Ecological limits and diversification rate: alternative paradigms to explain the variation in species richness among clades and regions

Transcription

1 Ecology Letters, (2009) 12: doi: /j x IDEA AND PERSPECTIVE Ecological limits and diversification rate: alternative paradigms to explain the variation in species richness among clades and regions Daniel L. Rabosky 1,2 * 1 Department of Ecology and Evolutionary Biology, Cornell University, Ithaca, NY, USA 2 Cornell Lab of Ornithology, 159 Sapsucker Woods Road, Ithaca, NY, USA *Correspondence: dlr32@cornell.edu Abstract Diversification rate is one of the most important metrics in macroecological and macroevolutionary studies. Here I demonstrate that diversification analyses can be misleading when researchers assume that diversity increases unbounded through time, as is typical in molecular phylogenetic studies. If clade diversity is regulated by ecological factors, then species richness may be independent of clade age and it may not be possible to infer the rate at which diversity arose. This has substantial consequences for the interpretation of many studies that have contrasted rates of diversification among clades and regions. Often, it is possible to estimate the total diversification experienced by a clade but not diversification rate itself. I show that the evidence for ecological limits on diversity in higher taxa is widespread. Finally, I explore the implications of ecological limits for a variety of ecological and evolutionary questions that involve inferences about speciation and extinction rates from phylogenetic data. Keywords Biodiversity, biogeography, diversification, evolutionary rates, extinction, latitudinal diversity gradient, macroevolution, speciation, species richness. Ecology Letters (2009) 12: INTRODUCTION: DIVERSIFICATION RATE AND SPECIES RICHNESS One of the most striking features of the natural world is the disparity in species richness among groups of organisms and across geographic regions. As Haldane famously (and perhaps apocryphally) quipped, there are an awful lot of beetles on this planet relative to other groups of organisms (Hutchinson 1959). Given this disparity, we are compelled to explain not only the stunning diversity of life, but also the manner in which that diversity is apportioned: why do some groups have so many species, and why do others have so few? The spatial distribution of biological diversity has likewise garnered broad interest, because geographic regions can differ profoundly in species richness. Perhaps no pattern better illustrates this than the latitudinal gradient in species diversity, which is surely one of the most general large-scale patterns in all of ecology (Hillebrand 2004). We are now in the midst of a major integration of ecology with evolutionary biology (Webb et al. 2002; Johnson & Stinchcombe 2007), with increasing recognition that spatial patterns of diversity cannot be divorced from evolutionary history (Ricklefs 2004). This has been fueled in part by the ever-increasing availability of molecular phylogenies and new analytical tools, but it is perhaps even more a result of a new conceptual landscape that emphasizes the cumulative effects of differential speciation and extinction through time on diversity. In this framework, diversification rate the balance between speciation and extinction is presumed to exert a potent effect on species richness. All things being equal, clades with higher net diversification rates should be more diverse than clades with lower net diversification rates, just as older clades should be more diverse on average than younger clades (Stephens & Wiens 2003; McPeek & Brown 2007). This of course applies only to clades that have some living descendants in the present, as no age-diversity relationship can exist for extinct clades. Hypotheses about the extent to which spatial diversity patterns reflect variation in diversification rates have been

2 736 D. L. Rabosky Idea and Perspective discussed for decades (Fischer 1960) and the ability to reconstruct diversification rates from phylogenetic data has transformed the study of regional diversity differences (Wiens & Donoghue 2004; Mittelbach et al. 2007; Ricklefs 2007). Although methods for analysing diversification rates have become increasingly sophisticated (Mooers & Heard 1997; Paradis 2005; Maddison et al. 2007), they are fundamentally based on the relationship between lineage diversity and lineage age. This applies equally to taxonomic data (Magallon & Sanderson 2001) and to molecular phylogenies with complete taxon sampling, where the Ôwaiting timesõ between successive speciation events in the phylogeny serve as a source of inference about evolutionary rates (Nee et al. 1994). Statistical methods for estimating diversification rates assume that diversity accumulates according to an exponential growth process, with the rate of increase through time depending on the difference between speciation and extinction rates. Almost all methods fundamentally assume that, on some level, the net rate of species diversification is proportional to log(n) t, where N is species richness and t is time for diversification. The estimators themselves may become analytically complex when extinction is considered, but the basic idea remains the same and hinges on the critical assumption that diversity increases through time (Ricklefs 2007, 2009). Here I argue that inferences about diversification rates and their relationship to species richness, of both clades and regions, are frequently compromised by the assumption that species diversity increases unbounded through time. I suggest that much evidence from both the fossil record and molecular phylogenies implies the existence of ecological limits on diversity. If limits on clade regional diversity exist, we are faced with three immediate problems of surprisingly broad relevance to ecological and evolutionary studies. The first is that diversification rate, as typically estimated, is a flawed metric of total diversification rather than an estimate of diversification