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Environment, Area and Diversification in the Species-Rich Flowering Plant Family Iridaceae

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Environment, Area and Diversification in the Species-Rich Flowering Plant Family Iridaceae vol. 166, no. 3 the american naturalist september 2005 ൴ Notes and Comments Environment, Area, and Diversification in the Species-Rich Flowering Plant Family Iridaceae T. Jonathan Davies,1,2,* Vincent Savolainen,2,† Mark W. Chase,2,‡ Peter Goldblatt,3,§ and Timothy G. Barraclough1,2,k 1. Division of Biology and Natural Environmental Research The distribution of species richness among branches of Council Centre for Population Biology, Imperial College London, the tree of life is highly uneven, with a small number of Silwood Park Campus, Ascot, Berkshire SL5 7PY, United clades possessing a disproportionately large number of Kingdom; 2. Molecular Systematics Section, Jodrell Laboratory, Royal Botanic species (Marzluff and Dial 1991). Similarly, species rich- Gardens, Kew TW9 3DS, United Kingdom; ness varies markedly among different geographic regions 3. Missouri Botanical Garden, St. Louis, Missouri 63166 (Gaston 2000). To date, approaches for studying these two patterns have been largely separate. The causes of taxo- Submitted August 5, 2004; Accepted April 12, 2005; nomic imbalance have been explored using phylogenetic Electronically published June 28, 2005 approaches, focusing largely on finding biological traits that explain variation in species richness. Although such Online enhancements: appendix, tables. traits have been found (Hodges and Arnold 1995; Heilbuth 2000; Sargent 2003; Gianoli 2004; Ree 2005), the propor- tion of variation in species richness they explain tends to be low (Harvey and Purvis 2003; Ricklefs 2003). In con- abstract: Phylogenetic analyses provide a means to explore evo- trast, most work on geographic variation in species rich- lutionary explanations for regional variation in species richness. The ness has followed an ecological approach, for example, environment might also explain much of the previously unexplained looking at the effects of area on species richness or for imbalance of phylogenetic trees. We use data on geographic distri- bution and phylogenetic affinity to examine correlates of species regional differences in the abiotic environment that explain richness among genera of irises (family: Iridaceae). Irises display spatial variation of species richness (Willig et al. 2003; strong phylogenetic imbalance, with a few clades containing a dis- Currie et al. 2004; see also Currie and Francis 2004; Qian proportionate number of species, most notably those found in the and Ricklefs 2004). dry Mediterranean climate of the Cape of South Africa. The abiotic Combining these approaches can provide further in- environment and area are strong predictors of iris species richness, sights into both areas. Phylogenetics provides a means to but environment alone is insufficient to explain the high diversity evaluate the importance of evolutionary history in deter- of Cape clades. One possible explanation is that the interaction be- mining geographic patterns in diversity. For example, do tween biological traits and environment resulted in the unusually high diversification rates in the region. regions with more species have older clades or clades with faster net diversification rates (Cardillo 1999)? In addition, Keywords: species richness, environment, diversification rates, Iri- the environment might provide the missing explanation daceae, Cape of South Africa. for taxonomic imbalance in species richness: clades occupy regions with different areas or different abiotic environ- ments, thereby influencing net diversification rates (Rick- lefs 2003). For example, Davies et al. (2004) showed that * Present address: Department of Biology, Gilmer Hall, University of Virginia, area and measures of environmental energy, such as tem- Charlottesville, Virginia 22904; e-mail: [email protected]. perature, explained ∼40% and ∼20%, respectively, of the † E-mail: [email protected]. variation in species richness between sister families of ‡ E-mail: [email protected]. angiosperms. § E-mail: [email protected]. Here we use a generic-level phylogenetic analysis of Iri- k E-mail: [email protected]. daceae to examine environmental correlates of species Am. Nat. 2005. Vol. 166, pp. 418–425. ᭧ 2005 by The University of Chicago. richness. By comparing younger and more narrowly dis- 0003-0147/2005/16603-40565$15.00. All rights reserved. tributed taxa than Davies et al. (2004), it was hoped to Environment, Area, and Diversification 419 more precisely discriminate differences in environments Geographic Data between clades. We chose Iridaceae largely because a nearly complete genus-level phylogenetic analysis was already Generic distribution maps were assembled using a range available and also because