The University of Chicago

Testing for Ecological Limitation of Diversification: A Case Study Using Parasitic . Author(s): Nate B. Hardy and Lyn G. Cook Source: The American Naturalist, Vol. 180, No. 4 (October 2012), pp. 438-449 Published by: The University of Chicago Press for The American Society of Naturalists Stable URL: http://www.jstor.org/stable/10.1086/667588 . Accessed: 06/10/2015 22:57

Your use of the JSTOR archive indicates your acceptance of the Terms & Conditions of Use, available at . http://www.jstor.org/page/info/about/policies/terms.jsp

. JSTOR is a not-for-profit service that helps scholars, researchers, and students discover, use, and build upon a wide range of content in a trusted digital archive. We use information technology and tools to increase productivity and facilitate new forms of scholarship. For more information about JSTOR, please contact [email protected].

.

The University of Chicago Press, The American Society of Naturalists, The University of Chicago are collaborating with JSTOR to digitize, preserve and extend access to The American Naturalist.

http://www.jstor.org

This content downloaded from 23.235.32.0 on Tue, 6 Oct 2015 22:57:07 PM All use subject to JSTOR Terms and Conditions vol. 180, no. 4 the american naturalist october 2012

Testing for Ecological Limitation of Diversification: A Case Study Using Parasitic Plants

Nate B. Hardy1,* and Lyn G. Cook2

1. Department of Invertebrate Zoology, Cleveland Museum of Natural History, Cleveland, Ohio 44108; 2. University of Queensland, School of Biological Sciences, Brisbane, Queensland 4072, Australia Submitted February 14, 2012; Accepted June 12, 2012; Electronically published August 20, 2012 Online enhancement: appendix. Dryad data: http://dx.doi.org/10.5061/dryad.g6r70.

if there are extrinsic, ecological limits on the absolute di- abstract: Imbalances in phylogenetic diversity could be the result versity of clades, those limits might be more important of variable diversification rates, differing limits on diversity, or a combination of the two. We propose an approach to distinguish than differences in diversification rate in determining ex- between rates and limits as the primary cause of phylogenetic im- tant diversities (Raup 1972; Sepkoski 1978; Rabosky balance, using parasitic plants as a model. With sister-taxon com- 2009a). parisons, we show that parasitic lineages are typically much Several studies have detected a temporal decline in di- less diverse than their autotrophic sisters. We then use age estimates versification rates within clades (e.g., Harmon et al. 2003; for taxa used in the sister-taxon comparisons to test for correlations between clade age and clade diversity. We find that parasitic plant Weir 2006; Rabosky and Lovette 2008), and for many diversity is not significantly correlated with the age of the lineage, groups, diversity appears to be unrelated to clade age (e.g., whereas there is a strong positive correlation between the age and Magallo´n and Sanderson 2001; Ricklefs 2006; Ricklefs et diversity of nonparasitic sister lineages. The sister pair al. 2007; McPeek 2008). Rabosky (2009b) used a simu- Monotropoideae (parasitic) and Arbutoideae (autotrophic) is suffi- lation approach to test three possible explanations for why ciently well sampled at the level to allow more parametric a positive clade age–to–clade diversity relationship might comparisons of diversification patterns. Model fitting for this group supports ecological limitation in Monotropoideae and unconstrained break down: (1) extreme variation in diversification rate diversification in Arbutoideae. Thus, differences in diversity between among lineages; (2) clade volatility (Gilinsky 1994), in parasitic plants and their autotrophic sisters might be caused by a which extinction rate covaries with speciation rate; and combination of ecological limitation and exponential diversification. (3) density-dependent diversification (Sepkoski 1978; Nee A combination of sister-taxon comparisons of diversity and age, et al. 1992), in which diversification rates decrease as a coupled with model fitting of well-sampled phylogenies of focal taxa, function of the number of species within a clade. In Ra- provides a powerful test of likely causes of asymmetry in the diversity of lineages. bosky’s simulations, a positive clade age–to–clade diversity relationship broke down only under density-dependent Keywords: diversification rates, sister-taxon comparisons, dated phy- simulations. One potential biological mechanism that logenies, parasitic plants, ecological limitation. could result in density-dependent diversification (and the only mechanism that has been proposed in the literature) Introduction is ecological limitation of diversity. Under this scenario, speciation is more likely when resources are abundant and Some evolutionary lineages are exceptionally species rich, unexploited, and diversification slows when intra- and in- whereas others are species poor. Stochastic models of phy- terspecies competition increases (Walker and Valentine logenetic diversification fail to account for much of the 1984; Schluter 2000). observed unevenness of diversity across lineages (Guyer Processes other than those tested by Rabosky (2009b) and Slowinski 1993). Deterministic explanations have fo- could also result in diversities being unrelated to lineage cused almost exclusively on among-clade differences in age. In the continuous-decline model of Rabosky and diversification rates (Eriksson and Bremer 1992; Sanderson Lovette (2008), interactions among species within a clade and Donoghue 1994, 1996; Jones et al. 2005). However, do not limit diversity. Diversification decreases continu-

* Corresponding author; e-mail: [email protected]. ously through time but not directly as a function of the number of species in the lineage. Rabosky and Lovette Am. Nat. 2012. Vol. 180, pp. 438–449. ᭧ 2012 by The University of Chicago. 0003-0147/2012/18004-53658$15.00. All rights reserved. (2008) proposed the continuous-decline model as a null DOI: 10.1086/667588 hypothesis, to be rejected before a density-dependent

