The evolution of red blood cell shape in fishes

Abstract

The size and shape of red blood cells (RBCs) provide key information on life‐history strategies in vertebrates. However, little is known about how RBC shape evolved in response to environmental factors, body size and the role of evolutionary rate. Here, we analysed RBC morphometrics in a set of Teleostei (bony fishes) and Elasmobranchii (sharks and rays) species testing the hypothesis that phylogenetic relationship explains species occupation of morphospace. We collected data on cell and nucleus area and volume, nucleus:cytoplasm ratio and shape factor for 65 species belonging to 28 orders. Then, we built phylomorphospaces separately for bony fish and sharks and rays. To test whether phylogenetic relationships predicted phenotypic similarity, we calculated multivariate phylogenetic signal. We also estimated the evolutionary rate of RBC shape for each node and tip using ridge regression. Finally, we tested whether habitat and body size influenced RBC shape using a PGLS. We found a significant phylogenetic signal in RBC shape for bony fish, but not sharks and rays. Saltwater teleost species were more clustered than freshwater ones in the phylomorphospace, suggesting clade disparity. Accordingly, the rate of evolution was highly heterogeneous, with significant decrease in Acanthopterygii. Neither habitat nor body size influenced RBC shape. In conclusion, RBC shape seems to have evolved in fishes in response to multiple selective pressures independent of life‐history characters.

Hematological parameters of a Neotropical wild frog population, with a phylogenetic perspective on blood cell composition in Anura

“…This result suggests that the amount of hemoglobin in red blood cells has a phylogenetic pattern (see also Glomski et al 1997 ), whereas the hematocrit and the number of erythrocytes are more plastic variables, varying at shallow phylogenetic scales. The phylogenetic pattern in the erythrogram may be due to the morphometry of red blood cells (see Martins et al, 2021 for an example with fish), because red blood cell volume is negatively correlated with hemoglobin concentration ( Lay and Baldwin, 1999 ). This emphasizes the importance of collecting these data when evaluating hematological parameters in frogs, as we did with L. podicipinus .…”

Ecological and life‐history correlates of erythrocyte size and shape in Lepidosauria

“…Erythrocyte shape is poorly studied, but is known to vary plastically within‐species, for example, elongated erythrocytes were reported in alpine accentors breeding at high altitudes (Haas & Janiga, 2020; Janiga et al, 2017), whereas across bird species, erythrocytes were more elongated at higher altitudes and for species migrating long distances (Soulsbury et al, 2022). In contrast, cell shape (PCA of cell shape components) also varies extensively in teleosts, but did not vary with habitat or body size (Martins et al, 2021). To date, erythrocyte shape is relatively unexplored and key drivers of shape variation are uncertain.…”

“…Positive interspecific relationships between erythrocyte size and body mass have been demonstrated in geckos (Starostová et al, 2005) and birds (Kostelecka‐Myrcha & Chołostiakow‐Gromek, 2001; Soulsbury et al, 2022). In mammals and teleost fish, there is no relationship between erythrocyte size and body mass or size (mammals: Promislow, 1991; Savage et al, 2007; teleosts: Martins et al, 2021), although for mammals there is a significant positive correlation when analysed with independent contrasts (Promislow, 1991).…”

“…Other sources of variation in erythrocyte size are less well studied, but again thought to be related to oxygen demand. For example, in tropical reef teleosts, species with a higher aerobic capacity and greater activity levels have smaller erythrocytes (Well & Baldwin, 1990), but more broadly across teleosts, erythrocyte shape was unrelated to habitat or body size (Martins et al, 2021). Similarly, birds with greater energetic demands (e.g.…”

Energetic Lifestyle Drives Size and Shape of Avian Erythrocytes

“…For example, in teleosts, species with higher aerobic capacity and greater activity levels have smaller erythrocytes ( Wells and Baldwin 1990 ), and active foraging squamates have smaller erythrocytes (Penman et al, submitted for publication). More broadly across teleosts, erythrocyte shape was unrelated to habitat or body size ( Martins et al 2021 ). In summary, existing work has looked at erythrocyte size and shape both broadly and in a handful of specific studies, for specific drivers.…”