The evolution of body size in birds. I. Evidence for non-random diversification

The hypothesis that evolution of body size in birds was a random process coupled with an absolute lower boundary on body mass was tested using data on 6217 species of extant birds. The test was based on the fact that subclades within birds that have body masses much larger than this minimum should not have skewed log body mass distributions, while clades close to this boundary should. Bird species were classified into 23 orders suggested by Sibley and Monroe (1988). Thirteen orders that had average log body masses greater than the average for all birds had significantly skewed log body mass distributions. This is inconsistent with the hypothesis that evolution of body size in birds is random, but is constrained only at the smallest body masses. Most orders of birds cannot be considered random samples from the parental distribution of all birds. When the pattern of body mass evolution in birds is reconstructed using an estimate of the phylogenetic relationships among orders, there are many more instances where a large taxon putatively originated from a smaller one than vice versa. The non-random nature of body mass evolution in birds is consistent with models that postulate that evolution is constrained by the ability of individuals to turn resources into offspring.     

Interspecific geographic range size–body size relationship and the diversification dynamics of Neotropical furnariid birds

Among the earliest macroecological patterns documented, is the range and body size relationship, characterized by a minimum geographic range size imposed by the species’ body size. This boundary for the geographic range size increases linearly with body size and has been proposed to have implications in lineages evolution and conservation. Nevertheless, the macroevolutionary processes involved in the origin of this boundary and its consequences on lineage diversification have been poorly explored. We evaluate the macroevolutionary consequences of the difference (hereafter the distance) between the observed and the minimum range sizes required by the species’ body size, to untangle its role on the diversification of a Neotropical species‐rich bird clade using trait‐dependent diversification models. We show that speciation rate is a positive hump‐shaped function of the distance to the lower boundary. The species with highest and lowest distances to minimum range size had lower speciation rates, while species close to medium distances values had the highest speciation rates. Further, our results suggest that the distance to the minimum range size is a macroevolutionary constraint that affects the diversification process responsible for the origin of this macroecological pattern in a more complex way than previously envisioned.     

Brain size and the expression of pheomelanin-based colour in birds

Eumelanin and pheomelanin are the most common vertebrate pigments. They generate different colours and are synthesized under different physiological conditions. While pheomelanogenesis requires high levels of a key intracellular antioxidant (glutathione, GSH), eumelanogenesis is inhibited by GSH. This implies that species that present the molecular basis to produce large amounts of pheomelanin might be more limited to perform other costly processes that generate oxidative stress than species that produce eumelanin. Brain development requires large amounts of energy and antioxidants during ontogeny, so that large-brained species may be constrained in their simultaneous synthesis of large amounts of pheomelanin, but not in their synthesis of eumelanin. Here, we tested this hypothesis in a large dataset of 323 bird species. After controlling for the effects of phylogeny, latitude and sexual dichromatism, the proportion of pheomelanic plumage colour was strongly negatively related to the relative brain mass of species, whereas no relationship was found for the proportion of eumelanic colour. This indicates that the production of pheomelanin is a costly process that cannot evolve together with complex neural structures and thus with large cognitive capacity. This is the first time that the expression of melanic traits is found to correlate with another phenotypic character across species.     

Global biogeography and ecology of body size in birds

In 1847, Karl Bergmann proposed that temperature gradients are the key to understanding geographic variation in the body sizes of warm-blooded animals. Yet both the geographic patterns of body-size variation and their underlying mechanisms remain controversial. Here, we conduct the first assemblage-level global examination of 'Bergmann's rule' within an entire animal class. We generate global maps of avian body size and demonstrate a general pattern of larger body sizes at high latitudes, conforming to Bergmann's rule. We also show, however, that median body size within assemblages is systematically large on islands and small in species-rich areas. Similarly, while spatial models show that temperature is the single strongest environmental correlate of body size, there are secondary correlations with resource availability and a strong pattern of decreasing body size with increasing species richness. Finally, our results suggest that geographic patterns of body size are caused both by adaptation within lineages, as invoked by Bergmann, and by taxonomic turnover among lineages. Taken together, these results indicate that while Bergmann's prediction based on physiological scaling is remarkably accurate, it is far from the full picture. Global patterns of body size in avian assemblages are driven by interactions between the physiological demands of the environment, resource availability, species richness and taxonomic turnover among lineages.     