This content downloaded from 23.235.32.0 on Tue, 6 Oct 2015 22:57:07 PM All use subject to JSTOR Terms and Conditions Ecological Limitation of Diversification 439 model is assumed for cases in which diversification rates In this study, we aim to develop an approach that can decrease over time. However, even when the continuous- tease apart the likely causes of trait-associated differences decline model fits the pattern of diversification better than in diversity. First, we test whether a binary trait affects density-dependent models, ecological regulation remains diversity, using sister-taxon comparisons (Vamosi and Va- a plausible explanation. The diversification process could mosi 2005). Then, we attempt to distinguish between two be a function of the number of contemporaneous co- likely causes for trait-associated diversity differences: dif- occurring species from multiple clades, or diversification ferences in diversification rates and differences in ecolog- rates could decrease as ecosystems shrink. ical limits on diversity. Sister-taxon comparisons have been Diversification heterochrony, in which diversification used extensively to test whether specific traits (e.g., key rates within a clade fluctuate over time, could also result innovations) are associated with changes in diversification in lineage diversities being independent from lineage age. across clades (e.g., Mitter et al. 1988; Wiegmann et al. Methods designed to detect changes in intraclade diver- 1993; Lengyel et al. 2009; Hardy and Cook 2010). Intra- sification through DNA sequence–based phylogenies of ex- clade tests of temporal diversification rate variation can tant taxa commonly assume that speciation rates are, on be confounded by interactions between speciation and ex- average, greater than extinction rates (e.g., Hey 1992). Pa- tinction rates and the inability to sample from extinct leontological data are more consistent with alternating species (Quental and Marshall 2010; Rabosky 2010; Par- phases of increasing (low extinction) and decreasing (high adis 2011a, 2011b). Sister-taxon comparisons make fewer extinction) diversity (Niklas 1997; Quental and Marshall assumptions about the diversification process and there- 2010). Mass-extinction events (e.g., those caused by biome fore do not share these problems. Sister-taxon compari- shrinking associated with climate change) could lower the sons can also be performed without detailed estimates of ecological lineage-carrying capacity of a particular envi- phylogenetic relationships within focal clades and are thus ronment to a level that erases previous differences in di- able to incorporate elements of extant biodiversity that versity among lineages. More pervasively, any clade of ex- could not be the subject of intraclade approaches. tant species purported to have undergone a temporal In this study, we expand on ideas proposed by Rabosky decrease in diversification rate and assumed to have ap- (2009a) and extend the sister-taxon comparison approach proached an equilibrium level of diversity might instead in what we call the “sister-taxon-age” approach. We use be in a period of declining diversity (Quental and Marshall the timing of sister-taxon divergences to help distinguish 2010). between diversification rate differences and bounds on di- Hardy and Cook (2010) classified factors that could versity as the cause of phylogenetic diversity imbalance. modulate species diversity as attributes of individuals, spe- We use parasitic plants as the model system because they cies, ecosystems, and environments, but attributes across are well suited for this application. A parasitic trophic classes are interconnected. Species-level traits such as pop- mode has evolved repeatedly among seed plants (Nickrent ulation size are produced by interactions between indi- et al. 2005; Merckx and Freudenstein 2010; Westwood et vidual phenotypes (e.g., trophic mode, reproductive rate), al. 2010), and phylogenetic relationships and divergence environmental parameters (e.g., primary productivity, ge- times between parasitic plant lineages and their auto- ology), and ecosystem parameters (e.g., niche space). Like- trophic sister taxa are reasonably well known (table 1). We wise, ecosystem traits result from integration of the phe- expect that host association in parasitic species will impose notypic variation present in a community of species and niche constraints that limit diversity of parasitic clades. environmental features. For diversification studies it is use- Rabosky (2009a) first suggested that diversification rate ful to combine species-level and ecosystem attributes into variation could be differentiated from ecological limitation a single ecological class so that a distinction can be drawn in the context of sister-taxon analyses if the timing of between the direct impacts of ecological parameters on sister-taxon divergence were considered. A positive cor- diversification rates and the indirect effects of individual- relation between the difference in diversity of sister lin- and environmental-level traits. As an example, an indi- eages and the age of their most recent common ancestor vidual-level attribute such as trophic mode affects diver- (MRCA) is indicative of differences in diversification rate; sification rates only indirectly through its effect on a lack of correlation points to ecological limitation. Ra- ecological attributes such as population size, genetic struc- bosky’s models of the diversification of sister lineages ture, resource availability, and niche dimensions. It is also through time are symmetric, with both lineages diversi- important to note that whereas the population genetic or fying exponentially (without ecological limitation) or lo- species-level components of the ecological class might di- gistically (with ecological limitation; fig. 1A,1B). Alter- rectly contribute to differences in diversification rates, only natively, only one lineage of the sister pair might be under the ecosystem components can impose limitations on ab- ecological regulation. If sister lineages diversified expo- solute diversity. nentially until one saturated an adaptive zone, the size of

This content downloaded from 23.235.32.0 on Tue, 6 Oct 2015 22:57:07 PM All use subject to JSTOR Terms and Conditions

Table 1: Species diversities of parasitic and mycoheterotroph plant lineages with ages of most recent common ancestors No. species in No. species in autotrophic

This content downloadedfrom 23.235.32.0on Tue,6Oct2015 22:57:07PM parasitic group Sister taxon sister group Tree source MRCA Date source Parasite: Rafflesiaceae 27 Euphorbiaceae 5,735 APG 119 Davis et al. 2007 Lennooideae 7 Tiquilia 27 This study ?

All usesubject toJSTORTerms andConditions Mitrastemonaceae 2 {} \ {Balsaminaceae, Marcgravi- 10,275 This study 99 This study aceae, Tetrameristaceae, Monotropo- ideae, Arbutoideae} Cytinaceae 10 Muntigiaceae 3 APG ? Krameriaceae 18 Zygophyllaceae 285 APG 79 TimeTree Cassytha 17 Cryptocaryaceae 550 Rohwer and Rudolph 2005 ? Hydnoraceae 7 Aristolochiaceae 480 Nickrent et al. 2002 120 Davies et al. 2003 {Santalales} \ {Coulaceae, Strom- bosiaceae, Erythropalaceae} 1,935 Coulaceae 3 Nickrent et al. 2010 96 Moore et al. 2010 Cuscuta 145 {Jacquemontieae, Maripeae, Cresseae, 197 Stefanovic et al. 2003 ? Dichondreae} {} \ {Rehmannia, Trianeophora} 2,036 Lindenbergia 12 This study 48 Bremer et al. 2004 Mycoheterotroph: Burmanniaceae 95 Dioscoreaceae 870 APG 116 TimeTree Corsiaceae 30 1,417 Fay et al. 2006 117–124 TimeTree Geosiris 1 {Aristoideae, Nivenioideae, Crocoideae} 1,065 Goldblatt et al. 2008 47 TimeTree Petrosaviales 4 {Monocots} \ {Acorales, Alismatales} 55,606 APG 126 TimeTree Triuridaceae 48 Velloziaceae 240 Graham et al. 2005 102 TimeTree Parasitaxus 1{Lagarostrobus, Manoao} 2 Kelch 1998 40 This study Salomonia 2{Heterosamara, part of Polygala} 7 Forest et al. 2007 37 Forest et al. 2007 Monotropoideae 13 Arbutoideae 87 This study 70 This study Note: Complex sister groups are expressed with set notation. Sets of taxa are separated by a comma and enclosed within braces. Set differences are expressed with a backslash. For example, interpret “{Monocots} \ {Acorales, Alismatales}” as all of the monocot species that are not members of Acorales or Alismatales. APG p Angiosperm Phylogeny Group III; MRCA p most recent common ancestor (in millions of years ago [Ma]). TimeTree (http://www.timetree.org/) dates are averages of published divergence dates. MRCA ages that have not been estimated are indicated with a question mark. Ecological Limitation of Diversification 441

the difference between sister-lineage diversities should also be positively correlated with MRCA age (fig. 1C). We can distinguish among these models by comparing the relationship between MRCA age and diversity inde- A pendently across taxa having a trait of interest and sister taxa lacking that trait (fig. 2). Using parasitic plants as an example, if diversity is positively correlated to MRCA age across parasitic plant lineages and in their autotrophic sister groups, the data fit the symmetric unbounded model (fig. 2A). If diversity is unrelated to lineage age in both parasitic and autotrophic lineages, the data fit the sym-

Log-diversity metric ecological limitation model (fig. 2B); both lineages are ecologically limited. On the other hand, if diversity of parasitic plants is not related to lineage age, whereas the diversity of autotrophic sister groups is, the data fit an asymmetric ecological limitation model (fig. 2C). We complement a sister-taxon-age analysis of the effect of parasitism on plant diversity with an intraclade inves- B tigation of diversification rate evolution within a group that has been well sampled phylogenetically: parasitic Monotropoideae (Ericaceae) and its autotrophic sister group Arbutoideae. We examine lineage through time (LTT) plots and compute the gamma statistic (Pybus and Harvey 2000) to assess whether diversification has been constant through time or whether it has slowed. We then

Log-diversity compare the fit of explicit density-dependent, continuous- decline, and constant-rate birth-death models of diversification.

