OVERVIEW
The importance of islands in revealing evolutionary processes has been recognized since Darwin’s work on the Galapagos (Darwin, 1909) and Wallace’s work in the Malay Archipelago (Wallace, 1876). Since, island biogeography has provided many elegant examples of the evolutionary mechanisms involved in generating biodiversity, including geological processes and colonization and isolation (Emerson, 2008; Gillespie et al., 2008a; Parent et al., 2008). Archipelagos such as Hawaii and the Galapagos (photograph above) provide examples where cycles of evolutionary radiation have produced replicated patterns of endemic, often bizarre, forms (Cowie & Holland, 2008; Dunbar-Co et al., 2008; Parent et al., 2008). Yet, the extreme isolation of these islands reduces the interplay between islands and continents—interchange is one-way (islands as sinks) and limited to rare chance dispersal events (Cowie and Holland 2008). The West Indies and island chains in the Indian Ocean (Madagascar, Comoros, Seychelles, Mascarenes) are remarkable as they are sufficiently old and isolated to have generated endemic forms, but close enough continents to sustain a dynamic two-way interaction with diverse continental landmasses.
Our island biogeography projects seek to understand the generation of biodiversity on island archipelagos in relation to geographical isolation and dispersal abilities of taxa.
The importance of islands in revealing evolutionary processes has been recognized since Darwin’s work on the Galapagos (Darwin, 1909) and Wallace’s work in the Malay Archipelago (Wallace, 1876). Since, island biogeography has provided many elegant examples of the evolutionary mechanisms involved in generating biodiversity, including geological processes and colonization and isolation (Emerson, 2008; Gillespie et al., 2008a; Parent et al., 2008). Archipelagos such as Hawaii and the Galapagos (photograph above) provide examples where cycles of evolutionary radiation have produced replicated patterns of endemic, often bizarre, forms (Cowie & Holland, 2008; Dunbar-Co et al., 2008; Parent et al., 2008). Yet, the extreme isolation of these islands reduces the interplay between islands and continents—interchange is one-way (islands as sinks) and limited to rare chance dispersal events (Cowie and Holland 2008). The West Indies and island chains in the Indian Ocean (Madagascar, Comoros, Seychelles, Mascarenes) are remarkable as they are sufficiently old and isolated to have generated endemic forms, but close enough continents to sustain a dynamic two-way interaction with diverse continental landmasses.
Our island biogeography projects seek to understand the generation of biodiversity on island archipelagos in relation to geographical isolation and dispersal abilities of taxa.
From Bocas del Toro, islets off the Caribbean coast of Panama
BRIEF RECAP OF THE EARLY HISTORY OF BIOGEOGRAPHY
Much current work on island biogeography, including our project, focuses on phylogenetics, understanding the relationship among populations and species and how they relate to the geological history of islands. Thus emphasis is on genetic structuring of data, reflecting historical patterns, including patterns of species formation. This is a focus that has not always been central in island biogeography. The famous island biogeography model of McArthur and Wilson (1963), for example, does not consider the process of speciation. Below is a brief summary of the history of biogeography, with some emphasis on McArhtur and Wilson's model, and recent advances in biogeography and phylogeography.
