Mass extinctions do not explain skew in interspecific body size distributions

In several higher animal taxa, such as mammals and birds, the distribution of species body sizes is heavily skewed towards small size. Previous studies have suggested that small‐bodied organisms are less prone to extinction than large‐bodied species. If small body size is favourable during mass extinction events, a post mass extinction excess of small‐bodied species may proliferate and maintain skewed body size distributions sometime after. Here, we modelled mass extinctions and found that even unrealistically strong body mass selection has little effect on the skew of interspecific body size distributions. Moreover, selection against large body size may, counter intuitively, skew size distributions towards large body size. In any case, subsequent evolutionary diversification rapidly erases these rather small effects mass extinctions may have on size distributions. Next, we used body masses of extant species and phylogenetic methods to investigate possible changes in body size distributions across the Cretaceous–Paleogene (K‐Pg) mass extinction. Body size distributions of extant clades that originated during the Cretaceous are on average more skewed than their subclades that originated during the Paleogene, but the difference is only minor in mammals, and in birds, it can be explained by a positive relationship between species richness and skewness that is also present in clades that originated after the transition. Hence, we cannot infer from extant species whether the K‐Pg mass extinctions were size‐selective, but they are not the reason why most extant bird and mammal species are small‐bodied.     

THE MICRO AND MACRO IN BODY SIZE EVOLUTION

The diversity of body sizes of organisms has traditionally been explained in terms of microevolutionary processes: natural selection owing to differential fitness of individual organisms, or to macroevolutionary processes: species selection owing to the differential proliferation of phylogenetic lineages. Data for terrestrial mammals and birds indicate that even on a logarithmic scale frequency distributions of body mass among species are significantly skewed towards larger sizes. We used simulation models to evaluate the extent to which macro- and microevolutionary processes are sufficient to explain these distributions. Simulations of a purely cladogenetic process with no bias in extinction or speciation rates for different body sizes did not produce skewed log body mass distributions. Simulations that included size-biased extinction rates, especially those that incorporated anagenetic size change within species between speciation and extinction events, regularly produced skewed distributions. We conclude that although cladogenetic processes probably play a significant role in body size evolution, there must also be a significant anagenetic component. The regular variation in the form of mammalian body size distributions among different-sized islands and continents suggests that environmental conditions, operating through both macro- and microevolutionary processes, determine to a large extent the diversification of body sizes within faunas. Macroevolution is not decoupled from microevolution.     

The evolution of high summit metabolism and cold tolerance in birds and its impact on present-day distributions

Summit metabolic rate ( M_sum , maximum cold-induced metabolic rate) is positively correlated with cold tolerance in birds, suggesting that high M_sum is important for residency in cold climates. However, the phylogenetic distribution of high M_sum among birds and the impact of its evolution on current distributions are not well understood. Two potential adaptive hypotheses might explain the phylogenetic distribution of high M_sum among birds. The cold adaptation hypothesis contends that species wintering in cold climates should have higher M_sum than species wintering in warmer climates. The flight adaptation hypothesis suggests that volant birds might be capable of generating high M_sum as a byproduct of their muscular capacity for flight; thus, variation in M_sum should be associated with capacity for sustained flight, one indicator of which is migration. We collected M_sum data from the literature for 44 bird species and conducted both conventional and phylogenetically informed statistical analyses to examine the predictors of M_sum variation. Significant phylogenetic signal was present for log body mass, log mass-adjusted M_sum , and average temperature in the winter range. In multiple regression models, log body mass, winter temperature, and clade were significant predictors of log M_sum . These results are consistent with a role for climate in determining M_sum in birds, but also indicate that phylogenetic signal remains even after accounting for associations indicative of adaptation to winter temperature. Migratory strategy was never a significant predictor of log M_sum in multiple regressions, a result that is not consistent with the flight adaptation hypothesis.     

Intraspecific body size frequency distributions of insects

Although interspecific body size frequency distributions are well documented for many taxa, including the insects, intraspecific body size frequency distributions (IaBSFDs) are more poorly known, and their variation among mass-based and linear estimates of size has not been widely explored. Here we provide IaBSFDs for 16 species of insects based on both mass and linear estimates and large sample sizes (n ≥ 100). In addition, we review the published IaBSFDs for insects, though doing so is complicated by their under-emphasis in the literature. The form of IaBSFDs can differ substantially between mass-based and linear measures. Nonetheless, in non-social insects they tend to be normally distributed (18 of 27 species) or in fewer instances positively skewed. Negatively skewed distributions are infrequently reported and log transformation readily removes the positive skew. Sexual size dimorphism does not generally cause bimodality in IaBSFDs. The available information on IaBSFDs in the social insects suggests that these distributions are usually positively skewed or bimodal (24 of 30 species). However, only c. 15% of ant genera are polymorphic, suggesting that normal distributions are probably more common, but less frequently investigated. Although only 57 species, representing seven of the 29 orders of insects, have been considered here, it appears that whilst IaBSFDs are usually normal, other distribution shapes can be found in several species, though most notably among the social insects. By contrast, the interspecific body size frequency distribution is typically right-skewed in insects and in most other taxa.     

