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.     

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.     

Body size evolution in Mesozoic birds

The tendency for the mean body size of taxa within a clade to increase through evolution (Cope's Rule) has been demonstrated in a number of terrestrial vertebrate groups. However, because avian body size is strongly constrained by flight, any increase in size during the evolution of this lineage should be limited - there is a maximum size that can be attained by a bird for it to be able to get off the ground. Contrary to previous interpretations of early avian evolution, we demonstrate an overall increase in body size across Jurassic and Cretaceous flying birds: taxon body size increases from the earliest Jurassic through to the end of the Cretaceous, across a time span of 70 Myr. Although evidence is limited that this change is directional, it is certainly nonrandom. Relative size increase occurred presumably as the result of an increase in variance as the avian clade diversified after the origin of flight: a progression towards larger body size is seen clearly within the clades Pygostylia and Ornithothoraces. In contrast, a decrease in body size characterizes the most crownward lineage Ornithuromorpha, the clade that includes all extant taxa, and potentially may explain the survival of these birds across the Cretaceous-Palaeogene boundary. As in all other dinosaurs, counter selection for small size is seen in some clades, whereas body size is increasing overall.     

The evolution of large brain size in birds is related to social,not genetic,monogamy

There are several hypotheses suggesting that social complexity, including pair bonding, is important in the evolution of increased brain size. I examined whether genetic or social monogamy was related to large brain size in birds. Recent work has indicated that the length and strength of pair bonds are associated with large brain size. I tested several hypotheses for the evolution of large brain size in 42 species of bird by including life history variables in a regression model. A test on 100 phylogenetic trees revealed no phylogenetic signal in brain size. Controlling for body size, a principal components analysis was run on the life history variables and degrees of extra‐pair paternity. The main principal component (PC1) was regressed on brain size revealing a strong, positive association. Social, but not genetic, monogamy was positively related to brain size. Large brain size is related to the selective pressures of procuring extra‐pair copulations whilst maintaining a social partnership. However, other life history variables also loaded positively and significantly on brain size. These results indicate that the evolution of large brain size in birds was driven by several important selective pressures. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 111 , 668–678.     

Coevolution of body size and metabolic rate in vertebrates: a life‐history perspective

Despite many decades of research, the allometric scaling of metabolic rates (MRs) remains poorly understood. Here, we argue that scaling exponents of these allometries do not themselves mirror one universal law of nature but instead statistically approximate the non‐linearity of the relationship between MR and body mass. This ‘statistical’ view must be replaced with the life‐history perspective that ‘allows’ organisms to evolve myriad different life strategies with distinct physiological features. We posit that the hypoallometric allometry of MRs (mass scaling with an exponent smaller than 1) is an indirect outcome of the selective pressure of ecological mortality on allocation ‘decisions’ that divide resources among growth, reproduction, and the basic metabolic costs of repair and maintenance reflected in the standard or basal metabolic rate (SMR or BMR), which are customarily subjected to allometric analyses. Those ‘decisions’ form a wealth of life‐history variation that can be defined based on the axis dictated by ecological mortality and the axis governed by the efficiency of energy use. We link this variation as well as hypoallometric scaling to the mechanistic determinants of MR, such as metabolically inert component proportions, internal organ relative size and activity, cell size and cell membrane composition, and muscle contributions to dramatic metabolic shifts between the resting and active states. The multitude of mechanisms determining MR leads us to conclude that the quest for a single‐cause explanation of the mass scaling of MRs is futile. We argue that an explanation based on the theory of life‐history evolution is the best way forward.     