rate. Second, if diversity does not increase unbounded through time, species richness may be unrelated to both the age of clades as well as diversification rate (Ricklefs 2007). While this may be unsurprising in the ecological literature, which has long emphasized equilibrium mechanisms for the maintenance of diversity (Chesson 2000; Hawkins et al. 2003; Silvertown 2004), it is rarely considered in modern studies of diversification, where clade age and diversification rates are frequently considered to represent dichotomous alternative explanations for differential species richness (McPeek & Brown 2007; Rabosky et al. 2007). Finally, the existence of ecological limits on diversity challenges the idea that contrasts in species richness among sister clades reflect differences in the underlying rates of species diversification. EVIDENCE FOR ECOLOGICAL LIMITS ON DIVERSITY The idea of carrying capacity is fundamental to population ecology, and it is not difficult to imagine that finite resources place a crude limit on the total number of species that can occur within a region. However, ecological limits may also apply to clades (Ricklefs 2009), particularly if we typically study higher taxa that have been recognized on the basis of geographic or ecological attributes. In this case, apparent limits on clade size might arise as an epiphenomenon of evolutionary species-area relationships or other factors (Losos & Schluter 2000; Ricklefs 2006; Rabosky 2009). Here, I use the phrase Ôdiversity regulationõ to refer to conditions where diversity shows approximate constancy through time (Ricklefs 2007, 2009). This includes the possibility that diversity is regulated at equilibria within clades or regions. However, apparent diversity regulation might also result from a balanced speciation-extinction process, with stochastic fluctuations in diversity, that results in semi-stable species numbers over long periods of time (Nee 2006; Ricklefs 2007). If diversity is regulated by ecological limits, this implies that species richness should be unrelated to the amount of time available for diversification, once time exceeds that required to reach carrying capacity. In an obvious parallel with population ecology, paleobiologists frequently describe diversity regulation in the fossil record as consistent with a logistic model, as opposed to an exponential model of unbounded diversity increase (Sepkoski 1978; Benton 2009). How and why clades might show properties consistent with diversity regulation remains an open question, but such limits appear to be more common than is typically assumed. Three major pieces of evidence for diversity limits include: (i) constancy of diversity through time in the fossil record; (ii) the absence of a relationship between clade age and species richness in extant taxa; and (iii) diversity-dependence of speciation and extinction rates. Diversity through time in the fossil record The question of whether biotic factors result in more-or-less constant diversity levels through time has been a central question in paleobiological studies for decades (Benton 2009). Sepkoski s (1984) curve of marine invertebrate diversity through time strongly suggested that diversity in the marine realm increased exponentially and without limits, at least since the early Mesozoic. However, it has long been appreciated that sampling biases in the fossil record might lead to spurious diversity trends (Raup 1972), and new data and analytical techniques are forcing a radical reinterpretation of traditional views on diversity through time. Most prominently, Alroy (1996) and others (Miller & Foote 1996; Connolly & Miller 2001) have developed

3 Idea and Perspective Diversification rate and ecological limits 737 sophisticated methods for addressing the problem of differential sampling through time in the fossil record. The fundamental problem is that the availability of fossils for analysis can vary widely through time, perhaps due to differential exposure and availability of sedimentary rock outcrops (Peters 2005). Recent studies with these methods strongly suggest that diversity has not increased unbounded through time; rather, diversity appears to be relatively constant for long periods of time, and there is little evidence for sustained increases in diversity. Alroy et al. (2008) re-analysed the marine invertebrate fossil record and found that, despite periodic diversity expansions, large expanses of time are characterized by no clear trend in diversity, including most of the Paleozoic and Cenozoic. Rabosky & Sorhannus (2009) used samplingstandardization methods to assess the diversity of marine diatoms across the Cenozoic and found no evidence for the explosive recent rise in diversity that had previously been proposed (Falkowski et al. 2004). Alroy (1996, 2009) showed that diversity trends in mammals across the Cenozoic cannot be explained by a stochastic random walk model and, in contrast, exhibits a relatively flat diversity trajectory consistent with ecological limits. This apparent limit on diversity was reached almost immediately after the mass extinction at the Cretaceous-Tertiary boundary. Clearly, periodic expansions of the biosphere have occurred over time (Valentine 1969), as illustrated by the increase in the number of ecological guilds in marine faunas during the Paleozoic (Bambach et al. 2007). But the overall pattern in the fossil record is more of diversity constancy than of unbounded increase (Ricklefs 2007), because such intermittent expansions are frequently accompanied by long periods of time with little net change in diversity. No relationship between clade age and species richness Perhaps the best evidence in favour of diversity regulation at the level of clades comes from the observation that, for many groups, there is no relationship between clade age and species richness (Ricklefs 2007, 2009). If clade diversity is generally increasing through time, then a positive relationship between age and diversity should be apparent (Fig. 1), even when clades themselves differ dramatically