Shai Meiri

The island rule: made to be broken?

The island rule is a hypothesis whereby small mammals evolve larger size on islands while large insular mammals dwarf. The rule is believed to emanate from small mammals growing larger to control more resources and enhance metabolic efficiency, while large mammals evolve smaller size to reduce resource requirements and increase reproductive output. We show that there is no evidence for the existence of the island rule when phylogenetic comparative methods are applied to a large, high-quality dataset. Rather, there are just a few clade-specific patterns: carnivores; heteromyid rodents; and artiodactyls typically evolve smaller size on islands whereas murid rodents usually grow larger. The island rule is probably an artefact of comparing distantly related groups showing clade-specific responses to insularity. Instead of a rule, size evolution on islands is likely to be governed by the biotic and abiotic characteristics of different islands, the biology of the species in question and contingency.

THE ISLAND RULE IN LARGE MAMMALS: PALEONTOLOGY MEETS ECOLOGY

Abstract 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.

Body Size of Insular Carnivores: Little Support for the Island Rule

Large mammals are thought to evolve to be smaller on islands, whereas small mammals grow larger. A negative correlation between relative size of island individuals and body mass is termed the “island rule.” Several mechanisms—mainly competitive release, resource limitation, dispersal ability, and lighter predation pressure on islands, as well as a general physiological advantage of modal size—have been advanced to explain this pattern. We measured skulls and teeth of terrestrial members of the order Carnivora in order to analyze patterns of body size evolution between insular populations and their near mainland conspecifics. No correlations were found between the size ratios of insular/mainland carnivore species and body mass. Only little support for the island rule is found when individual populations rather than species are considered. Our data are at odds with those advanced in support of theories of optimal body size. Carnivore size is subjected to a host of selective pressures that do not vary uniformly from place to place. Mass alone cannot account for the patterns in body size of insular carnivores.

Island Species Richness Increases with Habitat Diversity

Species richness is commonly thought to increase with habitat diversity. However, a recent theoretical model aiming to unify niche and island biogeography theories predicted a hump‐shaped relationship between richness and habitat diversity. Given the contradiction between model results and previous knowledge, we examine whether the relationship between species richness and habitat diversity is consistently monotonically increasing and under which circumstances, if at all, such relationships could be hump shaped. We review the empirical evidence about the shape of such relationships and show that species richness on islands usually increases with habitat diversity and that it never decreases. We also critically examine the assumptions of the theoretical model and modify them to incorporate a less restrictive definition of niche width. The modified assumptions lead to simulations that better capture real patterns, using either simple parameters or observed distributions of niche breadth. Further work is needed to incorporate ecological interactions and metacommunity dynamics if the aim is to merge niche and island biogeography theories in a realistic modeling framework.

Intraspecific competition and high food availability are associated with insular gigantism in a lizard

Resource availability, competition, and predation commonly drive body size evolution. We assess the impact of high food availability and the consequent increased intraspecific competition, as expressed by tail injuries and cannibalism, on body size in Skyros wall lizards (Podarcis gaigeae). Lizard populations on islets surrounding Skyros (Aegean Sea) all have fewer predators and competitors than on Skyros but differ in the numbers of nesting seabirds. We predicted the following: (1) the presence of breeding seabirds (providing nutrients) will increase lizard population densities; (2) dense lizard populations will experience stronger intraspecific competition; and (3) such aggression, will be associated with larger average body size. We found a positive correlation between seabird and lizard densities. Cannibalism and tail injuries were considerably higher in dense populations. Increases in cannibalism and tail loss were associated with large body sizes. Adult cannibalism on juveniles may select for rapid growth, fuelled by high food abundance, setting thus the stage for the evolution of gigantism.

Body Size Diversification in Anolis: Novel Environment and Island Effects

Extreme morphologies of many insular taxa suggest that islands have unusual properties that influence the tempo and mode of evolution. Yet whether insularity per se promotes rapid phenotypic evolution remains largely untested. We extend a phylogenetic comparative approach to test the influence of novel environments versus insularity on rates of body size and sexual size dimorphism diversification in Anolis. Rates of body size diversification among small-island and mainland species were similar to those of anole species on the Greater Antilles. However, the Greater Antilles taxa that colonized small islands and the mainland are ecologically nonrandom: rates of body size diversification among small-island and mainland species are high compared to their large-island sister taxa. Furthermore, rates of diversification in sexual size dimorphism on small islands are high compared to all large-island and mainland lineages. We suggest that elevated diversifying selection, particularly as a result of ecological release, may drive high rates of body size diversification in both small-island and mainland novel environments. In contrast, high abundance (prevalent among small-island lizard communities) mediating intraspecific resource competition and male—male competition may explain why sexual size dimorphism diversifies faster among small-island lineages than among their mainland and large-island relatives.