The evolution of parental care in freshwater leeches

Summary The life-history strategies of a selection of the most common European freshwater leeches (Euhirudinea) are described. On the basis of this information and results from the literature, the probable phylogenetic development of parental care in the Euhirudinea is reconstructed. The jawless worm leeches (Erpobdellidae) secrete a protective cocoon, cement it to the substrate and sometimes ventilate it before they leave the egg capsules. This behaviour represents the most ancient state in leech evolution. Members of the jawed Hirudinidae deposit desiccation-resistant cocoons on land. All known Glossiphoniidae (leeches equipped with a proboscis) have evolved the habit of brooding the eggs and young. These unique parental care patterns within one family of extant freshwater leeches can be arranged schematically in a series of increasing complexity which may reflect the evolution of brooding behaviour. Glossiphoniid leeches of the genus Helobdella, which have a world-wide distribution, display the most highly developed parental care system: they not only protect but also feed the young they carry. This results in the young being much larger when they leave the parent and, presumably, in higher subsequent survival. Isolated cocoons of all aquatic leeches are rapidly destroyed by predators, primarily water snails. In erpobdellids (but not glossiphoniids, which protect the cocoons) a large portion of the cocoons are lost due to predatory attacks. We conclude that the major selective pressure driving the evolution of parental care in leeches may have been predation on eggs and juvenile stages. Dedicated to Professor Dr. G. Osche on the occasion of his 75th birthday     

Time‐limited environments affect the evolution of egg–body size allometry

Initial offspring size is a fundamental component of absolute growth rate, where large offspring will reach a given adult body size faster than smaller offspring. Yet, our knowledge regarding the coevolution between offspring and adult size is limited. In time‐constrained environments, organisms need to reproduce at a high rate and reach a reproductive size quickly. To rapidly attain a large adult body size, we hypothesize that, in seasonal habitats, large species are bound to having a large initial size, and consequently, the evolution of egg size will be tightly matched to that of body size, compared to less time‐limited systems. We tested this hypothesis in killifishes, and found a significantly steeper allometric relationship between egg and body sizes in annual, compared to nonannual species. We also found higher rates of evolution of egg and body size in annual compared to nonannual species. Our results suggest that time‐constrained environments impose strong selection on rapidly reaching a species‐specific body size, and reproduce at a high rate, which in turn imposes constraints on the evolution of egg sizes. In combination, these distinct selection pressures result in different relationships between egg and body size among species in time‐constrained versus permanent habitats.     

Body size evolution in Mesozoic birds: little evidence for Cope's rule

Cope's rule, the tendency towards evolutionary increases in body size, is a long-standing macroevolutionary generalization that has the potential to provide insights into directionality in evolution; however, both the definition and identification of Cope's rule are controversial and problematic. A recent study [J. Evol. Biol. 21 (2008) 618] examined body size evolution in Mesozoic birds, and claimed to have identified evidence of Cope's rule occurring as a result of among-lineage species sorting. We here reassess the results of this study, and additionally carry out novel analyses testing for within-lineage patterns in body size evolution in Mesozoic birds. We demonstrate that the nonphylogenetic methods used by this previous study cannot distinguish between among- and within-lineage processes, and that statistical support for their results and conclusions is extremely weak. Our ancestor-descendant within-lineage analyses explicitly incorporate recent phylogenetic hypotheses and find little compelling evidence for Cope's rule. Cope's rule is not supported in Mesozoic birds by the available data, and body size evolution currently provides no insights into avian survivorship through the Cretaceous-Paleogene mass extinction.     

Toward a synthetic understanding of the role of phenology in ecology and evolution

Phenology affects nearly all aspects of ecology and evolution. Virtually all biological phenomena—from individual physiology to interspecific relationships to global nutrient fluxes—have annual cycles and are influenced by the timing of abiotic events. Recent years have seen a surge of interest in this topic, as an increasing number of studies document phenological responses to climate change. Much recent research has addressed the genetic controls on phenology, modelling techniques and ecosystem-level and evolutionary consequences of phenological change. To date, however, these efforts have tended to proceed independently. Here, we bring together some of these disparate lines of inquiry to clarify vocabulary, facilitate comparisons among habitat types and promote the integration of ideas and methodologies across different disciplines and scales. We discuss the relationship between phenology and life history, the distinction between organismal- and population-level perspectives on phenology and the influence of phenology on evolutionary processes, communities and ecosystems. Future work should focus on linking ecological and physiological aspects of phenology, understanding the demographic effects of phenological change and explicitly accounting for seasonality and phenology in forecasts of ecological and evolutionary responses to climate change.     