in their rates of diversification (Rabosky 2009). The lack of relationship between age and diversity is widespread, occurring across a range of taxa and temporal scales. Ricklefs (2006) found that tribes of passerine birds showed no relationship between age and diversity, but when several tribes were subdivided into younger constituent clades, diversity was positively related to age. An apparent logistic rise in diversity with clade age, as predicted by the ecological limits hypothesis (Fig. 1), is also observed among subclades of the Proteaceae that live in Mediterranean environments Log (species richness) Species (a) Clade age Species (b) Clade age (a) (b) (c) Time Clade age Figure 1 The relationship between clade age and species richness when diversity within clades is limited by ecological or other factors. Individual clades vary in age, with orange and purple clades being the oldest and youngest clades, respectively; and clades vary in diversification rate during the ÔgrowthÕ phase, where the slope of the log-diversity curve is proportional to the net rate of diversification. The relationship between clade age and species richness depends on our temporal frame of reference. If we observe a set of young clades undergoing exponential increase (a), we will note a positive relationship between clade age and species richness, even if diversification rates vary dramatically among clades (Rabosky 2009). When some clades have reached diversity limits and others continue to grow (b), an apparent logistic relationship between clade age and species richness will be noted. Finally, if diversity within clades is regulated, there will be no relationship between clade age and species richness. Most higher taxa that have been studied show age-diversity relationships consistent with (c). (Sauquet et al. 2009). Cardillo et al. (2005) found that the importance of diversification rate for the latitudinal gradient in avian species richness depended on clade age: while there appears to be a relationship between diversity and diversification rate in young clades, the relationship is much weaker in older clades, suggesting that they may already have reached limiting diversity levels or carrying capacity. For many other groups, no signal of increasing diversity with age is present. Diversity within these clades may be regulated at approximate constancy by a host of ecological factors. Although this is true for many old clades, such as squamate reptiles (Ricklefs et al. 2007), angiosperms (Magallon & Sanderson 2001), and teleost fish orders (Rabosky 2009), it is sometimes true for very young clades. These include cichlids within African rift lakes, which also lack a positive relationship between clade age and species diversity (Seehausen 2006). Despite a general lack of relationship with age, species richness is sometimes associated with the area of the biogeographic region in which clades have diversified (Ricklefs 2006; Ricklefs et al. 2007; Species (c)

4 738 D. L. Rabosky Idea and Perspective Rabosky 2009). Although some younger clades may show a positive age-diversity relationship (Wiens et al. 2006, 2009), most higher taxa which have been examined do not. Diversity-dependence of speciation and extinction Speciation and extinction rates frequently show evidence for diversity-dependence. This has long been proposed for paleontological data, where diversity often shows a ÔreboundÕ effect following mass extinction events (Erwin 1998; Sepkoski 1998). Foote (2000) and Alroy (2008) showed that this phenomenon is not limited to mass extinctions and that diversity-dependence of speciation and extinction are general processes that regulate the shapes of taxonomic diversity curves. By reconstructing speciation and extinction rates for marine invertebrates across the Phanerozoic, Alroy (2008) found that decreases in diversity were correlated with a drop in extinction rates immediately thereafter, and also that high extinction was associated with a spike in speciation during the next period in time. These general findings are not limited to the fossil record, and a number of studies with time-calibrated molecular phylogenies have demonstrated that speciation rates are often highest during the early stages of evolutionary radiations (McPeek 2008; Phillimore & Price 2008; Rabosky & Lovette 2008a). This pattern of temporally decelerating speciation during the course of clade radiation has been interpreted as diversity-dependence of speciation rates (Weir 2006; Phillimore & Price 2008; Rabosky & Lovette 2008b). ECOLOGICAL LIMITS ON DIVERSITY AND ISLAND RABBITS If clade diversity is regulated by ecological factors, this implies that species diversity can be independent of the rate of diversification of the clade. Moreover, the existence of such ecological limits suggests that it is not possible, even in principle, to use information on the age of clades and their standing (extant) diversities to estimate diversification rates. This is best illustrated by analogy. Imagine that a single pregnant rabbit was introduced to a small, rabbit-free island some 500 years before the present. Rabbits being rabbits, we might predict that this population would undergo an initial population explosion, ultimately reaching a semistable or oscillatory equilibrium diversity determined by resource availability, predation, and other factors. Suppose that a modern-day visitor to this island finds a census size of N = 1000 rabbits on our hypothetical island. Would it be appropriate to use this census population size to estimate the yearly number of births per individual rabbit? A simple estimator, based on these numbers, would lead to an estimate of r = log(1000) 500, or r = rabbits per year. This is nonsense, of course, because the population is at carrying capacity. Estimates of r in this case are based on a meaningless function of time: if we counted 1000 rabbits 50 years or 5000 years after introduction, we would obtain radically different estimates of r, despite the fact the population may have been approximately constant throughout