Biogeography of body size in Pacific island birds

Many insular vertebrates have undergone rapid and dramatic changes in body size compared to their mainland counterparts. Here we explore the relationship between two well known patterns of island body size – the tendency for large‐bodied species to dwarf and small‐bodied species to get larger on islands, known as the “island rule”, and the scaling of maximum and minimum body size of island assemblages with island area. Drawing on both fossil and modern data, we examined the relationship between body size and island area in Pacific island birds, both within clades and at the island assemblage level. We found that the size of the smallest bird on each island decreased with island area while the maximum body size increased with island area. Similarly, within clades the body size of small‐bodied groups decreased and large‐bodied groups increased from small to large islands, consistent with the island rule. However, the magnitude of size change within clades was not sufficient to explain the overall scaling of maximum size with island area. Instead, the pattern was driven primarily by the evolution of very large, flightless birds on large islands. Human‐mediated extinctions on islands over the past few millennia severely impacted large, flightless birds, to the effect that this macroecological pattern has been virtually erased. After controlling for effects of biogeographic region and island area, we found island productivity to be the best predictor of maximum size in flightless birds. This result, and the striking similarities in maximum body size between flightless birds and island mammals, suggests a common energetic mechanism linking body size and landmass area in both the island rule and the scaling of island body size extremes.     

Brain size, development and metabolism in birds and mammals

Recent hypotheses that variation in brain size among birds and mammals result from differences in metabolic allocation during ontogeny are tested.
Indices of embryonic and post-embryonic brain growth are defined. Precocial birds and mammals have high embryonic brain growth indices which are compensated for by low post-embryonic indices (with the exception of Homo supiens ). In contrast, altricial birds and mammals have low embryonic and high post-embryonic indices. Altricial birds have relatively small brains at hatching and develop relatively large brains as adults, but among mammals there is no equivalent correlation between variation in adult relative brain sizes and state of neonatal development.
Compensatory brain development in both birds and mammals is associated with compensatory parental metabolic allocation. In comparison with altricial development, precocial development is characterized by higher levels of brain growth and parental metabolic allocation prior to hatching or birth and lower levels subsequently. Differences between degrees of postnatal investment by the parents in the young of precocial birds versus precocial mammals may result in the different patterns of adult brain size associated with precociality versus altriciality in the two groups.
The allometric exponent scaling brain on body size differs among taxonomic levels in birds. The exponent is higher for some parts of the brain than others, irrespective of taxonomic level. Unlike mammals, the exponents for birds do not show a general increase with taxonomic level. These pattcrns call into question recent interpretations of the allometric exponent in birds. and the reason for changes in exponent with taxonomic level.     

Climate,body condition and spleen size in birds

Climatic conditions may impact on the body condition of animals and thereby affect their survival prospects. However, climate may also impact directly on the survival prospects of animals by affecting the size of immune defence organs that are used for defence against parasites. We used a large long-term database on body condition and size of the spleen in birds to test for immediate and delayed relationships between climatic conditions as indexed by the North Atlantic Oscillation (NAO) and body condition and spleen mass, respectively. Across 14 species of birds, spleen mass was significantly positively correlated with the NAO index, while the delayed effect of NAO on spleen mass was not significant. Spleen mass was positively related to body condition, but body condition did not depend significantly on NAO or delayed NAO effects. Bird species with a strong positive effect of NAO on spleen mass tended to have small spleens for their body size, while species with a strong negative effect of NAO on spleen mass tended to have relatively large spleens. Since bird species with relatively large spleen have been shown to suffer more from the negative effects of parasites, we can infer that the effects of climate as indexed by NAO on the size of the spleen depends on the importance of parasite-mediated natural selection.Due to an error in the citation line, this revised PDF (published in December 2003) deviates from the printed version, and is the correct and authoritative version of the paper.     