Parasites favour intermediate nestling mass and brood size in cliff swallows

A challenge of life‐history theory is to explain why animal body size does not continue to increase, given various advantages of larger size. In birds, body size of nestlings and the number of nestlings produced (brood size) have occasionally been shown to be constrained by higher predation on larger nestlings and those from larger broods. Parasites also are known to have strong effects on life‐history traits in birds, but whether parasitism can be a driver for stabilizing selection on nestling body size or brood size is unknown. We studied patterns of first‐year survival in cliff swallows (Petrochelidon pyrrhonota) in western Nebraska in relation to brood size and nestling body mass in nests under natural conditions and in those in which hematophagous ectoparasites had been removed by fumigation. Birds from parasitized nests showed highest first‐year survival at the most common, intermediate brood‐size and nestling‐mass categories, but cliff swallows from nonparasitized nests had highest survival at the heaviest nestling masses and no relationship with brood size. A survival analysis suggested stabilizing selection on brood size and nestling mass in the presence (but not in the absence) of parasites. Parasites apparently favour intermediate offspring size and number in cliff swallows and produce the observed distributions of these traits, although the mechanisms are unclear. Our results emphasize the importance of parasites in life‐history evolution.     

Body mass is less important than bird order in determining the molecular rate for bird mitochondrial DNA

A negative relationship between body mass and molecular evolution rates has been suggested, and recently a correlation equation has been published based on mitochondrial genomic data of 475 bird species and their body masses. Here, we re‐analysed these data and show that the bird order as a proxy of monophyletic groups was a stronger predictor of the molecular rate than the body mass. We provide order‐specific molecular substitution rates. Only three orders (Galliformes, Gruiformes, Pelecaniformes) showed a very clear negative correlation, and specific correlation equations are given for these. The molecular rates of bird orders differed strongly at similar mean body masses, and we suggest that the previously described trend across all birds may arise as smaller species also tend to have characteristic life histories, namely faster turnover of generations, higher fecundity and shorter lifespans.     

Generalised Extreme Value Distributions Provide a Natural Hypothesis for the Shape of Seed Mass Distributions

Among co-occurring species, values for functionally important plant traits span orders of magnitude, are uni-modal, and generally positively skewed. Such data are usually log-transformed “for normality” but no convincing mechanistic explanation for a log-normal expectation exists. Here we propose a hypothesis for the distribution of seed masses based on generalised extreme value distributions (GEVs), a class of probability distributions used in climatology to characterise the impact of event magnitudes and frequencies; events that impose strong directional selection on biological traits. In tests involving datasets from 34 locations across the globe, GEVs described log10 seed mass distributions as well or better than conventional normalising statistics in 79% of cases, and revealed a systematic tendency for an overabundance of small seed sizes associated with low latitudes. GEVs characterise disturbance events experienced in a location to which individual species’ life histories could respond, providing a natural, biological explanation for trait expression that is lacking from all previous hypotheses attempting to describe trait distributions in multispecies assemblages. We suggest that GEVs could provide a mechanistic explanation for plant trait distributions and potentially link biology and climatology under a single paradigm.     

Pattern and process in the geographical ranges of freshwater fishes

North American freshwater fishes were studied to determine whether they displayed the same relationships between log (geographical range size) and log (body size) and the same pattern of range shape as found among North American birds and mammals. The forces that produce these patterns were also investigated. The log (geographical range size) : log (body size) relationship was analysed for 121 North American freshwater fish species. Thirty‐two imperilled species were compared with 89 non‐imperilled species to determine if the overall relationship could result from differential extinction. Range geometries were analysed, within and among habitat guilds, to determine if general patterns could be detected. The log (geographical range size) : log (body size) pattern among freshwater fish species was triangular and qualitatively similar to that found for North American birds and mammals. The results suggest that below a minimum geographical range, the likelihood of extinction increases dramatically for freshwater fishes and that this minimum range size increases with body size. The pattern of fish species’ range shapes differs from that found for other North American vertebrate taxa because, on average, fish possess much smaller ranges than terrestrial species and most fish species’ geographical ranges extend further on a north–south axis than on an east–west axis. The log (geographical range size) : log (body size) pattern reveals that fish species’ geographical ranges are more constrained than those of terrestrial species. The triangular relationship may be caused by differential extinction of species with large bodies and small geographical ranges as well as higher speciation rates of small‐bodied fish. The restricted geographical ranges of freshwater fishes gives them much in common with terrestrial species on oceanic islands. Range shape patterns within habitat guilds reflect guild‐specific historical and current ecological forces. The overall pattern of range shapes emerges from the combination of ecologically different subunits.     

