The Impact of Ecology and Biogeography on Legume Diversity, Endemism, and Phylogeny in the Caribbean Region: A New Direction in Historical Biogeography
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- Lavin, M. & Matos, A.B. Bot. Rev (2008) 74: 178. doi:10.1007/s12229-008-9006-8
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The legume family is so well represented in the Caribbean that if a preserve was needed somewhere on earth to harbor all of the primary lineages in this family, the flora of just Cuba would suffice. Molecular phylogenetic, biogeographic, and evolutionary rates analysis all suggest that legume diversity and endemism in the Caribbean are mostly of recent origin and are likely a function of the abundance of seasonally dry tropical forests (SDTFs) throughout the neotropics. Legumes have a strong ecological affinity for SDTFs, and the Caribbean basin is well covered by this forest type. Rate-variable molecular clock analysis suggests that the majority of worldwide island lineages of legumes have ages of much less than 30 Ma. Singular historical events invoking land bridges or mobile continental plates are thus not needed to explain Caribbean legume diversity and endemism. The Greater Antilles are large islands located close to the American continent. They are therefore expected to fairly represent the diverse continental lineages of legumes. Yet, they are distant enough to be dispersal limited. As such, island lineages can speciate and diversify over evolutionary time unimpeded by high rates of immigration from the mainland. Vicariance and other standard phylogenetic methods of historical biogeography are likely to be replaced by those of ecological and island biogeography. This is because model selection approaches derived from the neutral concept of isolation by distance will be able to quantify patterns of alpha and beta diversity and detect niche assembly and phylogenetic niche conservatism within and among metacommunities that are hypothesized to constrain phylogeny.
La familia leguminosa está tan bien representada en el Caribe, que si fuera necesario preservar algún sitio sobre la tierra, que albergue todos los linajes principales de esta familia, la isla de Cuba, con su flora endémica, podría ser seleccionada entre las áreas que cumplen esta condición. Todos los análisis moleculares, filogeneticos, biogeográficos y de tasas de evolución sugieren que la diversidad y endemismo de las leguminosas en la región del Caribe, es en la mayoría de los casos, de origen reciente y es probablemente una función de la abundancia de los bosques tropicales estacionalmente secos (SDTFs) a lo largo del neotrópico. Las leguminosas tienen una preferencia ecológica fuerte por los bosques tropicales estacionalmente secos (SDTFs), y la cuenca del Caribe está bien cubierta por este tipo de bosque. El análisis molecular de tasa variable sugiere que la mayoría de los linajes de leguminosas de las islas tienen edades mucho menores que 30 millones de años. De este modo, los eventos históricos singulares que invocan puentes terrestres o placas continentales móviles, no necesariamente explican la diversidad y endemismo de Leguminosas del Caribe. Las Antillas Mayores son islas grandes localizadas relativamente cerca del continente americano. Por consiguiente, se espera que en estas islas, estén bien representados los diversos linajes continentales de leguminosas. A pesar de todo, estas islas están bastante distantes de las lagunas oceánicas, lo cual rinde en las islas grandes una dispersión algo limitada. De esta manera, los linajes de estas islas pueden especiar y diversificarse a escala de tiempo evolutivo, sin impedimento por altas tasas de inmigración desde el continente. Así, los métodos de biogeografía de la vicarianza y otros métodos filogenéticos estándar de Biogeografía Histórica tienen la probabilidad de ser sustituidos por los métodos ecológicos y de Biogeografía de las islas. Esto se debe a que los métodos de selección del modelo derivado del concepto neutral de aislamiento por distancia permitirá cuantificar los patrones de alfa y beta diversidad y detectar desviaciones de la relación positiva fuerte entre las distancias geográficas y genéticas (niche assembly) y la conservación de las preferencias ecológicas ancestrales que tienden a heredar las especies (phylogenetic niche conservatism) dentro y entre comunidades que son ensayadas para formular hipótesis sobre el papel de la Biogeografía y la Ecología en la determinación de la filogenia.
Molecular phylogenetic analysis has been revealing of many unsuspected findings, and this has been particularly true of studies in the legume family. For example, phylogenies that exhaustively sample at the species level and below have shown that geography and ecology are often as good or better predictors of relatedness than is morphology. In addition, the estimated age of the divergences of legume clades separated from each other either by an ocean gap or on different continents typically postdates the estimated ages of the putative tectonic explanations for continental vicariance biogeography (e.g., Lavin et al., 2004), which is a general finding (e.g., Queiroz, 2005). If such ecological and geographic structure is commonly found among legume phylogenies, and tectonic history is not responsible for such structure, then ecological processes including island biogeographical ones must explain the phylogenetic structure that has so profoundly influenced recent legume taxonomies (summarized in Lewis et al., 2005).
