Abstract
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.
Highlights
Organisms have evolved a plethora of different body plans and life strategies, resulting in dramatic differences in body mass among taxo nomic groups (Kozlowski and Weiner, 1997; Meiri and Thomas, 2007)
It is tempting to infer the potential fitness consequences of this variance in the absence of other traits, doing so would ignore that dif ferences in body mass are often linked to other fitness-related traits, such as physiological capacity or the risk of mortality (Roff, 1993; Stearns, 1992), and they can originate via a change in cell number and/or cell size
This finding indicates that the origin of the detected interdependence among cell size, body mass and metabolic rate was not significantly biased by shared evolutionary history
Summary
Organisms have evolved a plethora of different body plans and life strategies, resulting in dramatic differences in body mass among taxo nomic groups (Kozlowski and Weiner, 1997; Meiri and Thomas, 2007). The costs and benefits of having a certain number and size of cells in tissues and organs would impact the cellular composition of the entire body and the cellular mechanisms involved in body mass evolution. Following Szarski (1983), TOCS considers that the diversity of life strategies, and 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 review by Kozlowski et al (2020). Frugal strategies are considered to be linked to the presence of larger cells in a body, which reduces the amount of cell membrane per unit of tissue volume and, the metabolic requirements of an organism per body mass unit ((Kozlowski et al (2003), for review see Kozlowski et al (2020)). Whether a wasteful or frugal strategy per sists in an environment will depend on selective factors that shape the balance between the oxygen supply and/or energy demand of an or ganism (Czarnoleski et al, 2018)
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