that entire time. Only during the earliest phases of population expansion would there have been any causal relationship between individual reproductive rates and population size. It is certainly true that the population size at equilibrium depends on net rates of individual reproduction; were this not equal to zero, the population would either decrease or increase accordingly. However, the fact that net reproduction is zero is caused by the existence of ecological limits on population growth. No population ecologist would claim that Ôlow birth ratesõ are the explanation in any meaningful sense for the fact that our hypothetical island has a population size of merely 1000 rabbits after 500 years. If one accepts the idea that diversity limits on clades are possible, it is not difficult to extend the island rabbit analogy by substituting speciation, extinction, and clade for birth, death, and population. In this sense, the diversity of clades may be independent of both speciation and extinction rates; these parameters are only meaningful in the sense that they influence the rate at which clades approach equilibria or limiting diversities (Fig. 1). Likewise, a clade whose diversity is approximately constant in time provides information about the total net diversification that has occurred, but not necessarily about underlying rates of speciation and extinction. In the rabbit analogy, the existence of a carrying capacity led to the decoupling of population size and population age. In this same fashion, ecological limits on clade diversity imply a decoupling of clade age and species richness, and diversification estimates will vary arbitrarily with the point in time when we observe the clade (Fig. 1). Old clades will be inferred to have low diversification rates, and young clades will be inferred to have high diversification rates, even if both clades have had identical speciation and extinction rates throughout their history. This basic model need not be limited to clades and can apply to regional biotas, as regions might vary in their equilibrium diversities (Cardillo et al. 2005). Indeed, this is the basic assumption of the entire literature on nonevolutionary hypotheses for the latitudinal diversity gradient (Mittelbach et al. 2007). But the critical point is that if ecological limits on clade diversity exist and are realized, both clade age and diversification rate will provide incomplete and potentially misleading explanations for large-scale patterns of biological diversity (Fig. 1). Explaining the dramatic variation in species richness among clades and regions thus requires that we expand our inferential framework to encompass not only the factors that influence speciation and extinction but also those which affect

5 Idea and Perspective Diversification rate and ecological limits 739 ecological limits across a range of spatial and phylogenetic scales. TOTAL DIVERSIFICATION VS. DIVERSIFICATION RATE In concert with evidence from the fossil record, the lack of relationship between clade age and species richness in many groups of organisms suggests that clade diversity is regulated, in the sense that no net increase in diversity is occurring over time. This challenges what is perhaps the most fundamental assumption of many phylogenetic diversification studies, because diversification rates typically cannot be estimated from clade age and species richness data if diversity is not increasing through time. If clades are at equilibrium, a simple estimator of diversification based on log(n) t will be positively misleading: old and young clades with the same diversity will be inferred to have radically different diversification rates (Fig. 2), and neither of these estimated ÔratesÕ will necessarily have much to do with actual rates of speciation and extinction during either the initial period of diversity increase nor the subsequent diversity regulation phase when the net rate is effectively zero. (a) Log (species) (b) Rate estimate Time y x (c) Log (species) Time Figure 2 Limits on diversity can lead to positively misleading inferences about diversification rate when diversity is assumed to grow without bounds. (a) Two clades, x (black) and y (grey) grow with identical net diversification rates but different limiting values on diversity, or Ôcarrying capacitiesõ. (b) Net diversification rates estimated as log(n ) t for clades shown in (a) as a function of time. Even after both clades have reached their respective limits, clade y will always be inferred to have a higher net diversification rate than clade x. Arrows indicate the period of time for which inferences about diversification rate will be misleading. (c) Species richness for two clades with identical diversification-through-time curves that differ in clade age. The older clade reaches the limit first, but diversifies at precisely the same rate as the younger clade. (d) When diversification rates are estimated for the clades in (c), the younger clade is always inferred to have a higher diversification rate, despite no difference in the underlying rates of speciation and extinction. (d) Rate estimate A great number of studies have assessed the extent to which diversification rates vary across the tree of life (Davies et al. 2004; Hunt et al. 2007), as well as the relationship between species traits and diversification rates (Hodges & Arnold 1995; Adamowicz et al. 2008; Seddon et al. 2008). The central idea here is that, by estimating diversification rate as some function of extant diversity and clade age, we can derive insights into the manner in which speciation and extinction vary among clades and, importantly, how different traits alter speciation and extinction rates (Nee 2001; Coyne & Orr 2004; Jablonski 2008). But if diversity within clades is regulated, differences in diversity will be uncoupled from variation in speciation and extinction rates. This provides an immediate explanation for the widespread finding that younger clades typically appear to have higher diversification rates than older clades (Ricklefs 2006; McPeek & Brown 2007; Magallon & Castillo 2009). All clades may have undergone approximately the same total diversification and with precisely the same speciation and extinction rates, but if they vary in age, high rates will be estimated for young clades and low rates will be estimated for old clades (Fig. 2). I suggest that, if diversity is regulated, we cannot estimate diversification rate using clade age and species richness data. Rather, the best we can do is to estimate the total diversification that a clade has undergone, a quantity that I will denote by W. This is simply the time-integrated difference between speciation and extinction, or Z X ¼ ½kðÞ l t ðþ t Šdt ð1þ where k(t ) and l (t ) are speciation and extinction rates as functions of time. In general, the expected species richness for a simple diversification process is N ¼ e X ð2þ and thus, W can be estimated simply as the log of species richness. This estimator has the desirable property that, for clades that are no longer growing through time, W is independent of clade age. Of course, if diversity is still increasing within clades, then analyses of total diversification (W) will be based on the flawed assumption that diversity differences reflect variation in ecological limits or Ôcarrying capacityõ rather than diversification rate. Clearly, it will sometimes be more appropriate to estimate diversification rate as log(n) t rather than total diversification W, and some datasets may present a challenging mixture of clades with apparent equilibrium and non-equilibrium diversities (Cardillo et al. 2005; Sauquet et al. 2009). But which diversity model is best for a given analysis should be treated as a hypothesis to be tested; the evidence from molecular phylogenies and fossils

6 740 D. L. Rabosky Idea and Perspective overwhelmingly suggests that the absence of diversity limits cannot be assumed a priori. DIVERSITY LIMITS AND THE SPATIAL ORGANIZATION OF BIODIVERSITY There is now ample evidence that tropical and temperate clades might differ systematically in both age and rates of speciation and extinction (Mittelbach et al. 2007). Such variation in clade age with respect to latitude is a fundamental component of the tropical conservatism hypothesis for the latitudinal diversity gradient (Wiens & Donoghue 2004; Hawkins et al. 2007), which proposes that tropical clades are more diverse in part because of their greater age, or time for speciation (Stephens & Wiens 2003) relative to temperate clades. While many studies of latitudinal variation in diversification rates have implicitly assumed that diversity within clades is increasing through time, studies from the fossil record and recently diverged taxa should be relatively robust to violations of this assumption (Buzas et al. 2002; Allen & Gillooly 2006; Jablonski et al. 2006; Weir & Schluter 2007). However, if diversity within clades is regulated, then latitudinal gradients in both diversification rates and clade ages may have nothing to do with observed differences in diversity (Marshall 2007). For example, a finding that temperate clades are typically younger than tropical clades does not imply that age has been a causal factor in the latitudinal diversity gradient, if these clades differ systematically in carrying capacity. Yet it is straightforward to test, at least in broad outline, whether patterns of diversity conform to a model with or without ecological limits on species richness. In the context of the latitudinal diversity gradient, a first step would be to assess the relationship between clade age and species richness, controlling for latitude. If no such relationship exists, then it is difficult to see how either clade age or diversification rate could be the dominant factor underlying the latitudinal diversity gradient. While few studies have tackled this directly, this should be an important aspect of testing niche conservatism-based explanations for diversity gradients, because such models generally propose that species richness is a function of evolutionary time or clade age. Phylogenetic scale is of critical consideration here: nonequilibrial mechanisms will be of greater importance for younger clades, simply because they will be more likely to lie on the growth phase of the diversity curve (Fig. 1). The need to explore the intersection between diversification rate, clade age, and diversity limits is not limited to the latitudinal diversity gradient but applies to any large-scale spatial variation in species richness. The Australian deserts, for example, contain far more species of lizards than physiographically comparable regions in North America and Africa (Pianka 1986). Differences in both diversification rate (Pianka 1972) and time for diversification (Pianka 1986) have been proposed to explain this variation in species richness. Yet a critical piece in explaining this and other puzzling diversity contrasts (Latham & Ricklefs 1993; Cowling et al. 1996; Ellison et al. 1999) will be to test a basic prediction of the ecological limits model for clade diversity by assessing the relationship between clade age and species richness. SISTER CLADE CONTRASTS AND COMPARATIVE STUDIES OF DIVERSIFICATION Evolutionary studies of speciation and extinction from phylogenies are typically predicated on the assumption that differences in diversity, corrected for taxon age, reflect variation in net rates of species diversification. Contrasts between sister clades have been especially useful in this regard, because sister clades are by definition the same age. By comparing diversity differences across multiple sets of sister clades with respect to a trait of interest, it is possible to assess statistically whether a trait is associated with increased diversification (Mitter et al. 1988; Barraclough et al. 1995). Many studies have now demonstrated relationships between traits and diversity (reviewed in Coyne & Orr 2004). The standard interpretation of sister clade contrasts and other methods for inferring relationships between traits and diversification is that these methods can potentially