Fossil evidence sheds light on sexual selection during the early evolution of birds.

The impact of sexual selection on the evolution of birds has been widely acknowledged. Although sexual selection has been hypothesized as a driving force in the occurrences of numerous morphological features across theropod evolution, this hypothesis has yet to be comprehensively tested due to challenges in identifying the sex of fossils and by the limited sample size. Confuciusornis sanctus is arguably the best-known early avialan and is represented by thousands of well-preserved specimens from the Early Cretaceous Jehol lagerstätte, which provides us with a chance to decipher the strength of sexual selection on extinct vertebrates. Herein, we present a morphometric study of C. sanctus based on the largest sample size of this taxon collected up to now. Our results indicate that the characteristic elongated paired rectrices is a sexually dimorphic trait and statistically robust inferences of the sexual dimorphism in size, shape, and allometry that have been established, providing the earliest known sexual dimorphism in avian evolution. Our findings suggest that sexual selection, in conjunction with natural selection, does act upon body size and limb length ratio in early birds, thereby promoting a deeper understanding of the role of sexual selection in large-scale phylogenetic evolution.

Two different jumping mechanisms of water striders are determined by body size.

Current theory for surface tension-dominant jumps on water, created for small- and medium-sized water strider species and used in bioinspired engineering, predicts that jumping individuals are able to match their downward leg movement speed to their size and morphology such that they maximize the takeoff speed and minimize the takeoff delay without breaking the water surface. Here, we use empirical observations and theoretical modeling to show that large species (heavier than ~80 mg) could theoretically perform the surface-dominated jumps according to the existing model, but they do not conform to its predictions, and switch to using surface-breaking jumps in order to achieve jumping performance sufficient for evading attacks from underwater predators. This illustrates how natural selection for avoiding predators may break the theoretical scaling relationship between prey size and its jumping performance within one physical mechanism, leading to an evolutionary shift to another mechanism that provides protection from attacking predators. Hence, the results are consistent with a general idea: Natural selection for the maintenance of adaptive function of a specific behavior performed within environmental physical constraints leads to size-specific shift to behaviors that use a new physical mechanism that secure the adaptive function.

The Promise of a Pointillist Perspective for Comparative Immunology.

Most studies in comparative immunology involve investigations into the detailed mechanisms of the immune system of a non-model organism. Although this approach has been insightful, it has promoted a deep understanding of only a handful of species, thus inhibiting the recognition of broad taxonomic patterns. Here, we call for investigating the immune defenses of numerous species within a pointillist framework, that is, the meticulous, targeted collection of data from dozens species and investigation of broad patterns of organismal, ecological, and evolutionary forces shaping those patterns. Without understanding basic immunological patterns across species, we are limited in our ability to extrapolate and/or translate our findings to other organisms, including humans. We illustrate this point by focusing predominantly on the biological scaling literature with some integrations of the pace of life literature, as these perspectives have been the most developed within this framework. We also highlight how the more traditional approach in comparative immunology works synergistically with a pointillist approach, with each approach feeding back into the other. We conclude that the pointillist approach promises to illuminate comprehensive theories about the immune system and enhance predictions in a wide variety of domains, including host-parasite dynamics and disease ecology.

Human shoulder development is adapted to obstetrical constraints.

In humans, obstetrical difficulties arise from the large head and broad shoulders of the neonate relative to the maternal birth canal. Various characteristics of human cranial development, such as the relatively small head of neonates compared with adults and the delayed fusion of the metopic suture, have been suggested to reflect developmental adaptations to obstetrical constraints. On the other hand, it remains unknown whether the shoulders of humans also exhibit developmental features reflecting obstetrical adaptation. Here we address this question by tracking the development of shoulder width from fetal to adult stages in humans, chimpanzees, and Japanese macaques. Compared with nonhuman primates, shoulder development in humans follows a different trajectory, exhibiting reduced growth relative to trunk length before birth and enhanced growth after birth. This indicates that the perinatal developmental characteristics of the shoulders likely evolved to ease obstetrical difficulties such as shoulder dystocia in humans.

