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1. The impacts of body mass on immune cell concentrations in birds

   https://doi.org/10.1098/rspb.2020.0655  

   Ruhs, Emily Cornelius ; Martin, Lynn B. ; Downs, Cynthia J. ( September 2020 , Proceedings of the Royal Society B: Biological Sciences)

   null (Ed.)

   Body mass affects many biological traits, but its impacts on immune defences are fairly unknown. Recent research on mammals found that neutrophil concentrations disproportionately increased (scaled hypermetrically) with body mass, a result not predicted by any existing theory. Although the scaling relationship for mammals might predict how leucocyte concentrations scale with body mass in other vertebrates, vertebrate classes are distinct in many ways that might affect their current and historic interactions with parasites and hence the evolution of their immune systems. Subsequently, here, we asked which existing scaling hypothesis best-predicts relationships between body mass and lymphocyte, eosinophil and heterophil concentrations—the avian functional equivalent of neutrophils—among more than 100 species of birds. We then examined the predictive power of body mass relative to life-history variation, as extensive literature indicates that the timing of key life events has influenced immune system variation among species. Finally, we ask whether avian scaling patterns differ from the patterns we observed in mammals. We found that an intercept-only model best explained lymphocyte and eosinophil concentrations among birds, indicating that the concentrations of these cell types were both independent of body mass. For heterophils, however, body mass explained 31% of the variation in concentrations among species, much more than life-history variation (4%). As with mammalian neutrophils, avian heterophils scaled hypermetrically ( b = 0.19 ± 0.05), but more steeply than mammals (approx. 1.5 ×; 0.11 ± 0.03). As such, we discuss why birds might require more broadly protective cells compared to mammals of the same body size. Overall, body mass appears to have strong influences on the architecture of immune systems. 

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2. Estimating the effects of non‐native species on nutrient recycling using species‐specific and general allometric models

   https://doi.org/10.1111/fwb.13092  

   Fritschie, Keith J. ; Olden, Julian D. ( February 2018 , Freshwater Biology)

   Non‐native species are now common in community assemblages, but the influence of multiple introductions on ecosystem functioning remains poorly understood. In highly invaded systems, one promising approach is to use functional traits to scale measured individuals’ effects on ecosystem function up to the community level. This approach assumes that functional traits provide a common currency among species to relate individuals to ecosystem functioning.

   The goals of this study were to (i) test whether the relationship between body size and ecosystem functioning (per capita nutrient recycling) was best described by general or species‐specific scaling models; (ii) relate community structure (total biomass, average body size, non‐native dominance) to aggregated, community‐level nutrient recycling rates and ratios; and (iii) determine whether conclusions regarding the relationships between community structure and aggregate ecosystem functioning differed between species‐specific and general scaling approaches.

   By combining experimental incubations and field surveys, we compare consumer‐mediated nutrient recycling of fish communities along a non‐native dominance gradient in the Verde River watershed of central Arizona,USA. Data from ˜340 field‐sampled freshwater fish demonstrated support for general allometric relationships predicted by the metabolic theory of ecology (NH₄‐N scaling coefficient = 0.72 [0.64–0.80];PO₄‐P = 0.67 [0.47–0.86]). However, the best‐fit models for N and P included species‐specific random effects for both allometric slopes and intercepts.

   According to species‐specific models, stream fish communities recycled 1–12 mmolNH₄‐N/hr (median = 2.8 mmol/hr) and 0.02–0.74 mmolPO₄‐P/hr (median = 0.07 mmol/hr) at N:P ratios between 13.3 and 83.5 (median = 28.8). General models generated similar estimates forNH₄‐N recycling but less accurate estimates forPO₄‐P. Stochastic simulations that incorporated error around allometric parameter estimates led to qualitatively similar but larger differences between general and species‐specific results.

   Community structure influenced aggregate nutrient recycling, but specific conclusions depended on the scaling approach. Total biomass explained much of the among‐community variation in aggregateNH₄‐N andPO₄‐P for both model types, whereas non‐native dominance alone best predicted variation in aggregate N:P. Surprisingly, species‐specific and general models both reached significant yet quantitatively opposing conclusions regarding the relationship between N:P supply and non‐native dominance.

   Study results indicate that shifting fish community structure can substantially alter ecosystem functioning in this river system. However, some inferred relationships between community structure and aggregate nutrient recycling varied depending on whether general or species‐specific scaling approaches were taken. Although trait‐based approaches to link environmental change, community structure and ecosystem function hold much promise, it will be important to consider when species‐specific versus general models are necessary to scale from individuals to ecosystems.

