Of mice and mammoths: generality and antiquity of the island rule

Aim

We assessed the generality of the island rule in a database comprising 1593 populations of insular mammals (439 species, including 63 species of fossil mammals), and tested whether observed patterns differed among taxonomic and functional groups.

Location

Islands world‐wide.

Methods

We measured museum specimens (fossil mammals) and reviewed the literature to compile a database of insular animal body size (S_i = mean mass of individuals from an insular population divided by that of individuals from an ancestral or mainland population, M). We used linear regressions to investigate the relationship between S_i and M, and ANCOVA to compare trends among taxonomic and functional groups.

Results

S_i was significantly and negatively related to the mass of the ancestral or mainland population across all mammals and within all orders of extant mammals analysed, and across palaeo‐insular (considered separately) mammals as well. Insular body size was significantly smaller for bats and insectivores than for the other orders studied here, but significantly larger for mammals that utilized aquatic prey than for those restricted to terrestrial prey.

Main conclusions

The island rule appears to be a pervasive pattern, exhibited by mammals from a broad range of orders, functional groups and time periods. There remains, however, much scatter about the general trend; this residual variation may be highly informative as it appears consistent with differences among species, islands and environmental characteristics hypothesized to influence body size evolution in general. The more pronounced gigantism and dwarfism of palaeo‐insular mammals, in particular, is consistent with a hypothesis that emphasizes the importance of ecological interactions (time in isolation from mammalian predators and competitors was 0.1 to > 1.0 Myr for palaeo‐insular mammals, but < 0.01 Myr for extant populations of insular mammals). While ecological displacement may be a major force driving diversification in body size in high‐diversity biotas, ecological release in species‐poor biotas often results in the convergence of insular mammals on the size of intermediate but absent species.     

Body size evolution in insular vertebrates: generality of the island rule

Aim My goals here are to (1) assess the generality of the island rule – the graded trend from gigantism in small species to dwarfism in larger species – for mammals and other terrestrial vertebrates on islands and island‐like ecosystems; (2) explore some related patterns of body size variation in insular vertebrates, in particular variation in body size as a function of island area and isolation; (3) offer causal explanations for these patterns; and (4) identify promising areas for future studies on body size evolution in insular vertebrates. Location Oceanic and near‐shore archipelagos, and island‐like ecosystems world‐wide. Methods Body size measurements of insular vertebrates (non‐volant mammals, bats, birds, snakes and turtles) were obtained from the literature, and then regression analyses were conducted to test whether body size of insular populations varies as a function of body size of the species on the mainland (the island rule) and with characteristics of the islands (i.e. island isolation and area). Results The island rule appears to be a general phenomenon both with mammalian orders (and to some degree within families and particular subfamilies) as well as across the species groups studied, including non‐volant mammals, bats, passerine birds, snakes and turtles. In addition, body size of numerous species in these classes of vertebrates varies significantly with island isolation and island area. Main conclusions The patterns observed here – the island rule and the tendency for body size among populations of particular species to vary with characteristics of the islands – are actually distinct and scale‐dependent phenomena. Patterns within archipelagos reflect the influence of island isolation and area on selective pressures (immigration filters, resource limitation, and intra‐ and interspecific interactions) within particular species. These patterns contribute to variation about the general trend referred to as the island rule, not the signal for that more general, large‐scale pattern. The island rule itself is an emergent pattern resulting from a combination of selective forces whose importance and influence on insular populations vary in a predictable manner along a gradient from relatively small to large species. As a result, body size of insular species tends to converge on a size that is optimal, or fundamental, for a particular bau plan and ecological strategy.     