Longevity is associated with relative brain size in birds

Brain size of vertebrates has long been recognized to evolve in close association with basic life‐history traits, including lifespan. According to the cognitive buffer hypothesis, large brains facilitate the construction of behavioral responses against novel socioecological challenges through general cognitive processes, which should reduce mortality and increase lifespan. While the occurrence of brain size–lifespan correlation has been well documented in mammals, much less evidence exists for a robust link between brain size and longevity in birds. The aim of this study was to use phylogenetically controlled comparative approach to test for the relationship between brain size and longevity among 384 avian species from 23 orders. We used maximum lifespan and maximum reproductive lifespan as the measures of longevity and accounted for a set of possible confounding effects, such as allometry, sampling effort, geographic patterns, and life‐history components (clutch size, incubation length, and mode of development). We found that both measures of longevity positively correlated with relative (residual) brain size. We also showed that major diversification of brain size preceded diversification of longevity in avian evolution. In contrast to previous findings, the effect of brain size on longevity was consistent across lineages with different development patterns, although the relatively low strength of this correlation could likely be attributed to the ubiquity of allomaternal care associated with the altricial mode of development. Our study indicates that the positive relationship between brain size and longevity in birds may be more general than previously thought.     

Correlated evolution of host and parasite body size: tests of Harrison's rule using birds and lice

Large-bodied species of hosts often harbor large-bodied parasites, a pattern known as Harrison's rule. Harrison's rule has been documented for a variety of animal parasites and herbivorous insects, yet the adaptive basis of the body-size correlation is poorly understood. We used phylogenetically independent methods to test for Harrison's rule across a large assemblage of bird lice (Insecta: Phthiraptera). The analysis revealed a significant relationship between louse and host size, despite considerable variation among taxa. We explored factors underlying this variation by testing Harrison's rule within two groups of feather-specialist lice that share hosts (pigeons and doves). The two groups, wing lice (Columbicola spp.) and body lice (Physconelloidinae spp.), have similar life histories, despite spending much of their time on different feather tracts. Wing lice showed strong support for Harrison's rule, whereas body lice showed no significant correlation with host size. Wing louse size was correlated with wing feather size, which was in turn correlated with overall host size. In contrast, body louse size showed no correlation with body feather size, which also was not correlated with overall host size. The reason why body lice did not fit Harrison's rule may be related to the fact that different species of body lice use different microhabitats within body feathers. More detailed measurements of body feathers may be needed to explore the precise relationship of body louse size to relevant components of feather size. Whatever the reason, Harrison's rule does not hold in body lice, possibly because selection on body size is mediated by community-level interactions between body lice.     

Exceptional avian herbivores: multiple transitions toward herbivory in the bird order Anseriformes and its correlation with body mass

Herbivory is rare among birds and is usually thought to have evolved predominately among large, flightless birds due to energetic constraints or an association with increased body mass. Nearly all members of the bird order Anseriformes, which includes ducks, geese, and swans, are flighted and many are predominately herbivorous. However, it is unknown whether herbivory represents a derived state for the order and how many times a predominately herbivorous diet may have evolved. Compiling data from over 200 published diet studies to create a continuous character for herbivory, models of trait evolution support at least five independent transitions toward a predominately herbivorous diet in Anseriformes. Although a nonphylogenetic correlation test recovers a significant positive correlation between herbivory and body mass, this correlation is not significant when accounting for phylogeny. These results indicate a lack of support for the hypothesis that a larger body mass confers an advantage in the digestion of low‐quality diets but does not exclude the possibility that shifts to a more abundant food source have driven shifts toward herbivory in other bird lineages. The exceptional number of transitions toward a more herbivorous diet in Anseriformes and lack of correlation with body mass prompts a reinterpretation of the relatively infrequent origination of herbivory among flighted birds.     