    

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3. Body size affects immune cell proportions in birds and non-volant mammals, but not bats

   https://doi.org/10.1242/jeb.241109  

   Cornelius Ruhs, Emily ; Becker, Daniel J. ; Oakey, Samantha J. ; Ogunsina, Ololade ; Fenton, M. Brock ; Simmons, Nancy B. ; Martin, Lynn B. ; Downs, Cynthia J. ( July 2021 , Journal of Experimental Biology)

   ABSTRACT Powered flight has evolved several times in vertebrates and constrains morphology and physiology in ways that likely have shaped how organisms cope with infections. Some of these constraints probably have impacts on aspects of immunology, such that larger fliers might prioritize risk reduction and safety. Addressing how the evolution of flight may have driven relationships between body size and immunity could be particularly informative for understanding the propensity of some taxa to harbor many virulent and sometimes zoonotic pathogens without showing clinical disease. Here, we used a comparative framework to quantify scaling relationships between body mass and the proportions of two types of white blood cells – lymphocytes and granulocytes (neutrophils/heterophils) – across 63 bat species, 400 bird species and 251 non-volant mammal species. By using phylogenetically informed statistical models on field-collected data from wild Neotropical bats and from captive bats, non-volant mammals and birds, we show that lymphocyte and neutrophil proportions do not vary systematically with body mass among bats. In contrast, larger birds and non-volant mammals have disproportionately higher granulocyte proportions than expected for their body size. Our inability to distinguish bat lymphocyte scaling from birds and bat granulocyte scaling from all other taxa suggests there may be other ecological explanations (i.e. not flight related) for the cell proportion scaling patterns. Future comparative studies of wild bats, birds and non-volant mammals of similar body mass should aim to further differentiate evolutionary effects and other aspects of life history on immune defense and its role in the tolerance of (zoonotic) infections. 

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4. Network‐regulated organ allometry: The developmental regulation of morphological scaling

   https://doi.org/10.1002/wdev.391  

   Vea, Isabelle M. ; Shingleton, Alexander W. ( June 2020 , WIREs Developmental Biology)

   Morphological scaling relationships, or allometries, describe how traits grow coordinately and covary among individuals in a population. The developmental regulation of scaling is essential to generate correctly proportioned adults across a range of body sizes, while the mis‐regulation of scaling may result in congenital birth defects. Research over several decades has identified the developmental mechanisms that regulate the size of individual traits. Nevertheless, we still have poor understanding of how these mechanisms work together to generate correlated size variation among traits in response to environmental and genetic variation. Conceptually, morphological scaling can be generated by size‐regulatory factors that act directly on multiple growing traits (trait‐autonomous scaling), or indirectly via hormones produced by central endocrine organs (systemically regulated scaling), and there are a number of well‐established examples of such mechanisms. There is much less evidence, however, that genetic and environmental variation actually acts on these mechanisms to generate morphological scaling in natural populations. More recent studies indicate that growing organs can themselves regulate the growth of other organs in the body. This suggests that covariation in trait size can be generated by network‐regulated scaling mechanisms that respond to changes in the growth of individual traits. Testing this hypothesis, and one of the main challenges of understanding morphological scaling, requires connecting mechanisms elucidated in the laboratory with patterns of scaling observed in the natural world.

   This article is categorized under:

   Establishment of Spatial and Temporal Patterns > Regulation of Size, Proportion, and Timing

   Comparative Development and Evolution > Organ System Comparisons Between Species

    

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5. Whole-limb scaling of muscle mass and force-generating capacity in amniotes

   https://doi.org/10.7717/peerj.12574  

   Bishop, Peter J. ; Wright, Mark A. ; Pierce, Stephanie E. ( January 2021 , PeerJ)

   Skeletal muscle mass, architecture and force-generating capacity are well known to scale with body size in animals, both throughout ontogeny and across species. Investigations of limb muscle scaling in terrestrial amniotes typically focus on individual muscles within select clades, but here this question was examined at the level of the whole limb across amniotes generally. In particular, the present study explored how muscle mass, force-generating capacity (measured by physiological cross-sectional area) and internal architecture (fascicle length) scales in the fore- and hindlimbs of extant mammals, non-avian saurians (‘reptiles’) and bipeds (birds and humans). Sixty species spanning almost five orders of magnitude in body mass were investigated, comprising previously published architectural data and new data obtained via dissections of the opossum Didelphis virginiana and the tegu lizard Salvator merianae . Phylogenetic generalized least squares was used to determine allometric scaling slopes (exponents) and intercepts, to assess whether patterns previously reported for individual muscles or functional groups were retained at the level of the whole limb, and to test whether mammals, reptiles and bipeds followed different allometric trajectories. In general, patterns of scaling observed in individual muscles were also observed in the whole limb. Reptiles generally have proportionately lower muscle mass and force-generating capacity compared to mammals, especially at larger body size, and bipeds exhibit strong to extreme positive allometry in the distal hindlimb. Remarkably, when muscle mass was accounted for in analyses of muscle force-generating capacity, reptiles, mammals and bipeds almost ubiquitously followed a single common scaling pattern, implying that differences in whole-limb force-generating capacity are principally driven by differences in muscle mass, not internal architecture. In addition to providing a novel perspective on skeletal muscle allometry in animals, the new dataset assembled was used to generate pan-amniote statistical relationships that can be used to predict muscle mass or force-generating capacity in extinct amniotes, helping to inform future reconstructions of musculoskeletal function in the fossil record. 

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