Underlying the diversity trajectory are several significant transitions in the taxonomic compositions of marine bio- tas; a snorkelling excursion over a Palaeozoic seafloor would have revealed a seemingly alien world. Applying multivariate statistical analyses of diversity patterns within clades, Sepkoski (1981) recognised three Phanerozoic ‘evolutionary faunas’, each characterised by distinct taxonomic classes (Figure 1): the trilobite-rich Cambrian fauna, which dominated Cambrian seas, but declined in diversity thereafter; the Palaeozoic fauna, rich in articulate brachiopods, stalked crinoids, stenolaemate bryozoans and tabulate and rugose corals, which diversified dramatically during the Ordovician radiation and characterised seafloors for the remainder of the Palaeozoic; and the Modern fauna, dominated by gastropods, bivalves, crustaceans, echinoids, gymnolaemate bryozoans and fish, which also underwent an initial radiation early in the Palaeozoic, but diversified much more appreciably in the post-Palaeozoic, far outstripping the diversity levels of earlier evolutionary faunas. Terrestrial diversity
Extreme estimates of modern terrestrial diversity can be up to 25 times greater than estimates of current marine diversity (Benton, 2001). The bulk of this diversity is made up of insects, nematodes and plants, but also important are vertebrates. Early on, patterns of terrestrial diversity where tabulated in much the same way as it is in the marine realm – by counting up the number of taxa that occurred in each interval in the past. More recently, however, terrestrial diversity has been estimated largely using phylogenetic methods. This works largely by extending ranges back in time from the observed fossil occurrences to the maximum extent predicted by phylogenetic relationships, assuming that sister taxa have the same time of origin (Norell and Novacek, 1992).
Benton (Benton, 2001; Benton and Emerson, 2007) maintains that patterns of terrestrial diversity are distinctly different from the marine realm. On land, diversity increases considerably faster than in the sea; diversification begins much later in history on land and possibly a larger number of species exist there today. This is undoubtedly true, but in addition, he finds this pattern sufficient evidence for unconstrained diversification in terrestrial organisms. If we consider the lessons learned about the influence of the Pull of the Recent in the marine taxa, there is reason not to take the long-term exponential increase observed in terrestrial datasets at face value. Logistic growth with maximum diversification early and flattening thereafter is also expected on land when counting and sampling methods are applied rigorously.
Diversity patterns of major groups
Vertebrate diversity analyses at the family level is high- lighted by several notable transitions: among fish, a Palaeozoic biota gave way in the late Mesozoic and Cenozoic to an assemblage dominated by teleosts; in the terrestrial realm, the initial, mid-Palaeozoic domination by amphibians was followed in the late Palaeozoic and, especially, the Mesozoic by an increased diversity of reptiles; the Cenozoic was highlighted by significant radiations of mammals and birds, which achieved diversity levels far in excess of other vertebrate classes (Figure 2b).
Most vertebrate-wide diversity data are restricted to raw data of age ranges for families. Sampling-standardised diversity patterns have been constructed for mammals and dinosaurs. As in the marine diversity curve, the major biological signal in John Alroy’s mammalian curve is its only modest increase in diversity over time (Alroy, 2009). The subsampled diversity curve of dinosaurs (Lloyd et al., 2008) is also quite stable over time. However, if dinosaur diversity is instead measured phylogenetically a 7-fold increase in species richness is observed, but most of the change in diversity is concentrated early in dinosaur history
There are a shockingly large number of beetle species today. And they are just a part of the approximately 9000000 insect species estimated to be extant (Benton, 2001). The family-level diversity curve for insects (Benton, 1993) shows their remarkable diversification (Figure 2c). Interestingly, it is the low extinction rates of insect families that underpin their high diversity (Labandeira and Sep- koski, 1993).
The broad outlines of Phanerozoic floral diversity, described in a series of publications by Karl Niklas (e.g. Niklas, 1997), reveal that the majority of Phanerozoic plant species can be classified into three sequential groups: pteridophytes (e.g. ferns, lycopods and sphenopsids), which dominated floral assemblages of the Palaeozoic; gymnosperms (e.g. pines and conifers), which became increasingly diverse during the Mesozoic; and angiosperms (flowering plants), which first radiated during the Cretaceous period and became the most diverse of the three groups during the Cenozoic. Unfortunately, there is a dearth of recent work on patterns of plant diversity. In Figure 2d, we plot family-level diversity for land plants, based on the compilation of Benton (1993).