Patterns of maximum body size evolution in Cenozoic land mammals: eco-evolutionary processes and abiotic forcing

There is accumulating evidence that macroevolutionary patterns of mammal evolution during the Cenozoic follow similar trajectories on different continents. This would suggest that such patterns are strongly determined by global abiotic factors, such as climate, or by basic eco-evolutionary processes such as filling of niches by specialization. The similarity of pattern would be expected to extend to the history of individual clades. Here, we investigate the temporal distribution of maximum size observed within individual orders globally and on separate continents. While the maximum size of individual orders of large land mammals show differences and comprise several families, the times at which orders reach their maximum size over time show strong congruence, peaking in the Middle Eocene, the Oligocene and the Plio-Pleistocene. The Eocene peak occurs when global temperature and land mammal diversity are high and is best explained as a result of niche expansion rather than abiotic forcing. Since the Eocene, there is a significant correlation between maximum size frequency and global temperature proxy. The Oligocene peak is not statistically significant and may in part be due to sampling issues. The peak in the Plio-Pleistocene occurs when global temperature and land mammal diversity are low, it is statistically the most robust one and it is best explained by global cooling. We conclude that the macroevolutionary patterns observed are a result of the interplay between eco-evolutionary processes and abiotic forcing.     

Body size of insular carnivores: evidence from the fossil record

Aim Our goals here are to: (1) assess the generality of one aspect of the island rule – the progressive trend towards decrease in size in larger species – for fossil carnivores on islands; (2) offer causal explanations for this pattern and deviations from it – as far as fossil carnivores are concerned; and (3) estimate the speed of this trend. Location Oceanic and oceanic‐like islands world‐wide. Methods Body size estimates of fossil insular carnivores and of their phylogenetically closest mainland relative were obtained from our own data and the published literature. Our dataset consisted of 18 species from nine islands world‐wide. These data were used to test whether the body size of fossil insular carnivores varies as a function of body size of the mainland species in combination with characteristics of the island ecosystem. Results Dwarfism was observed in two canid species. Moderate decrease in body mass was observed in one hyena species. Gigantism was observed in one otter species. Moderate body mass increase was observed in two otter species, one galictine mustelid and perhaps one canid. Negligible or no change in body mass at all was observed in five otter species, three galictine mustelids and one genet. Size changes in teeth do not lag behind in comparison to skeletal elements in the dwarfed canids. The evolutionary speed of dwarfism in a canid lineage is low. Main conclusions Size change in fossil terrestrial insular carnivores was constrained by certain ecological conditions, especially the availability of prey of appropriate body size. When such alternative prey was not available, the carnivores retained their mainland size. The impact of competitive carnivores seems negligible. The case of (semi‐)aquatic carnivores is much less clear. The species that maintained their ancestral body mass may have changed their diet, as is evidenced by their dentition. Among the otters, one case of significant size increase was observed, perhaps best explained as being due to it entering the niche of an obligate aquatic otter. Dwarfism was not observed in otters. The island rule seems to apply to fossil carnivores, but with exceptions. The dependency of the island rule on resource availability is emphasized by the present study.     

The evolution of body armor in mammals: plantigrade constraints of large body size

Predictions associated with opposing selection generating minimum variance in basal metabolic rate (BMR) in mammals at a constrained body mass (CBM; 358 g) were tested. The CBM is presumed to be associated with energetic constraints linked to predation and variable resources at intermediate sizes on a logarithmic mass scale. Opposing selection is thought to occur in response to energetic constraints associated with predation and unpredictable resources. As body size approaches and exceeds the CBM, mammals face increasing risks of predation and daily energy requirements. Fast running speeds may require high BMRs, but unpredictable and low resources may select for low BMRs, which also reduce foraging time and distances and thus predation risks. If these two selection forces oppose each other persistently, minimum BMR variance may result. However, extreme BMR outliers at and close to the CBM should be indicative of unbalanced selection and predator avoidance alternatives (escapers vs. defenders), and may therefore provide indirect support for opposing selection. It was confirmed that body armor in defenders evolves at and above the CBM, and armored mammals had significantly lower BMRs than their nonarmored counterparts. However, analyses comparing the BMR of escapers--the fastest nonarmored runners (Lagomorpha)--with similar-sized counterparts were inconclusive and were confounded by limb morphology associated with speed optimization. These analyses suggest that the risks and costs of predation and the speed limitations of the plantigrade foot may constrain the evolution of large body sizes in plantigrade mammals.     