reveal causal relationships between traits and diversification rates. These methods have been widely used to study the types of traits most likely to contribute directly to speciation, such as pollinator specificity in plants (Hodges & Arnold 1995; Kay et al. 2006), dispersal (Phillimore et al. 2006), and sexual selection in animal taxa (Coyne & Orr 2004). Yet a major alternative explanation is that traits influence the total diversification of clades (W) without directly affecting either speciation or extinction rates. For traits associated with reproduction, such as pollination mode and sexual selection, this may not be a particularly viable possibility. However, a number of ecological traits have been shown to covary with species richness, and for some of these, the effect of the trait on diversity may have more to do with ecological limits than speciation and extinction rates (Fig. 3). For example, acquisition of traits that increase the possible number of ecological niches might be expected to increase clade diversity; such traits might include phytophagy in insects (Mitter et al. 1988), angiosperm feeding in beetles (Farrell 1998), and host diversity in butterflies (Janz et al. 2006). This is not to suggest that these traits have not directly influenced speciation and extinction rates, but rather that their effects on ecological limits represent an equally viable alternative hypothesis that cannot be ruled out based on sister clade contrasts. This likewise applies to latitudinal contrasts in diversification rate (Cardillo 1999), where apparent relationships between latitude

7 Idea and Perspective Diversification rate and ecological limits 741 (a) Log (species) (b) Log (species) Time Figure 3 Clades can become exceptionally diverse through increases in the net rate of diversification (a), presumably through a decrease in extinction rates or an increase in speciation rates. Alternatively, clades may undergo an increase in the level at which diversity is regulated, equivalent to an increase in the Ôcarrying capacityõ for the clade (b). Note that in (a), diversity continues to increase with time, but diversity is independent of time in (b), once the clade has reached a hypothetical limit. Both intrinsic, lineagespecific traits as well as extrinsic environmental factors can influence diversification rates, ecological limits, or potentially some combination thereof. and diversification rate may arise solely as a result of correlations between W and latitude, with no dependency on underlying speciation and extinction rates. Can we distinguish between variation in diversification rates and variation in W in contrast-based analyses? This is not an insoluble problem. Consider a set of sister clades which differ in a trait of interest, such as degree of floral symmetry (Sargent 2004) or limb complexity (Adamowicz et al. 2008). If the effects of the trait are mediated by differential speciation and extinction (Fig. 3a), then the absolute difference in species richness between sister clades should be positively correlated with the age of their shared ancestor. Note that this is not true for the difference in logtransformed species richness, which is standard for diversity contrasts. If two clades differ in their rate of diversification and if diversity is not limited, then the absolute difference in diversity will continue to increase with time since divergence. In contrast, if a trait alters the level at which diversity is regulated (Fig. 3b), then the difference in diversity between sister clades will be independent of time. This suggests a simple test for sister-taxon comparisons, based on the ratio of (unlogged) sister clade diversities (N 1 N 2 ) and the age of their common ancestor. If the correlation between N 1 N 2 and clade age is positive, older sister clades show a greater disparity in diversity, consistent with the effects of a trait on speciation and or extinction rates. However, if the correlation is zero, it is more likely that the trait influences W rather than diversification rate. CONCLUSIONS I have argued that ecological limits represent an alternative interpretation for differences in species richness among clades and regions that is rarely acknowledged. At least within higher taxa, diversity generally appears to be regulated and shows little evidence for sustained increases through time. This poses a number of challenges for phylogenetic diversification studies, because the estimation of diversification rate from phylogenetic data typically assumes that there are no limits on diversity. Violation of this assumption has a number of consequences, but generally leads to diversification estimates that are confounded by differences in apparent carrying capacity (Fig. 2a) or by variation in clade age (Fig. 2b). I suggested that, when diversity is regulated at a more-or-less stable level, researchers should explore the causes of variation in total time-integrated diversification (W), rather than diversification rate. This is because diversity regulation implies that variation in species richness among clades is effectively decoupled from variation in diversification rates. This certainly does not negate the potential importance of differential speciation and extinction as causal explanations for variation in species richness. Intrinsic, lineage-specific traits can lead to contrasting patterns of species diversity via their effects on diversification rates (Fig. 3a), or by their effect on the ecological limits that appear to govern diversity dynamics across longer timescales (Fig. 3b). Likewise, temperature, energy, and other extrinsic factors can potentially influence both the rate of diversity accumulation through time as well as carrying capacities at regional and global scales (Hawkins et al. 2003; Davies et al. 2005; Evans & Gaston 2005). But additional analyses, such as those suggested for sister clades, will likely be needed in some cases to distinguish between these alternatives. Regardless, we cannot properly interpret diversification analyses until we have addressed the possibility of ecological limits on diversity. It will be exciting to see what we discover about the importance of factors that influence ecological limits relative to those that influence speciation and extinction in generating large-scale diversity patterns. ACKNOWLEDGEMENTS I thank I. Lovette, A. McCune and A. Agrawal for comments on the manuscript and discussion. This research was supported by NSF-DEB

