Eliot T. Miller

Functional distinctiveness of major plant lineages

Summary Plant traits vary widely across species and underpin differences in ecological strategy. Despite centuries of interest, the contributions of different evolutionary lineages to modern-day functional diversity remain poorly quantified. Expanding data bases of plant traits plus rapidly improving phylogenies enable for the first time a data-driven global picture of plant functional diversity across the major clades of higher plants. We mapped five key traits relevant to metabolism, resource competition and reproductive strategy onto a phylogeny across 48324 vascular plant species world-wide, along with climate and biogeographic data. Using a novel metric, we test whether major plant lineages are functionally distinctive. We then highlight the trait–lineage combinations that are most functionally distinctive within the present-day spread of ecological strategies. For some trait–clade combinations, knowing the clade of a species conveys little information to neo- and palaeo-ecologists. In other trait–clade combinations, the clade identity can be highly revealing, especially informative clade–trait combinations include Proteaceae, which is highly distinctive, representing the global slow extreme of the leaf economic spectrum. Magnoliidae and Rosidae contribute large leaf sizes and seed masses and have distinctively warm, wet climatic distributions. Synthesis. This analysis provides a shortlist of the most distinctive trait–lineage combinations along with their geographic and climatic context: a global view of extant functional diversity across the tips of the vascular plant phylogeny.

Mixed species flock, nest height, and elevation partially explain avian haemoparasite prevalence in Colombia

The high avian biodiversity present in the Neotropical region offers a great opportunity to explore the ecology of host-parasite relationships. We present a survey of avian haemoparasites in a megadiverse country and explore how parasite prevalences are related to physical and ecological host characteristics. Using light microscopy, we documented the presence of haemoparasites in over 2000 individuals belonging to 246 species of wild birds, from nine localities and several ecosystems of Colombia. We analysed the prevalence of six avian haemoparasite taxa in relation to elevation and the following host traits: nest height, nest type, foraging strata, primary diet, sociality, migratory behaviour, and participation in mixed species flocks. Our analyses indicate significant associations between both mixed species flocks and nest height and Haemoproteus and Leucocytozoon prevalence. The prevalence of Leucocytozoon increased with elevation, whereas the prevalence of Trypanosoma and microfilariae decreased. Plasmodium and Haemoproteus prevalence did not vary significantly with elevation; in fact, both parasites were found up to 3300m above sea level. The distribution of parasite prevalence across the phylogeny of bird species included in this study showed little host phylogenetic signal indicating that infection rates in this system are evolutionarily labile. Vector distribution as well as the biology of transmission and the maintenance of populations of avian haemoparasites deserve more detailed study in this system.

The Evolution of Energetic Scaling across the Vertebrate Tree of Life

Metabolism is the link between ecology and physiology—it dictates the flow of energy through individuals and across trophic levels. Much of the predictive power of metabolic theories of ecology derives from the scaling relationship between organismal size and metabolic rate. There is growing evidence that this scaling relationship is not universal, but we have little knowledge of how it has evolved over macroevolutionary time. Here we develop a novel phylogenetic comparative method to investigate how often and in which clades the macroevolutionary dynamics of the metabolic scaling have changed. We find strong evidence that the metabolic scaling relationship has shifted multiple times across the vertebrate phylogeny. However, shifts are rare and otherwise strongly constrained. Importantly, both the estimated slope and intercept values vary widely across regimes, with slopes that spanned across theoretically predicted values such as 2/3 or 3/4. We further tested whether traits such as ecto-/endothermy, genome size, and quadratic curvature with body mass (i.e., energetic constraints at extreme body sizes) could explain the observed pattern of shifts. Though these factors help explain some of the variation in scaling parameters, much of the remaining variation remains elusive. Our results lay the groundwork for further exploration of the evolutionary and ecological drivers of major transitions in metabolic strategy and for harnessing this information to improve macroecological predictions.

