FURTHER READING Agardy, D. T. 2001. Scientific research opportunities at Palmyra atoll. A report submitted to The Nature Conservancy. Cobb, K. M., C. D. Charles, H. Cheng, and R. L. Edwards. 2003. El Niño Southern Oscillation and tropical Pacific climate during the last millennium. Nature 424: 271 276. Davis, A. S., L. B. Gray, D. A. Clague, and J. R. Hein. 2002. The Line Islands revisited: New 40 Ar/ 39 Ar geochronologic evidence for episodes of volcanism due to lithospheric extension. Geochemistry, Geophysics, Geosystems: doi: 10.1029/2001GC000190. Dawson, E. Y. 1959. Changes in Palmyra atoll and its vegetation through the activities of man 1913 1958. Pacific Naturalist 1: 51. Dinsdale, E. A., O. Pantos, S. Smriga, R. A. Edwards, F. Angly, L. Wegley, M. Hatay, D. Hall, E. Brown, M. Haynes, L. Krause, E. Sala, S. A. Sandin, R. Vega Thurber, B. L. Willis, F. Azam, N. Knowlton, and F. Rohwer. 2008. Microbial ecology of four coral atolls in the northern Line Islands. PLoS ONE 3: e1584. Handler, A. T., D. S. Gruner, W. P. Haines, M. W. Lange, and K. Y. Kaneshiro. 2007. Arthropod surveys on Palmyra atoll, Line Islands, and insights into the decline of the native tree Pisonia grandis (Nyctaginaceae). Pacific Science 61: 485 502. Keating, B. H. 1992. Insular geology of the Line Islands, in Geology and offshore mineral resources of the central Pacific basin, Circum-Pacific Council for Energy and Mineral Resources Earth Science Series, vol. 14. B. H. Keating and B. R. Bolton, eds. New York: Springer-Verlag, 77 99. Sandin, S. A., J. E. Smith, E. E. DeMartini, E. A. Dinsdale, S. D. Donner, A. M. Friedlander, T. Konotchick, M. Malay, J. E. Maragos, D. Obura, O. Pantos, G. Paulay, M. Richie, F. Rohwer, R. E. Schroeder, S. Walsh, J. B. C. Jackson, N. Knowlton, and E. Sala. 2008. Baselines and degradation of coral reefs in the northern Line Islands. PLoS ONE 3: e1548. UNESCO. 2003. Central Pacific World Heritage Project, International Workshop Report. Woodrofe, C. D., and R. F. McLean. 1998. Pleistocene morphology and Holocene emergence of Christmas (Kiritimati) Island, Pacific Ocean. Coral Reefs 17: 235 248. LIZARD RADIATIONS MIGUEL VENCES Technical University of Braunschweig, Germany Lizards belong to the clade Squamata, together with snakes, and among nonflying terrestrial vertebrates, they are the ones most commonly observed on islands. Lizards are characterized by a great facility in colonizing islands and adapting to novel ecological circumstances by changes in their morphology, physiology, and reproductive biology. They have consequently become an important model group for the inferential and experimental study of adaptive radiations. LIZARDS ON ISLANDS On major land-bridge islands with favorable climates (i.e., in the tropical, dry, and temperate zones) both liz- FIGURE 1 Emblematic island lizards. (A) Gallotia stehlini, Gran Canaria. (B) Gallotia galloti, Tenerife. (C) Chalcides sexlineatus, Gran Canaria. (D) Tarentola delalandii, Tenerife. These species and their relatives have originated on the Canary Islands. Photographs by Miguel Vences. 558 LIZARD RADIATIONS Gillespie08_L.indd 558 4/20/09 11:46:45 AM
ards and snakes are commonly encountered, with snake species richness often being similar to lizard species richness. On 14 major islands and island groups of the Mediterranean Sea, there are 152 occurrences of 30 species of lizards and 28 species of snakes. However, native extant snakes are missing on many smaller islands and on oceanic archipelagoes such as the Macaronesian Islands (Canary and Cape Verde Islands, Savage Islands, Madeira, and the Azores), where native species and even endemic radiations of lizards are present (Fig. 1). The most remote oceanic islands (e.g., Hawaii) are devoid of both native lizards and snakes. Although within-island diversification is rare in snakes and is limited to very large islands such as Madagascar, lizards have diversified on medium-sized islands such as the Greater Antilles as well (see below). Of the currently known ~5000 species and 26 families of lizards, representatives of the Gekkonidae, Iguanidae, Lacertidae, and Scincidae are most commonly encountered on islands. Continental islands, especially, may frequently act as an evolutionary reservoir by enabling the survival of remnants of lineages that became extinct or very rare on the mainland. Such is the case of the tuataras, two species of lizard-like reptiles which are the last extant representatives of the Sphenodontia (the sister group of squamates). At present, tuataras are confined to various small islands off New Zealand, although fossil remains demonstrate their past presence on the New Zealand mainland, and that of their relatives on other continents. On the Balearic