8 742 D. L. Rabosky Idea and Perspective REFERENCES Adamowicz, S.J., Purvis, A. & Wills, M.A. (2008). Increasing morphological complexity in multiple parallel lineages of the Crustacea. Proc. Natl Acad. Sci. USA, 105, Allen, A.P. & Gillooly, J.F. (2006). Assessing latitudinal gradients in speciation rates and biodiversity at the global scale. Ecol. Lett., 9, Alroy, J. (1996). Constant extinction, constrained diversification, and uncoordinated stasis in North American mammals. Palaeogeogr. Palaeoclimatol. Palaeoecol., 127, Alroy, J. (2008). The dynamics of origination and extinction in the marine fossil record. Proc. Nat. Acad. Sci. USA, 105, Alroy, J. (2009). Speciation and extinction in the fossil record of North American mammals. In: Ecology and Speciation (eds Butlin, R., Bridle, J. & Schluter, D.). Cambridge University Press, Cambridge, pp Alroy, J., Aberhan, M., Bottjer, D.J., Foote, M., Fürsich, F.T., Harries, P.J. et al. (2008). Phanerozoic trends in the global diversity of marine invertebrates. Science, 321, Bambach, R.K., Bush, A.M. & Erwin, D.H. (2007). Autecology and the filling of ecospace: key metazoan radiations. Palaeontology, 50, Barraclough, T.G., Harvey, P.H. & Nee, S. (1995). Sexual selection and taxonomic diversity in passerine birds. Proc. R. Soc. Lond. B Biol. Sci., 259, Benton, M.J. (2009). The red queen and the court jester: species diversity and the role of biotic and abiotic factors through time. Science, 323, Buzas, M.A., Collins, L.S. & Culver, S.J. (2002). Latitudinal difference in biodiversity caused by higher tropical rate of increase. Proc. Natl Acad. Sci. USA, 99, Cardillo, M. (1999). Latitude and rates of diversification in birds and butterflies. Proc. R. Soc. Lond. B Biol. Sci., 266, Cardillo, M., Orme, C.D.L. & Owens, I.P.F. (2005). Testing for latitudinal bias in diversification rates: an example using new world birds. Ecology, 86, Chesson, P. (2000). Mechanisms of maintenance of species diversity. Annu. Rev. Ecol. Syst., 31, Connolly, S.R. & Miller, A.I. (2001). Joint estimation of sampling and turnover rates from fossil databases: capture-mark-recapture methods revisited. Paleobiology, 27, Cowling, R.M., Rundel, P.W., Lamont, B.B., Arroyo, M.K. & Arianoutsou, M. (1996). Plant diversity in Mediterranean-climate regions. Trends Ecol. Evol., 11, Coyne, J. & Orr, H. (2004). Speciation. Sinauer, Sunderland, MA. Davies, T.J., Barraclough, T.G., Chase, M.W., Soltis, P.S., Soltis, D.E. & Savolainen, V. (2004). DarwinÕs abominable mystery: insights from a supertree of the angiosperms. Proc. Natl Acad. Sci. USA, 101, Davies, T.J., Savolainen, V., Chase, M.W., Goldblatt, P. & Barraclough, T.G. (2005). Environment, area, and diversification in the species-rich flowering plant family Iridaceae. Am. Nat., 166, Ellison, A.M., Farnsworth, E.J. & Merkt, R.E. (1999). Origins of mangrove ecosystems and the mangrove biodiversity anomaly. Global. Ecol. Biogeogr., 8, Erwin, D.H. (1998). The end and the beginning: recoveries from mass extinctions. Trends Ecol. Evol., 13, Evans, K.L. & Gaston, K.J. (2005). Can the evolutionary-rates hypothesis explain species-energy relationships? Funct. Ecol., 19, Falkowski, P.G., Katz, M.E., Knoll, A.H., Quigg, A., Raven, J.A., Schofield, O. et al. (2004). The evolution of modern eukaryotic phytoplankton. Science, 305, Farrell, B.D. (1998). Inordinate fondness explained: why are there so many beetles? Science, 281, Fischer, A.G. (1960). Latitudinal variations in organic diversity. Evolution, 14, Foote, M. (2000). Origination and extinction components of taxonomic diversity: paleozoic and post-paleozoic dynamics. Paleobiology, 26, Hawkins, B.A., Field, R., Cornell, H.V., Currie, D.J., Guegan, J.F., Kaufman, D.M. et al. (2003). Energy, water, and broadscale geographic patterns of species richness. Ecology, 84, Hawkins, B.A., Diniz- Filho, J.A.F., Jaramillo, C.A. & Soeller, S.A. (2007). Climate, niche conservatism, and the global bird diversity gradient. Am. Nat., 170, S16 S27. Hillebrand, H. (2004). On the generality of the latitudinal diversity gradient. Am. Nat., 163, Hodges, S.A. & Arnold, M.L. (1995). Spurring plant diversification: are floral nectar spurs a key innovation? Proc. R. Soc. Lond. B Biol. Sci., 262, Hunt, T., Bergsten, J., Levkanicova, Z., Papadopoulou, A., John, O.S., Wild, R. et al. (2007). A comprehensive phylogeny of beetles reveals the evolutionary origins of a superradiation. Science, 318, Hutchinson, G.E. (1959). Homage to santa rosalia. Am. Nat., 93, Jablonski, D. (2008). Species selection: theory and data. Annu. Rev. Ecol. Evol. Syst., 39, Jablonski, D., Roy, K. & Valentine, J.W. (2006). Out of the tropics: evolutionary dynamics of the latitudinal diversity gradient. Science, 314, Janz, N., Nylin, S. & Wahlberg, N. (2006). Diversity begets diversity: host expansions and the diversification of plant-feeding insects. BMC Evol. Biol., 6, e4. Johnson, M.T.J. & Stinchcombe, J.R. (2007). An emerging synthesis between community ecology and evolutionary biology. Trends Ecol. Evol., 22, Kay, K., Voelckel, C., Yan, J., Hufford, K., Kaska, D. & Hodges, S.A. (2006). Floral characters and species diversification. In: Ecology and Evolution of Flowers (eds Harder, L. & Barrett, S.). Oxford University Press, Oxford, pp Latham, R.E. & Ricklefs, R.E. (1993). Global patterns of tree species richness in moist forests energy-diversity theory does not account for variation in species richness. Oikos, 67, Losos, J.B. & Schluter, D. (2000). Analysis of an evolutionary species-area relationship. Nature, 408, Maddison, W.P., Midford, P.E. & Otto, S.P. (2007). Estimating a binary characterõs effect on speciation and extinction. Syst. Biol., 56, Magallon, S. & Castillo, A. (2009). Angiosperm diversification through time. Am. J. Bot., 96, Magallon, S. & Sanderson, M.J. (2001). Absolute diversification rates in angiosperm clades. Evolution, 55, Marshall, C.R. (2007). Explaining latitudinal diversity gradients. Science, 317,