The genus Strophostyles exemplifies the influence of ecology and biogeography on phylogeny (Riley-Hulting et al., 2004). With three species confined to open woodland sites in southeastern United States, Strophostyles is not related to an Asian lineage, as might be expected (e.g., Tiffney, 1985), but rather is sister to Dolichopsis, which comprises two endemic species to the Chaco region in South America. The chaco is forest vegetation distinguished in part from other adjacent tropical dry forests or tropical woody savannas by having a frost period (Pennington et al., 2000). No morphology predicts the sister relationship of Strophostyles and Dolichopsis, but geography and ecology does. This sister group relationship is confined to New World temperate savanna-type vegetation. Because ecology and geography are often excellent predictors of phylogenetic relatedness, they should get as much attention from a methodological perspective as does morphology.
The important ecological focus in terms of Caribbean legumes is on the seasonally dry tropical forests (SDTFs sensu Prado & Gibbs, 1993; Pennington et al., 2000, 2004). SDTFs are rich in cacti, euphorbs, and other succulent taxa, in addition to families like legumes. SDTFs are poor in grasses and other taxa adapted to regular burning. These two facets of SDTFs strongly suggest that this vegetation type is persistent, or that residents do not suffer routine wholesale death and replacement especially from immigrants. This vegetation occurs as fragments scattered throughout the neotropics including the Caribbean Islands and adjacent North and South American mainland, as well as the African Horn region (Somalia-Masai) and southwestern Africa (the Karoo-Namib; Schrire et al., 2005).
Legume clades are very often confined to this vegetation, which suggests that a species tends to inherit its ancestral ecological predilection (i.e., phylogenetic niche conservatism; Harvey & Pagel, 1991). Legume clades also are very often confined to one patch of STDF (e.g., Zygocarpum and Wajira in the Somalia-Masai; Thulin & Lavin, 2001; Thulin et al., 2004), which suggests that SDTF species tend to inherit their approximate ancestral geographic position (i.e., dispersal limitation; Hubbell, 2001). The genus Chapmannia, for example, is endemic to SDTF-type vegetation and comprises a Somalia–Masai clade sister to a Florida–Mesoamerican clade (Thulin, 2000; Lavin et al., 2001). The estimated age of the trans-Atlantic Chapmannia crown is 14.2 ± 1.7 Ma (Lavin et al., 2004). Stochastic dispersal is therefore the only explanation for this ecologically confined and highly geographically structured Chapmannia phylogeny.
The general points to be drawn from the above discussion and that pertain to island biogeography are first, dispersal is not an ad hoc explanation or an “anything goes” concept, as suggested by Nelson and Platnick (1981). It is a stochastic process operating within potentially definable ecological confines and under specific island biogeographic rules. Quantifying these confines and rules should be part of dispersal biogeography. Second, oceanic and continental islands are no different from the ecological or geographical (e.g., topographical) islands located within continents, from an island biogeographic perspective. Islands surrounded by water may be discrete to the human eye. Openness to visual inspection, however, is not a prerequisite to the study of the processes causing niche conservation and dispersal limitation on ecologically and geographically determined islands lying within continents.
The Recency of Legumes in the Antilles
Islands of the Antilles for which Data on Total Number of Legume Species and Infraspecific Taxa (N) and the Number of Endemic Legume Species and Infraspecific Taxa (Nend) Could be Estimated Using Floristic Accounts, which were Updated with More Recent Monographic Treatments of Particular Legume Genera (Lavin et al., 2001)
Howard et al. (1988)
Gooding et al. (1965)
Correll and Correll (1982)
Sauget and Liogier (1951); A. Barreto Valdés and A. Beyra Matos (unpublished data)
Howard et al. (1988)
Howard et al. (1988)
Howard et al. (1988)
Howard et al. (1988)
Britton and Wilson (1924)
Howard et al. (1988)
Howard et al. (1988)
Howard et al. (1988)
An Ecological and Island Biogeographic Alternative for Historical Biogeography
Cladistic vicariance and related approaches to the study of historical biogeography have been preoccupied with detecting the influence of historical events on phylogenetic patterns. An influence is explained by the fit of a taxon-area cladogram to competing continental tectonic hypotheses. In the Caribbean basin, such competing tectonic hypotheses have involved the eastward movement and reconfiguration of the Greater Antillean islands (Rosen, 1978) or the presence of a once-emergent but now submerged Aves Ridge (Iturralde-Vinent & MacPhee, 1999). The fit of the taxon-area cladogram via component, three-area statements, or Brooks Parsimony Analysis has always been a nebulous affair and without definitive results. In part this is because these different approaches each involve multiple or different assumptions, none of which can be objectively evaluated one against the other (e.g., Lavin et al., 2001). Also, choosing among taxon-area cladograms with the same histories (a requirement for vicariance analysis) is difficult given that absolute ages cannot be estimated from a cladogram and relative ages are at best weakly implicit. Finally, clade support is generally weak for area cladograms. For example, a minor change in the area coding for a single wide spread species (e.g., adding an additional area of endemism to its distribution) can result in an entirely different area cladogram (e.g., Pennington et al., 2004).
