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Cyperaceae) and the Area-Richness Correlation in Plants Daniel Spalink1*, Bryan T

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Cyperaceae) and the Area-Richness Correlation in Plants Daniel Spalink1*, Bryan T Journal of Biogeography (J. Biogeogr.) (2016) SPECIAL Biogeography of the cosmopolitan PAPER sedges (Cyperaceae) and the area-richness correlation in plants Daniel Spalink1*, Bryan T. Drew2, Matthew C. Pace2,3, John G. Zaborsky1, Julian R. Starr4, Kenneth M. Cameron1, Thomas J. Givnish1 and Kenneth J. Sytsma1 1Department of Botany, University of ABSTRACT Wisconsin-Madison, Madison, WI 53706, Aim Across angiosperm families, the area occupied by a family is strongly cor- USA, 2Department of Biology, University of related with its richness. We explore the causes of this area-richness correlation Nebraska at Kearny, Kearny, NE 68849, USA, 3The New York Botanical Garden, using the cosmopolitan family, Cyperaceae Juss., as a model. We test the Bronx, NY 10458, USA, 4Department of hypothesis that, despite a proposed tropical origin, temperate lineages in the Biology, University of Ottawa, ON family diversified at elevated rates. We test the hypothesis that the area-richness K1N 6N5, Canada correlation is maintained within intrafamilial clades, and that this relationship could be described as a function of niche space. We also test the hypothesis that the partitioning of geographical and ecological space, not the extent of this space, is the factor most closely associated with clade richness. Location Cosmopolitan. Methods We use molecular data from four genes sequenced in 384 taxa to develop a chronogram of Cyperaceae. We then develop a model of ancestral ranges and measure rates of diversification throughout the history of the fam- ily. Integrating data from over 4,800,000 digitized herbarium records, we char- acterize the range and niche of more than 4500 species and test for correlations of the species richness maintained within clades with range size, range partitioning, range overlap, niche, clade age and rate of diversification. Results Cyperaceae originated in South America in the late Cretaceous and subsequently dispersed throughout the globe. Of three increases in diversifica- tion rate, two occurred in the temperate Northern Hemisphere. The variable most closely associated with clade richness is the partitioning of geographical space by species within each clade. Main conclusions We show that species-rich clades in Cyperaceae are not only more widespread, occupy more niche space, and diversify more quickly, but also exhibit patterns that are consistent with the partitioning of geographi- cal and ecological space as a major correlate to diversification. *Correspondence: Daniel Spalink, Department Keywords of Botany, University of Wisconsin-Madison, area-richness correlation, BAMM, beast, BioGeoBEARS, Cyperaceae, WI 53706, USA. E-mail: [email protected] herbarium specimens, historical biogeography, Poales of net diversification rate and clade age. In integrating INTRODUCTION geography and ecology, however, both the physical location Explaining why some clades are species rich and others are and extent of clade ranges are also related to species richness. species poor, and how these patterns of diversity are dis- For example, the tropics are the location of origination tributed throughout the globe, remain central tasks in biol- (i.e. ‘museum’) and subsequent diversification (i.e. ‘cradle’) ogy and require the multiple perspectives afforded by in many clades owing to the climatic stability, high evolution, geography, and ecology. From an evolutionary productivity and large geographical extent of the tropics over perspective, in its simplest form species richness is a function geological time-scales (Pianka, 1966; Chown & Gaston, 2000; ª 2016 John Wiley & Sons Ltd http://wileyonlinelibrary.com/journal/jbi 1 doi:10.1111/jbi.12802 D. Spalink et al. Jablonski et al., 2006; Mittelbach et al., 2007). Some lineages the tropics and significant increases in diversification rate are actually more diverse in temperate than tropical regions occurring in temperate regions. (Kindlmann et al., 2007; Sanchez-Ramırez et al., 2015), Sedge genera vary considerably in richness and geographi- however, despite the propensity of these temperate lineages cal extent, ranging from monotypic to containing over 2000 to be nested within tropical clades (i.e. tropical museum and species, and from narrowly restricted to essentially cos- temperate cradle of diversification; Mittelbach et al., 2007). mopolitan. Some genera (e.g. Eriophorum L.) are adapted to Furthermore, clades that occupy both tropical and extratrop- long-distance wind dispersal, but the majority lack obvious ical regions are more than five times more species rich than dispersal adaptations and are carried short distances by grav- strictly tropical clades (Ricklefs & Renner, 1994), and