Islands in the Mediterranean Sea, the lizard Podarcis lilfordi is present only on tiny offshore islands surrounding the larger islands of Mallorca and Menorca, where they are extinct. On Madagascar, the radiation of snakes in the subfamily Pseudoxyrhophiinae is very diverse, but FIGURE 2 The largest lizard worldwide, the Komodo dragon, Varanus komodoensis. Photograph by Thomas Ziegler. FIGURE 3 Both of the smallest lizards worldwide occur on islands. (A) The gecko Sphaerodactylus ariasae occurs on Isla Beata and adjacent areas of Hispaniola. Photograph by S. Blair Hedges. (B) Adult male Malagasy leaf chameleon of an undescribed species in the genus Brookesia from the extreme north of Madagascar. Photograph by Frank Glaw. this lineage has only a few representatives in Africa, where it probably has been replaced by other snakes. Both the largest and smallest extant lizards occur on islands: The largest is the Komodo dragon (Varanus komodoensis) with a maximum snout vent length of over 1500 mm (Fig. 2); the smallest (Fig. 3) are two species of Sphaerodactylus geckos (S. ariasae and S. parthenopion) from the Caribbean, with adult snout vent lengths of about 16 mm, and several species of Malagasy leaf chameleons (Brookesia) with adult snout vent lengths of 14 19 mm. Lizards appear to show a trend of island gigantism and dwarfism opposite to what is generally considered as a rule: In lineages of small lizards, the island populations and species become even smaller, and in lineages of large forms, the island representatives become even larger, especially in carnivorous taxa. Snakes also show size changes in island populations and species, and snakes that evolved to become small on islands did so to a relatively greater degree than those that became large. The observed pattern suggests that snake body size is principally influenced by prey size, with large snakes mainly feeding on nesting seabirds and small snakes mainly feeding on lizards. Many island lizards have adapted to resources that differ from those available on the nearby mainland. The most famous is the marine iguana from the Galápagos (Amblyrhynchus cristatus), the only lizard that feeds on algae while diving in the ocean. Many lizards of the family Lacertidae were originally insectivorous but became herbivorous on islands. In fact, herbivory in mainland lineages may be an important preadaptation that allows for successful colonization of island habitats. A further intriguing difference between island and mainland populations of lizards is population density, which is generally one order of magnitude higher on islands. This phenomenon is likely driven by distinctly lower numbers of predators and competitors. These same factors may also have allowed island lizards to expand LIZARD RADIATIONS 559 Gillespie08_L.indd 559 4/20/09 11:46:46 AM
their diet to include nectar, pollen, and fruit. Indeed, in several island ecosystems, lizards also occupy an important role as pollinators and seed dispersers. Few studies have addressed changes in reproductive strategy in island populations of lizards, but in species of the family Lacertidae a trend of reduced clutch size and larger egg size on islands has been noted. COLONIZATION OF ISLANDS BY LIZARDS Recent years have seen a paradigm shift in our understanding of the occurrence of many taxa on islands. This has involved a shift from the dominance of vicariance explanations to hypotheses in which dispersal plays at least an equally important role. In general, the mode of reproduction of lizards and snakes, with internal fertilization, favors overseas dispersal because the arrival of a single gravid female to an island can be sufficient to give rise to a new population. For lizards, there is no doubt that their dispersal capacities are high and that they have on many occasions colonized islands over water from the mainland or from other islands. For green iguanas, direct evidence exists that after a hurricane in 1995, at least 15 individuals arrived on a mat of logs and uprooted trees on the eastern beaches of Anguilla and other islands in the Caribbean, and some specimens survived there for at least three years. Molecular genetic analyses have provided evidence for various events of long-distance dispersal between Africa and South America (e.g., in geckos of the genera Tarentola and Hemidactylus, and in skinks of the genus Trachylepis). For example, Trachylepis atlantica from the Fernando de Noronha Archipelago in the Atlantic, 350 km east of the Brazilian coast, belongs to this mainly African and Malagasy genus rather than to the related Neotropical genus Mabuya. Its ancestors presumably colonized by overseas dispersal from Africa rather than from nearby South America. Native