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

Czarnołęski, Marcin; Łabęcka, Anna Maria; Dragosz-Kluska, Dominika; Pis, T.; Pawlik, Katarzyna; Kapustka, Filip; Kilarski, Wincenty; Kozłowski, Jan

doi:10.1242/bio.029603

Cited by 24 publications

(48 citation statements)

References 53 publications

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“…We should also consider here that cell size and, thus, the total area of plasma membranes in tissue might not affect metabolic performance if animals are studied in their resting state, as was the case here. In contrast to our findings, some previous studies have demonstrated an inverse relationship between cell size and metabolic rate (e.g., Chown et al., 2007; Czarnoleski et al., 2018; Hermaniuk, Rybacki, & Taylor, 2017; Maciak et al., 2014; Starostová et al., 2013; Starostová, Kubička, Konarzewski, Kozłowski, & Kratochvíl, 2009). Also against the pattern revealed here for P. scaber , comparisons of thermal sensitivity of Carabidae beetles showed that large species were characterized by higher metabolic responses to thermal change than small species (Gudowska, Schramm, Czarnoleski, Kozłowski, & Bauchinger, 2017).…”

Section: Discussioncontrasting

confidence: 99%

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

Antoł

Łabęcka

Horváthová

et al. 2020

Ecology and Evolution

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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.

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Section: Discussioncontrasting

confidence: 99%

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

Antoł

Łabęcka

Horváthová

et al. 2020

Ecology and Evolution

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“…Kozłowski et al (2010) found support for such concerted changes at the interspecific level in birds and amphibians, although in mammals, not all cell types changed in complete synchrony. A comparative study of species of galliforms and rodents showed that larger species consistently evolved larger cells of five cell types (erythrocytes, enterocytes, chondrocytes, skin epithelial cells, and kidney proximal tubule cells) and smaller hepatocytes (Czarnoleski et al, 2018). Savage et al (2007) reported diverse interspecific relationships between body mass and the size of different cell types in mammals by applying a phylogenetically noninformed analysis.…”

Section: Mechanistic Explanation Of Hypoallometric Mr Scalingmentioning

confidence: 99%

“…The genes that control these pathways in flies are differentiated along latitudinal clines in conjunction with cell size and body size (De Jong & Bochdanovits, 2003). The activities of such pathways also explain coordinated cell size changes in different tissues during evolutionary differentiation of species of mammals, birds and amphibians (Kozłowski et al ., 2010; Czarnoleski et al ., 2018). A ubiquitous correlation between nucleus size and cell size, which is visible at intraspecific (Maciak et al ., 2014) and interspecific levels (Kozłowski et al ., 2010), suggests the involvement of a cytological mechanism in cell size regulation.…”

Section: Mechanistic Explanation Of Hypoallometric Mr Scalingmentioning

confidence: 99%

Coevolution of body size and metabolic rate in vertebrates: a life‐history perspective

2020

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Despite many decades of research, the allometric scaling of metabolic rates (MRs) remains poorly understood. Here, we argue that scaling exponents of these allometries do not themselves mirror one universal law of nature but instead statistically approximate the non‐linearity of the relationship between MR and body mass. This ‘statistical’ view must be replaced with the life‐history perspective that ‘allows’ organisms to evolve myriad different life strategies with distinct physiological features. We posit that the hypoallometric allometry of MRs (mass scaling with an exponent smaller than 1) is an indirect outcome of the selective pressure of ecological mortality on allocation ‘decisions’ that divide resources among growth, reproduction, and the basic metabolic costs of repair and maintenance reflected in the standard or basal metabolic rate (SMR or BMR), which are customarily subjected to allometric analyses. Those ‘decisions’ form a wealth of life‐history variation that can be defined based on the axis dictated by ecological mortality and the axis governed by the efficiency of energy use. We link this variation as well as hypoallometric scaling to the mechanistic determinants of MR, such as metabolically inert component proportions, internal organ relative size and activity, cell size and cell membrane composition, and muscle contributions to dramatic metabolic shifts between the resting and active states. The multitude of mechanisms determining MR leads us to conclude that the quest for a single‐cause explanation of the mass scaling of MRs is futile. We argue that an explanation based on the theory of life‐history evolution is the best way forward.

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“…Variation in body mass can result from changes in cell number, cell size or a combination of both [39,40], but usually larger-bodied species tend to have larger cells, as documented in arthropods [40,41], fish [42] and birds and mammals [43]. The theory of optimal cell size [44] highlights how differences in cell size have repercussions for oxygen uptake at the cellular level.…”

Section: Introductionmentioning

confidence: 99%

Scaling of thermal tolerance with body mass and genome size in ectotherms: a comparison between water- and air-breathers

Leiva

Calosi

Verberk

2019

Phil. Trans. R. Soc. B

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Global warming appears to favour smaller-bodied organisms, but whether larger species are also more vulnerable to thermal extremes, as suggested for past mass-extinction events, is still an open question. Here, we tested whether interspecific differences in thermal tolerance (heat and cold) of ectotherm organisms are linked to differences in their body mass and genome size (as a proxy for cell size). Since the vulnerability of larger, aquatic taxa to warming has been attributed to the oxygen limitation hypothesis, we also assessed how body mass and genome size modulate thermal tolerance in species with contrasting breathing modes, habitats and life stages. A database with the upper (CTmax) and lower (CTmin) critical thermal limits and their methodological aspects was assembled comprising more than 500 species of ectotherms. Our results demonstrate that thermal tolerance in ectotherms is dependent on body mass and genome size and these relationships became especially evident in prolonged experimental trials where energy efficiency gains importance. During long-term trials, CTmax was impaired in larger-bodied water-breathers, consistent with a role for oxygen limitation. Variation in CTmin was mostly explained by the combined effects of body mass and genome size and it was enhanced in larger-celled, air-breathing species during long-term trials, consistent with a role for depolarization of cell membranes. Our results also highlight the importance of accounting for phylogeny and exposure duration. Especially when considering long-term trials, the observed effects on thermal limits are more in line with the warming-induced reduction in body mass observed during long-term rearing experiments. This article is part of the theme issue ‘Physiological diversity, biodiversity patterns and global climate change: testing key hypotheses involving temperature and oxygen’.

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

Cited by 24 publications

References 53 publications

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

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

Coevolution of body size and metabolic rate in vertebrates: a life‐history perspective

Scaling of thermal tolerance with body mass and genome size in ectotherms: a comparison between water- and air-breathers

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