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.     

Global change and carnivore body size: data are stasis

Aim  Global warming and other anthropogenic changes to the environment affect many aspects of biology and have often been invoked as causing body size changes in vertebrates. Here we examine a diverse set of carnivore populations in search of patterns in body size change that could reflect global warming (in accord with Bergmann's rule).
Location  Global.
Methods  We used > 4400 specimens representing 22 carnivore species in 52 populations collected over the last few decades to examine whether size changed with collection date when geography and sex are accounted for. We then examined several factors related to global warming, body mass, diet, and the attributes of the different datasets, to see whether they affect the standardized slope (β) of the size versus time regression.
Results  Six of 52 populations we examined show a significant effect of year of collection on body size at the 0.05 probability level. The response of size to global warming does not reflect spatial patterns of size variation, nor do diet or body mass affect tendency of populations to change in body size. Size changes are no more pronounced in populations that have been sampled more recently. However, change, where it occurs, is rapid.
Main conclusions  There may be a tendency in the literature to report only cases where recent changes are prevalent. Although in our data only a minority of populations show body size changes, we may see changes accelerating in the future in response to more drastic climatic changes and other anthropogenic changes.     

Climatic change and body size in two species of Japanese rodents

Using museum specimens, we studied temporal changes in skull size in two species of Japanese rodents, the large Japanese field mouse ( Apodemus speciosus ) and Pratt's vole ( Eothenomys smithii  =  E. kageus ) during the 20th century. We used the greatest length of the skull (GTL), zygomatic breadth (ZB), narrowest width of the skull across the interorbital region (IC) and the length of the upper cheek teeth row (M) as indicators to such changes. We found that GTL and ZB (but not IC and M) increased during the study period in mice, and that IC and M (but not GTL and ZB) increased marginally in voles. We attribute these changes to elevated ambient minimal temperatures, which increased food availability and energy savings for the mice, and required diet change in the voles.  © 2004 The Linnean Society of London, Biological Journal of the Linnean Society , 2004, 82 , 263–267.     

Relative effects of climate change, isolation and competition on body-size evolution in the Japanese field mouse, Apodemus argenteus

Aim This paper examines body size variation in both recent and Quaternary populations of the Japanese field mouse Apodemus argenteus in order to assess the relative effects on body size of climate change, isolation and competitive interactions with its congeneric A. speciosus. Both temporal (since the Last Glacial Maximum, LGM) and spatial (over the Japanese archipelago) scales are considered. Location The small field mouse is widespread in Japan, and the specimens examined were collected from 10 localities on islands of widely differing area (from 4 km² to 230,510 km²) and at latitudes ranging from 30.3° N to 45.1° N. Methods The effects of geographical factors such as latitude and island area on the size variation of A. argenteus were investigated, using the lower incisor size. In addition, the size of some specimens from two Quaternary localities was compared with the size of the extant specimens. Evolutionary rates of size change since the LGM were calculated in darwins. Hutchinson size ratios were used to examine the pattern of variation of the size segregation between the two Japanese field mice, A. argenteus and A. speciosus, in relation to time and space. Results There was a negative relationship between size and latitude among living A. argenteus populations. In addition, there was no effect of island area on body size, especially at higher latitudes. At lower latitudes, A. argenteus were larger on smaller islands, although this trend was not statistically significant. Quaternary specimens of A. argenteus were smaller in size than their living representatives. The interspecific size ratio between the two Japanese Apodemus was larger on smaller islands and at higher latitudes, and there has been a decrease in the size ratio between the two Apodemus since the LGM. Lastly, in accordance with the theory of character displacement, the small A. argenteus was larger in allopatry than in sympatry, whereas the large A. speciosus was smaller in allopatry than in sympatry. Main conclusions These results indicate that A. argenteus does not conform to Bergmann's rule or to the island rule. The variation in size for the small Japanese field mouse at both spatial and temporal scales may be related to climate change, with an additional effect of competition with the large field mouse, especially on smaller islands. The size convergence between the two Japanese Apodemus observed over the last 21,000 years may be explained by the diminution of available food resources due to the reduction of land mass areas following the LGM. It may also be the result of an evolution towards an optimal body size; a hypothesis previously proposed to explain the evolution of body size in island mammals. Lastly, the evolutionary rates of body size calculated for A. argenteus since the LGM are typical of rates calculated for other Quaternary mainland mammals, thus suggesting that the evolution in this species was not particularly rapid, as is often thought for island mammals.     