C Material and Methods Data and Phylogeny

We compared the diversities of 10 haustorial (parasitizing other plants) and eight mycoheterotrophic (parasitizing mycorrhizae) parasitic plant lineages (4,398 species, cov- ering about 80% of the known parasitic plant lineages) to

Log-diversity their sister groups (76,861 species; table 1). Phylogenetic relationships followed those of the Angiosperm Phylogeny Group website (http://www.mobot.org/mobot/research Time (Ma) /apweb/) and published studies (table 1), or, in two cases (Ericales and ), they were estimated here. DNA sequence data sets were downloaded as unaligned Fasta files via PhyLoTA rel 1.5 (Sanderson et al. 2008). To Figure 1: Theoretical models of diversity through time. Rabosky’s (2009a) symmetric models in which sister lineages diversify (A) ex- limit the size of the data sets, one sequence was retained ponentially, without ecological limits on diversity (symmetric un- per species. DNA sequences were aligned with MAFFT bounded model), or (B) logistically, under ecological regulation (Katoh 2008). Noncoding alignments were filtered through (symmetric ecological limitation model). Alternatively, only one in Gblocks to remove hypervariable regions (Talavera and a pair of sister lineages could be under ecological regulation. In C, Castresana 2007). For Gblocks executions the allowed gap diversification rates of each sister lineage are exponential, until one approaches ecological limits and slows (asymmetric ecological lim- positions was set to half, the minimum length of a block itation model). In each, the diversity of one sister taxon is indicated was set to 5, and the maximum number of contiguous by a dashed line and the diversity of the other sister by a solid line. nonconserved positions was set to 12. Filtered, noncoding

This content downloaded from 23.235.32.0 on Tue, 6 Oct 2015 22:57:07 PM All use subject to JSTOR Terms and Conditions 442 The American Naturalist

A MRCA age

MRCA age

Time MRCA age Log-diversity

log(diversity) 5 10152025 taxon 1 taxon 2 taxon 3 5 10 15 20 B MRCA age Time Log-diversity log(diversity)

taxon 1 taxon 2 taxon 3 0 5 10 15 20 5 10 15 20 MRCA age C Time Log-diversity

log(diversity)

taxon 1 taxon 2 taxon 3 5 10152025 5 10 15 20 MRCA age

Figure 2: Uncovering trait-associated diversity dynamics with the sister-taxon-age approach. Different relationships between diversity and most recent common ancestor (MRCA) age are expected under the (A) symmetric unbounded model, (B) symmetric ecological limitation model, and (C) asymmetric ecological limitation model. From each replicated evolution of the trait of interest, we estimate the diversity of the clade that has the trait, the diversity of its sister clade, and the age of the MRCA of those two clades (i.e., for each MRCA age we record two diversities). We then test for correlation between MRCA age and (1) diversity of clades with the trait and (2) diversity of sister clades that lack the trait. In the tree schematics, clades of species having the focal trait are shown in white, clades of species lacking that trait are shown in gray, and clade width is proportional to species diversity. For each model we show three sister relationships, but scatterplots represent data from 20 relationships. In scatterplots, diversities of clades with the trait are represented by open circles, and the best-fitting linear model for the relationship between diversity and clade age is shown with a solid line, whereas diversities of clades lacking the trait are represented by filled squares, and the linear models are shown with dashed lines. Lines with a zero slope indicate cases in which there is no correlation between clade diversity and clade age (and a linear model is a poor fit). Note that in contrast to figure 1, which shows lineage-through-time plots for diversities of a single sister pair, here scatterplots show relationship of diversity to time across clades. alignments were then combined with protein-coding align- logenies were estimated with RAxML v 7.0.4 (Stamatakis ments in Mesquite v 2.73 (Maddison and Maddison 2012). 2006). Each data set was partitioned by genome and codon The first-pass data sets we used for Ericales and Bora- position, and parameters of a general time-reversible ginaceae were large (Ericales, 2,651 species and 11,443 (GTR) nucleotide substitution model with CAT approxi- alignment positions; Boraginaceae, 555 species and 4,055 mation of among-site substitution rate variation were es- positions). A Python script was used to subsample the one timated independently for each partition for 100 non- (Boraginaceae) or two (Ericales) exemplars per genus with parametric bootstrap (BS) pseudoreplicates. Every fifth BS the most sequence data. Maximum likelihood (ML) phy- tree was then used as the starting tree for a more thorough

This content downloaded from 23.235.32.0 on Tue, 6 Oct 2015 22:57:07 PM All use subject to JSTOR Terms and Conditions Ecological Limitation of Diversification 443 optimization of the original data set under GTR ϩ G. verse than autotrophic sisters. If there was ambiguity as Support for relationships in ML trees was evaluated in two to which lineage was sister to a parasitic lineage, we tried ways: BS values and Shimodaira-Hasegawa (SH) test scores to minimize our chance of confirming our expectations on nearest-neighbor interchange topologies at each node by choosing the least species-rich autotrophic sister lineage (Shimodaira and Hasagawa 1999). SH scores were cal- to include in analyses. We therefore assumed that the sister culated by using the ML tree as a constraint in a FastTree group to Triuridaceae is Velloziaceae (the less diverse of search (Price et al. 2010). Thus, the SH likelihood cal- the two potential sister groups; the other is much more culations were performed under a single global GTR model diverse than Triuridaceae). Likewise, DNA sequence–based and not the multipartition GTR model used in the original estimates of relationships among Convolvulaceae lineages RAxML estimate. (Stefanovic et al. 2003) have recovered the parasitic genus Published DNA sequence–based phylogeny estimates Cuscuta as either sister to (1) a clade composed of Ipo- (Smith and dePamphilis 1998; Smith et al. 2000; Olmstead meeae, “Merremieae,” and Convolvulae or (2) a clade and Ferguson 2001) have recovered Lennooideae either composed of Jacquemontieae, Maripeae, Cresseae, and Di- (1) as sister to Ehretioideae or (2) in an unresolved po- chondreae. Both possible sister groups are more diverse sition within Ehretioideae. Here we estimated relationships than Cuscuta, and here we use the less diverse of the two among Boraginaceae lineages using sequences of matK, (i.e., the latter). rbcL, ndhF, and ITS from GenBank. The concatenated The mostly parasitic broomrape family (Orobancha- alignment had 4,055 positions and 82 species after all but ceae) includes one genus (Lindenbergia) of nonparasitic one species from each sampled genus was excluded. species. Published DNA sequence–based estimates of re- Phylogenetic analyses of DNA sequence data have typ- lationships among Orobanchaceae lineages have recovered ically recovered Mitrastemonaceae in an unresolved po- conflicting relationships for Lindenbergia. It has been re- sition within Ericales (Barkman et al. 2004; Nickrent et covered as sister to the rest of the family excluding Reh- al. 2004). Monotropoideae (including Pyroloideae) has mannia (Young et al. 1999; Oxelman et al. 2005; Wolfe et been recovered as sister to the rest of Ericaceae except al. 2005). Alternatively, it has been recovered as sister to Enkianthoideae (Kron et al. 2002) or (excluding Pyrolo- a small group of parasitic species (represented by species ideae) as sister to Arbutoideae (Freudenstein et al. 2010). in the genera Bungea, Cymbaria, Monochasma, Schwalbea, Here we estimate relationships among Ericales lineages and Siphonostegia), with Lindenbergia plus this group as from an alignment with 11,443 positions and 520 species, sister to the rest of Orobanchaceae (Bennett and Mathews using sequences from 18S, 26S, atp1, atpB, ITS, matK, 2006). Here, we have conservatively assumed that Linden- matR, rbcL, nadhF,andtrnL-F. bergia is sister to the rest of Orobanchaceae excluding Rehmannia, since our expectation is that parasitic lineages are less diverse than their autotrophic sister groups and Sister-Taxon Comparisons this arrangement minimizes our chance of accepting this We performed classic sister-taxon comparisons (Vamosi hypothesis. and Vamosi 2005) on the 18 available paired comparisons to test whether the evolution of parasitism in plants is Divergence Dating associated with shifts in diversity. The comparisons were automated with the Systers Python script (Hardy and Cook MRCA ages for only 14 of 18 sister pairs used in the 2010) using the Wilcoxon signed-rank test. Orchids (Or- diversity contrasts have been published or could be esti- chidaceae) are dependent on mycorrhizal fungi for seed mated (table 1). Therefore, four of the sister groups used germination (Smith and Read 1997), and approximately in the diversity comparisons could not be included in 200 orchid species are achlorphyllous and mycohetero- analyses seeking correlation between clade age and clade trophic throughout development (Gebauer and Meyer diversity. Stem ages were taken from the TimeTree of Life 2003). We were unable to compare the diversity of my- (Hedges et al. 2006; http://www.timetree.org/; the average coheterotrophic and autotrophic orchids because phylo- of the MRCA ages for each split was used) and other genetic relationships among mycoheterotrophic and au- published studies or were estimated here using PATHd8 totrophic orchid lineages are poorly known. (Britton et al. 2007) to accommodate among-lineage rate DNA sequence–based estimates have recovered Triuri- variation using the mean path length method. We used daceae in an unresolved position within (Chase stem ages because the stem node represents the time of et al. 2000; Graham et al. 2005). It is unclear whether divergence of the two sister lineages and, hence, sisters are Triuridaceae is more closely related to Velloziaceae or to of equal age. Fossil calibrations used in divergence time (Stemonaceae, [Pandanaceae, Cyclanthaceae]). Before the estimates are provided in table A1, available online. analyses, we expected that parasitic lineages were less di- Corsiaceae has been recovered as sister to the Liliales