populations of lizards (and often endemic species) are found on many oceanic islands: on major archipelagos such as Macaronesia, the Galápagos, the Gulf of Guinea islands, the Comoros, and the Mascarenes, but also on many small and isolated islands. The Australian region, including small islands such as those of the Solomon and Bismarck archipelagoes, harbors a massive radiation of the scincid genus Sphenomorphus, and other skinks (genus Emoia) have radiated on most islands in the southwestern Pacific, including, among many others, the Fiji, New Caledonia, Solomon, and Bismarck archipelagoes. This further demonstrates the capacity for overseas dispersal of lizards. FIGURE 4 An endemic species of chameleon from the Comoro island of Mayotte, Furcifer polleni. Photograph by Frank Glaw. Inverse routes of colonization, from islands back to the mainland, have occurred as well. This appears to be the case for a Central and South American clade within the genus Anolis, which probably originated from a West Indian ancestor, and it is possibly also true for chameleons, which may have dispersed multiple times from Madagascar to mainland Africa, and which certainly have dispersed from Madagascar to Mayotte (Fig. 4). On the Gulf of Guinea islands (São Tomé, Principe, and Annobon), a relatively high proportion of endemic burrowing species of lizards and snakes occur, indicating that the capacity of overseas dispersal also extends to species living in humid soil and leaf litter. A combination of ocean currents, floating islands, and reduced surface salinity caused by freshwater discharges from large rivers may be favorable to overseas dispersal events in general and may also enable such soil-dwelling species to colonize islands. Eggs of some lizards are known to be resistant to immersion in seawater. In the case of Anolis sagrei, this may explain the survival of populations of this lizard on small islands vulnerable to hurricanes, but it also may allow the overseas rafting of lizard eggs in tree holes or mats of vegetation. In some cases, commensal species of lizards have been translocated by humans. Several species of geckos of the genus Hemidactylus have a transcontinental distribution that in some cases is due to natural colonization but often may reflect deliberate or, more probably, accidental introductions. Lipinia noctua, a scincid lizard that lives alongside humans on islands of the central and eastern Pacific, displays a phylogeographic pattern concordant with the express train hypothesis: Specimens may have been transported as stowaways on early Polynesian canoes during the rapid human colonization of Polynesian islands. 560 LIZARD RADIATIONS Gillespie08_L.indd 560 4/20/09 11:46:46 AM
PATTERNS OF INSULAR LIZARD RADIATIONS FIGURE 5 Galápagos iguanas. (A) The marine iguana, Amblyrhynchus cristatus. Photograph by Ylenia Chiari. (B) A terrestrial iguana, Conolophus subcristatus. Photograph by Scott Glaberman. The process of speciation can be either (1) adaptive (i.e., the process of an ancestral population diverging and giving rise to two daughter lineages adapted to different niches) or (2) nonadaptive (e.g., the separation of the daughter species by geographic barriers or by differentiation of features that serve for species recognition). Most lizard radiations on smaller islands probably belong to the category of nonadaptive and allopatric speciation on different islands. This same mode of speciation has also taken place within some islands of sufficient size. A few possible examples also exist for sympatric adaptive speciation within an island. As an instance of nonadaptive speciation on different islands, the western Canary Islands are populated by small radiations of skinks and geckos (Chalcides and Tarentola), but on each island or group of islands, only one species of each genus occurs. The situation is slightly more complex in the Canarian lacertid lizards, genus Gallotia: Here an initial split is observed between large-sized and small-sized species, and sympatry occurs only between (ecologically strongly differentiated) representatives of either group (on Hierro, Gomera, Tenerife, and probably La Palma, if extant species and natural occurrences are considered). Day geckos of the genus Phelsuma have radiated on the Seychelles and Mascarenes, and on each of these two archipelagoes there is a monophyletic lineage of various species and subspecies. At least on the Seychelles, the available evidence favors allopatric speciation of the three endemic taxa on different islands, with secondary sympatry in some cases. Crucial to test hypotheses of radiation on islands are robust phylogenies. However, critical data on the interplay of dispersal and vicariance can be