What Causes Global-Scale Biotic Transitions?
One aspect common to marine and terrestrial diversity curves is the sequential domination by different groups over time. Even if the dramatic Cenozoic increases depicted in the vertebrate and plant graphs prove to be due to similar sampling artefacts that influence the shape of the marine curve, the underlying transitions in biotic composition exhibited in all three cases are probably real. The obvious question is, what caused them? Most proposed answers lie somewhere on a continuum between purely abiotic and purely biotic causes. At one end of this spectrum are explanations that invoke global-scale competition among groups, with one group out-competing another over the long term and ultimately supplanting it. At the other end are suggestions that global-scale transitions have little to do with long-term competitive advantages but, rather, result from ‘chance’ events that induce mass extinctions and decimate incumbent groups, thereby emptying eco- space worldwide and providing opportunities for the diversification of new groups. Although a dispassionate look at the geometries of diversity increase and decrease exhibited by two groups under comparison should differentiate between such alternatives, in reality, nearly every major biotic transition remains contentious. Two classic examples are the marine transition from articulate brachiopods (major elements of the Palaeozoic evolutionary fauna) to bivalve molluscs (‘clams’; important constituents of the Modern evolutionary fauna), and the terrestrial transition from dinosaurs to mammals. In both cases, arguments continue about whether clams were competitively superior to brachiopods or mammals to dinosaurs. That each transition is closely associated in time with a mass extinction – the end-Permian event in the case of brachiopods versus clams and the end-Cretaceous extinction in the case of dinosaurs versus mammals – has obviously motivated the counterargument that mass extinctions played more than passing roles in both transitions.
Limits to Diversity – Equilibrium and Expansion Models
What governs the shape of the overall diversity trajectory throughout the Phanerozoic? Early in the history of diversification of marine organisms, there was an initial phase during which diversity increased rapidly (Figure 1, Figure 2a, and Figure 3). This was followed by an interval during which diversity stabilised. It is perhaps not surprising that this should be the case: the Earth offers a finite amount of ecospace, and it is logical that the world should eventually fill up with organisms, thereby inhibiting further diversification unless major evolutionary innovations allow conquering new ecospace. In fact, the body of theory related to the colonisation and eventual biological saturation of newly emergent islands supports this view (e.g. MacArthur and Wilson, 1967). As diversity increases, the rate of origination should decrease and the rate of extinction should increase; eventually, the two rates should counterbalance one another, resulting in the achievement of equilibrium diversity. Under these conditions, the pat- tern of diversity over time can be modelled with a logistic equation. After an initial phase of exponential growth, diversity will slow down as an upper limit of diversity is reached. The final diversity pattern has a sigmoidal shape. The role, if any, of equilibrium models in producing the observed diversity pattern has been contentious, with three different models figuring prominently.
Analyses of raw data have been used to variously argue for equilibrium and expansion models. Publication of the Paleobiology Database diversity curve (Alroy et al., 2008) and the associated development of counting methods and sampling-standardised analyses require revisiting these issues. The new curve, with its 2-fold increase in diversity over time, has rekindled efforts to find equilibrium dynamics and any diversity dependence that could generate them (Alroy, 2008; Aberhan and Kiessling, 2010). Alroy found that diversity in an interval of time is positively correlated with extinction rates in the next interval and that a high extinction rate in one interval is often followed by a high origination rate in the next interval.
Additional insight into the relative frequency of equilibrium and expansion models has come out of recent work on time-calibrated molecular phylogenies (McPeek, 2008; Rabosky, 2009a, b; Rabosky and Lovette, 2008). McPeek showed that out of 245 molecular phylogenies ranging across various taxa of plants, vertebrates, insects and molluscs, a majority show evidence for a decline in diversification. Only a small minority of cases show accelerating lineage diversification. If these results turn out to be robust, then this new evidence – independent from the fossil record – clearly favours some form of equilibrium model. As John Alroy (2009) puts it ‘Thus, the open issue is not whether limits exist, but rather whether they are approached quickly on a geological time scale’.