9 Idea and Perspective Diversification rate and ecological limits 743 McPeek, M.A. (2008). Ecological dynamics of clade diversification and community assembly. Am. Nat., 162, E270 E284. McPeek, M.A. & Brown, J.M. (2007). Clade age and not diversification rate explains species richness among animal taxa. Am. Nat., 169, E97 E106. Miller, A.I. & Foote, M. (1996). Calibrating the ordovician radiation of marine life: implications for phanerozoic diversity trends. Paleobiology, 22, Mittelbach, G.G., Schemske, D.W., Cornell, H.V., Allen, A.P., Brown, J.M., Bush, M.B. et al. (2007). Evolution and the latitudinal diversity gradient: speciation, extinction and biogeography. Ecol. Lett., 10, Mitter, C., Farrell, B. & Wiegmann, B. (1988). The phylogenetic study of adaptive zones has phytophagy promoted insect diversification? Am. Nat., 132, Mooers, A.O. & Heard, S.B. (1997). Evolutionary process from phylogenetic tree shape. Q. Rev. Biol., 72, Nee, S. (2001). Inferring speciation rates from phylogenies. Evolution, 55, Nee, S. (2006). Birth-death models in macroevolution. Annu. Rev. Ecol. Evol. Syst., 37, Nee, S., May, R.M. & Harvey, P.H. (1994). The reconstructed evolutionary process. Philos. Trans. R. Soc. London, 344, Paradis, E. (2005). Statistical analysis of diversification with species traits. Evolution, 59, Peters, S.E. (2005). Geologic constraints on the macroevolutionary history of marine animals. Proc. Natl Acad. Sci. USA, 102, Phillimore, A.B. & Price, T.D. (2008). Density dependent cladogenesis in birds. PLoS Biol., 6, e71. Phillimore, A.B., Freckleton, R.P., Orme, C.D.L. & Owens, I.P.F. (2006). Ecology predicts large-scale patterns of phylogenetic diversification in birds. Am. Nat., 168, Pianka, E.R. (1972). Zoogeography and speciation of Australian desert lizards ecological perspective. Copeia, 1972, Pianka, E.R. (1986). Ecology and Natural History of Desert Lizards. Princeton University Press, Princeton, NJ. Rabosky, D.L. (2009). Ecological limits on clade diversification in higher taxa. Am. Nat., 173, Rabosky, D.L. & Lovette, I.J. (2008a). Density dependent diversification in North American wood warblers. Proc. R. Soc. Lond. B Biol. Sci., 275, Rabosky, D.L. & Lovette, I.J. (2008b). Explosive evolutionary radiations: decreasing speciation or increasing extinction through time? Evolution, 62, Rabosky, D.L. & Sorhannus, U. (2009). Diversity dynamics of marine planktonic diatoms across the Cenozoic. Nature, 457, Rabosky, D.L., Donnellan, S.C., Talaba, A.L. & Lovette, I.J. (2007). Exceptional among-lineage variation in diversification rates during the radiation of AustraliaÕs most diverse vertebrate clade. Proc. R. Soc. Lond. B Biol. Sci., 274, Raup, D.M. (1972). Taxonomic diversity during the Phanerozoic. Science, 177, Ricklefs, R.E. (2004). A comprehensive framework for global patterns in biodiversity. Ecol. Lett., 7, Ricklefs, R.E. (2006). Global variation in the diversification rate of passerine birds. Ecology, 87, Ricklefs, R.E. (2007). Estimating diversification rates from phylogenetic information. Trends Ecol. Evol., 22, Ricklefs, R.E. (2009). Speciation, extinction, and diversity. In: Ecology and Speciation (eds Butlin, R., Bridle, J. & Schluter, D.). Cambridge University Press, pp Ricklefs, R.E., Losos, J.B. & Townsend, T.M. (2007). Evolutionary diversification of clades of squamate reptiles. J. Evol. Biol., 20, Sargent, R.D. (2004). Floral symmetry affects speciation rates in angiosperms. Proc. R. Soc. Lond. B Biol. Sci., 271, Sauquet, H., Weston, P.H., Anderson, C.L., Barker, N.P., Cantrill, D.J., Mast, A.R. et al. (2009). Contrasted patterns of hyperdiversification in Mediterranean hotspots. Proc. Natl Acad. Sci. USA, 106, Seddon, N., Merrill, R.M. & Tobias, J.A. (2008). Sexually selected traits predict patterns of species richness in a diverse clade of suboscine birds. Am. Nat., 171, Seehausen, O. (2006). African cichlid fish: a model system in adaptive radiation research. Proc. R. Soc. Lond. B Biol. Sci., 273, Sepkoski, J.J. (1978). A kinetic-model of phanerozoic taxonomic diversity. 1. Analysis of marine orders. Paleobiology, 4, Sepkoski, J.J. (1984). A kinetic-model of phanerozoic taxonomic diversity. 3. Post-paleozoic families and mass extinctions. Paleobiology, 10, Sepkoski, J.J. (1998). Rates of speciation in the fossil record. Philos. Trans. R. Soc. Lond. B Biol. Sci., 353, Silvertown, J. (2004). Plant coexistence and the niche. Trends Ecol. Evol., 19, Stephens, P.R. & Wiens, J.J. (2003). Explaining species richness from continents to communities: the time-for-speciation effect in emydid turtles. Am. Nat., 161, Valentine, J.W. (1969). Patterns of taxonomic and ecological structure of the shelf benthos during Phanerozoic time. Paleontology, 12, Webb, C.O., Ackerly, D.D., McPeek, M.A. & Donoghue, M.J. (2002). Phylogenies and community ecology. Annu. Rev. Ecol. Evol. Syst., 33, Weir, J.T. (2006). Divergent timing and patterns of species accumulation in lowland and highland neotropical birds. Evolution, 60, Weir, J.T. & Schluter, D. (2007). The latitudinal gradient in recent speciation and extinction rates of birds and mammals. Science, 315, Wiens, J.J. & Donoghue, M.J. (2004). Historical ecology, biogeography, and species richness. Trends Ecol. Evol., 19, Wiens, J.J., Graham, C.H., Moen, D.S., Smith, S.A. & Reeder, T.W. (2006). Evolutionary and ecological causes of the latitudinal diversity gradient in hylid frogs: treefrog trees unearth the roots of high tropical diversity. Am. Nat., 168, Wiens, J.J., Sukumaran, J., Pyron, R.A. & Brown, R.A. (2009). Evolutionary and biogeographic origins of high tropical diversity in old world frogs (Ranidae). Evolution, 63, Editor, Paul Rainey Manuscript received 14 March 2009 First decision made 21 April 2009 Manuscript accepted 6 May 2009