Responses of intraspecific metabolic scaling to temperature and activity differ between water- and air-breathing ectothermic vertebrates.

Metabolism underpins all life-sustaining processes and varies profoundly with body size, temperature and locomotor activity. A current theory explains some of the size-dependence of metabolic rate (its mass exponent, b) through changes in metabolic level (L). We propose two predictive advances that: (a) combine the above theory with the evolved avoidance of oxygen limitation in water-breathers experiencing warming, and (b) quantify the overall magnitude of combined temperatures and degrees of locomotion on metabolic scaling across air- and water-breathers. We use intraspecific metabolic scaling responses to temperature (523 regressions) and activity (281 regressions) in diverse ectothermic vertebrates (fish, reptiles and amphibians) to show that b decreases with temperature-increased L in water-breathers, supporting surface area-related avoidance of oxygen limitation, whereas b increases with activity-increased L in air-breathers, following volume-related influences. This new theoretical integration quantitatively incorporates different influences (warming, locomotion) and respiration modes (aquatic, terrestrial) on animal energetics.

Developmental changes in lung function of mice are independent of sex as a biological variable.

Pulmonary function testing (PFT) in mice includes biomechanical assessment of lung function relevant to physiology in health and its alteration in disease, hence, it is frequently used in preclinical modeling of human lung pathologies. Despite numerous reports of PFT in mice of various ages, there is a lack of reference data for developing mice collected using consistent methods. Therefore, we profiled PFTs in male and female C57BL/6J mice from 2 to 23 wk of age, providing reference values for age- and sex-dependent changes in mouse lung biomechanics during development and young adulthood. Although males and females have similar weights at birth, females weigh significantly less than males after 5 wk of age (P < 0.001) with largest weight gain observed between 3 and 8 wk in females and 3 and 13 wk in males, after which weight continued to increase more slowly up to 23 wk of age. Lung function parameters including static compliance and inspiratory capacity also increased rapidly between 3 and 8 wk in female and male mice, with male mice having significantly greater static compliance and inspiratory capacity than female mice (P < 0.001). Although these parameters appear higher in males at a given age, allometric scaling showed that static compliance and inspiratory compliance were comparable between the two sexes. This suggests that differences in measurements of lung function are likely body weight-based rather than sex-based. We expect these data to facilitate future lung disease research by filling a critical knowledge gap in our field.NEW & NOTEWORTHY This study provides reference values for changes in mouse lung biomechanics from 2 to 23 wk of age. There are rapid developmental changes in lung structure and function of male and female mice between the ages of 3 and 8 wk. Male mice become noticeably heavier than female mice at or about 5 wk of age. We identified that differences in normal lung function measurements are likely weight-based, not sex-based.

Utilizing geometric morphometrics to investigate gene function during organ growth: Insights through the study of beetle horn shape allometry.

Static allometry is a major component of morphological variation. Much of the literature on the development of allometry investigates how functional perturbations of diverse pathways affect the relationship between trait size and body size. Often, this is done with the explicit objective to identify developmental mechanisms that enable the sensing of organ size and the regulation of relative growth. However, changes in relative trait size can also be brought about by a range of other distinctly different developmental processes, such as changes in patterning or tissue folding, yet standard univariate biometric approaches are usually unable to distinguish among alternative explanations. Here, we utilize geometric morphometrics to investigate the degree to which functional genetic manipulations known to affect the size of dung beetle horns also recapitulate the effect of horn shape allometry. We reasoned that the knockdown phenotypes of pathways governing relative growth should closely resemble shape variation induced by natural allometric variation. In contrast, we predicted that if genes primarily affect alternative developmental processes, knockdown effects should align poorly with shape allometry. We find that the knockdown effects of several genes (e.g., doublesex, Foxo) indeed closely aligned with shape allometry, indicating that their corresponding pathways may indeed function primarily in the regulation of relative trait growth. In contrast, other knockdown effects (e.g., Distal-less, dachs) failed to align with allometry, implicating these pathways in potentially scaling-independent processes. Our findings moderate the interpretation of studies focusing on trait length and highlight the usefulness of multivariate approaches to study allometry and phenotypic plasticity.