The modern science of biogeography dates back at least to the 18th century, with the writings of giants like Buffon (1761) and Linnaeus (1781). Buffon, for example, observed that different regions, even if similar in climate and other conditions, had distinct biotas, a phenomenon that was later dubbed "Buffon's law''. Buffon was also one of the first to speculate that the New and Old world were once connected, and had shared biotas, before waters "divided Africa and America" (Buffon 1791: 451), thus laying a foundation for vicariance biogeography (explaining biogeographical patterns purely through geological history and formation of barriers). Important early contributions were also made by Forster (1778), who pointed out fundamental biogeographical patterns such as basic area-richness relationships and latitudinal gradient in diversity. The next major advances were made by what might be referred to as "Darwin's generation", Darwin himself and several contemporaries. Joseph Dalton Hooker (1844-60, 1861), for example, laid further foundations for vicariance biogeography and postulated the historical existence of great landmasses that correspond roughly to the major landmasses resulting from the early breakup of Gondwana. Sclater (1858) divided the terrestrial world into biogeographical regions, that still are recognized largely as originally proposed. He developed the idea that regions and relationships among them can be discovered through studying their biota and degree of endemism, which was further advanced by Wallace (1876), who offered a more detailed division of the world, and famously proposed a biogeographical regional division occurring across a seemingly strangely placed line in between the Indonesian islands of Borneo and Sulawesi, later dubbed the "Wallace Line". Darwin (1859) integrated biogeography directly into his theory of evolution by natural selection, where the distribution of species across different landmasses, and the relationships among these, provided direct evidence for natural selection. Darwin's focus was in particular on geological barriers, and dispersal across these barriers, and how these factors interplay in the formation of new species. In effect, he argued that barriers, given enough time, would allow differences to accumulate through the slow process of natural selection, and thus different species would form on each side of a barrier. Darwin also suggested a general pattern where a species is formed in one place, and subsequently disperses to occupy suitable habitats elsewhere, an early 'centers of origin' idea. Darwin and some of his contemporaries differed dramatically in their view of vicariance and dispersal. Darwin had little faith in landbridge hypotheses, various ideas of how continents might have been linked in the past, and emphasized dispersal. Hooker, in contrast, had equally little faith in Darwin's long distance dispersal hypotheses and thought vicariance was more important. At the time, both seemed to require series of unlikely scenarios, however, the view of vicariance as primarily the construction of ancient 'land bridges' was to change dramatically as plausible mechanisms for continental movements were proposed. Wegener (1924-1936) proposed then radical ideas about continental drift, that were never generally accepted during his life, but became mainstream during the later half of the 20th century. With strong geological evidence of continental drift, and ancient connections among continents, vicariance biogeography was demystified and became mainstream. The emphasis on vicariance immediately following acceptance of continental drift, indeed, was so strong as to completely marginalize dispersal as a biogeographical force, despite Darwin's many elegant experiments demonstrating dispersal ability, and possible dispersal means for a variety of organisms. It is only recently, through advances in phylogenetics providing evidence of both relationship among species as well as historical dating of speciation events, that the importance of dispersal is again starting to be appreciated. Although many phylogenetic studies reveal patterns supporting vicariance hypotheses, countless other phylogenetic analyses of taxa throughout the world are revealing patterns or ages that are partially or wholly inconsistent with vicariance, Modern biogeography in many ways revolves around understanding the relative importance of vicariance and dispersal explanations, for different taxa and regions.
The modern science of biogeography dates back at least to the 18th century, with the writings of giants like Buffon (1761) and Linnaeus (1781). Buffon, for example, observed that different regions, even if similar in climate and other conditions, had distinct biotas, a phenomenon that was later dubbed "Buffon's law''. Buffon was also one of the first to speculate that the New and Old world were once connected, and had shared biotas, before waters "divided Africa and America" (Buffon 1791: 451), thus laying a foundation for vicariance biogeography (explaining biogeographical patterns purely through geological history and formation of barriers). Important early contributions were also made by Forster (1778), who pointed out fundamental biogeographical patterns such as basic area-richness relationships and latitudinal gradient in diversity. The next major advances were made by what might be referred to as "Darwin's generation", Darwin himself and several contemporaries. Joseph Dalton Hooker (1844-60, 1861), for example, laid further foundations for vicariance biogeography and postulated the historical existence of great landmasses that correspond roughly to the major landmasses resulting from the early breakup of Gondwana. Sclater (1858) divided the terrestrial world into biogeographical regions, that still are recognized largely