This content downloaded from 23.235.32.0 on Tue, 6 Oct 2015 22:57:07 PM All use subject to JSTOR Terms and Conditions 444 The American Naturalist

(Neyland 2002; Davis et al. 2004), although without strong and Monotropoideae separately, we produced LTT plots support. The monophyly of Liliales, excluding Campy- and computed gamma statistics (Pybus and Harvey 2000) nemataceae, has been strongly supported (Fay et al. 2006). using the R package APE (Paradis et al. 2004). We then Published estimates of divergence times among monocot used the Monte Carlo constant rates (MCCR) test imple- lineages (Janssen and Bremer 2004) have not included data mented in the R package LASER (Rabosky 2006) to assess from Corsiaceae, but if we accept that Corsiaceae is sister whether the value of the gamma statistic was significant, to Liliales, there is a narrow window of about 5 million given the number of unsampled lineages in our data set. years (Ma) between the stem and crown ages of Liliales. It should be stressed that the diversification rate compar- We repeated our correlation analyses using crown (117 ison here is not between a parasitic clade and an auto- Ma) and stem (124 Ma) ages of Liliales to bracket the trophic clade but within a parasitic clade and within an range of possible Corsiaceae stem ages. Because the phy- autotrophic clade. Using this approach (arbitrarily choos- logenetic relationships of Triuridaceae are relatively un- ing which sister clades to compare), if we detect a depar- resolved, we use an estimate of 102 Ma for the crown age ture from rate constancy in Monotropoideae, it might stem of Pandanales (Magallo´n and Castillo 2009) as the age of from rate inconstancy from a subgroup within Monotro- a split between Triuridaceae and Velloziaceae. poideae; that is, the change in the gamma statistic might not be contemporaneous with the origin of the parasitic trophic mode. Therefore, to help determine where a shift Correlation Tests might have occurred, N. B. Hardy wrote an R script We tested relationships between MRCA age and (1) log (GammaSpot.R) that takes a Newick tree as input, com- diversity of parasitic plant lineages and (2) log diversity putes the gamma statistic for each subtree with more than of nonparasitic sister lineages. We computed Kendall’s t four tips, and sorts subtrees by gamma statistic value. and Spearman rank correlations and two-tailed P values We also used LASER to compare the fit of density- and assessed the fit on linear models for the relationship dependent (DDL, DDX) constant-decline (Rabosky and between MRCA age and log diversity using the R statistical Lovette 2008; SPVAR, EXVAR, BOTHVAR) and constant- software environment. rate (pure birth and birth-death) models using Akaike Information Criterion (AIC) scores. Models were grouped into two classes: constant-rate models and changing-rate Diversification of Monotropoideae ϩ Arbutoideae models. Significance of the difference in AIC scores be- In our estimate of relationships among Ericales lineages, tween the best-fitting model and the best-fitting model in Monotropoideae (excluding Pyroloideae) was recovered as the other class (the dAICrc test statistic) was assessed sister to Arbutoideae, as in Freudenstein et al. (2010; see through simulation. One hundred birth-death trees were “Results”). Because phylogenetic data sets of the parasitic simulated of the same size as the observed phylogeny, using Monotropoideae and Arbutoideae have near-perfect sam- birth and death rates estimated from the real tree, with pling of species, we performed a more in-depth analysis the birthdeathSim function in LASER. For each simulated of diversification in that group. We aligned sequences sam- tree, dAICrc statistics were calculated and used to create pled from 10 of 11 species of Monotropoideae and 82 of a null distribution for comparison to observed dAICrc 101 species of Arbutoideae spanning 5,124 positions from statistics. the loci matK, rps2, 18S, 28S, ITS1, and ITS2. We used BEAST v1.6.1 (Drummond and Rambaut 2007) to esti- mate the joint posterior probability of a phylogenetic tree Results with branch lengths proportional to time, along with the Phylogenetic Analysis and Divergence Times parameters of a Yule model of the phylogenetic branching process and an HKY ϩ G model of nucleotide substitution In the ML estimate of relationships among Boraginaceae that was unlinked across data partitions (each codon po- lineages, Lennooideae (represented by sequences sampled sition, ITS, and 28S ϩ 18S). The BEAST analysis assumed from ) was recovered within the Eh- a relaxed-clock, uncorrelated lognormal model of among- retioidea as sister to Tiquilia (fig. A1, available online), lineage substitution rate variation. The estimate was fossil although the relationships had little BS support (0.23) and calibrated with an exponential prior with an offset of 15.8 the SH support was marginally nonsignificant (0.93). The Ma on the age of (Wolfe 1964). The Markov ML estimate of Ericales relationships (fig. A2, available chain Monte Carlo analysis was run for 10 million iter- online) recovered very strong support (BS p 0.94 ; ations, saving trees every 1,000 iterations after the chain SH p 1) for a sister relationship between - began to sample from the stationary distribution (deter- aceae and the rest of Ericales excluding Balsaminaceae, mined by examining parameter traces). For Arbutoideae Marcgraviaceae, and Tetrameristaceae (divergence age p