Size scaling in collective cell growth.

Size is a fundamental feature of living entities and is intimately tied to their function. Scaling laws, which can be traced to D'Arcy Thompson and Julian Huxley, have emerged as a powerful tool for studying regulation of the growth dynamics of organisms and their constituent parts. Yet, throughout the 20th century, as scaling laws were established for single cells, quantitative studies of the coordinated growth of multicellular structures have lagged, largely owing to technical challenges associated with imaging and image processing. Here, we present a supervised learning approach for quantifying the growth dynamics of germline cysts during oogenesis. Our analysis uncovers growth patterns induced by the groupwise developmental dynamics among connected cells, and differential growth rates of their organelles. We also identify inter-organelle volumetric scaling laws, finding that nurse cell growth is linear over several orders of magnitude. Our approach leverages the ever-increasing quantity and quality of imaging data, and is readily amenable for studies of collective cell growth in other developmental contexts, including early mammalian embryogenesis and germline development.

Geometric morphometric analysis of an ontogenetic cranial series of the Permian dicynodont Diictodon feliceps.

The Karoo Basin of South Africa is renowned for its abundance and diversity of therapsid fossils. Among the most ubiquitous and persistent of the Permian fauna is the small herbivorous dicynodont Diictodon feliceps. Intraspecific variation in Diictodon is historically confounding, and while ontogeny is frequently cited as a potential source of variation, observable developmental changes have never been calibrated. The present study revisits this issue, comparing three-dimensional landmark configurations of 82 Diictodon crania to investigate the association between shape, size and dimorphism. Beyond the statistically significant relationship between shape and allometry, our results determine the shape differences between juvenile and adult skulls of Diictodon, aligned with common craniofacial features documented in other tetrapod taxa. Functionally, these changes are attributed to development of the jaw musculature for feeding on larger, tougher plant matter during later ontogeny. Cranial morphological variation owing to sexual dimorphism is negligible, but distinct differences are noted in the allometric trajectories of each morphotype. A component of non-allometric variation cannot be accounted for, and we propose that this represents natural variation, rather than an artefact of taphonomic deformation.

Trophic guilds differ in blood glucose concentrations: a phylogenetic comparative analysis in birds.

Glucose is a central metabolic compound used as an energy source across all animal taxa. There is high interspecific variation in glucose concentration between taxa, the origin and the consequence of which remain largely unknown. Nutrition may affect glucose concentrations because carbohydrate content of different food sources may determine the importance of metabolic pathways in the organism. Birds sustain high glucose concentrations that may entail the risks of oxidative damage. We collected glucose concentration and life-history data from 202 bird species from 171 scientific publications, classified them into seven trophic guilds and analysed the data with a phylogenetically controlled model. We show that glucose concentration is negatively associated with body weight and is significantly associated with trophic guilds with a moderate phylogenetic signal. After controlling for allometry, glucose concentrations were highest in carnivorous birds, which rely on high rates of gluconeogenesis to maintain their glycaemia, and lowest in frugivorous/nectarivorous species, which take in carbohydrates directly. However, trophic guilds with different glucose concentrations did not differ in lifespan. These results link nutritional ecology to physiology and suggest that at the macroevolutionary scale, species requiring constantly elevated glucose concentrations may have additional adaptations to avoid the risks associated with high glycaemia.

Bacterial sepsis triggers stronger transcriptomic immune responses in larger primates.