Local and Regional Patterns
Any variation in global diversity must be manifested at smaller scales, either in variations of diversity on the level of communities or in biogeographic regions. For example, an increase of global diversity could be achieved by higher species packing within communities, greater differences in taxonomic composition along environmental gradients or a greater number of or greater difference among bio- geographic regions. Several studies of long-term trajectories of marine within-community (alpha) diversity have established that there is evidence for increase. The earliest such study by Richard Bambach (1977) used raw species numbers and concluded that alpha diversity has increased 3-fold since the Early Palaeozoic in open marine environments. A more rigorous approach was forwarded by Wagner and col- leagues in 2006. Rather than analysing simple diversity metrics, the authors looked at rank-abundance distributions and found that there was just one major change in the community structure during the Phanerozoic, coinciding with the end-Permian mass extinction. Wagner et al. (2006) distinguished ecologically simple communities that follow a geometric series in a rank-abundance plot from ecologically complex communities, which exhibit a log-normal distribution. They found that simple and complex communities were about equally common in the Palaeozoic but complex communities dominated by far in younger communities. Because complex communities can maintain much greater species packing than simple communities, there is now good evidence for an abrupt increase of alpha diversity in the Triassic period.
Patterns of between-community (beta) diversity are less well constrained. There are indications that increasing specialisation of taxa during the Ordovician radiation led to greater beta diversity along environmental gradients (Sepkoski, 1988), but there was apparently little net increase thereafter. A recent analysis of beta diversity through the entire Phanerozoic has shown great variability without an underlying trend (Aberhan and Kiessling, 2010). A similar pattern is evident at the level of bio- geographic disparity. Arnold Miller et al. (2009) have shown that there is no evidence for increasing marine provincialism through time. Faunal differences among equal-distance grids were as pronounced in the Early Palaeozoic as they are today.
Sources of Biodiversity
New taxa are thought to first evolve in fairly localised regions because speciation is largely a process involving the subdivision of the ancestral species. Jablonski and others (Jablonski, 1993; Jablonski and Bottjer, 1991; Jablonski et al., 1983) first described the pattern that new orders tend to originate nearshore and in the tropics. At lower taxonomic levels, Jablonski et al. (2006) showed that new genera of marine bivalves tend to originate in the tropics before expanding out to higher latitudes. The causes of these geographical patterns are thought to be caused by physical disturbance, energy availability and biotic interactions (Jablonski et al., 2006; Valentine et al., 2008; Willig et al., 2003). Recently, Kiessling et al. (2010) explicitly tested several possible hypotheses about the environmental location of the biodiversity cradle. They found that nearshore, tropical and carbonate environments are all common cradles. But more importantly, it was reef habitats, which are a combination of all three environmental parameters, where the origin of genera was concentrated.
There are several intervals of global diversity increase depicted in Figure 1, Figure 2 and Figure 3 that could rightly be viewed as radiations. These include the so-called Cambrian explosion and Ordovician radiation of marine animals, which are most appropriately viewed as two unique intervals, rather than as a single Early Palaeozoic diversification; the post-Palaeozoic expansion of the Modern Evolutionary Fauna following the end-Permian mass extinction; the first major diversification of land plants in the Devonian; the subsequent radiations of gymnosperms in the mid- to late Palaeozoic and angiosperms in the Cretaceous and Cenozoic; the diversification of several different kinds of fish in the Devonian and the later, more extensive, radiation of teleosts; the colonisation of land by vertebrates, followed by a major radiation of tetrapods; and the Cenozoic radiations of mammals and birds, which achieved diversity levels far in excess of their Mesozoic numbers.
Each of these radiations was characterised by, and contingent on, certain unique parameters. For example, while the precise reason(s) for the Cambrian explosion remain open to debate, the palette of likely explanations (e.g. the crossing of a threshold level of oxygen in the atmosphere or a sudden increase in the complexity of Hox genes) were important uniquely to the biological and physical attributes of the Neoproterozoic through Early Cambrian interval and probably had little relevance, say, to the Cenozoic radiations of birds and mammals.
Nevertheless, this review suggests that there are macro- evolutionary themes relevant to all global radiations. These include a spectrum of possible prerequisites to radiation: the evolutionary advent of key morphological innovations; the competitive superiority of the diversifying biota relative to the incumbents that were supplanted or replaced; the removal of incumbents through extinction and the resultant emptying of ecospace; and ‘random chance’. In a given case, any, all or none of these factors may prove to be of importance.
These themes remind us that, in reconstructing the history of life, it is important to look beyond what is unique to single events and to search for general macroevolutionary ‘laws’. Perhaps more than anything else, the study of the diversity of life through time is emblematic of this quest.
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