This content downloaded from 23.235.32.0 on Tue, 6 Oct 2015 22:57:07 PM All use subject to JSTOR Terms and Conditions Ecological Limitation of Diversification 445

correlated with MRCA age (Corsiaceae stem age, 117 Ma: Kendall’st p 0.54 ,P p .0067 ; Spearman’sr p 0.69 , P p .0079; Corsiaceae stem age, 124 Ma: Kendall’s t p 0.54,P p .0067 ; Spearman’sr p 0.70 ,P p .0069 ). A lin- ear model was a poor fit to the relationship between MRCA age and diversity in parasitic plants (adjusted R 2 p 0.0044,P p .51 ) but a good fit to the data from autotrophs (adjustedR 2 p 0.42 ,P p .0070 ; fig. 3). LTT plots for Monotropoideae and Arbutoideae (fig. 4) show a striking difference in diversification between these sister groups. Whereas Arbutoideae appears to be diver- Log-diversity sifying exponentially (g p 4.10 ; MCCR,P p 1 ), the rate of Monotropoideae diversification has slowed significantly

246810 (g p Ϫ2.02 ; MCCR,P p 0.020 ). The GammaSpot.R script returned Monotropoideae in its entirety as the sub- tree with the most extreme value of the gamma statistic. For Arbutoideae, the best-fitting model was a constant- 40 60 80 100 120 rate birth-death model (speciation rate p 0.060, extinc- MRCA age tion rate p 0.051, dAICrc p Ϫ2.57,P p .001 ). For Monotropoideae, the best-fitting model was a density- dependent model in which the rate of decline of diversi- Figure 3: Relationship between most recent common ancestor fication increases with the number of species in a clade (MRCA) age and clade diversity for parasitic plants and their au- p totrophic sister groups. Parasitic plant diversities are represented by (DDX: r1 [initial speciation rate] 0.26, x [parameter open circles; autotrophic sister group diversities are represented by controlling magnitude of rate change] p 1.21), although filled squares. Note that there is a pair of diversity records for each the fit of this model was not significantly better than a MRCA age, one from the parasitic clade and the other from its pure birth model (dAICrc p 1.52,P p .11 ). autotrophic sister clade (in two cases the parasitic group had a di- versity of log(1) p 0 and is not shown). Parasitic plant diversity was unrelated to MRCA age (adjustedR2 p 0.0044 ,P p .51 ); this re- lationship is represented by the solid horizontal line, with a y-inter- cept equal to the mean value for parasitic clade diversity. Autotrophic sister-group diversity was strongly correlated with MRCA age (ad- justedR2 p 0.42 ,P p .0070 ); the best-fitting linear model is rep- resented by the dashed line. This figure matched the pattern expected by the asymmetric limitation model, shown in figure 2C.

99 Ma). Monotropoideae (excluding Pyroloideae) was re- covered as sister to Arbutoideae with strong support (BS p 0.88 ; SH p 0.99 ; divergence age p 70 Ma). Pyr- oloideae was estimated to be sister to this group, with weak support (BS p 0.37 ; SH p 0.66 ). The age of the diver- Log-diversity gence between Parasitaxus and Lagarostrobus ϩ Manoao was estimated as 40 Ma. 12 5102050

Comparative Analysis −40 −30 −20 −10 0 Parasitic lineages are much less diverse than their non- Time (Ma) parasitic sister groups (15 of 18 comparisons; P value from all contrast metrics !.01). The diversity of parasitic plant lineages was not related to MRCA age (Corsiaceae stem Figure 4: Lineage-through-time plots for parasitic Monotropoideae age, 117 Ma: Kendall’st p 0.12 ,P p .55 ; Spearman’s and its nonparasitic sister group, Arbutoideae. Species accumulation p p in a parasitic plant lineage (Monotropoideae, solid line) appears r 0.29,P .31 ; Corsiaceae stem age, 124 Ma: Kendall’s logistic and is in striking contrast to exponential diversification in t p 0.17,P p .41 ; Spearman’sr p 0.31 ,P p .27 ). In the nonparasitic sister group (Arbutoideae, dashed line). Log diversity contrast, the diversity of nonparasitic sister groups was is plotted as a function of time (Ma).

This content downloaded from 23.235.32.0 on Tue, 6 Oct 2015 22:57:07 PM All use subject to JSTOR Terms and Conditions 446 The American Naturalist

Discussion ter group Arbutoideae mirrored the results of the sister- taxon-age analysis. For Monotropoideae, the gamma sta- Identifying ecological factors that shape the process of evo- tistic was negative, indicative of decreasing diversification lutionary diversification is an important challenge in evo- rates, and the best-fitting model was a form of density- lutionary biology. Another challenge is to understand how dependent diversification. For Arbutoideae, the gamma those factors shape diversification. Several traits have been statistic was strongly positive, and a constant-rate birth- associated with changes in taxon diversity (e.g., trophic death model was a better fit than any of the rate-variable generalization in birds; Phillimore et al. 2006). For the models. However, a positive value for the gamma statistic most part, it has been assumed that diversity-changing can also be generated under declining diversification traits alter diversification rates or, more precisely, they alter through time (Quental and Marshall 2009, 2010). There- the value of a within-clade constant diversification rate. fore, we cannot rule out decreasing diversification in Ar- However, ecosystems might be able to support only a finite butoideae on the basis of the gamma statistic alone. To- amount of species diversity (Rabosky and Glor 2010). Fur- gether with the intraclade model-fitting and cross-clade thermore, many extant clades might be in a phase of de- sister-taxon-age analysis, though, a fairly robust picture clining diversity (Quental and Marshall 2010) that is emerges for the effect of parasitism on plant poorly reflected by constant-rate intraclade diversification diversification. models. In our interpretation, intraclade diversity decline, Our results are therefore consistent with the hypothesis as well as equilibrium, might be the result of ecological that parasitic plants are species poor due to ecological limitation on diversity. limitation. Of the three theoretical models resolvable by Sister-taxon comparisons are less prone than are intra- sister-taxon-age comparisons, diversification of parasitic clade approaches to confounding interactions between plants and their sister groups best fits the asymmetrical speciation and extinction and to the problems of not sam- ecological limitation model (cf. figs. 2C, 3). The diversities pling extinct lineages (Paradis 2011a). Also, through com- of parasitic plant lineages grow logistically and are pri- parisons of clades with replicated origins of the trait of marily limited by ecological constraints, whereas the di- interest, sister-taxon comparisons return a more robust versities of nonparasitic sister groups grow exponentially test of the correlation between the focal trait and changes and are primarily limited by diversification rate. None of in diversity. We find strong evidence that parasitic lineages the approaches used in this study resolves among specific are, in general, not as diverse as their nonparasitic sister, forms of ecological limitation. We cannot distinguish be- indicating either lower diversification rates or ecological tween the density-dependent, constant-decline, and het- limitation to diversity. If the cause is low diversification erochrony models, but for Monotropoideae ϩ Arbuto- rate rather than ecological limitation, there should be a ideae, LTT plots did not show the signature of mass positive relationship between clade diversity and age, as extinction (Crisp and Cook 2009), reducing the likelihood expected for unbounded diversification. However, our use of at least one type of diversification heterochrony. of the sister-taxon-age test finds that clade age and clade Parasitic Orobanchaceae and Santalales are major ex- diversity are unrelated (i.e., no pattern) in parasitic plants, ceptions to the generalization that parasitic plants are less rejecting unbounded diversification in favor of ecological diverse than their autotrophic sister groups. This might limitation. be due to most parasitic species in these groups being Wiens (2011) has been critical of the assumption that hemiparasitic (and sometimes only facultatively hemipar- a lack of relationship between clade age and clade diversity asitic) rather than holoparasitic. Hemiparasitic species are is indicative of ecological limitation on diversity, suggest- more loosely tied to host species than are holoparasitic ing instead that it could reflect variation among clade di- species (e.g., Gibson and Watkinson 1989). For hemipar- versification rates. However, for interclade diversification asites we might expect the niche-expanding factors of a rate variation to destroy the clade age–to–clade diversity parasitic trophic mode (i.e., release from constraints such relationship, clade diversification rates would need to be as mineral and water acquisition) to outweigh factors likely strongly biased by clade age; that is, the older the clade, to constrict niche breadth (i.e., additional host-related the slower the diversification rate. Otherwise, diversifica- niche parameters). This could be interpreted as further tion rate variation is just noise, and the clade age should evidence that host-use constraints (Thorogood and His- be positively related to clade diversity (Rabosky 2009b). cock 2010) are causing ecological limitation of parasitic The sister-taxon-age approach has shown that clade age plant diversity. is a poor predictor of species diversity in parasitic plants Before this study, the primary ecological parameter that but is a good predictor in their nonparasitic sister groups. has been associated with limits on diversity is geographic Intraclade analyses of diversification rate evolution in the range size (Losos and Schluter 2000; Birand et al. 2012). parasitic clade Monotropoideae and in its autotrophic sis- This study suggests that parasitism in plants is an attribute