Global Taxonomic Diversity of Living Reptiles

Reptiles are one of the most ecologically and evolutionarily remarkable groups of living organisms, having successfully colonized most of the planet, including the oceans and some of the harshest and more environmentally unstable ecosystems on earth. Here, based on a complete dataset of all the world’s diversity of living reptiles, we analyse lineage taxonomic richness both within and among clades, at different levels of the phylogenetic hierarchy. We also analyse the historical tendencies in the descriptions of new reptile species from Linnaeus to March 2012. Although (non-avian) reptiles are the second most species-rich group of amniotes after birds, most of their diversity (96.3%) is concentrated in squamates (59% lizards, 35% snakes, and 2% amphisbaenians). In strong contrast, turtles (3.4%), crocodilians (0.3%), and tuataras (0.01%) are far less diverse. In terms of species discoveries, most turtles and crocodilians were described early, while descriptions of lizards, snakes and amphisbaenians are multimodal with respect to time. Lizard descriptions, in particular, have reached unprecedented levels during the last decade. Finally, despite such remarkably asymmetric distributions of reptile taxonomic diversity among groups, we found that the distributions of lineage richness are consistently right-skewed, with most clades (monophyletic families and genera) containing few lineages (monophyletic genera and species, respectively), while only a few have radiated greatly (notably the families Colubridae and Scincidae, and the lizard genera Anolis and Liolaemus). Therefore, such consistency in the frequency distribution of richness among clades and among phylogenetic levels suggests that the nature of reptile biodiversity is fundamentally fractal (i.e., it is scale invariant). We then compared current reptile diversity with the global reptile diversity and taxonomy known in 1980. Despite substantial differences in the taxonomies (relative to 2012), the patterns of lineage richness remain qualitatively identical, hence reinforcing our conclusions about the fractal nature of reptile biodiversity.

VARIABILITY AND SEXUAL SIZE DIMORPHISM IN CARNIVORES: TESTING THE NICHE VARIATION HYPOTHESIS

The niche variation hypothesis predicts greater morphological variability in populations occupying wide ecological niches than in those occupying narrow ones. Island populations of carnivores are often assumed to have wider niches than mainland populations, because the number of competing species on islands is usually smaller. We compared coefficients of variation and degrees of sexual size dimorphism in skulls and canines of pairs of related insular and mainland populations belonging to 39 carnivore species. Mainland populations were more variable than insular ones. Averaging population values for the different species, we found no significant differences in the variability of insular and mainland taxa. There was no consistent difference in the degree of sexual size dimorphism between insular and mainland carnivores for either skull length or canine diameter. We hypothesize that gene flow is the main source of the greater variability in mainland populations. The niche variation hypothesis is not supported.

Insular Carnivore Biogeography: Island Area and Mammalian Optimal Body Size

Patterns of size variation in insular mammals have been used to support the claim that mammals have a single optimal body size. This hypothesis enjoys wide support, despite having been questioned on both theoretical and empirical grounds. It is claimed that species of optimal size maintain the highest population densities. Therefore these species are thought to inhabit the smallest islands, where larger and smaller species are generally absent. We sought such a pattern by testing how area affects the body sizes of the largest and smallest carnivore species on islands. Using data on carnivores from 322 islands, we found that the sizes of carnivores on small islands tend to be close to the order’s mode. Furthermore, we found that the size distribution of carnivore species that inhabit islands resembles that of those whose range is entirely continental. We conclude that insular carnivores provide no support for theories proposing a single optimal size, and we suspect such theories are also flawed on theoretical grounds.

New taxonomy and the origin of species.

The trend for elevating known subspecies to the status of species on the basis of inappropriate evidence can potentially divert important conservation funds away from other species.