as originally proposed. He developed the idea that regions and relationships among them can be discovered through studying their biota and degree of endemism, which was further advanced by Wallace (1876), who offered a more detailed division of the world, and famously proposed a biogeographical regional division occurring across a seemingly strangely placed line in between the Indonesian islands of Borneo and Sulawesi, later dubbed the "Wallace Line". Darwin (1859) integrated biogeography directly into his theory of evolution by natural selection, where the distribution of species across different landmasses, and the relationships among these, provided direct evidence for natural selection. Darwin's focus was in particular on geological barriers, and dispersal across these barriers, and how these factors interplay in the formation of new species. In effect, he argued that barriers, given enough time, would allow differences to accumulate through the slow process of natural selection, and thus different species would form on each side of a barrier. Darwin also suggested a general pattern where a species is formed in one place, and subsequently disperses to occupy suitable habitats elsewhere, an early 'centers of origin' idea. Darwin and some of his contemporaries differed dramatically in their view of vicariance and dispersal. Darwin had little faith in landbridge hypotheses, various ideas of how continents might have been linked in the past, and emphasized dispersal. Hooker, in contrast, had equally little faith in Darwin's long distance dispersal hypotheses and thought vicariance was more important. At the time, both seemed to require series of unlikely scenarios, however, the view of vicariance as primarily the construction of ancient 'land bridges' was to change dramatically as plausible mechanisms for continental movements were proposed. Wegener (1924-1936) proposed then radical ideas about continental drift, that were never generally accepted during his life, but became mainstream during the later half of the 20th century. With strong geological evidence of continental drift, and ancient connections among continents, vicariance biogeography was demystified and became mainstream. The emphasis on vicariance immediately following acceptance of continental drift, indeed, was so strong as to completely marginalize dispersal as a biogeographical force, despite Darwin's many elegant experiments demonstrating dispersal ability, and possible dispersal means for a variety of organisms. It is only recently, through advances in phylogenetics providing evidence of both relationship among species as well as historical dating of speciation events, that the importance of dispersal is again starting to be appreciated. Although many phylogenetic studies reveal patterns supporting vicariance hypotheses, countless other phylogenetic analyses of taxa throughout the world are revealing patterns or ages that are partially or wholly inconsistent with vicariance, Modern biogeography in many ways revolves around understanding the relative importance of vicariance and dispersal explanations, for different taxa and regions.
THE ECOLOGIAL MODEL OF ISLAND BIOGEOGRAPHY
A modified version of the classical island biogeography model proposed by MacArthur and Wilson (1963) is depicted above. The model considers the interaction of two main parameters, colonization and extinction, and then considers island size and distance from mainland as predictors of the species richness found on each island. Both colonization and extinction can be thought of in terms of rates or probabilities, and the size and isolation of islands impacts the probability of colonization and of extinction. Simply, Islands close to the mainland will more readily receive colonists from that mainland and, similarly, probability of colonization of large islands will be higher than that of small islands. Thus the larger the island and closer to the mainland, the more potential species will arrive. Species will also more readily go extinct on small islands than large, due to factors such as smaller population sizes and less available habitat. These parameters go hand in hand predicting that species richness will peak in large islands near mainlands, and be lowest in small islands far away from the mainland.
This simple model is quite powerful, and remains fundamentally important in biogeography. Species-area curves for multiple organisms across many archipelagos demonstrate forcefully that island area, in particular, is a strong predictor of species richness. However, this model downplays a major element: speciation. Species arriving on oceanic islands may undergo speciation (parameter G in the McArthur and Wilson model), sometimes adaptive radiation, such that even species richness can be created in situ and does not entirely depend on colonization. Thus many isolated islands are rich in species that occur nowhere else, island endemics, that have radiated within the islands. A striking example are the Hawaiian fruit flies (Drosophila), having diverged into an estimated 500 species or more, a spectacular fruit fly diversity not paralleled in any region of any larger landmass. Although the original model includes G as one parameter, the authors concluded that it could propably be safely omitted in 'most cases'. Hence, this parameter is rarely considered. Doubtless, one reason why the area-richness relationship has been so well established is that the impact of speciation on richness can be expected to be in the same direction as the impacts of colonization-extinction; larger islands will generate more species through within island speciation. Thus, speciation reinforces the area-richness relationship and thus the predictions of the island biogeography model, even when it is omitted as a parameter in the model.