Radiating despite a Lack of Character: Ecological Divergence among Closely Related, Morphologically Similar Honeyeaters (Aves: Meliphagidae) Co-occurring in Arid Australian Environments

Quantifying the relationship between form and function can inform use of morphology as a surrogate for ecology. How the strength of this relationship varies continentally can inform understanding of evolutionary radiations; for example, does the relationship break down when certain lineages invade and diversify in novel habitats? The 75 species of Australian honeyeaters (Meliphagidae) are morphologically and ecologically diverse, with species feeding on nectar, insects, fruit, and other resources. We investigated Meliphagidae ecomorphology and community structure by (1) quantifying the concordance between morphology and ecology (foraging behavior), (2) estimating rates of trait evolution in relation to the packing of ecological space, and (3) comparing phylogenetic and trait community structure across the broad environmental gradients of the continent. We found that morphology explained 37% of the variance in ecology (and 62% vice versa), and we uncovered well-known bivariate relationships among the multivariate ecomorphological data. Ecological trait diversity declined less rapidly than phylogenetic diversity along a gradient of decreasing precipitation. We employ a new method (trait fields) and extend another (phylogenetic fields) to show that while species in phylogenetically clustered, arid-environment assemblages are similar morphologically, they are as varied in foraging behavior as those from more diverse assemblages. Thus, although closely related and similar morphologically, these arid-adapted species have diverged in ecological space to a similar degree as their mesic counterparts.

HormoneBase, a population-level database of steroid hormone levels across vertebrates

Hormones are central regulators of organismal function and flexibility that mediate a diversity of phenotypic traits from early development through senescence. Yet despite these important roles, basic questions about how and why hormone systems vary within and across species remain unanswered. Here we describe HormoneBase, a database of circulating steroid hormone levels and their variation across vertebrates. This database aims to provide all available data on the mean, variation, and range of plasma glucocorticoids (both baseline and stress-induced) and androgens in free-living and un-manipulated adult vertebrates. HormoneBase (www.HormoneBase.org) currently includes >6,580 entries from 476 species, reported in 648 publications from 1967 to 2015, and unpublished datasets. Entries are associated with data on the species and population, sex, year and month of study, geographic coordinates, life history stage, method and latency of hormone sampling, and analysis technique. This novel resource could be used for analyses of the function and evolution of hormone systems, and the relationships between hormonal variation and a variety of processes including phenotypic variation, fitness, and species distributions.

Metabolic scaling of stress hormones in vertebrates

Glucocorticoids (GCs) are stress hormones that can strongly influence physiology, behavior, and an organisms ability to cope with environmental change. Despite their importance, and the wealth of studies that have sought to understand how and why GC concentrations vary within species, we do not have a clear understanding of how circulating GC levels vary within and across the major vertebrate clades. New research has proposed that much interspecific variation in GC concentrations can be explained by variation in metabolism and body mass. Specifically, GC concentrations should vary proportionally with mass-specific metabolic rates and, given known scaling relationships between body mass and metabolic rate, GC concentrations should scale to the -1/4 power of body mass and to the power of 1 with mass-specific metabolic rate. Here, we use HormoneBase, the newly compiled database that includes plasma GC concentrations from free-living and unmanipulated vertebrates, to evaluate this hypothesis. Specifically, we explored the relationships between body mass or mass-specific metabolic rate and either baseline or stress-induced GC (cortisol or corticosterone) concentrations in tetrapods. Our phylogenetically-informed models suggest that, whereas the relationship between GC concentrations and body mass across tetrapods and among mammals is close to -1/4 power, this relationship does not exist in amphibians, reptiles, and birds. Moreover, with the exception of a positive association between stress-induced GC concentrations and mass-specific metabolic rate in birds, we found little evidence that GC concentrations are linked to metabolic rate, although the number of species sampled was quite limited for amphibians and somewhat so for reptiles and mammals. Nevertheless, these results stand in contrast to the generally accepted association between the two and suggest that our observed positive association between body mass and GC concentrations may not be due to the well-established link between mass and metabolism. Large-scale comparative approaches can come with drawbacks, such as pooling and pairing observations from separate sources. However, these broad analyses provide an important counterbalance to the majority of studies examining variation in GC concentrations at the population or species level, and can be a powerful approach to testing both long-standing and new questions in biology.

