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The University of Chicago Testing for Ecological Limitation of Diversification: A Case Study Using Parasitic Plants. 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 plant 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 Ericaceae 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 species 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
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