This content downloaded from 23.235.32.0 on Tue, 6 Oct 2015 22:57:07 PM All use subject to JSTOR Terms and Conditions Ecological Limitation of Diversification 447 of individuals (trophic mode) that is also associated with Acknowledgments diversity limitation. Parasites in general, including para- This study was partly supported by an Australian Biolog- sitic plants, require adaptations for living, feeding, and ical Resources grants to N.B.H. and an Australian Research reproducing on or in their hosts and for resisting host Council Discovery Projects grant to L.G.C. Thanks to G. defenses (Wiegmann et al. 1993; Thorogood and Hiscock Svenson for access to computational resources. This man- 2010). Parasites might also need to synchronize their life uscript was improved considerably after constructive cri- cycles with those of hosts, especially if hosts are short lived. tiques from three anonymous reviewers; we are very grate- All plant species are constrained by some aspects of their ful for their help. environment, such as pollinators (Campbell 1985; Brown and Mitchell 2001), soil chemistry and microbial associates (Reynolds et al. 2003), and light requirements (Kobe Literature Cited 1999). Parasitic plants are likely to be more ecologically constrained than nonparasitic plants because they are sub- Barkman, T. J., S.-H. Lim, K. M. Salleh, and K. Nais. 2004. Mito- ject to an extra set of host-related constraints, in addition chondrial DNA sequences reveal the photosynthetic relatives of to the set of constraints that are shared among all terrestrial Rafflesia, the world’s largest flower. Proceedings of the National plants (albeit indirectly in some parasites). Academy of Sciences of the USA 101:787–792. As noted above, attributes of individuals can alter di- Bennett, J. R., and S. Mathews. 2006. Phylogeny of the parasitic plant versification only indirectly though their influence on eco- family Orobanchaceae inferred from phytochrome A. American logical parameters such as population size and resource Journal of Botany 93:1039–1051. Birand, A., A. Vose, and S. Gavrilets. 2012. Patterns of species ranges, availability (e.g., host constraints). The design of this study speciation and extinction. American Naturalist 179:1–21. does not allow us to identify the proximate, ecological Bremer, K., E. Friis, and B. Bremer. 2004. Molecular phylogenetic factors shaping parasitic plant diversity. Parasitic plants dating of asterid flowering plants shows early diver- might compete with their hosts for services sification. Systematic Biology 53:496–505. (Ollerton et al. 2006) or might suffer a fitness cost from Britton, T., C. L. Anderson, D. Jacquet, S. Lundqvist, and K. Bremer. interspecific pollination transfer from the host (Morales 2007. Estimating divergence times in large phylogenetic trees. Sys- tematic Biology 56:741–752. and Traveset 2008). For host-specific parasitic species, Brown, B. J., and R. J. Mitchell. 2001. Competition for pollination: maximum geographic ranges are constrained by those of effects of of an invasive plant on seed set of a native con- hosts, although parasitic species with high host specificity gener. Oecologia (Berlin) 129:43–49. tend to occur on abundant and broadly distributed hosts Campbell, D. R. 1985. Pollinator sharing and seed set of Stellaria (Norton and Carpenter 1998). On the other hand, parasitic pubera: competition for pollination. Ecology 66:544–553. species having low host specificity could range over geo- Chase, M. W., D. E. Soltis, P. S. Soltis, P. J. Rudall, M. F. Fay, W. H. Hahn, S. Sullivan, et al. 2000. Higher-level systematics of the graphic areas broader than occupied by any one host spe- : an assessment of current knowledge and a new cies. Likewise, dispersal success should be proportional to classification. Pages 3–16 in K. L. Wilson and D. A. Morrison, eds. the abundance of host species in the environment. Where Monocots: systematics and evolution. CSIRO, Collingwood. hosts are abundant, it is possible that parasitic species Crisp, M. D., and L. G. Cook. 2009. Explosive radiation or cryptic could have access to more suitable sites for development mass extinction? interpreting signatures in molecular phylogenies. than nonparasitic species, which must compete for light, Evolution 63:2257–2265. Davies, T. J., T. G. Barraclough, M. W. Chase, P. S. Soltis, D. E. Soltis, water, and nutrients. Finally, if parasitic species exact fit- and V. Savolainen. 2003. Darwin’s abominable mystery: insights ness costs on their hosts, parasitism could increase ex- from a supertree of the angiosperms. Proceedings of the National tinction risk for host and parasite species alike. Academy of Sciences of the USA 101:1904–1909. In conclusion, in contrast to the widely held assumption Davis, C. C., M. Latvis, D. L. Nickrent, K. J. Wurdack, and D. A. that phylogenetic imbalance stems from differences in di- Baum. 2007. Floral gigantism in Rafflesiaceae. Science 315:1812. versification rates, differences in absolute ecological limits Davis, J. I., D. W. Stevenson, G. Petersen, O. Seberg, L. M. Campbell, J. V. Freudenstein, D. H. Goldman, et al. 2004. A phylogeny of on species diversities are also likely to be important, as the monocots, as inferred from rbcL and atpA sequence variation, illustrated here for parasitic plants. In this study we find and a comparison of methods for calculating jackknife and boot- evidence both for models of effectively unlimited diversity strap values. Systematic Botany 29:467–510. and for models of diversity limitation. A combination of Drummond, A. J., and A. Rambaut. 2007. BEAST: Bayesian evolu- approaches incorporating sister-taxon comparisons of di- tionary analysis by sampling trees. BMC Evolutionary Biology 7:214. versity and age, coupled with LTT plots and diversification Eriksson, O., and B. Bremer. 1992. Pollination systems, dispersal modes, life forms, and diversification rates in angiosperm families. model fitting of well-sampled phylogenies of focal taxa, Evolution 46:258–266. appears to provide a powerful test of likely causes of di- Fay, M. F., M. W. Chase, N. Rønsted, D. S. Devey, Y. Pillon, J. C. versity and asymmetry. Pires, G. Petersen, O. Seberg, and J. I. Davis. 2006. Phylogenetics