This simple model is quite powerful, and remains fundamentally important in biogeography. Species-area curves for multiple organisms across many archipelagos demonstrate forcefully that island area, in particular, is a strong predictor of species richness. However, this model downplays a major element: speciation. Species arriving on oceanic islands may undergo speciation (parameter G in the McArthur and Wilson model), sometimes adaptive radiation, such that even species richness can be created in situ and does not entirely depend on colonization. Thus many isolated islands are rich in species that occur nowhere else, island endemics, that have radiated within the islands. A striking example are the Hawaiian fruit flies (Drosophila), having diverged into an estimated 500 species or more, a spectacular fruit fly diversity not paralleled in any region of any larger landmass. Although the original model includes G as one parameter, the authors concluded that it could propably be safely omitted in 'most cases'. Hence, this parameter is rarely considered. Doubtless, one reason why the area-richness relationship has been so well established is that the impact of speciation on richness can be expected to be in the same direction as the impacts of colonization-extinction; larger islands will generate more species through within island speciation. Thus, speciation reinforces the area-richness relationship and thus the predictions of the island biogeography model, even when it is omitted as a parameter in the model.
PHYLOGENETICS AND PHYLOGEOGRAPHY
The study of biogeography has increasingly become tree-based, especially after the routine application of molecular data to reconstruct phylogenies. Phylogenies are used to reveal genetic relathionship among taxa and in turn relate these to their geographic distributions. Whether revealing relationships among species or among populations within species (phylogeography), phylogenies reflect historical patterns that can be used to infer vicariance and dispersal events and mode and tempo of speciation, especially when trees are dated. If relationships and dates match the geological history of the landmasses in question, biogeographical patterns can be explained primarily with reference to earths geology, or vicariance. Discordance between phylogeny and geology, on the other hand, implies other kinds of biogeographical factors at play, including dispersal--often across distinct barriers--and extinction events, among others.
Three steps in biogeographical analyses using phylogenetic data
A three-pronged approach to reconstructing biogeographical histories through phylognetic tools is becoming increasingly standard, especially where vicariance is thought to have played a potential role in island colonization. In some sense we could consider vicariance as a kind of a 'null hypothesis' that we need to reject before proposing more 'ad hoc' hypotheses of dispersal. On many volcanic oceanic islands, vicariance can be ruled out as no connection has ever existed between the island and any other landmasses. But, many islands, such as the Greater Antilles, Madagascar, and countless others, have continental building blocks and/or have possibly been connected to continental landmasses at some point in their history. With a known, or hypothesized, vicariant history of an island, the first test of vicariance would be if the phylogeny of a given group under study is consistent with the vicariant history, for example reflecting single (monophyletic) island clades, rather than multiple phylogenetically isolated clades. The latter would imply multiple colonization events among relatively close relatives, more consistent with multiple dispersal events. The second test of vicariance hypotheses would be dating phylogenetic trees where the vicariance expectation would be that the time of colonization matched with the timing of the vicariant 'event' - such as the time when an island fragmented from a mainland, or the period during which a hypothetical landbridge existed to connect islands to mainland (e.g. GAARlandia). Absent matching time, vicariance can be ruled out. The third test of vicariance would be explicit hypothesis testing. If a clade passes tests one and two, then a model can be constructed with or without a vicariance parameter and using approaches such as maximum likelihood ratio test, the fit of competing hypotheses to data can be evaluated. If all three are consistent with vicariance, ad hoc hypothesis of (long distance-, overwater-) dispersal are unnecessary.
To be continued...