Slaying dragons: limited evidence for unusual body size evolution on islands

Aim Island taxa often attain forms outside the range achieved by mainland relatives. Body size evolution of vertebrates on islands has therefore received much attention, with two seemingly conflicting patterns thought to prevail: (1) islands harbour animals of extreme size, and (2) islands promote evolution towards medium body size (‘the island rule’). We test both hypotheses using body size distributions of mammal, lizard and bird species. Location World‐wide. Methods We assembled body size and insularity datasets for the world’s lizards, birds and mammals. We compared the frequencies with which the largest or smallest member of a group is insular with the frequencies expected if insularity is randomly assigned within groups. We tested whether size extremes on islands considered across mammalian phylogeny depart from a null expectation under a Brownian motion model. We tested the island rule by comparing insular and mainland members of (1) a taxonomic level and (2) mammalian sister species, to determine if large insular animals tend to evolve smaller body sizes while small ones evolve larger sizes. Results The smallest species in a taxon (order, family or genus) are insular no more often than would be expected by chance in all groups. The largest species within lizard families and bird genera (but no other taxonomic levels) are insular more often than expected. The incidence of extreme sizes in insular mammals never departs from the null, except among extant genera, where gigantism is marginally less common than expected under a Brownian motion null. Mammals follow the island rule at the genus level and when comparing sister species and clades. This appears to be driven mainly by insular dwarfing in large‐bodied lineages. A similar pattern in birds is apparent for species within orders. However, lizards follow the converse pattern. Main conclusions The popular misconception that islands have more than their fair share of size extremes may stem from a greater tendency to notice gigantism and dwarfism when they occur on islands. There is compelling evidence for insular dwarfing in large mammals, but not in other taxa, and little evidence for the second component of the island rule – gigantism in small‐bodied taxa.     

Geographic gradients in body size: a clarification of Bergmann's rule

1997 marked the sesquicentenary of the publication by Carl Bergmann of the observation that, in general, large-bodied animal species tend to live further north than their small-bodied relatives. This has been dubbed Bergmann's rule in his honour. However, more than 150 years on, we appear to be little closer to a general understanding of the rule, or even to any consensus as to whether it exists. This is due in large part to confusion about the taxonomic level at which the rule is considered to operate, and to the conflation of pattern and mechanism. In this paper, we attempt to resolve this confusion by highlighting its sources, and by providing a definition of Bergmann's rule that is practical and useful, yet that retains the essential features of its original formulation. We conclude by briefly reviewing the mechanisms proposed to explain Bergmann's rule as we define it.     

Area, isolation and body size evolution in insular carnivores

Body sizes of insular mammals often differ strikingly from those of their mainland conspecifics. Small islands have reduced numbers of competitor and predator species, and more limited resources. Such reductions are believed to select for predictable changes in body sizes, with large mammals growing progressively smaller as island area decreases, while small ones grow progressively larger. Medium-sized mammals are thought to be largest on intermediate-sized islands. Increased isolation is seen as promoting insular gigantism. We searched for such patterns using a large database of insular carnivore specimens. Neither small nor large carnivores show a consistent area/body size relationship. Medium-sized carnivores are no more likely to attain large size on medium-sized islands then they are to be small there. We found no consistent patterns of body size variation in relation to isolation.     