Experimental analysis of an early life‐history stage: avian predation selects for larger body size of hatchling turtles

One common life‐history pattern involves an elevated rate and nonrandom distribution of neonatal mortality. However, the mechanisms causing this pattern and the specific traits that confer a survival benefit are not always evident. We conducted a manipulative field experiment using red‐eared slider turtles to test the hypothesis that diurnal avian predators are a primary cause of size‐specific neonatal mortality. Body size was a significant predictor of recapturing hatchlings alive and of finding hatchlings dead under natural conditions, but was unimportant when diurnal predators were excluded from the field site. Overall recapture rates also more than doubled when predators were excluded compared to natural conditions (72.4 vs. 34.9%). We conclude that birds are an important cause of size‐specific mortality of recently emerged hatchling turtles and that ‘bigger is better’ in this system, which has important implications for life‐history evolution in organisms that experience size‐specific neonatal mortality.     

Migrate small,sound big: functional constraints on body size promote tracheal elongation in cranes

Organismal traits often represent the outcome of opposing selection pressures. Although social or sexual selection can cause the evolution of traits that constrain function or survival (e.g. ornamental feathers), it is unclear how the strength and direction of selection respond to ecological shifts that increase the severity of the constraint. For example, reduced body size might evolve by natural selection to enhance flight performance in migratory birds, but social or sexual selection favouring large body size may provide a countervailing force. Tracheal elongation is a potential outcome of these opposing pressures because it allows birds to convey an auditory signal of exaggerated body size. We predicted that the evolution of migration in cranes has coincided with a reduction in body size and a concomitant intensification of social or sexual selection for apparent large body size via tracheal elongation. We used a phylogenetic comparative approach to examine the relationships among migration distance, body mass and trachea length in cranes. As predicted, we found that migration distance correlated negatively with body size and positively with proportional trachea length. This result was consistent with our hypothesis that evolutionary reductions in body size led to intensified selection for trachea length. The most likely ultimate causes of intensified positive selection on trachea length are the direct benefits of conveying a large body size in intraspecific contests for mates and territories. We conclude that the strength of social or sexual selection on crane body size is linked to the degree of functional constraint.     

Condition‐dependent mortality exacerbates male (but not female) reproductive senescence and the potential for sexual conflict

Disentangling the relationship between age and reproduction is central to understand life‐history evolution, and recent evidence shows that considering condition‐dependent mortality is a crucial piece of this puzzle. For example, nonrandom mortality of ‘low‐condition’ individuals can lead to an increase in average lifespan. However, selective disappearance of such low‐condition individuals may also affect reproductive senescence at the population level due to trade‐offs between physiological functions related to survival/lifespan and the maintenance of reproductive functions. Here, we address the idea that condition‐dependent extrinsic mortality (i.e. simulated predation) may increase the age‐related decline in male reproductive success and with it the potential for sexual conflict, by comparing reproductive ageing in Drosophila melanogaster male/female cohorts exposed (or not) to condition‐dependent simulated predation across time. Although female reproductive senescence was not affected by predation, male reproductive senescence was considerably higher under predation, due mainly to an accelerated decline in offspring viability of ‘surviving’ males with age. This sex‐specific effect suggests that condition‐dependent extrinsic mortality can exacerbate survival‐reproduction trade‐offs in males, which are typically under stronger condition‐dependent selection than females. Interestingly, condition‐dependent extrinsic mortality did not affect mating success, hinting that accelerated reproductive senescence is due to a decrease in male post‐copulatory fitness components. Our results support the recent proposal that male ageing can be an important source of sexual conflict, further suggesting this effect could be exacerbated under more natural conditions.     