provided by the geological age of an island or of its last connection to the mainland, and hence the age of evolutionary splits in the lineage under study. For example, the two Galápagos iguanas (the terrestrial genus Conolophus and the marine iguana Amblyrhynchus; Fig. 5) occur on the same islands and do form a monophyletic group. This could be interpreted as an example of speciation by ecological specialization under sympatric conditions. However, the age of the evolutionary divergence between these species predates the geological origin of the current Galápagos Islands. This indicates that either (1) they must have diverged on a previous, now submerged land mass, or (2) both species originated on the mainland, they colonized the Galápagos independently, and their mainland relatives subsequently went extinct. In general, the possibility of extinction must always be taken into account to understand the biogeographic history of lizard populations on islands. The best-studied case of an insular lizard radiation is that of the Caribbean genus Anolis (Iguanidae), the anoles, which are among the most common terrestrial vertebrates in the Caribbean and are found on almost every island in this region. There are over 400 species of anoles, of which nearly 150 are Caribbean. Their origin has been estimated at around 40 million years ago, and fossil specimens preserved in amber are known from the Oligocene to the Miocene of the Dominican Republic. The patterns of anole radiation have been intensively studied by Jonathan B. Losos and colleagues. Summaries are found in Losos (1998) and Losos and Thorpe (2004), from where much of the following information has been extracted. Anoles are very good dispersers, evidenced by cases of related taxa occurring on islands of great geographic distance. However, by far the highest proportion of Caribbean anoles are endemic to single island banks (more than 85%). A few cases of natural hybridization are known, but LIZARD RADIATIONS 561 Gillespie08_L.indd 561 4/20/09 11:46:47 AM
in general, mismating among species of these lizards is prevented by the throat fans ( dewlaps ) of males, which show specific colors and patterns used in species recognition. In fact, sympatric species of anoles always differ in the size, color, or patterning of their dewlaps. Up to 11 species of anoles can coexist at a single site, and such sympatric species almost always differ in terms of habitat use and morphology or physiology. The number of anole species coexisting on a certain island is significantly correlated with island size. Considering only small islands (i.e., islands of a surface of 1500 km 2 or less), the species area relationship is stronger for islands that were in the past connected by land bridges to other land masses than for isolated islands, highlighting the importance of historical effects: Land-bridge islands probably had a higher number of species at the time of isolation, and through subsequent extinctions, species numbers adjusted to the island-specific ecological carrying capacity. In contrast, isolated islands depend fully on over-water colonization as the source for species. Isolated islands mostly are populated by a single species of anole only, with a maximum of two species per island (which then differ in their ecology). Apparently, colonization of small isolated islands by anoles can be successful only if (1) the island does not yet harbor any anole population or (2) the island is populated by an anole species that differs in ecological requirements from the new colonizers. Evolutionary diversification of anoles appears to occur on a single island when its size is above a certain threshold. In the Caribbean, within-island diversification has occurred on the Greater Antilles (Jamaica, Puerto Rico, Hispaniola, and Cuba). Each of these large islands harbors endemic divergent lineages, which contain various species and, hence, very probably originated on the island. Within-island speciation can be invoked for at least 70% of the Greater Antillean anoles. A few examples from smaller islands or island groups exist of cooccurrence of endemic taxa that could have arisen on the same island, but these cases are not compelling. Hence, a certain island area is necessary for within-island speciation, a conclusion that highlights the importance of geography for this process. The Anolis radiations on the four Greater Antillean islands (although phylogenetically independent) show recurrent patterns. As was first pointed out by Ernest Williams, different types of habitat specialists (ecomorphs) occur on all or most of the Greater Antilles. These are usually represented by several species on each island (Figs. 6 8). Initially six ecomorphs were proposed, but others have since been distinguished. Interestingly, molecular FIGURE 6 Ecomorphs of Caribbean Anolis. All species shown are from Hispaniola. Names roughly denote the preferred habitat of each ecomorph. (A) Crown giant: Anolis baleatus. (B) Trunk crown: A. coelestinus. Note that the photographs are not to scale; Crown Giants are much larger than all other ecomorphs. Photographs by S. Blair Hedges. FIGURE 7 Ecomorphs of Caribbean Anolis, continued. (A) Trunk: A. christophei. (B) Trunk ground: A. cybotes. Photographs are not to scale. Photographs by S. Blair Hedges. 562 LIZARD RADIATIONS Gillespie08_L.indd 562 4/29/09 4:19:04 PM