The scaling of eye size with body mass in birds

We developed a simple method that uses skulls to estimate the diameter, and hence the mass, of birds'' eyes. Allometric analysis demonstrated that, within five orders (parrots, pigeons, petrels, raptors and owls) and across 104 families of flying birds, eye mass is proportional to (body mass)^0.68 over a range of body masses (6 g to 11.3 kg). As expected from their habits and visual ecology, raptors and owls have enlarged eyes, with masses 1.4 and 2.2 times greater than average birds of the same weight. Taking existing relationships for flight speed on body mass, we find that resolution increases close to (flight speed)^1.333. Consequently, large birds resolve objects at a longer time to contact than small birds. Eye radius and skull size co-vary in strict proportion, suggesting common physiological, aerodynamic and mechanical constraints. Because eye mass scales close to brain mass, metabolic rate and information processing could also be limiting, but the precise factors determining the scaling of eye to body have not been identified.     

Brain size, innovative propensity and migratory behaviour in temperate Palaearctic birds

The evolution of migration in birds remains an outstanding, unresolved question in evolutionary ecology. A particularly intriguing question is why individuals in some species have been selected to migrate, whereas in other species they have been selected to be sedentary. In this paper, we suggest that this diverging selection might partially result from differences among species in the behavioural flexibility of their responses to seasonal changes in the environment. This hypothesis is supported in a comparative analysis of Palaearctic passerines. First, resident species tend to rely more on innovative feeding behaviours in winter, when food is harder to find, than in other seasons. Second, species with larger brains, relative to their body size, and a higher propensity for innovative behaviours tend to be resident, while less flexible species tend to be migratory. Residence also appears to be less likely in species that occur in more northerly regions, exploit temporally available food sources, inhabit non-buffered habitats and have smaller bodies. Yet, the role of behavioural flexibility as a response to seasonal environments is largely independent of these other factors. Therefore, species with greater foraging flexibility seem to be able to cope with seasonal environments better, while less flexible species are forced to become migratory.     

Brain size and resource specialization predict long-term population trends in British birds

Large-scale population declines have been documented across many faunal assemblages. However, there is much variation in population trends for individual species, and few indications of which specific ecological and behavioural characteristics are associated with such trends. We used the British Common Birds Census (1968-1995) to identify specific traits associated with long-term abundance trends in UK farmland birds. Two factors, resource specialization and relative brain size, were significantly associated with population trend, such that species using atypical resources and with relatively small brains were most likely to have experienced overall declines. Further analyses of specific brain components indicated that the relative size of the telencephalon, the part of the brain associated with problem solving and complex behaviours, and the brain stem might be better predictors of population trend than overall brain size. These results suggest that flexibility in resource use and behaviour are the most important characteristics for determining a species' ability to cope with large-scale habitat changes.     

A statistical test of unbiased evolution of body size in birds

Abstract.— Of the approximately 9500 bird species, the vast majority is small-bodied. That is a general feature of evolutionary lineages, also observed for instance in mammals and plants. The avian interspecific body size distribution is right-skewed even on a logarithmic scale. That has previously been interpreted as evidence that body size evolution has been biased. However, a procedure to test for unbiased evolution from the shape of body size distributions was lacking. In the present paper unbiased body size evolution is defined precisely, and a statistical test is developed based on Monte Carlo simulation of unbiased evolution. Application of the test to birds suggests that it is highly unlikely that avian body size evolution has been unbiased as defined. Several possible explanations for this result are discussed. A plausible explanation is that the general model of unbiased evolution assumes that population size and generation time do not affect the evolutionary variability of body size; that is, that micro- and macroevolution are decoupled, which theory suggests is not likely to be the case.     

Latitudinal variation in subspecific diversification of birds

Patterns of evolution are believed to vary latitudinally, but our understanding of this variation remains limited. Here we examine how patterns of subspecific diversification vary within species of birds, specifically addressing three questions: (1) Are subspecies more numerous at lower latitudes within species, consistent with greater phenotypic differentiation at lower latitudes? (2) If there are more subspecies at lower latitudes within species, can area of breeding range explain this relationship? and (3) how do latitudinal differences in subspecies within species vary geographically across the globe? Using all species with five or more subspecies from 12 of the most diverse families of birds in the world, we found consistently more subspecies at lower latitudes across all families, both hemispheres, and all continents examined. Despite the positive influence of area on the number of subspecies within species, area did not explain the greater number of subspecies at lower latitudes within species. Global patterns of subspecies support the idea that phenotypic differentiation of populations is greater at lower latitudes within species. If subspecies density provides an index of rates of incipient speciation, then our results support evolutionary hypotheses for the latitudinal diversity gradient that invoke higher tropical speciation rates.     