The effect of island area on body size in a primate species from the Sunda Shelf Islands

Aim  We examine the effect of island area on body dimensions in a single species of primate endemic to Southeast Asia, the long-tailed macaque ( Macaca fascicularis ). In addition, we test Allen's rule and a within-species or intraspecific equivalent of Bergmann's rule (i.e. Rensch's rule) to evaluate body size and shape evolution in this sample of insular macaques.
Location  The Sunda Shelf islands of Southeast Asia.
Methods  Body size measurements of insular macaques gathered from the literature were analysed relative to island area, latitude, maximum altitude, isolation from the mainland and other islands, and various climatic variables using linear regression.
Results  We found no statistically significant relationship between island area and body length or head length in our sample of insular long-tailed macaques. Tail length correlated negatively with island area. Head length and body length exhibited increases corresponding to increasing latitude, a finding seemingly consistent with the expression of Bergmann's rule within a single species. These variables, however, were not correlated with temperature, indicating that Bergmann's rule is not in effect. Tail length was not correlated with either temperature or increasing latitude, contrary to that predicted by Allen's rule.
Main conclusions  The island rule dictating that body size will covary with island area does not apply to this particular species of primate. Our study is consistent with results presented in the literature by demonstrating that skull and body length in insular long-tailed macaques do not, strictly speaking, conform to Rensch's rule. Unlike previous studies, however, our findings suggest that tail-length variation in insular macaques does not support Allen's rule.     

The island rule in large mammals: paleontology meets ecology

The island rule is the phenomenon of the miniaturization of large animals and the gigantism of small animals on islands, with mammals providing the classic case studies. Several explanations for this pattern have been suggested, and departures from the predictions of this rule are common among mammals of differing body size, trophic habits, and phylogenetic affinities. Here we offer a new explanation for the evolution of body size of large insular mammals, using evidence from both living and fossil island faunal assemblages. We demonstrate that the extent of dwarfism in ungulates depends on the existence of competitors and, to a lesser extent, on the presence of predators. In contrast, competition and predation have little or no effect on insular carnivore body size, which is influenced by the nature of the resource base. We suggest dwarfism in large herbivores is an outcome of the fitness increase resulting from the acceleration of reproduction in low-mortality environments. Carnivore size is dependent on the abundance and size of their prey. Size evolution of large mammals in different trophic levels has different underlying mechanisms, resulting in different patterns. Absolute body size may be only an indirect predictor of size evolution, with ecological interactions playing a major role.     

Intra- and interspecific morphological variation in the field mouse species Apodemus argenteus and A. speciosus in the Japanese archipelago: the role of insular isolation and biogeographic gradients

Two species of field mice, Apodemus argenteus and A. speciosus, occur in sympatry across the Japanese archipelago. The inter- and intraspecific patterns of morphological differentiation have been evaluated, using a Fourier analysis of the mandible outline. The relative importance of the effect of insular isolation and latitudinal climatic gradient on the size and shape of the two species was assessed by a comparison of the populations from the large island of Honshu and the surrounding small-island populations. The size variation in A. argenteus is correlated with the climatic gradient whilst the shape variation corresponds mainly to a random differentiation of the small-island populations from a Honshu-like basic morphological pattern. A. speciosus displays increased size on small islands, and its shape variation is related to both the climatic gradient and insularity. Finally, the two species are differentiated by both the size and shape of the mandible across the Japanese archipelago, suggesting that interspecific competition between both species is reduced via niche partitioning. Our results emphasize the importance of insular isolation on shape differentiation, but a part of the morphological differentiation is also related to the latitudinal climatic gradient. Isolation on small islands could have favoured such a response to environmental factors by lowering the gene flow that prevents almost any significant differentiation within Honshu populations.     

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.     

Maximum body size in a radiating clade as a function of time

The behavior of the maximum body size (body length) in an evolving clade is exemplified by the evolutionary histories of Bivalvia, Cetacea, and Camerata (Crinoidea). Changes of the maximum size with time track closely diversification history: when a clade diversifies exponentially, the maximum size also increases exponentially, and when the number of species changes irregularly (at varying rates), the maximum size also changes in that manner. However, within any given clade, the maximum body size changes at lower rates than diversity does. The observed shifts in maximum body size approximate the rate of diversification per unit of time to the power of about 0.5.     