Empirical data relating body mass to immune defence against infections remain limited. Although the metabolic theory of ecology predicts that larger organisms would have weaker immune responses, recent studies have suggested that the opposite may be true. These discoveries have led to the safety factor hypothesis, which proposes that larger organisms have evolved stronger immune defences because they carry greater risks of exposure to pathogens and parasites. In this study, we simulated sepsis by exposing blood from nine primate species to a bacterial lipopolysaccharide (LPS), measured the relative expression of immune and other genes using RNAseq, and fitted phylogenetic models to determine how gene expression was related to body mass. In contrast to non-immune-annotated genes, we discovered hypermetric scaling in the LPS-induced expression of innate immune genes, such that large primates had a disproportionately greater increase in gene expression of immune genes compared to small primates. Hypermetric immune gene expression appears to support the safety factor hypothesis, though this pattern may represent a balanced evolutionary mechanism to compensate for lower per-transcript immunological effectiveness. This study contributes to the growing body of immune allometry research, highlighting its importance in understanding the complex interplay between body size and immunity over evolutionary timescales.

Body size shapes song in honeyeaters.

Birdsongs are among the most distinctive animal signals. Their evolution is thought to be shaped simultaneously by habitat structure and by the constraints of morphology. Habitat structure affects song transmission and detectability, thus influencing song (the acoustic adaptation hypothesis), while body size and beak size and shape necessarily constrain song characteristics (the morphological constraint hypothesis). Yet, support for the acoustic adaptation and morphological constraint hypotheses remains equivocal, and their simultaneous examination is infrequent. Using a phenotypically diverse Australasian bird clade, the honeyeaters (Aves: Meliphagidae), we compile a dataset consisting of song, environmental, and morphological variables for 163 species and jointly examine predictions of these two hypotheses. Overall, we find that body size constrains song frequency and pace in honeyeaters. Although habitat type and environmental temperature influence aspects of song, that influence is indirect, likely via effects of environmental variation on body size, with some evidence that elevation constrains the evolution of song peak frequency. Our results demonstrate that morphology has an overwhelming influence on birdsong, in support of the morphological constraint hypothesis, with the environment playing a secondary role generally via body size rather than habitat structure. These results suggest that changing body size (a consequence of both global effects such as climate change and local effects such as habitat transformation) will substantially influence the nature of birdsong.

Different currencies for calculating resource phenology result in opposite inferences about trophic mismatches.

Shifts in phenology are among the key responses of organisms to climate change. When rates of phenological change differ between interacting species they may result in phenological asynchrony. Studies have found conflicting patterns concerning the direction and magnitude of changes in synchrony, which have been attributed to biological factors. A hitherto overlooked additional explanation are differences in the currency used to quantify resource phenology, such as abundance and biomass. Studying an insectivorous bird (the sanderling) and its prey, we show that the median date of cumulative arthropod biomass occurred, on average, 6.9 days after the median date of cumulative arthropod abundance. In some years this difference could be as large as 21 days. For 23 years, hatch dates of sanderlings became less synchronized with the median date of arthropod abundance, but more synchronized with the median date of arthropod biomass. The currency-specific trends can be explained by our finding that mean biomass per arthropod specimen increased with date. Using a conceptual simulation, we show that estimated rates of phenological change for abundance and biomass can differ depending on temporal shifts in the size distribution of resources. We conclude that studies of trophic mismatch based on different currencies for resource phenology can be incompatible with each other.

Plant size-dependent influence of foliar fungal pathogens promotes diversity through allometric growth.