Latitude and rates of diversification in birds and butterflies

Central to many explanations of latitudinal diversity gradients is the idea that rates of species diversification increase towards the equator. However, there have been few explicit tests of whether or not this pattern exists. Using sister-group analyses to compare 48 clades of passerine birds and swallowtail butterflies from different latitudes, I found evidence that relative rates of diversification per unit time are indeed higher towards the equator. This pattern is explicable in terms of abiotic factors which vary continuously with latitude, and may be further enhanced by diversity-dependent speciation and extinction processes.     

Global diversification rates of passerine birds

The distribution of species richness in families of passerine birds suggests that the net rate of diversification was significantly higher than average in as many as 7 out of 47 families. However, the absence of excess species richness among the 106 tribes within these families indicates that these high rates were transient, perhaps associated in some cases with tectonic movements or dispersal events that extended geographical ranges. Thus, large clade size among passerine birds need not represent intrinsic key innovations that influence the rate of diversification. Approximately 17 families and 30 tribes have too few species relative to other passerine taxa. Many of these are ecologically or geographically marginal, being especially overrepresented in the Australasian region. Observed intervals between lineage splitting suggest that extinction has occurred ca. 90% as frequently as speciation (waiting times of 1.03 and 0.93 Myr) and that the 47 modern families comprising 5712 species descended from approximately 430 passerine lineages extant 24 Myr ago. Speciation and extinction rates among small, marginal families might be 1-2 orders of magnitude lower.     

Larger brains spur species diversification in birds

Evidence is accumulating that species traits can spur their evolutionary diversification by influencing niche shifts, range expansions, and extinction risk. Previous work has shown that larger brains (relative to body size) facilitate niche shifts and range expansions by enhancing behavioral plasticity but whether larger brains also promote evolutionary diversification is currently backed by insufficient evidence. We addressed this gap by combining a brain size dataset for >1900 avian species worldwide with estimates of diversification rates based on two conceptually different phylogenetic‐based approaches. We found consistent evidence that lineages with larger brains (relative to body size) have diversified faster than lineages with relatively smaller brains. The best supported trait‐dependent model suggests that brain size primarily affects diversification rates by increasing speciation rather than decreasing extinction rates. In addition, we found that the effect of relatively brain size on species‐level diversification rate is additive to the effect of other intrinsic and extrinsic factors. Altogether, our results highlight the importance of brain size as an important factor in evolution and reinforce the view that intrinsic features of species have the potential to influence the pace of evolution.     

The 'island rule' in birds: medium body size and its ecological explanation

Do birds show a different pattern of insular evolution from mammals? Mammals follow the ''island rule'', with large-bodied species getting smaller on islands and small-bodied species getting bigger. By contrast, the traditional view on birds is that they follow no general island rule for body size, but that there is an insular trend for large bills. Insular shifts in feeding ecology are, therefore, widely assumed to be the primary cause of divergence in island birds. We use a comparative approach to test these ideas. Contrary to the traditional view, we find no evidence for increased bill size in insular populations. Instead, changes in both bill size and body size obey the ''island rule''. The differences between our results and the traditional view arise because previous analyses were based largely on passerines. We also investigate some ecological factors that are thought to influence island evolution. As predicted by the traditional view, shifts in bill size are associated with feeding ecology. By contrast, shifts in body size are associated with the potential for intraspecific competition and thermal ecology. All these results remain qualitatively unchanged when we use different methods to score the ecological factors and restrict our analyses to taxa showing pronounced morphological divergence. Because of strong covariation between ecological factors, however, we cannot estimate the relative importance of each ecological factor. Overall, our results show that the island rule is valid for both body size and bill length in birds and that, in addition to feeding ecology, insular shifts in the level of intraspecific competition and the abiotic environment also have a role.