Bison body size and climate change

The relationship between body size and temperature of mammals is poorly resolved, especially for large keystone species such as bison (Bison bison). Bison are well represented in the fossil record across North America, which provides an opportunity to relate body size to climate within a species. We measured the length of a leg bone (calcaneal tuber, DstL) in 849 specimens from 60 localities that were dated by stratigraphy and ¹⁴C decay. We estimated body mass (M) as M = (DstL/11.49)³. Average annual temperature was estimated from δ¹⁸O values in the ice cores from Greenland. Calcaneal tuber length of Bison declined over the last 40,000 years, that is, average body mass was 37% larger (910 ± 50 kg) than today (665 ± 21 kg). Average annual temperature has warmed by 6°C since the Last Glacial Maximum (~24–18 kya) and is predicted to further increase by 4°C by the end of the 21st century. If body size continues to linearly respond to global temperature, Bison body mass will likely decline by an additional 46%, to 357 ± 54 kg, with an increase of 4°C globally. The rate of mass loss is 41 ± 10 kg per°C increase in global temperature. Changes in body size of Bison may be a result of migration, disease, or human harvest but those effects are likely to be local and short‐term and not likely to persist over the long time scale of the fossil record. The strong correspondence between body size of bison and air temperature is more likely the result of persistent effects on the ability to grow and the consequences of sustaining a large body mass in a warming environment. Continuing rises in global temperature will likely depress body sizes of bison, and perhaps other large grazers, without human intervention.     

Rapid evolution of great kiskadees on Bermuda: an assessment of the ability of the island rule to predict the direction of contemporary evolution in exotic vertebrates

Aim To determine whether an exotic bird species, the great kiskadee (Pitangus sulphuratus), has diverged in morphology from its native source population, and, if so, has done so in a manner predicted by the island rule. The island rule predicts that insular vertebrates will tend towards dwarfism or gigantism when isolated on islands, depending on their body size. For birds, the island rule predicts that species with body sizes below 70–120 g should increase in size. The great kiskadee has a mean mass of c. 60 g in its native range, therefore we predicted that it would increase in size within the exotic, and more insular, Bermudan range. Location The islands of Bermuda (exotic population) and Trinidad (native source population). Methods We took eight morphological measurements on 84 individuals captured in the exotic (Bermudan) population and 62 individuals captured in the native source (Trinidadian) population. We compared morphological metrics between populations using univariate and principal components analyses. We assessed whether the effects of genetic drift could explain observed differences in morphology. We calculated divergence rates in haldanes and darwins for comparison with published examples of contemporary evolution. Finally, we used mark–recapture analysis to determine the effects of the measured morphological characters on survivorship within the exotic Bermudan population. Results Individuals in the exotic Bermudan population have larger morphological dimensions than individuals in the native source population on Trinidad. The degree of divergence in body mass (g) and bill width (mm) is probably not due to genetic drift. This rate of divergence is nearly equal to that observed amongst well‐documented examples of contemporary bird evolution, and is within the mid‐range of rates reported across taxa. There is no clear effect of body size on survivorship as only one character (bill width) was found to have an influence on individual survivorship. Main conclusions Exotic species provide useful systems for examining evolutionary predictions over contemporary time‐scales. We found that divergence between the exotic and native populations of this bird species occurred over c. 17 generations, and was in the direction predicted by the island rule, a principle based on the study of native species.     

The island rule and the evolution of body size in the deep sea

Aim  Our goal is to test the generality of the island rule – a graded trend from gigantism in small-bodied species to dwarfism in large-bodied species – in the deep sea, a non-insular but potentially analogous system.
Location  Shallow-water and deep-sea benthic habitats in the western Atlantic Ocean from the North to South Poles.
Methods  We conducted regression analyses of body size of deep-sea gastropods species relative to their shallow-water congeners using measurements from the Malacolog ver. 3.3.3 database.
Results  Our results indicate that, consistent with the island rule, gastropod genera with small-bodied, shallow-water species have significantly larger deep-sea representatives, while the opposite is true for genera that are large-bodied in shallow water. Bathymetric body size clines within the deep sea are also consistent with predictions based on the island rule.
Main conclusions  Like islands, the deep sea is characterized by low absolute food availability, leading us to hypothesize that the island rule is a result of selection on body size in a resource-constrained environment. The body size of deep-sea species tends to converge on an optimal size for their particular ecological strategy and habitat.     