In contrast, ecological and island biogeographic approaches to the study of biogeography are concerned with detecting enduring processes that influence phylogenetic patterns. Such approaches integrate plant phylogeny with information on plant community composition to ask questions such as: How does island size affect endemic speciation (cf. Losos & Schluter, 2000)? Does the patchy distribution of SDTFs on the Caribbean Islands influence ecological (e.g., beta diversity) and phylogenetic patterns (e.g., geographic structure) in the same manner as the patchy distribution of SDTFs on the mainland? To what degree are Caribbean clades ecologically structured? For example, how common is the phylogenetic niche conservatism exemplified by Poitea, a clade confined to Antillean SDTFs excepting the subclade comprising P. florida, P. sabinea, and P. carinalis that occupies wet forest? Do particular vegetation types impose different phylogenetic histories on constituent clades? That is, do wet forest clades have greater success at over-water dispersal because of the intrinsic attributes of this vegetation (e.g., successful immigration facilitated by high rates of resident death due to drought)? After all, Poitea carinalis from the wet forests of Dominica is the only species of the genus to occur outside the Greater Antilles (Lavin, 1993), whereas SDTF-confined Pictetia has no occurrence outside the Greater Antilles (Beyra-Matos & Lavin, 1999). Do the SDTFs (sensu Prado & Gibbs, 1993; Pennington et al., 2000) in the Caribbean and elsewhere impose a different history on phylogenies compared to other dry tropical vegetation types? Savannas could be much like wet forest in experiencing higher rates of resident mortality because of drought, for example, which facilitates high rates immigration. In contrast, drought-resistant SDTFs show little evidence of fire-resistance, indicating little if any historical disturbance via fire. Thus, SDTFs could be much more dispersal limited than other tropical forest types because of their persistent nature (e.g., Lavin, 2006) and because of the fragmented distribution of this vegetation. If dispersal limited as such, then constituent clades of SDTFs will show phylogenies with a higher degree of geographical structure and constituent SDTF communities will show lower degrees of alpha and higher degrees of beta diversity compared to constituent clades or communities from other types of tropical vegetation types, including wet forests and savannas.
An ecological and island biogeographic approach to ecology that involves phylogeny has been suggested by Hubbell (2001), where speciation rates and the degree of dispersal limitation shape the phylogeny of constituent lineages within a metacommunity. The abundant recent literature on neutral ecological theory is not explicit about how ecology impacts phylogeny, however (e.g., Holyoak & Loreau, 2006; Hu et al., 2007; Munoz et al., 2007; Volkov et al., 2007). An explicit approach to investigating the role of biogeography and ecology in shaping phylogeny can be derived from the population genetics concept of isolation by distance (e.g., Grefen et al., 2004; Jensen et al., 2005). A strong positive relationship between genetic and geographic distance is essentially a neutral assumption. Such a relationship could illuminate relevant community level properties such as dispersal limitation (dispersal assembly) caused by, for example, the patchy but persistent distribution of a metacommunity. Species may not occupy their total potential range because of inherent properties of the metacommunity that render geographically close local communities similar in species or sister species composition. This is akin to the population genetic findings for North American wolves, where geographically close populations are on average genetically similar (Grefen et al., 2004). Deviations from a strong positive relationship between geographical and genetic distances imply a deterministic cause or niche assembly. Wolves from cold temperate habitats were genetically dissimilar from those of warmer southern latitudes regardless of the distance separating populations (Grefen et al., 2004). This implicates an interaction of climate (niche assembly) and geographic distance (dispersal assembly) in structuring wolf populations.