The effect of pathogens on host diversity has attracted much attention in recent years, yet how the influence of pathogens on individual plants scales up to affect community-level host diversity remains unclear. Here, we assessed the effects of foliar fungal pathogens on plant growth and species richness using allometric growth theory in population-level and community-level foliar fungal pathogen exclusion experiments. We calculated growth scaling exponents of 24 species to reveal the intraspecific size-dependent effects of foliar fungal pathogens on plant growth. We also calculated the intercepts to infer the growth rates of relatively larger conspecific individuals. We found that foliar fungal pathogens inhibited the growth of small conspecific individuals more than large individuals, resulting in a positive allometric growth. After foliar fungal pathogen exclusion, species-specific growth scaling exponents and intercepts decreased, but became positively related to species' relative abundance, providing a growth advantage for individuals of abundant species with a higher growth scaling exponent and intercept compared with rare species, and thus reduced species diversity. By adopting allometric growth theory, we elucidate the size-dependent mechanisms through which pathogens regulate species diversity and provide a powerful framework to incorporate antagonistic size-dependent processes in understanding species coexistence.

Evolutionary pathways to lower biomass allocation to the seed coat in crops: insights from allometric scaling.

Crops generally have seeds larger than their wild progenitors´ and with reduced dormancy. In wild plants, seed mass and allocation to the seed coat (a proxy for physical dormancy) scale allometrically so that larger seeds tend to allocate less to the coats. Larger seeds and lightweight coats might thus have evolved as correlated traits in crops. We tested whether 34 crops and 22 of their wild progenitors fit the allometry described in the literature, which would indicate co-selection of both traits during crop evolution. Deviations from the allometry would suggest that other evolutionary processes contribute to explain the emergence of larger, lightweight-coated seeds in crops. Crops fitted the scaling slope but deviated from its intercept in a consistent way: Seed coats of crops were lighter than expected by their seed size. The wild progenitors of crops displayed the same trend, indicating that deviations cannot be solely attributed to artificial selection during or after domestication. The evolution of seeds with small coats in crops likely resulted from a combination of various pressures, including the selection of wild progenitors with coats smaller than other wild plants, further decreases during early evolution under cultivation, and indirect selection due to the seed coat-seed size allometry.

Agroecological genetics of biomass allocation in wheat uncovers genotype interactions with canopy shade and plant size.

How plants distribute biomass among organs influences resource acquisition, reproduction and plant-plant interactions, and is essential in understanding plant ecology, evolution, and yield production in agriculture. However, the genetic mechanisms regulating allocation responses to the environment are largely unknown. We studied recombinant lines of wheat (Triticum spp.) grown as single plants under sunlight and simulated canopy shade to investigate genotype-by-environment interactions in biomass allocation to the leaves, stems, spikes, and grains. Size-corrected mass fractions and allometric slopes were employed to dissect allocation responses to light limitation and plant size. Size adjustments revealed light-responsive alleles associated with adaptation to the crop environment. Combined with an allometric approach, we demonstrated that polymorphism in the DELLA protein is associated with the response to shade and size. While a gibberellin-sensitive allelic effect on stem allocation was amplified when plants were shaded, size-dependent effects of this allele drive allocation to reproduction, suggesting that the ontogenetic trajectory of the plant affects the consequences of shade responses for allocation. Our approach provides a basis for exploring the genetic determinants underlying investment strategies in the face of different resource constraints and will be useful in predicting social behaviours of individuals in a crop community.

Negative allometry of leaf xylem conduit diameter and double-wall thickness: implications for implosion safety.

Xylem conduits have lignified walls to resist crushing pressures. The thicker the double-wall (T) relative to its diameter (D), the greater the implosion safety. Having safer conduits may incur higher costs and reduced flow, while having less resistant xylem may lead to catastrophic collapse under drought. Although recent studies have shown that conduit implosion commonly occurs in leaves, little is known about how leaf xylem scales T vs D to trade off safety, flow efficiency, mechanical support, and cost. We measured T and D in > 7000 conduits of 122 species to investigate how T vs D scaling varies across clades, habitats, growth forms, leaf, and vein sizes. As conduits become wider, their double-cell walls become proportionally thinner, resulting in a negative allometry between T and D. That is, narrower conduits, which are usually subjected to more negative pressures, are proportionally safer than wider ones. Higher implosion safety (i.e. higher T/D ratios) was found in asterids, arid habitats, shrubs, small leaves, and minor veins. Despite the strong allometry, implosion safety does not clearly trade off with other measured leaf functions, suggesting that implosion safety at whole-leaf level cannot be easily predicted solely by individual conduits' anatomy.