Three steps in biogeographical analyses using phylogenetic data
A three-pronged approach to reconstructing biogeographical histories through phylognetic tools is becoming increasingly standard, especially where vicariance is thought to have played a potential role in island colonization. In some sense we could consider vicariance as a kind of a 'null hypothesis' that we need to reject before proposing more 'ad hoc' hypotheses of dispersal. On many volcanic oceanic islands, vicariance can be ruled out as no connection has ever existed between the island and any other landmasses. But, many islands, such as the Greater Antilles, Madagascar, and countless others, have continental building blocks and/or have possibly been connected to continental landmasses at some point in their history. With a known, or hypothesized, vicariant history of an island, the first test of vicariance would be if the phylogeny of a given group under study is consistent with the vicariant history, for example reflecting single (monophyletic) island clades, rather than multiple phylogenetically isolated clades. The latter would imply multiple colonization events among relatively close relatives, more consistent with multiple dispersal events. The second test of vicariance hypotheses would be dating phylogenetic trees where the vicariance expectation would be that the time of colonization matched with the timing of the vicariant 'event' - such as the time when an island fragmented from a mainland, or the period during which a hypothetical landbridge existed to connect islands to mainland (e.g. GAARlandia). Absent matching time, vicariance can be ruled out. The third test of vicariance would be explicit hypothesis testing. If a clade passes tests one and two, then a model can be constructed with or without a vicariance parameter and using approaches such as maximum likelihood ratio test, the fit of competing hypotheses to data can be evaluated. If all three are consistent with vicariance, ad hoc hypothesis of (long distance-, overwater-) dispersal are unnecessary.
To be continued...
References
Cowie, R.H. and Holland, B.S. 2008. Molecular biogeography
and diversification of the endemic terrestrial fauna of the Hawaiian Islands.
Philosophical Transactions of the Royal Society B-Biological Sciences, 363:
3363-3376.
Darwin, C. 1909. The voyage of the beagle. New York, NY: P.F. Collier.
Dunbar-Co, S., Wieczorek, A.M. and Morden, C.W. 2008. Molecular phylogeny and adaptive radiation of the endemic Hawaiian Plantago species (Plantaginaceae). American Journal of Botany, 95: 1177-1188.
Emerson, B.C. 2008. Speciation on islands: what are we learning? Biological Journal of the Linnean Society, 95: 47-52.
Gillespie, R.G., Claridge, E.M. and Goodacre, S.L. 2008a. Biogeography of the fauna of French Polynesia: diversification within and between a series of hot spot archipelagos. Philosophical Transactions of the Royal Society B-Biological Sciences, 363: 3335-3346.
Parent, C.E., Caccone, A. and Petren, K. 2008. Colonization and diversification of Galapagos terrestrial fauna: a phylogenetic and biogeographical synthesis. Philosophical Transactions of the Royal Society B-Biological Sciences, 363: 3347-3361.
Wallace, A.R. 1876. The Geographical Distribution of Animals: With a Study of the Relations of Living and Extinct Faunas as Elucidating the Past Changes of the Earth's Surface: Harper and brothers.
Darwin, C. 1909. The voyage of the beagle. New York, NY: P.F. Collier.
Dunbar-Co, S., Wieczorek, A.M. and Morden, C.W. 2008. Molecular phylogeny and adaptive radiation of the endemic Hawaiian Plantago species (Plantaginaceae). American Journal of Botany, 95: 1177-1188.
Emerson, B.C. 2008. Speciation on islands: what are we learning? Biological Journal of the Linnean Society, 95: 47-52.
Gillespie, R.G., Claridge, E.M. and Goodacre, S.L. 2008a. Biogeography of the fauna of French Polynesia: diversification within and between a series of hot spot archipelagos. Philosophical Transactions of the Royal Society B-Biological Sciences, 363: 3335-3346.
Parent, C.E., Caccone, A. and Petren, K. 2008. Colonization and diversification of Galapagos terrestrial fauna: a phylogenetic and biogeographical synthesis. Philosophical Transactions of the Royal Society B-Biological Sciences, 363: 3347-3361.
Wallace, A.R. 1876. The Geographical Distribution of Animals: With a Study of the Relations of Living and Extinct Faunas as Elucidating the Past Changes of the Earth's Surface: Harper and brothers.