Cuba was fragmented during the Miocene. The Anolis alutaceus group, also on Cuba, contains 12 species with narrow distributions, mostly centered on different mountain ranges, a pattern that is also seen in other groups. Which prevalent pattern of species formation gave rise to the current diversity of anoles? Adaptive speciation in sympatry or parapatry may occur in Caribbean anoles, but it is probably not the main driving force explaining their diversity. In many cases, populations became isolated on small land-bridge islands or reached isolated small islands by overseas dispersal. Geographically and thus genetically separated from other anole populations, they evolved different morphologies and dewlaps, probably largely because of adaptation to new ecological conditions. On the larger islands, species belonging to the main ecomorphs underwent allopatric speciation (e.g., on different mountain ranges or on parts of their island that were separated by water barriers in periods of rising sea levels). As summarized in the following section, many examples indicate that adaptation can occur in the absence of speciation in Caribbean anoles. But it is still uncertain how the initial differentiation of ecomorphs on each of the Greater Antillean islands took place. FIGURE 8 Ecomorphs of Caribbean Anolis, continued. (A) Stream: A. eugenegrahami. (B) Grass: A. semilineatus. (C) Twig: A. placidus. Photographs are not to scale. Photographs by S. Blair Hedges. data show that, with two exceptions, the ecomorphs arose independently on the different islands: Different ancestors diversified independently and gave rise to the same ecological and morphological adaptations. Species belonging to different ecomorphs usually occur sympatrically, but species belonging to the same ecomorph generally are geographically separated within an island (and have different dewlap colors or patterning). In addition to the six main ecomorphs, many islands harbor further habitat specialists, but these usually occur on a single island only. In several cases, the different species of one ecomorph occur in geographically separated populations scattered across an island. In the Anolis carolinensis group, three evolutionary lineages can be distinguished and have ranges corresponding to three paleo-archipelagoes into which PHYLOGEOGRAPHY AND EXPERIMENTAL TESTS OF SELECTION Deciphering radiations is possible by looking at general patterns across a whole group or by examining in more detail the microevolutionary processes. Comparison of DNA sequences allows phylogeographical analyses where chiefly the geographical distribution of differentiated alleles (haplotypes) is mapped, and the phylogenetic relationships among these haplotypes is determined. The assumption is that haplotypes evolve through mutation, and different haplotypes get fixed in genetically isolated populations. In various studies on anoles and Canarian lizards, Roger S. Thorpe and colleagues have found evidence for discordance between historical and adaptive patterns. For example, in Gallotia lizards on the Canarian island of Tenerife, a historical boundary of mitochondrial haplotype lineages exists between western and northeastern areas, whereas within both groups, morphological differences were found between northern and southern populations, reflecting strong ecological differences between the humid north and arid south of the island. On Dominica, Anolis oculatus shows a complex phylogeographical structure that is not fully concordant with the phenotypic variability encountered. These examples demonstrate that morphological adaptations to local conditions, especially in terms of col- LIZARD RADIATIONS 563 Gillespie08_L.indd 563 4/29/09 4:19:06 PM