Cone allometry and seed protection from fire are similar in serotinous and nonserotinous conifers.

Serotiny is an adaptive trait that allows certain woody plants to persist in stand-replacing fire regimes. However, the mechanisms by which serotinous cones avoid seed necrosis and nonserotinous species persist in landscapes with short fire cycles and serotinous competitors remain poorly understood. To investigate whether ovulate cone traits that enhance seed survival differ between serotinous and nonserotinous species, we examined cone traits in 24 species within Pinaceae and Cupressaceae based on physical measurements and cone heating simulations using a computational fluid dynamics model. Fire-relevant cone traits were largely similar between cone types; those that differed (e.g. density and moisture) conferred little seed survival advantage under simulated fire. The most important traits influencing seed survival were cone size and seed depth within the cone, which was found to be an allometric function of cone mass for both cone types. Thus, nonserotinous cones should not suffer significantly greater seed necrosis than serotinous cones of equal size. Closed nonserotinous cones containing mature seeds may achieve substantial regeneration after fire if they are sufficiently large relative to fire duration and temperature. To our knowledge, this is the most comprehensive study of the effects of fire-relevant cone traits on conifer regeneration supported by physics-based fire simulation.

Structure and scaling of the middle ear in domestic dog breeds.

Although domestic dogs vary considerably in both body size and skull morphology, behavioural audiograms have previously been found to be similar in breeds as distinct as a Chihuahua and a St Bernard. In this study, we created micro-CT reconstructions of the middle ears and bony labyrinths from the skulls of 17 dog breeds, including both Chihuahua and St Bernard, plus a mongrel and a wolf. From these reconstructions, we measured middle ear cavity and ossicular volumes, eardrum and stapes footplate areas and bony labyrinth volumes. All of these ear structures scaled with skull size with negative allometry and generally correlated better with condylobasal length than with maximum or interaural skull widths. Larger dogs have larger ear structures in absolute terms: the volume of the St Bernard's middle ear cavity was 14 times that of the Chihuahua. The middle and inner ears are otherwise very similar in morphology, the ossicular structure being particularly well-conserved across breeds. The expectation that larger ear structures in larger dogs would translate into hearing ranges shifted towards lower frequencies is not consistent with the existing audiogram data. Assuming that the audiograms accurately reflect the hearing of the breeds in question, oversimplifications in existing models of middle ear function or limitations imposed by other parts of the auditory system may be responsible for this paradox.

Scaling of leaf area with biomass in trees reconsidered: constant metabolically active sapwood volume per unit leaf area with height growth.

Hypoallometric (slope<1) scaling between metabolic rate and body mass is often regarded as near-universal across organisms. However, there are compelling reasons to question hypoallometric scaling in woody plants, where metabolic rate is directly proportional to leaf area. This leaf area must provide carbon to the volume of the metabolically active sapwood (VMASW). Within populations of a species, variants in which VMASW increases per unit leaf area with height growth (e.g. ⅔ or ¾ scaling) would have proportionally less carbon for growth and reproduction as they grow taller. Therefore, selection should favor individuals in which, as they grow taller, leaf area scales isometrically with shoot VMASW (slope=1). Using tetrazolium staining, we measured total VMASW and total leaf area (LAtot) across 22 individuals of Ricinus communis and confirmed that leaf area scales isometrically with VMASW, and that VMASW is much smaller than total sapwood volume. With the potential of the LAtot-VMASW relationship to shape factors as diverse as the crown area-stem diameter relationship, conduit diameter scaling, reproductive output, and drought-induced mortality, our work indicates that the notion that sapwood increases per unit leaf area with height growth requires revision.