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.     

Differential rates of morphological divergence in birds

There are more small-bodied bird species than there are large-bodied, even on a logarithmic scale. In birds this pattern, which is also found in other higher taxa, appears not to be due to neutral evolution. It has often been suggested that the skew of body size frequency distributions is the result of a relationship between body size and the net rate of speciation, but phylogenetic analyses so far have rejected the hypothesis that small-bodied species are subject to higher net rates of speciation. On the contrary, we show that there exists a relationship between body size and its own evolutionary variability: avian families of small body size show less interspecific variation in body size than large-bodied families of similar age and species richness.     

Size‐dependent costs of migration: Migrant bird species are subordinate to residents,but only at small body sizes

Migrant species are commonly thought to be poor competitors in aggressive interactions with resident species. However, no studies have tested whether this relationship is widespread. Here, we compare the behavioural dominance of closely related species of migratory and nonmigratory birds, testing whether migrants are consistently subordinate to resident species in aggressive contests. We compiled published behavioural dominance data involving migrant and resident congeners, gathering additional data on the body mass and migratory distance of each species. Focal species included a diverse array of birds (28 taxonomic families, 12 orders) from around the world. We found that migrant species are usually subordinate to resident species, but that this relationship disappears at larger body sizes. For smaller birds (<500 g), resident species were behaviourally dominant in 83%–88% of comparisons; for larger birds (>500 g), resident species were dominant in only 25%–30% of comparisons. The relative difference in body mass best predicted dominance relationships among species, with larger species dominant in 80%–84% of comparisons. When migrant and resident masses were equal, however, resident species were still more likely to be dominant in smaller birds, suggesting that other factors may also contribute to the subordinate status of migrants. Overall, our results suggest that in smaller species, the evolution of migration is associated with lighter weights and other traits that compromise the competitive abilities of migrants relative to residents. In contrast, larger species appear able to evolve migration without compromising their size or competitive abilities in aggressive contests, suggesting size‐dependent constraints on the evolution of migration.     

Body weight distributions of European Hymenoptera

Species number–body weight distributions are generally thought to be skewed to the right. Hence it is assumed that the number of relatively small species is larger than the number of relatively large species. While this pattern is well documented in vertebrates, comparative studies on larger invertebrate taxa are still scarce. Here I show that the weight distributions of European Hymenoptera (based on 12 601 species body weight data compiled from major catalogues) do not exhibit a general trend towards right skewed species–body weight distributions. Skewness did not depend on the number of species per taxon. Species richness peaked at intermediate body weights irrespective of taxonomic level. Kernel density analysis revealed that hymenopteran taxa had between one and four peaks in their size distributions with larger taxa having fewer peaks. Within genus variability in body weight was allometrically related to mean body weight (σ²=μ^1.81) in line with a proportional rescaling pattern. These results call for a rethinking about the generality of current vertebrate centred models of body size evolution.     

Variability and size in mammals and birds

Body size, its variability, and their ecological correlates have long been important topics in evolutionary biology. Yet, the question of whether there is a general relationship between size and size-relative variability has not previously been addressed. Through an analysis of body-mass and length measurements from 65 074 individuals from 351 mammalian species, we show that size-relative variability increases significantly with mean species body size. Analysis of mean body mass and standard deviations for 237 species of birds revealed the same pattern. We present three plausible alternatives explanations and eliminate several others. Of these, the hypothesis that the increase in size-relative variability with mean body mass is related to the scaling of body mass components is most strongly supported. In effect, larger mammals and birds are more variable because their body mass is composed to greater relative degree of components with higher intrinsic variability (bone, fat, and muscle). In contrast, smaller mammals and birds have lower body mass variability because they are composed to a greater relative extent of components (viscera and nervous system) in which size variation is more highly constrained by energetic and functional factors.     