oration, can evolve very fast in island lizards. This is also witnessed by the large variability of lacertid lizard species inhabiting Mediterranean islands (e.g., Adriatic islands, satellite islands of the Balearics, or Tyrrhenic islands in Greece). From many of these archipelagoes, a plethora of subspecies have been described based on color patterns and partly on variation in scale numbers, but molecular studies have rarely found any significant differentiation between these populations, indicating that the external differences evolved extremely rapidly, on a geological timescale. Other work has yielded evidence that in Anolis sagrei, the number of body scales increases with increasing precipitation and with decreasing temperature in open arid habitats, and the variation in scale numbers is probably heritable. In further experiments, the effects of a potential predator (the ground-dwelling lizard Leiocephalus carinatus) on the behavior of Anolis sagrei was tested by introducing the potential predator on six small islands on the Bahamas and using six other predator-free islands as control sites. As a result, anoles altered their behavior by using the ground less often, but in addition, a strong selection took place: Surviving specimens on the experimental islands had larger body sizes and longer hindlimbs than those on control sites, probably reflecting their better capacities to escape. Evidence for strong selection pressures acting on island lizards also comes from further experimental studies. The Dominican Anolis oculatus displays various ecomorphological variants related to different conditions between the east and west coasts and the montane regions of the island. In experiments, lizards were translocated to large lizard-proof enclosures in regions occupied by other habitat types than those in their source population. Morphology (coloration, scale counts, body proportions) of the translocated lizards were scored, and each lizard individually marked. Several months later, survivors were collected and identified. Morphological differences were found between survivors and non-survivors (e.g., of specimens of the montane population in enclosures of the relatively xeric west coast), and the intensity of selection was dependent on the magnitude of ecological change experienced by the specimens in the enclosures. How these intraspecific processes of fast morphological variation relate to the actual process of species formation and adaptive radiation is not clear. Evidence of parapatric forms with restricted gene flow among them comes from the islands of Dominica and Martinique; on Martinique this may constitute evidence for adaptive (ecological) species formation because the forms are distinguished by current habitat and not by historical allopatry. It seems clear that these lizards have a strong potential to adapt to new ecological conditions by changes in morphology and coloration, and this may have favored adaptive speciation (mostly under allopatric conditions). This may also be a factor explaining the recurrent evolution of similar ecomorphs. SEE ALSO THE FOLLOWING ARTICLES Adaptive Radiation / Convergence / Dispersal / Komodo Dragons / Snakes FURTHER READING Losos, J. B. 1994. Integrative approaches to evolutionary ecology: Anolis lizards as model systems. Annual Reviews of Ecology and Systematics 25: 467 493. Losos, J. B. 1998. Ecological and evolutionary determinants of the speciesarea relationship in Caribbean anoline lizards, in Evolution on islands. P. R. Grant, ed. Oxford: Oxford University Press, 210 224. Losos, J. B., and R. S. Thorpe. 2004. Evolutionary diversification of Caribbean Anolis lizards, in Adaptive speciation. U. Dieckmann, M. Doebeli, J. A. J. Metz, and D. Tautz, eds. Cambridge: Cambridge University Press, 322 344. Olesen, J. M., and A. Valido. 2003. Lizards as pollinators and seed dispersers: an island phenomenon. Trends in Ecology and Evolution 18: 177 181. Williams, E. E. 1983. Ecomorphs, faunas, island size, and diverse end points in island radiations of Anolis, in Lizard ecology. R. B. Huey, E. R. Pianka, and T. W. Schoener, eds. Cambridge, MA: Harvard University Press, 326 370. LOPHELIA OASES SANDRA BROOKE Marine Conservation Biology Institute, Bellevue, WA The deep-water stony coral Lophelia pertusa (Linnaeus 1758) creates extensive and complex structures on hardbottomed areas in the deep sea, including continental shelf bedrock, lithified sediment mounds, volcanic basalt, and (microbially mediated) authigenic carbonate. Large colonies of L. pertusa have abundant tangled branches that provide habitats for diverse and abundant associated communities. These long-lived and slow-growing coral ecosystems are currently under threat globally from negative human impact, and although some areas have been placed under protective legislation, continued international effort is needed to ensure the future of these valuable resources. CORAL BIOLOGY There are several species of framework-building deep-water corals (Lophelia pertusa, Oculina varicosa, 564 LOPHELIA OASES Gillespie08_L.indd 564 4/20/09 11:46:50 AM