Climate change and evolution: disentangling environmental and genetic responses

Rapid climate change is likely to impose strong selection pressures on traits important for fitness, and therefore, microevolution in response to climate-mediated selection is potentially an important mechanism mitigating negative consequences of climate change. We reviewed the empirical evidence for recent microevolutionary responses to climate change in longitudinal studies emphasizing the following three perspectives emerging from the published data. First, although signatures of climate change are clearly visible in many ecological processes, similar examples of microevolutionary responses in literature are in fact very rare. Second, the quality of evidence for microevolutionary responses to climate change is far from satisfactory as the documented responses are often - if not typically - based on nongenetic data. We reinforce the view that it is as important to make the distinction between genetic (evolutionary) and phenotypic (includes a nongenetic, plastic component) responses clear, as it is to understand the relative roles of plasticity and genetics in adaptation to climate change. Third, in order to illustrate the difficulties and their potential ubiquity in detection of microevolution in response to natural selection, we reviewed the quantitative genetic studies on microevolutionary responses to natural selection in the context of long-term studies of vertebrates. The available evidence points to the overall conclusion that many responses perceived as adaptations to changing environmental conditions could be environmentally induced plastic responses rather than microevolutionary adaptations. Hence, clear-cut evidence indicating a significant role for evolutionary adaptation to ongoing climate warming is conspicuously scarce.     

Of mice and mammoths: evaluations of causal explanations for body size evolution in insular mammals

Aim We investigated the hypothesis that the insular body size of mammals results from selective forces whose influence varies with characteristics of the focal islands and the focal species, and with interactions among species (ecological displacement and release). Location Islands world‐wide. Methods We assembled data on the geographic characteristics (area, isolation, maximum elevation, latitude) and climate (annual averages and seasonality of temperature and precipitation) of islands, and on the ecological and morphological characteristics of focal species (number of mammalian competitors and predators, diet, body size of mainland reference populations) that were most relevant to our hypothesis (385 insular populations from 98 species of extant, non‐volant mammals across 248 islands). We used regression tree analyses to examine the hypothesized contextual importance of these factors in explaining variation in the insular body size of mammals. Results The results of regression tree analyses were consistent with predictions based on hypotheses of ecological release (more pronounced changes in body size on islands lacking mammalian competitors or predators), immigrant selection (more pronounced gigantism in small species inhabiting more isolated islands), thermoregulation and endurance during periods of climatic or environmental stress (more pronounced gigantism of small mammals on islands of higher latitudes or on those with colder and more seasonal climates), and resource subsidies (larger body size for mammals that utilize aquatic prey). The results, however, were not consistent with a prediction based on resource limitation and island area; that is, the insular body size of large mammals was not positively correlated with island area. Main conclusions These results support the hypothesis that the body size evolution of insular mammals is influenced by a combination of selective forces whose relative importance and nature of influence are contextual. While there may exist a theoretical optimal body size for mammals in general, the optimum for a particular insular population varies in a predictable manner with characteristics of the islands and the species, and with interactions among species. This study did, however, produce some unanticipated results that merit further study – patterns associated with Bergmann’s rule are amplified on islands, and the body size of small mammals appears to peak at intermediate and not maximum values of latitude and island isolation.     

陕北气候变化与生态植被变迁

分析了128万年以来陕北气候变化及其生态植被变迁。结果表明,陕北黄土高原气候经历了多次冷、暖、干、湿的周期变化。陕北植被变迁在地质时期以及历史时期早期,主要由气候条件所控制,植被类型随气候的冷暖干湿变化而变迁。随着人类活动的加剧,气候条件不再是影响植被变迁的唯一因素,人类活动对植被的影响愈来愈明显。明清时期,气候冷干,旱灾频繁．陕北生态环境脆弱,大规模垦殖和滥烧使自然植被迅速减少,陕北自然植被遭到毁灭性破坏。20世纪50年代,陕北逐步开始生态环境治理,在对生态环境治理的同时,又对部分地区自然植被进行破坏。20世纪80年代以后,生态环境总体上趋于好转。     

Cope's rule and the evolution of body size in Pinnipedimorpha (Mammalia: Carnivora)

Cope's rule describes the evolutionary trend for animal lineages to increase in body size over time. In this study, we tested the validity of Cope's rule for a marine mammal clade, the Pinnipedimorpha, which includes the extinct Desmatophocidae, and extant Phocidae (earless seals), Otariidae (fur seals and sea lions), and Odobenidae (walruses). We tested for the presence of Cope's rule by compiling a large dataset of body size data for extant and fossil pinnipeds and then examined how body size evolved through time. We found that there was a positive relationship between geologic age and body size. However, this trend is the result of differences between early assemblages of small-bodied pinnipeds (Oligocene to early Miocene) and later assemblages (middle Miocene to Pliocene) for which species exhibited greater size diversity. No significant differences were found between the number of increases or decreases in body size within Pinnipedimorpha or within specific pinniped clades. This suggests that the pinniped body size increase was driven by passive diversification into vacant niche space, with the common ancestor of Pinnipedimorpha occurring near the minimum adult body size possible for a marine mammal. Based upon the above results, the evolutionary history of pinnipeds does not follow Cope's rule.