Functional linkages for the pace of life, life-history, and environment in birds

For vertebrates, body mass underlies much of the variation in metabolism, but among animals of the same body mass, metabolism varies six-fold. Understanding how natural selection can influence variation in metabolism remains a central focus of Physiological Ecologists. Life-history theory postulates that many physiological traits, such as metabolism, may be understood in terms of key maturational and reproductive characteristics over an organism's life-span. Although it is widely acknowledged that physiological processes serve as a foundation for life-history trade-offs, the physiological mechanisms that underlie the diversification of life-histories remain elusive. Data show that tropical birds have a reduced basal metabolism (BMR), field metabolic rate, and peak metabolic rate compared with temperate counterparts, results consistent with the idea that a low mortality, and therefore increased longevity, and low productivity is associated with low mass-specific metabolic rate. Mass-adjusted BMR of tropical and temperate birds was associated with survival rate, in accordance with the view that animals with a slow pace of life tend to have increased life spans. To understand the mechanisms responsible for a reduced rate of metabolism in tropical birds compared with temperate species, we summarized an unpublished study, based on data from the literature, on organ masses for both groups. Tropical birds had smaller hearts, kidneys, livers, and pectoral muscles than did temperate species of the same body size, but they had a relatively larger skeletal mass. Direct measurements of organ masses for tropical and temperate birds showed that the heart, kidneys, and lungs were significantly smaller in tropical birds, although sample sizes were small. Also from an ongoing study, we summarized results to date on connections between whole-organism metabolism in tropical and temperate birds and attributes of their dermal fibroblasts grown in cell culture. Cells derived from tropical birds had a slower rate of growth, consistent with the hypothesis that these cells have a slower metabolism. We found that dermal fibroblasts from tropical birds resisted chemical agents that induce oxidative and non-oxidative stress better than do cells from temperate species, consistent with the hypothesis that birds that live longer invest more in self-maintenance such as antioxidant properties of cells.     

Testis asymmetry in birds: the influences of sexual and natural selection

Gonad size and shape asymmetries are particularly common in birds. Although some obvious size and shape differences between the left and right testes in birds were first documented more than a century ago, little is known about what influences the variation across species in either the degree or the direction of these asymmetries. Here we show that a left bias in size is the most likely ancestral state in most orders and families, and that there is a weak but significant negative relation between the degree of size and shape asymmetries. In extant species, testis size and shape symmetries increase with the degree of sperm competition (relative testes mass), but those relations are significant only in those species with left bias in each of these traits. When space is particularly constrained on the left side of the body cavity due to a large gizzard (e.g. in granivores), the left testis is more elongated and the degree of size symmetry is larger. Despite significant patterns, relative testes mass and gizzard complexity together explain < 10% of the variation in testis asymmetry in species with left biases. Thus our analyses suggest that some other factor is largely responsible for the evolution of gonad asymmetry in birds: 1) that a left bias in testis size might be a correlated response to selection for a left bias in the development of a single (left) ovary in females of most bird species, and/or 2) that physiological efficiency due to the dramatic and rapid increase in testis size of most species during the breeding season might favour enlargement of one testis. Our conclusions highlight the need to rethink and improve our understanding of the physiological processes underlying the investment in gonads by male birds.     

The “minimal boundary curve for endothermy” as a predictor of heterothermy in mammals and birds: a review

According to the concept of the “minimal boundary curve for endothermy”, mammals and birds with a basal metabolic rate (BMR) that falls below the curve are obligate heterotherms and must enter torpor. We examined the reliability of the boundary curve (on a double log plot transformed to a line) for predicting torpor as a function of body mass and BMR for birds and several groups of mammals. The boundary line correctly predicted heterothermy in 87.5% of marsupials (n = 64), 94% of bats (n = 85) and 82.3% of rodents (n = 157). Our analysis shows that the boundary line is not a reliable predictor for use of torpor. A discriminate analysis using body mass and BMR had a similar predictive power as the boundary line. However, there are sufficient exceptions to both methods of analysis to suggest that the relationship between body mass, BMR and heterothermy is not a causal one. Some homeothermic birds (e.g. silvereyes) and rodents (e.g. hopping mice) fall below the boundary line, and there are many examples of heterothermic species that fall above the boundary line. For marsupials and bats, but not for rodents, there was a highly significant phylogenetic pattern for heterothermy, suggesting that taxonomic affiliation is the biggest determinant of heterothermy for these mammalian groups. For rodents, heterothermic species had lower BMRs than homeothermic species. Low BMR and use of torpor both contribute to reducing energy expenditure and both physiological traits appear to be a response to the same selective pressure of fluctuating food supply, increasing fitness in endothermic species that are constrained by limited energy availability. Both the minimal boundary line and discriminate analysis were of little value for predicting the use of daily torpor or hibernation in heterotherms, presumably as both daily torpor and hibernation are precisely controlled processes, not an inability to thermoregulate.     