An integrated analysis of phenotypic selection on insect body size and development time

Most studies of phenotypic selection do not estimate selection or fitness surfaces for multiple components of fitness within a unified statistical framework. This makes it difficult or impossible to assess how selection operates on traits through variation in multiple components of fitness. We describe a new generation of aster models that can evaluate phenotypic selection by accounting for timing of life‐history transitions and their effect on population growth rate, in addition to survival and reproductive output. We use this approach to estimate selection on body size and development time for a field population of the herbivorous insect, Manduca sexta (Lepidoptera: Sphingidae). Estimated fitness surfaces revealed strong and significant directional selection favoring both larger adult size (via effects on egg counts) and more rapid rates of early larval development (via effects on larval survival). Incorporating the timing of reproduction and its influence on population growth rate into the analysis resulted in larger values for size in early larval development at which fitness is maximized, and weaker selection on size in early larval development. These results illustrate how the interplay of different components of fitness can influence selection on size and development time. This integrated modeling framework can be readily applied to studies of phenotypic selection via multiple fitness components in other systems.     

The role of birds in sustainable food production

Birds (Class Aves) are already an important source of food in most parts of the world. Only a few species have been successfully domesticated but many others are harvested from the wild. There is potential for greater use of birds as a food source. Existing domesticated species, especially galliforms, need to be better utilized. Certain new species could be brought into domestication. The efficiency and sustainability of harvesting methods for free-living birds might be improved and the harvesting of new species should be considered. These measures could be compatible with improved conservation of wild birds and their habitats, but careful planning and surveillance are essential prerequisites.     

Integration of Random Forest with population‐based outlier analyses provides insight on the genomic basis and evolution of run timing in Chinook salmon (Oncorhynchus tshawytscha)

Anadromous Chinook salmon populations vary in the period of river entry at the initiation of adult freshwater migration, facilitating optimal arrival at natal spawning. Run timing is a polygenic trait that shows evidence of rapid parallel evolution in some lineages, signifying a key role for this phenotype in the ecological divergence between populations. Studying the genetic basis of local adaptation in quantitative traits is often impractical in wild populations. Therefore, we used a novel approach, Random Forest, to detect markers linked to run timing across 14 populations from contrasting environments in the Columbia River and Puget Sound, USA. The approach permits detection of loci of small effect on the phenotype. Divergence between populations at these loci was then examined using both principle component analysis and F_ST outlier analyses, to determine whether shared genetic changes resulted in similar phenotypes across different lineages. Sequencing of 9107 RAD markers in 414 individuals identified 33 predictor loci explaining 79.2% of trait variance. Discriminant analysis of principal components of the predictors revealed both shared and unique evolutionary pathways in the trait across different lineages, characterized by minor allele frequency changes. However, genome mapping of predictor loci also identified positional overlap with two genomic outlier regions, consistent with selection on loci of large effect. Therefore, the results suggest selective sweeps on few loci and minor changes in loci that were detected by this study. Use of a polygenic framework has provided initial insight into how divergence in a trait has occurred in the wild.     

Lifetime selection on adult body size and components of body size in a waterstrider: opposing selection and maintenance of sexual size dimorphism

Abstract.— Sexual size dimorphism (SSD), the difference in body size between males and females, is common in almost all taxa of animals and is generally assumed to be adaptive. Although sexual selection and fecundity selection alone have often been invoked to explain the evolution of SSD, more recent views indicate that the sexes must experience different lifetime selection pressures for SSD to evolve and be maintained. We estimated selection acting on male and female adult body size (total length) and components of body size in the waterstrider Aquarius remigis during three phases of life history. Opposing selection pressures for overall body size occurred in separate episodes of fitness for females in both years and for males in one year. Specific components of body size were often the targets of the selection on overall body size. When net adult fitness was estimated by combining each individual's fitnesses from all episodes, we found stabilizing selection in both sexes. In addition, the net optimum overall body size of males was smaller than that of females. However, even when components of body size had experienced opposing selection pressures in individual episodes, no components appeared to be under lifetime stabilizing selection. This is the first evidence that contemporary selection in a natural population acts to maintain female size larger than male size, the most common pattern of SSD in nature.