they display important char- of revisionary and floristic accounts dealing with Iridaceae, acteristics relating to both taxonomic and geographic var- notably Mathew (1981), Goldblatt and Henrich (1987), iation in species richness. Taxonomically, Iridaceae are a and Goldblatt and Manning (2002). These were digitized highly diverse family with ∼65 genera. The family displays in ArcView (GIS 3.2, Environmental Systems Research In- a strong pattern of taxonomic imbalance: a few genera stitute). The total area of each distribution was calculated contain large numbers of species (e.g., Crocus [80 species], and log transformed. Iris [280], and Gladiolus [260]), whereas many genera con- For measures of abiotic environment, following broad tain only one or a few species (e.g., Isophysis [1], Devia ecological surveys of plant diversity (Currie 1991; [1], and Onira [1]; Goldblatt 2001). O’Brien et al. 2000; Francis and Currie 2003), we focused Geographically, Iridaceae favor dry Mediterranean-type on variables summarizing energy input, water availability, climates and are especially species rich in the Cape region and elevation in each region. We collated raster data sets of South Africa, defined here as the geographic region representing temperature (1931–1960, Global Ecosystem characterized by a Mediterranean climate and encom- database, http://www.ngdc.noaa.gov/seg/cdroms/ged_iia/ passing the Cape Folded Mountain Belt (Goldblatt and datasets/a03/lc.htm), ultraviolet (UV) radiation (1978– Manning 2002). The Cape is renowned for its high levels 1993, NASA/GSFC TOMS Team, http://jwocky.gsfc of plant species richness and endemism. As a small and .nasa.gov), actual evapotranspiration (AET; 1920–1980, GRID, UNEP, http://www.grid.unep.ch/data/data.php essentially temperate climate region, the Cape has been p highlighted as an unexplained outlier from global trends ?category atmosphere), elevation (GTOPO30, U.S. Geo- between the abiotic environment and species richness logical Survey’s EROS Data Center, http://edcdaac.usgs (Cowling et al. 1992; Simmons and Cowling 1996; Rich- .gov/gtopo30/gtopo30.html), and mean degrees latitude ardson et al. 2001; Goldblatt and Manning 2002; Linder from the equator. We calculated the mean value of each 2003). The two broad explanations for high species rich- variable within each generic distribution. To compare sister ness in the Cape are readily amenable to phylogenetic clades deeper in the phylogenetic tree, generic range dis- analyses: either the Cape represents an old, relatively un- tributions within each clade were combined to form a disturbed area able to accumulate species richness or the single polygon theme, and mean environmental values recent onset of its Mediterranean-type climate triggered were calculated as described above. The environmental data are resolved to between 0.25Њ and 0.5Њ, equating to rapid diversification. Here we ask two questions. First, are 2 2 measures of the abiotic environment sufficient to explain cell sizes of approximately 750 km and 3,025 km ,re- spectively, at the equator. The smallest geographic range the diversity of irises in the Cape and elsewhere? Although 2 the Cape departs from general trends between the envi- was that for Devia at around 12,000 km . ronment and flowering-plant species richness, it remains possible that those lineages that have radiated extensively Evolutionary Rates in the Cape fall within clades that follow a different func- tional response to the abiotic environment that can still Following Davies et al. (2004), we included a measure of explain the clades’ geographic variation in species richness. molecular evolution rates to attempt to distinguish Second, is high diversity of Iridaceae in the Cape due to whether any observed correlation between species richness rapid diversification or to the presence of old clades? and energy might be explained by the intermediate effect of environment on evolutionary rates (Rohde 1992). Max- imum likelihood branch lengths were estimated using the Material and Methods HKY85 model of DNA evolution (Hasegawa et al. 1985) Phylogenetic Data for synonymous and nonsynonymous changes. Further partitioning of the data was not supported by nested log- We use one of the two most parsimonious phylogenetic likelihood ratio tests (results not shown). A comparison trees from a recent molecular study by Goldblatt et al. with branch lengths estimated using a more complex (2005), sampling 58 of the 65 currently recognized genera model of DNA evolution (general time reversal using within Iridaceae. Species numbers were taken from Gold- a gamma distribution with an a shape parameter and a blatt (2001). Significant shifts in rates of diversification proportion of invariant sites) found strong correspon- were identified by contrasting species richness between dence between the two estimates (r 2 p 0.99 for the re- sister clades
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