Bergmann's rule in alien birds

Native bird species show latitudinal gradients in body size across species (Bergmann's rule), but whether or not such gradients are recapitulated in the alien distributions of bird species are unknown. Here, we test for the existence of Bergmann's rule in alien bird species worldwide, and investigate the causes of the observed patterns. Published databases were used to obtain the worldwide distributions of established alien bird populations, the locations of alien bird introductions, and bird body masses. Randomisation tests and linear models were used to assess latitudinal patterns in the body masses of introduced and established alien bird populations. Established alien bird species exhibit Bergmann's rule, but this is largely explained by where alien bird species have been introduced: latitudinal variation in the body masses of established alien bird species simply reflects latitudinal variation in the body masses of introduced species. There is some evidence that body mass is implicated in whether or not established species’ alien ranges spread towards or contract away from the Equator following establishment. However, most alien bird ranges are encompassed by the latitudinal band(s) to which the species was introduced. Bergmann's rule in alien birds is therefore a consequence of where humans have introduced different species, rather than of natural processes operating after population introduction.     

Reproductive investment in moa: a K-selected life-history strategy?

The exaggerated K-selected life-history strategy of moa has been suggested as an important factor causing their rapid extinction. Classically, this strategy is characterized by few, large offspring and low fecundity rates. Assuming clutches with one or two eggs as derived from the fossil record, we tested if eggs of moa were larger than the average of similar-sized birds, and estimated their unknown annual breeding frequencies. Therefore, we established allometries on body mass and different reproductive traits (i.e. egg mass, clutch mass and annual clutch mass). These were derived for r-selected (r-model) and for K-selected (K-model) bird species. In agreement with our initial expectations, moa had egg to body mass relations seen in “average” extant K-selected birds. While the K-model pointed to a clutch size of one or two eggs for moa corroborating fossil data and a K-selected life-history, the r-model predicted two to three times larger sizes. Under clutch sizes between one and two eggs and an annual clutch mass as observed in other similar-sized flightless island birds (e.g. rails, ratites), the annual clutch mass allometry suggested one to three clutches per year for moa. Even when assuming less than one brood per year (K-model predicts 0.5 clutches per year); annual clutch masses were still consistent with the K-model. Further studies are needed to clarify whether or not the reproductive strategy of flightless island birds and/or of the birds underlying the K-model fits better to the moa strategy. The approach presented herein, illustrates that combining biological and paleontological data can assist in the reconstruction of species traits, which are insufficiently or not preserved in fossils, but are necessary to understand the evolution of traits.     

Polyphagy and adult body size in geometrid moths

We compared the average body size (wing span) of Finnish geometrid moth species in relation to their degree of polyphagy and quality of food. The first hypothesis, originally constructed for mammals and birds, states that smaller species should more often be specialists than large species, because of the different relationships between body size and home range size, and body size and daily energy requirements. According to the second hypothesis, smaller species should feed more often on herbs than do larger species, because of the different defence mechanisms of herbs and woody plants. The results support both of these hypotheses. Specialist species are smaller than oligophagous or polyphagous species, and small species concentrate on herbs. We conclude that quality and quantity of food resources may explain the pattern.     

Body size trends in a Holocene island bird assemblage

Despite the robust observation in macroecology that there are many small-bodied species, recent comparative studies have found little evidence for elevated net rates of diversification among small-bodied species within taxa. Here we examine the relationship between body size and species richness using the New Zealand land bird fauna, a well resolved palaeoecological Holocene assemblage. We test whether there is any evidence that net cladogenesis depended on body size in an assemblage prior to the impact of human-induced extinction. We also test whether net cladogenesis depends on the level at which taxa are endemic to New Zealand, to see whether there is evidence for bursts of cladogenesis following taxon establishment, and examine how the body sizes of New Zealand land birds relate to those in Australia, the most likely source pool for colonising taxa. Most New Zealand land bird species are small-bodied. We find no evidence, however, that this is due to higher net cladogenesis in small-bodied taxa. The body mass distributions of endemic and recent colonist species do not differ statistically, but recent colonists tend to be smaller-bodied than their closest endemic relative. This tendency is more marked for small-bodied than large-bodied taxa. More endemic taxa do not tend to be more species rich in New Zealand, although there is a positive relationship between level of endemism and species richness for forest taxa. The body mass distribution of New Zealand birds is very similar to that for Australia. Body mass does not dictate the likelihood that a family has colonised New Zealand from Australia, but the number of species in the family does: it is the species rich Australian families that have successfully colonised. We discuss the implications of these results for the evolution of body size distributions, and for the "island rule" of body size evolution on islands.