The tempo of genetic evolution in birds: body mass and climate effects

Aim Negative relationships between body mass and substitution rates have previously been reported. However, most of these studies have involved contrasted taxa that, due to their highly divergent phylogenetic histories, also differ in many additional characteristics other than mass. In particular, there has been little examination of the potentially confounding effects of climate or population size. Here we test for differences in rates of microevolution among bird species that, although differing in mass, are nonetheless very closely related phylogenetic pairs. We additionally tested for latitudinal/elevational and population size effects across these contrasts. Location Global. Methods The tempo of microevolution within the cytochrome b gene of mitochondrial DNA was compared between closely related bird species that differed in body mass, using 130 phylogenetically independent species pairs. In order to minimize climate effects, pairs not having overlapping latitudinal ranges were discarded. In addition, a subset of pairs was identified and analysed that involved comparisons between species that have different latitudinal or elevational midpoints. Results Species with smaller mass had substitution rates marginally faster than those with larger mass (small : large median ratio = 1.05). However, this result was only statistically significant when data were pruned to eliminate comparisons in which population or range size also varied substantially between contrasted species. Latitude and elevation had a much stronger association with substitution rates than body mass within the subset of pairs (n = 30) that also differed in their spatial distributions: lower elevation or latitude species had substantially more substitutions than those at higher latitudes or elevations (low : high ratio = 1.35). Furthermore, when the dataset was pruned of pairs in which body mass was confounded by latitude or elevation, the body mass effect was eliminated. Main conclusions Body mass is known to correlate with latitude, so that the latitudinal/elevational association with microevolution we found might either be additive to, or causal of, the body mass effect. These results are consistent with the evolutionary speed hypothesis, which suggests that latitudinal diversity gradients derive from variation in the rate of microevolution. Our findings also serve to raise concerns about biogeographical studies that use genetic distances between taxa to estimate time since divergence.     

On size and area: Patterns of mammalian body size extremes across landmasses

We describe a biogeographic pattern in which mammalian body size extremes scale with landmass area. The relationship between the largest and the smallest mammal species found on different landbridge islands, mountaintops and continents shows that the size of the largest species increases, while that of the smallest species decreases, with increase in the area of the landmass. We offer two possible explanations: (1) that the pattern is the result of sampling artefacts, which we call the ‘statistical artefact hypothesis’, or (2) that the pattern is the result of processes related to the way body size affects the number of individuals that a particular species can pack in a given area, which we call the ‘area-scaling hypothesis’. Our results point out that the pattern is not a statistical artefact resulting from random sampling, but can be explained by considering the scaling of individual space requirements and its effect on population survival on landmasses of different area. This revised version was published online in July 2006 with corrections to the Cover Date.     

Mainland size variation informs predictive models of exceptional insular body size change in rodents

The tendency for island populations of mammalian taxa to diverge in body size from their mainland counterparts consistently in particular directions is both impressive for its regularity and, especially among rodents, troublesome for its exceptions. However, previous studies have largely ignored mainland body size variation, treating size differences of any magnitude as equally noteworthy. Here, we use distributions of mainland population body sizes to identify island populations as ‘extremely’ big or small, and we compare traits of extreme populations and their islands with those of island populations more typical in body size. We find that although insular rodents vary in the directions of body size change, ‘extreme’ populations tend towards gigantism. With classification tree methods, we develop a predictive model, which points to resource limitations as major drivers in the few cases of insular dwarfism. Highly successful in classifying our dataset, our model also successfully predicts change in untested cases.     

The geographic distribution of mammal body size in Europe

Aims  To describe the pattern of mean body size of native mammals in Europe, and to investigate its relationships with environmental predictors related to four hypotheses: (1) dispersal; (2) heat conservation; (3) heat dissipation; and (4) resource availability.
Location  Continental western Europe and Great Britain.
Methods  We used range maps to estimate the mean body size (average log mass) of mammals in 386 cells of 12,100 km² each. Environmental conditions in each cell were quantified using nine historical, climatic and primary production variables. We attempted to tease apart the effects of these variables using correlation, multiple regression and spatial autocorrelation analyses.
Results  In the part of the continent covered by ice during the Pleistocene, body mass decreases southwards, and annual average temperature explains 73% of the variance in body size, consistent with the heat-conservation hypothesis. However, in warmer, non-glaciated areas the best predictor is an estimate of seasonality in plant production, but it explains only 18% of the variance. Carnivores, omnivores and herbivores show similar relationships, but the pattern for herbivores is substantially weaker than for the other groups.
Main conclusions  Overall, the relationship between mean body size and temperature is non-linear, being strong in cold environments but virtually disappearing above a temperature threshold.     