The vocalisations and species status of the White-lined and Kimberley Honeyeaters

Abstract The genus Meliphaga includes five species found in Australia. Two of these, the White-lined (M. albilineata) and Kimberley (M. fordiana) Honeyeaters, are endemic to sandstone habitats in the Northern Territory and Western Australia respectively. Few details are known about their vocalisations. Although large molecular differences separate the taxa, they are morphologically similar, and not all have accepted their status as full species. To shed more light on their distinctness, we combined our recordings of song with all other known recorded vocalisations and analysed vocal differences between the species. We demonstrate large differences between the songs of the species. Specifically, the White-lined Honeyeater sings songs with longer and more tremulous notes, longer pauses between notes, and a higher minimum frequency. The evidence presented here supports the retention of the Kimberley Honeyeater as a distinct species.

Climate, habitat, and geographic range overlap drive plumage evolution

Organismal appearances are shaped by selection from both abiotic and biotic drivers 1–5. For example, Gloger’s rule describes the pervasive pattern that more pigmented populations are found in more humid areas 1,6,7, and substrate matching as a form of camouflage to reduce predation is widespread across the tree of life 8–10. Sexual selection is a potent driver of plumage elaboration 5,11, and species may also converge on nearly identical colours and patterns in sympatry, often to avoid predation by mimicking noxious species 3,4 To date, no study has taken an integrative approach to understand how these factors determine the evolution of colour and pattern across a large clade of organisms. Here we show that both habitat and climate profoundly shape avian plumage. However, we also find a strong signal that many species exhibit remarkable convergence not explained by these factors nor by shared ancestry. Instead, this convergence is associated with geographic overlap between species, suggesting strong, albeit occasional, selection for interspecific mimicry. Consequently, both abiotic and biotic factors, including interspecific interactions, are potent drivers of phenotypic evolution.

Detecting Bias in Large-Scale Comparative Analyses: Methods for Expanding the Scope of Hypothesis-Testing with HormoneBase

To address large-scale questions in evolutionary biology, the compilation of data from a variety of sources is often required. This is a major challenge in the development of databases in organismal biology. Here, we describe the procedure we used to reconstruct the phylogeny of the 474 species represented in HormoneBase, including fish, amphibians, mammals, birds, and reptiles. We also provide the methodology used to compile vertebrate environmental, life history, and metabolic rate data for use in conjunction with the HormoneBase database to test hypotheses of the evolution of steroid hormone traits. We then report a series of analyses using these data to determine the extent to which field measures of circulating hormones and associated life history data exhibit taxonomic and geographic bias. By providing a detailed description of the approaches used to compile and evaluate these data and identifying potential biases in the collection of these data, we hope to make the HormoneBase database a more broadly useful resource for the scientific community to address a diversity of comparative questions.

IUCN Conservation Status Does Not Predict Glucocorticoid Concentrations in Reptiles and Birds

Circulating glucocorticoids (GCs) are the most commonly used biomarkers of stress in wildlife. However, their utility as a tool for identifying and/or managing at-risk species has varied. Here, we took a very broad approach to conservation physiology, asking whether International Union for the Conservation of Nature (IUCN) listing status (concern versus no obvious concern) and/or location within a geographic range (edge versus non-edge) predicted baseline and post-restraint concentrations of corticosterone (CORT) among many species of birds and reptiles. Even though such an approach can be viewed as coarse, we asked in this analysis whether CORT concentrations might be useful to implicate species at risk. Indeed, our effort, relying on HormoneBase, a repository of data on wildlife steroids, complements several other large-scale efforts in this issue to describe and understand GC variation. Using a phylogenetically informed Bayesian approach, we found little evidence that either IUCN status or edge/non-edge location in a geographic distribution were related to GC levels. However, we did confirm patterns described in previous studies, namely that breeding condition and evolutionary relatedness among species predicted some GC variation. Given the broad scope of our work, we are reluctant to conclude that IUCN status and location within a range are unrelated to GC regulation. We encourage future more targeted efforts on GCs in at-risk populations to reveal how factors leading to IUCN listing or the environmental conditions at range edges impact individual performance and fitness, particularly in the mammals, amphibians, and fish species we could not study here because data are currently unavailable.