TREE-960; No of Pages 8 Review Are islands the end of the colonization road? Eva Bellemain1 and Robert E. Ricklefs2 1 Smithsonian Tropical Research Institute, Apartado 0843–03092, APO AA 34002, Balboa, Anco´ n, Panama´ , Republic of Panama´ 2 Department of Biology, University of Missouri–St. Louis, 8001 Natural Bridge Road, St. Louis, MO 63121-4499, USA Ecologists have, up to now, widely regarded colonization Based on a long tradition of thinking about invasion of islands from continents as a one-way journey, mainly ecology and the evolution of dispersal and competitive because of widely accepted assertions that less diverse ability in island taxa (Box 1), ecologists widely consider island communities are easier to invade. However, con- colonization of islands from continents as a one-way jour- tinents present large targets and island species should be ney. Nevertheless, ‘reverse colonization’ should be capable of making the reverse journey, considering they possible, if not likely, for several reasons. Island species are the direct descendants of successful colonists and are, for the most part, the direct descendants of successful provided that they have not lost their dispersal abilities. colonists and, provided that adaptation to island life has Recent mapping of geography onto molecular phyloge- not resulted in reduced dispersal ability, island inhabi- nies has revealed several cases of ‘reverse colonization’ tants should be capable of making the reverse journey. (from islands to continents). We suggest this phenom- Moreover, although islands tend to have fewer species, enon warrants closer attention in ecology and biogeo- continents present large targets for colonization. Explicit graphy. Assessing its significance will contribute to molecular phylogenies produced from DNA sequence data understanding the role of dispersal and establishment since the mid-1990s are beginning to reveal geographic in biogeographic distributions and the assembly of relationships most readily interpreted as cases of reverse natural biotas. colonization (e.g. [9–11]). In a recent review of hypotheses related to oceanic island biogeography, Heaney [12] An emerging paradigm shift for island biogeography emphasized that the increasing appreciation for this The discipline of island biogeography attempts to discover phenomenon might signal an emerging paradigm shift factors that affect species richness across insular commu- for island biogeography. nities [1–4]. MacArthur and Wilson [3] revolutionized the In this review, we first summarize factors that influence discipline when they suggested that diversity on islands the direction of colonization between continents and represents a balance between the arrival of new species islands. Second, we characterize the prevalence of reverse through colonization (or speciation) and the disappearance colonization and evaluate the degree to which islands of old species by extinction. Because open water presents a might be sources of biodiversity for continents. We then strong barrier to dispersal by terrestrial taxa, species emphasize the importance of considering reverse coloniza- richness is lower on oceanic islands than on continents, tion for interpreting biogeographic patterns and highlight in contrast to continental islands where geographic iso- the significance that reverse colonization might have for lation is not a significant determinant of species richness ecological theory in general. Finally, we suggest some [5]. The diversity–invasibility theory [6] further postulates that less diverse communities (e.g. islands compared to continents) should be more susceptible to invasion by Glossary exotic species because ecological space is less densely Colonization: dispersal by a species to an area not previously inhabited by that packed and interspecific competition is less intense. Con- species, with subsequent establishment of a viable population. versely, the more densely packed ecological space of con- Dispersal: the spread of organisms to a new area (a complex process comprising emigration, movement and establishment). tinental biotas should be difficult to invade, particularly by Establishment: the settling of an individual at a new locality where it island populations for which evolution in low-competition successfully reproduces; at the population level, long-term persistence. environments might have produced more generalized phe- Extinction: the disappearance of a population or species either locally or globally, depending on the context. notypes at a competitive disadvantage in diverse commu- Migration: seasonal migration between different habitats or regions which nities. The diversity–invasibility theory has received much does not result in dispersal. support from theoretical studies. However, empirical stu- Movement: for individuals, the displacement phase between leaving a source locality and arriving at a new locality. dies indicate a negative relationship between invasibility Phylogenetic analysis: use of reconstructed evolutionary relationships to and diversity only at local scales, competitive interactions determine the history of trait evolution and geographic distribution. being overridden by habitat suitability at larger scales Reverse colonization: expansion of a species range from an area of low species richness to one of high species richness, specifically from island to continent. [7,8]. Thus, the relationship between diversity and inva- Sink: for a species, an area in which extinction exceeds colonization. sibility remains unresolved. Source area: for a species, an area from which populations colonize new places. Vicariance: the splitting of a species range into two or more fragments by continental movements or climate change. Corresponding author: Bellemain, E. ([email protected]). 0169-5347/$ – see front matter ß 2008 Elsevier Ltd. All rights reserved. doi:10.1016/j.tree.2008.05.001 Available online xxxxxx 1 TREE-960; No of Pages 8 Review Trends in Ecology and Evolution Vol.xxx No.x social interactions, or required for escaping predators [13– Box 1. Why have ecologists accepted ‘unidirectional 15]. MacArthur and Wilson [3] stated that ‘several charac- colonization’? teristics of adaptation to insular environment can be There is a well-established asymmetry in the minds of ecologists, generalized and documented. The most conspicuous is who generally regard continents primarily as source areas and the tendency to lose dispersal power.’ Nevertheless, many islands as sinks. From Wilson [52] to the development of metapopulation theory, the concept of ‘unidirectional colonization’ species clearly retain the ability to move between islands. has been well accepted. This is particularly evident in species that have spread In 1961, one of the world’s leading naturalists and ecologists, over long distances by island hopping across the western Edward Wilson, championed the concept of unidirectional coloniza- Pacific Ocean to Polynesia and even as far as the Hawaiian tion. In his study of ants from the Moluccas and Melanesian islands, Islands [15–17]. Comparisons of indices of dispersal ability he stated ‘The headquarters (of a taxon) can be shifted from a larger to a smaller land mass ... but not in the reverse direction’ [52]. (e.g. wing size or flight muscle mass) in sister groups A few years later, Wilson and the mathematical ecologist Robert inhabiting islands and continents might reveal potential MacArthur collaborated to develop a theory of island biogeography loss of dispersal ability of species colonizing islands from [3]. Their equilibrium theory described a dynamic balance between the continent [14]. colonization and extinction and predicted increasing equilibrium Because of the restricted area, island populations pro- diversity with increasing island size and decreasing diversity with greater distance from a colonization source. Although expanded to duce fewer potentially dispersing individuals than larger include a stepping-stone model with the possibility of migration continental landmasses, thereby favoring continent-to- between islands, their theory designates continents as potential island dispersal. This bias is diminished somewhat by sources of colonization for islands. Three core observations and the typically higher densities of island populations, which conjectures have reinforced the notion of unidirectional coloniza- tion. First, more species are available as potential colonists in could produce more pressure for dispersal, and larger continental source areas because of their larger size. Second, proportions of individuals living closer to the edges of islands have less diverse biotic communities and underutilized islands owing to perimeter–area allometry. Indeed, large resources (ecological space), which are available for arriving continental populations might produce relatively few colonists. Finally, greater species richness on continents selects potential over-water colonists. Little is known about the increased competitive ability in continental populations, raising the probability that colonists will become established on islands. Loss factors that motivate individuals to undertake dispersal of competitive ability and dispersal ability by island populations movements, and so the numerical argument against further exaggerates the advantage of continental populations as island-to-continent colonization is difficult to evaluate. colonists. More diverse communities (i.e. continents compared to MacArthur and Wilson considered the dispersal of populations islands) are