One size does not fit all: no evidence for an optimal body size on islands

Aim Optimal body size theories predict that large clades have a single, optimal, body size that serves as an evolutionary attractor, with the full body size spectrum of a clade resulting from interspecific competition. Because interspecific competition is believed to be reduced on islands, such theories predict that insular animals should be closer to the optimal size than mainland animals. We test the resulting prediction that insular clade members should therefore have narrower body size ranges than their mainland relatives. Location World‐wide. Methods We used body sizes and a phylogenetic tree of 4004 mammal species, including more than 200 species that went extinct since the last ice age. We tested, in a phylogenetically explicit framework, whether insular taxa converge on an optimal size and whether insular clades have narrow size ranges. Results We found no support for any of the predictions of the optimal size theory. No specific size serves as an evolutionary attractor. We did find consistent evidence that large (> 10 kg) mammals grow smaller on islands. Smaller species, however, show no consistent tendency to either dwarf or grow larger on islands. Size ranges of insular taxa are not narrower than expected by chance given the number of species in their clades, nor are they narrower than the size ranges of their mainland sister clades – despite insular clade members showing strong phylogenetic clustering. Main conclusions The concept of a single optimal body size is not supported by the data that were thought most likely to show it. We reject the notion that inclusive clades evolve towards a body‐plan‐specific optimum.     

Recent spatial and temporal changes in body size of terrestrial vertebrates: probable causes and pitfalls

Geographical and temporal variations in body size are common phenomena among organisms and may evolve within a few years. We argue that body size acts much like a barometer, fluctuating in parallel with changes in the relevant key predictor(s), and that geographical and temporal changes in body size are actually manifestations of the same drivers. Frequently, the principal predictors of body size are food availability during the period of growth and ambient temperature, which often affects food availability. Food availability depends on net primary productivity that, in turn, is determined by climate and weather (mainly temperature and precipitation), and these depend mainly on solar radiation and other solar activities. When the above predictors are related to latitude the changes have often been interpreted as conforming to Bergmann's rule, but in many cases such interpretations should be viewed with caution due to the interrelationships among various environmental predictors. Recent temporal changes in body size have often been related to global warming. However, in many cases the above key predictors are not related to either latitude and/or year, and it is the task of the researcher to determine which particular environmental predictor is the one that determines food availability and, in turn, body size. The chance of discerning a significant change in body size depends to a large extent on sample size (specimens/year). The most recent changes in body size are probably phenotypic, but there are some cases in which they are partly genetic.     

Climatological correlates for body size of five species of Australian mammals

Size variation of body and skull of five species of Australian mammals (echidna, Tachyglossus aculeatus ; brush-tail possum, Trichosurus vulpecula ; eastern grey kangaroo, Macropus giganteus ; western grey kangaroo, M. fuliginosus ; red kangaroo, M. rufus ), is related to climatic factors. All five species show trends in body size that conform with Bergmann's rule, individuals from colder environments being larger than those from warmer areas. The western and eastern grey kangaroos also conform with Allen's rule, the relative size of their extremities being large in warmer areas. In four of the five species (not the red kangaroo) body size is also correlated with indices of biomass productivity. However, since biomass productivity and ambient temperature are related to some extent, it is difficult to separate the effects of these factors.     

Atmospheric oxygen level and the evolution of insect body size

Insects are small relative to vertebrates, possibly owing to limitations or costs associated with their blind-ended tracheal respiratory system. The giant insects of the late Palaeozoic occurred when atmospheric PO₂ (aPO₂) was hyperoxic, supporting a role for oxygen in the evolution of insect body size. The paucity of the insect fossil record and the complex interactions between atmospheric oxygen level, organisms and their communities makes it impossible to definitively accept or reject the historical oxygen-size link, and multiple alternative hypotheses exist. However, a variety of recent empirical findings support a link between oxygen and insect size, including: (i) most insects develop smaller body sizes in hypoxia, and some develop and evolve larger sizes in hyperoxia; (ii) insects developmentally and evolutionarily reduce their proportional investment in the tracheal system when living in higher aPO₂, suggesting that there are significant costs associated with tracheal system structure and function; and (iii) larger insects invest more of their body in the tracheal system, potentially leading to greater effects of aPO₂ on larger insects. Together, these provide a wealth of plausible mechanisms by which tracheal oxygen delivery may be centrally involved in setting the relatively small size of insects and for hyperoxia-enabled Palaeozoic gigantism.