across ity, wind, water or animals (Kern, 1974). As might be angiosperm families, the total area occupied by a family is expected in a lineage with poor dispersibility, diversification strongly correlated with its richness (Vamosi & Vamosi, rates are tightly correlated with rates of range and niche evo- 2011). lution among the North American sedges (Spalink et al., Although widespread families are generally species rich, 2016). Given this pattern, the lack of dispersal mechanisms the causes of this area-richness correlation remain untested. in most clades, and the disparity in clade range and species Speciation resulting from geographical barriers to gene flow richness within the family, we expect that geographical diver- should be dominant in families lacking obvious mechanisms gence and physiological adaptation at relatively small spatial for long-distance dispersal (Chown & Gaston, 2000; Givn- scales are key processes in the diversification within Cyper- ish, 2010), which we argue should lead to a positive rela- aceae on a global scale. If this is the case, diverse clades tionship between clade range and species richness and should be more widespread and occupy a broader niche would be manifest in the partitioning of total clade range space than species-poor clades, geographical and ecological by relatively narrowly distributed and largely allopatric spe- space should be more finely partitioned by species within cies. The diversification of widespread lineages could also diverse clades, and net diversification rates should be greater be ecologically driven, however, as differences in distribu- in clades where this partitioning occurs. tions among species within a clade might represent a form In this article, we explore the evolutionary, geographical of resource partitioning at regional scales, with greater and ecological patterns that are manifest in the distribution diversity expected the greater the overall range of geograph- of sedge richness throughout the globe. We construct a fos- ically structured conditions being partitioned by a clade. sil-calibrated chronogram of Poales, estimate the historical Given that environmental differences tend to increase with biogeographical divergence of Cyperaceae, and measure net geographical distance (e.g. Lichstein et al., 2002), and that rates of diversification to test the tropical museum-temperate the rate of niche evolution is positively correlated with the cradle hypothesis for the family. We then integrate this rate of diversification and overall richness (Kozak & Wiens, framework with millions of georeferenced herbarium records 2010; Gomez-Rodr ıguez et al., 2015; Spalink et al., 2016), to test the hypothesis that clades occurring over large geo- the area-richness correlation might just as rightly be called graphical and ecological extents are more diverse than spa- the niche space-richness correlation. Were this moniker jus- tially and ecologically restricted clades; that clade richness tified, we would expect to see that species-rich clades and diversification rate increase with the ratio of the average occupy a broader niche space, and that this niche space species range within a clade to the clade’s overall range; that was more finely partitioned by the species it contains, than clade richness and diversification rate similarly increase with species-poor clades. the ratio of the average species niche space within a clade to The sedge family (Cyperaceae Juss.) presents an ideal the clade’s overall niche space; and that clade richness is opportunity to explore the processes contributing to the more tightly correlated with these ratios than to clade age or diversification and maintenance of biodiversity in relation to speciation rate. clade age, diversification rate, area and niche space. Cyper- aceae is cosmopolitan in distribution, composed of roughly MATERIALS AND METHODS 5500 species in c. 98 genera and 15 tribes, and the 10th most species-rich family among the angiosperms (Govaerts et al., Molecular dating analysis 2015). The family is hyperdiverse in temperate regions despite a proposed tropical origin for the clade (Givnish The fossil record is poor within Cyperaceae (Smith et al., et al., 1999; Bremer, 2002). Although the subsequent geo- 2010), so we designed our sampling to accommodate as graphical diversification of Cyperaceae on a family-wide, glo- many fossils as possible from Poales rather than relying bal scale remains unexplored, this suggests that the species entirely on a secondary Cyperaceae crown prior and the few rich, temperate clades are derived from a tropical origin. sedge fossils. Through de novo sequencing of the chloroplast Thus, in a departure from the pattern observed among many DNA genes matK, ndhF, rbcL and trnL-F, and downloading angiosperm lineages, the tropics may be the museum of supplemental data from GenBank, we included a total of 384 Cyperaceae
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