Species abundance data and phylogeny. Tuomisto et al. (2003), Vormisto et al. (2004), Hardy and Sonke (2004), and particularly Hardy and Senterre (2007) show how biodiversity can be modeled using community composition distances or community phylogenetic distances as response variables. Hardy and co-workers show that the best form of plant community data is relative species abundances because such data can be modeled using derivations of Simpson’s diversity index. Hardy and Senterre (2007) derive community composition distances and community phylogenetic distances from the Fst statistic. In this manner, the response variables (community composition and community phylogenetic distances) are very explicit measures of alfa and beta diversity. The community phylogeny from which community phylogenetic distances are derived, however, must be ultrametric (e.g., chronograms or rate smoothed phylograms) in order to achieve unbiased estimates of community differentiation along a spatial, temporal, or environmental gradient. Chronograms with branch lengths measured in ages (Ma) can be produced from Phylomatic (http://www.phylodiversity.net/phylomatic/) or a community phylogeny can be generated from molecular data and then rate smoothed (e.g., via penalized likelihood rate smoothing; Sanderson, 2002) calibrated using absolute or relative time.
Species incidence data and phylogeny. Ultrametric community phylogenies may not be readily available for plant communities or confidence in the branch lengths of such phylogenies could be low. Also, relative species abundances may not be easily obtained because, for example, herbs, shrubs, and trees are being censused, or the plots or sampling sites may be highly altered by human activity. In this case, response variables such as the net relatedness index (Webb et al., 2002), a phylogenetic distance generated from Webb’s Phylocom (http://www.phylodiversity.net/phylocom/) using node numbers or branch lengths from non-ultrametric trees, could be utilized as the response variable. Similarly, Jaccard’s distances, or any community composition distance derived from species incidence rather than abundance data, could be modeled as the response variable.
Model selection approaches. Either using abundance or incidence data, hypothesis testing can involve whether a particular set of a priori targeted vegetation types, biomes, or habitats are differentially constraining the phylogeny of a taxonomic group or community from an ecological and geographical perspective (i.e., different metacommunities are potentially being identified). The general model includes geographic distance (e.g., Euclidean distances derived from geographical coordinates; Legendre, 1990) and at least a categorical variable indicating in which targeted vegetation type, biome, or habitat (i.e., hypothesized metacommunity) the particular sample sites are located. In this manner, an interaction between ecological setting and geographic distance can be evaluated. Using mantel correlations and model selection approaches (e.g., Burnham and Anderson, 2002; Johnson and Omland, 2004), within versus among metacommunity comparisons can be used to determine the significance of the interaction.
In either of the above examples, geographic distance no longer has to be considered a proxy for deterministic environmental variables. Specific quantitative environmental variables can be introduced into a model (cf. Vormisto et al., 2004; Hardy & Senterre, 2007) with or without geographic distance, and selection among competing models (cf. Burnham & Anderson, 2002) can settle the issue.
We have not yet undertaken an integrated study of tropical legume communities and phylogenies for the Caribbean, but are beginning to form collaborations among legume systematists and ecologists to conduct such studies on the American mainland (e.g., Oliveira-Filho et al., 2006, 2007) with the intention of expanding into the Caribbean region. The imaginary data set analyses (Figs. 8 and 9) are derived from current studies (e.g., Oliveira-Filho et al., 2007; Synder et al., 2007) and are intended only to illustrate the approach that should replace traditional phylogenetic methods of biogeography. Our ultimate intent will be to use this new approach to test the prediction that the SDTFs form a distinct metacommunity from other tropical vegetation, including seemingly similar savannas that are rich in grass species and prone to regular intervals of fire disturbance, in contrast to SDTFs. We also want to test the hypothesis that the SDTFs from the Caribbean Islands differ from American mainland SDTFs only as a function of dispersal limitation (e.g., Fig. 9). That is, they are neither ecologically distinct nor taxonomically depauperate, and harbor the same phylogenetic lines at similar levels of diversity as do the rest of the scattered patches of neotropical SDTFs. This would counter a traditional view generally applied to the Caribbean Island biota, as summarized in Hedges (2000), which is that it is depauperate at higher taxonomic levels; i.e., “the central problem” identified by Williams (1989).
We wish to thank Alfonso Delgado Salinas, R. Toby Pennington, Martin F. Wojciechowski and for constructive comments and other assistance, which greatly improved the manuscript.