size). The body and cell sizes decreased in response to a higher mean temperature and greater temperature fluctuations. This finding is in accordance with predictions of the temperature-size rule and optimal cell size theory and suggests that both the mean temperature and the magnitude of temperature fluctuations are important for determining body and cell sizes. Additionally, we observed that males of the red mason bee tend to have larger ommatidia in relation to their body mass than females, which might play an important role during mating flight.

Not all cells are equal: effects of temperature and sex on the size of different cell types in the Madagascar ground gecko Paroedura picta.

Cell size plays a role in evolutionary and phenotypically plastic changes in body size. To examine this role, we measured the sizes of seven cell types of geckos (Paroedura picta) reared at three constant temperatures (24, 27, and 30°C). Our results show that the cell size varies according to the body size, sex and developmental temperature, but the pattern of this variance depends on the cell type. We identified three groups of cell types, and the cell sizes changed in a coordinated manner within each group. Larger geckos had larger erythrocytes, striated muscle cells and hepatocytes (our first cell group), but their renal proximal tubule cells and duodenal enterocytes (our second cell group), as well as tracheal chondrocytes and epithelial skin cells (our third cell group), were largely unrelated to the body size. For six cell types, we also measured the nuclei and found that larger cells had larger nuclei. The relative sizes of the nuclei were not invariant but varied in a complex manner with temperature and sex. In conclusion, we provide evidence suggesting that changes in cell size might be commonly involved in the origin of thermal and sexual differences in adult size. A recent theory predicts that smaller cells speed up metabolism but demand more energy for their maintenance; consequently, the cell size matches the metabolic demand and supply, which in ectotherms, largely depends on the thermal conditions. The complex thermal dependency of cell size in geckos suggests that further advancements in understanding the adaptive value of cell size requires the consideration of tissue-specific demand/supply conditions.