This content downloaded from 23.235.32.0 on Tue, 6 Oct 2015 22:57:07 PM All use subject to JSTOR Terms and Conditions 448 The American Naturalist

of Liliales: summarized evidence from combined analyses of five Lengyel, S., A. D. Gove, A. M. Latimer, J. D. Majer, and R. R. Dunn. plastid and one mitochondrial loci. Pages 559–565 in J. T. Colum- 2009. Ants sow the seeds of global diversification in flowering bus, E. A. Friar, J. M. Porter, L. M. Prince, and M. G. Simpson, plants. PLoS One 4:e5480. eds. Monocots: comparative biology and evolution, excluding Po- Losos, J. B., and D. Schluter. 2000. Analysis of an evolutionary spe- ales. Rancho Santa Ana Botanical Garden, Claremont, CA. cies-area relationship. Nature 408:847–850. Forest, F., M. W. Chase, C. Persson, P. R. Crane, and J. A. Hawkins. Maddison, W. P., and D. R. Maddison. 2012. Mesquite: a modular 2007. The role of biotic and abiotic factors in the evolution of ant system for evolutionary analysis. Version 2.73. http:// dispersal in the milkwort family (Polygalaceae). Evolution 61: mesquiteproject.org. 1675–1694. Magallo´n, S., and A. Castillo. 2009. Angiosperm diversification Freudenstein, J. V., M. B. Broe, and E. R. Feldenkris. 2010. Resolving through time. American Journal of Botany 96:349–365. relationships at the base of Ericaceae: how do the leafless members Magallo´n, S. M., and M. J. Sanderson. 2001. Absolute diversification fit in? Paper presented at Botany 2010, Providence, RI, July 31– rates in angiosperm clades. Evolution 55:1762–1780. August 4. McPeek, M. A. 2008. The ecological dynamics of clade diversification Gebauer, G., and M. Meyer. 2003. 15N and 13C natural abundance of and community assembly. American Naturalist 172:E270–E284. autotrophic and myco-heterotrophic orchids provides insight into Merckx, V., and J. V. Freudenstein. 2010. Evolution of mycohetero- nitrogen and carbon gain from fungal association. New Phytologist trophy in plants: a phylogenetic perspective. New Phytologist 185: 160:209–223. 605–609. Gibson, C. C., and A. R. Watkinson. 1989. The host range and se- Mitter, C., B. Farrell, and B. Wiegmann. 1988. The phylogenetic study lectivity of a parasitic plant: Rhinanthus minor L. Oecologia (Ber- of adaptive zones: has phytophagy promoted insect diversification? lin) 78:401–406. American Naturalist 132:107–128. Gilinsky, N. L. 1994. Volatility and the Phanerozoic decline of back- Moore, T. E., G. A. Verboom, and F. Forest. 2010. Phylogenetics and ground extinction intensity. Paleobiology 20:445–458. biogeography of the parasitic genus Thesium (Santalaceae), with Goldblatt, P., A. Rodriguez, M. P. Powell, T. J. Davies, J. C. Manning, an emphasis on the Cape of South . Botanical Journal of M. van der Bank, and V. Savolainen. 2008. Iridaceae “out of Aus- the Linnean Society 162:435–452. tralia”? phylogeny, biogeography, and divergence time based on Morales, C., and A. Traveset. 2008. Interspecific pollen transfer: mag- plastid DNA sequences. Systematic Botany 33:495–508. nitude, prevalence and consequences for plant fitness. Critical Re- Graham, S. A., J. Hall, K. Sytsma, and S.-H. Shi. 2005. Phylogenetic views in Plant Sciences 27:221–238. analysis of the Lythraceae based on four gene regions and mor- Nee, S., A. Mooers, and P. H. Harvey. 1992. Tempo and mode of phology. International Journal of Plant Sciences 166:995–1017. evolution revealed from molecular phylogenies. Proceedings of the Guyer, C., and J. B. Slowinski. 1993. Adaptive radiation and the National Academy of Sciences of the USA 89:8322–8326. topology of large phylogenies. Evolution 47:253–263. Neyland, R. 2002. A phylogeny inferred from large-subunit (26S) Hardy, N. B., and L. G. Cook. 2010. Gall-induction in insects: evo- ribosomal DNA sequences suggests that Burmanniales are poly- lutionary dead-end or speciation driver? BMC Evolutionary Bi- phyletic. Australian Systematic Botany 15:19–28. ology 10:257. Nickrent, D. L., A. Blarer, Y.-L. Qiu, D. E. Soltis, P. S. Soltis, and M. Harmon, L. J., J. A. Shulte, A. Larson, and J. B. Losos. 2003. Tempo Zanis. 2002. Molecular data place Hydnoraceae with Aristolochi- and mode of evolutionary radiation in iguanian lizards. Science aceae. American Journal of Botany 89:1809–1817. 301:961–964. Nickrent, D. L., A. Blarer, Y.-L. Qiu, V. Vidal-Russel, and F. E. An- Hedges, S. B., J. Dudley, and S. Kumar. 2006. TimeTree: a public derson. 2004. Phylogenetic inference in Rafflesiales: the influence knowledge-base of divergence times among organisms. Bioinfor- of rate heterogeneity and horizontal gene transfer. BMC Evolu- matics 22:2971–2972. tionary Biology 4:40. Hey, J. 1992. Using phylogenetic trees to study speciation and ex- Nickrent, D. L., J. P. Der, and F. E. Anderson. 2005. Discovery of the tinction. Evolution 46:627–640. photosynthetic relatives of the “Maltese mushroom” Cynomorium. Janssen, T., and K. Bremer. 2004. The age of major monocot groups BMC Evolutionary Biology 5:38. inferred from 800ϩ rbcL sequences. Botanical Journal of the Lin- Nickrent, D. L., V. Male´cot, R. Vidal-Russel, and J. P. Der. 2010. A nean Society 146:385–398. revised classification of Santalales. Taxon 59:538–558. Jones, K. E., O. R. P. Bininda-Emonds, and J. L. Gittleman. 2005. Niklas, K. J. 1997. The evolutionary biology of plants. University of Bats, clocks, and rocks: diversification patterns in Chiroptera. Evo- Chicago Press, Chicago. lution 59:2243–2255. Norton, D. A., and M. A. Carpenter. 1998. Mistletoes as parasites: Katoh, T. 2008. Recent developments in the MAFFT multiple se- host specificity and speciation. Trends in Ecology & Evolution 13: quence alignment program. Briefings in Bioinformatics 9:286–298. 101–105. Kelch, D. G. 1998. Phylogeny of Podocarpaceae: comparison of evi- Ollerton, J., A. Stott, E. Allnutt, S. Shove, C. Taylor, and E. Lamborn. dence from morphology and 18S rDNA. American Journal of Bot- 2006. Pollination niche overlap between a parasitic plant and its any 85:986–996. host. Oecologia (Berlin) 151:473–485. Kobe, R. K. 1999. Light gradient partitioning among topical tree Olmstead, R. G., and D. Ferguson. 2001. A molecular phylogeny of species through differential seedling mortality and growth. Ecology the Boraginaceae/Hydrophyllaceae. Paper presented at Botany 80:187–201. 2001, Albuquerque, NM, August 12–16. Kron, K. A., W. S. Judd, P. F. Stevens, D. M. Crayn, A. A. Anderberg, Oxelman, B., P. Kornhall, R. G. Olmstead, and B. Bremer. 2005. P. A. Gadek, C. J. Quinn, and J. L. Luteyn. 2002. A phylogenetic Further disintegration of Scrophulariaceae. Taxon 54:411–425. classification of Ericaceae: molecular and morphological evidence. Paradis, E. 2011a. Shift in diversification in sister-clade comparisons: Botanical Review 68:335–423. a more powerful test. Evolution 66:288–295.

This content downloaded from 23.235.32.0 on Tue, 6 Oct 2015 22:57:07 PM All use subject to JSTOR Terms and Conditions Ecological Limitation of Diversification 449

———. 2011b. Time-dependent speciation and extinction from phy- Sepkoski, J. J. 1978. A kinetic model of Phanerozoic taxonomic di- logenies: a least squares approach. Evolution 65:661–672. versity. I. Analysis of marine orders. Paleobiology 4:223–251. Paradis, E., J. Claude, and K. Strimmer. 2004. APE: analyses of phy- Shimodaira, H., and M. Hasagawa. 1999. Multiple comparisons of logenetics and evolution in R language. Bioinformatics 20:289–290. log-likelihoods with applications to phylogenetic inference. Mo- Phillimore, A. B., R. P. Freckleton, C. D. L. Orme, and I. P. F. Owens. lecular Biology and Evolution 16:1114–1116. 2006. Ecology predicts large-scale patterns of phylogenetic diver- Smith, R. A., and C. W. dePamphilis. 1998. Phylogenetic placement sification in birds. American Naturalist 168:220–229. of the holoparasitic family Lennoaceae: preliminary molecular evi- Price, M. N., P. S. Dehal, and A. P. Arkin. 2010. FastTree 2: approx- dence. American Journal of Botany 65:157. imately maximum-likelihood trees for large alignments. PLoS ONE Smith, R. A., D. M. Ferguson, T. J. Barkman, and C. W. dePamphilis. 5:e9490. 2000. Molecular phylogenetic evidence for the origin of Lennoa- Pybus, O. G., and P. H. Harvey. 2000. Testing macro-evolutionary ceae: a case of adelphoparasitism in the angiosperms? American models using incomplete molecular phylogenies. Proceedings of Journal of Botany 87(suppl.):158. the Royal Society B: Biological Sciences 267:2267–2272. Smith, S. E., and D. J. Read. 1997. Mycorrhizal symbiosis. 2nd ed. Quental, T. B., and C. R. Marshall. 2009. Extinction during evolu- Academic Press, San Diego, CA. tionary radiations: reconciling fossil record with molecular phy- Stamatakis, A. 2006. RAxML-VI-HPC: maximum likelihood-based logenies. Evolution 63:3158–3167. phylogenetic analyses with thousands of taxa and mixed models. ———. 2010. Diversity dynamics: molecular phylogenies need the Bioinformatics 22:2688–2690. fossil record. Trends in Ecology & Evolution 25:434–441. Stefanovic, S., D. F. Austin, and R. G. Olmstead. 2003. Classification Rabosky, D. L. 2006. LASER: a maximum likelihood toolkit for de- of Convolvulaceae: a phylogenetic approach. Systematic Botany tecting temporal shifts in diversification rates from molecular phy- 28:791–806. logenies. Evolutionary Bioinformatics 2:247–250. Talavera, G., and J. Castresana. 2007. Improvement of phylogenies ———. 2009a. Ecological limits and diversification rate: alternative after removing divergent and ambiguously aligned blocks from paradigms to explain the variation in species richness among clades protein sequence alignments. Systematic Biology 56:564–577. and regions. Ecology Letters 12:735–743. Thorogood, C., and S. Hiscock. 2010. Specific developmental path- ———. 2009b. Ecological limits on clade diversification in higher ways underlie host specificity in the parasitic plant Orobanche. taxa. American Naturalist 173:662–674. Plant Signaling and Behavior 5:275–277. ———. 2010. Extinction rates should not be estimated from mo- Vamosi, S. M., and J. C. Vamosi. 2005. Endless tests: guidelines for lecular phylogenies. Evolution 64:1816–1824. analyzing non-nested sister-group comparisons. Evolutionary Rabosky, D. L., and R. E. Glor. 2010. Equilibrium speciation in a Ecology Research 7:567–579. model adaptive radiation of island lizards. Proceedings of the Na- Walker, T. D., and J. W. Valentine. 1984. Equilibrium models of tional Academy of Sciences of the USA 107:22178–22183. evolutionary species diversity and the number of empty niches. Rabosky, D. L., and I. J. Lovette. 2008. Density-dependent diversifi- American Naturalist 124:887–899. cation in North American wood warblers. Proceedings of the Royal Weir, J. T. 2006. Divergent timing and patterns of species accumu- Society B: Biological Sciences 275:2363–2371. lation in lowland and highland Neotropical birds. Evolution 60: Raup, D. 1972. Taxonomic diversity during the Phanerozoic. Science 842–855. 177:1065–1071. Westwood, J. H., J. I. Yoder, M. P. Timko, and C. W. dePamphilis. Reynolds, H. L., A. Packer, J. D. Bever, and K. Clay. 2003. Grassroots 2010. The evolution of parasitism in plants. Trends in Plant Science ecology: plant-microbe-soil interactions as drivers of plant com- 15:227–235. munity structure and dynamics. Ecology 84:2281–2291. Wiegmann, B. M., C. Mitter, and B. Farrell. 1993. Diversification of Ricklefs, R. E. 2006. Global variation in the diversification rate of carnivorous parasitic insects: extraordinary radiation or specialized passerine birds. Ecology 87:2468–2478. dead end? American Naturalist 142:737–754. Ricklefs, R. E., J. B. Losos, and T. M. Townsend. 2007. Evolutionary Wiens, J. 2011. The causes of species richness patterns across space, diversification of clades of squamate reptiles. Journal of Evolu- time, and clades and the role of “ecological limits.” Quarterly tionary Biology 20:1751–1762. Review of Biology 86:75–96. Rohwer, J. G., and B. Rudolph. 2005. Jumping genera: the phylo- Wolfe, A. D., C. P. Randle, L. Liu, and K. E. Steiner. 2005. Phylogeny genetic position of Cassytha, Hypodaphnis, and Neocinnamomum and biogeography of Orobanchaceae. Folia Geobotanica 40:115–134. (Lauraceae) based on different analyses of trnK intron sequences. Wolfe, J. A. 1964. Miocene floras from Fingerrock wash, southwestern Annals of the Missouri Botanical Garden 92:153–178. Nevada. U.S. Geological Survey Professional Paper 454-N:1–31. Sanderson, M. J., D. Boss, D. Chen, K. A. Cranston, and A. Wehe. Young, N. D., K. E. Steiner, and C. W. dePamphilis. 1999. The evo- 2008. The PhyLoTA browser: processing GenBank for molecular lution of parasitism in Scrophulariaceae/Orobanchaceae: plastid phylogenetic research. Systematic Biology 57:335–346. gene sequences refute an evolutionary transition series. Annals of Sanderson, M. J., and M. J. Donoghue. 1994. Shifts in diversification the Missouri Botanical Garden 86:876–893. rate with origin of angiosperms. Science 264:1590–1593. ———. 1996. Reconstructing shifts in diversification rates on phy- logenetic trees. Trends in Ecology & Evolution 11:15–20. Schluter, D. 2000. The ecology of adaptive radiation. Oxford Uni- Associate Editor: Anurag Agrawal versity Press, New York. Editor: Judith L. Bronstein

This content downloaded from 23.235.32.0 on Tue, 6 Oct 2015 22:57:07 PM All use subject to JSTOR Terms and Conditions