Diversity Partitioning During the Cambrian Radiation

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Diversity partitioning during the Cambrian radiation

Lin Naa,1 and Wolfgang Kiesslinga,b

aGeoZentrum Nordbayern, Paleobiology and Paleoenvironments, Friedrich-Alexander-Universität Erlangen-Nürnberg, 91054 Erlangen, Germany; and bMuseum für Naturkunde, Leibniz Institute for Research on Evolution and Biodiversity at the Humboldt University Berlin, 10115 Berlin, Germany

Edited by Douglas H. Erwin, Smithsonian National Museum of Natural History, Washington, DC, and accepted by the Editorial Board March 10, 2015 (received for review January 2, 2015)

The fossil record offers unique insights into the environmental and Results geographic partitioning of biodiversity during global diversifica- Raw gamma diversity exhibits a strong increase in the first three tions. We explored biodiversity patterns during the Cambrian Cambrian stages (informally referred to as early Cambrian in this radiation, the most dramatic radiation in Earth history. We as- work) (Fig. 1A). Gamma diversity dropped in Stage 4 and de- sessed how the overall increase in global diversity was partitioned clined further through the rest of the Cambrian. The pattern is between within-community (alpha) and between-community (beta) robust to sampling standardization (Fig. 1B) and insensitive to components and how beta diversity was partitioned among environ- including or excluding the archaeocyath sponges, which are po- ments and geographic regions. Changes in gamma diversity in the tentially oversplit (16). Alpha and beta diversity increased from Cambrian were chiefly driven by changes in beta diversity. The the Fortunian to Stage 3, and fluctuated erratically through the combined trajectories of alpha and beta diversity during the initial following stages (Fig. 2). Our estimate of alpha (and indirectly diversification suggest low competition and high predation within beta) diversity is based on the number of genera in published communities. Beta diversity has similar trajectories both among fossil collections and, thus, may be affected by monographic environments and geographic regions, but turnover between adja- biases. However, the same basic pattern is seen in diversity es- cent paleocontinents was probably the main driver of diversification. timates of paleocommunities with abundance data (Fig. S1). Our study elucidates that global biodiversity during the Cambrian Beta diversity can be biased by the variation of geographic radiation was driven by niche contraction at local scales and clustering among sites over time. Therefore, we test the corre- vicariance at continental scales. The latter supports previous argu- lation between the median paleogeographic distance of collec- ments for the importance of plate tectonics in the Cambrian radiation, tions and beta diversity, as well as between the median distance namely the breakup of Pannotia. of grid centroids and beta diversity. There is no significant correlation in both cases (median distance between collections/beta: Cambrian radiation | alpha diversity | beta diversity | low competition | ρ = 0.1, P = 0.727; median distance between grid centroids/beta: Pannotia ρ = −0.24, P = 0.418), implying that geographic clustering does not cause a significant bias. hittaker (1) decomposed regional (gamma) diversity into Mass extinctions may affect diversity at multiple levels. Several Wlocal (alpha) and turnover (beta) components. Although episodes of profound turnover and mass extinction have been this concept is widely used and the principal levels of biodiversity noted at the Ediacaran-Cambrian boundary and throughout the are well explored in time and space, there are few analyses on the Cambrian (17, 18). Our sampling-standardized analysis confirms relationship of alpha and beta diversity in deep time during major high extinction rates throughout the Cambrian (Fig. 3). There is evolutionary radiations. The potential of Whittaker’sconceptto no significant correlation between extinction rates and either provide insights into evolutionary processes has been demon- alpha or beta diversity (extinction rate/alpha: ρ = −0.35, P = strated in a few paleobiologic studies (e.g., refs. 2 and 3). The 0.266; extinction rate/beta: ρ = 0.287, P = 0.366), indicating that question as to how the Cambrian radiation was partitioned within the observed extinctions are unlikely to introduce a substantial and between communities is old (4), and not resolved. The bias on alpha-beta-gamma diversity patterns. Cambrian Explosion has been characterized as the rapid increase of both biodiversity and morphological disparity (5–7). Significance The causes of this unique evolutionary radiation have been suggested to be abiotic (8), ecologic (9, 10), and genetic (5, 11) Many mechanisms of the Cambrian Explosion have been pro- factors and their complex interplay (12, 13). Here, we derive po- posed, but rigorous quantitative analyses of biodiversity dy- tential triggers of the Cambrian radiation from the way diversity namics are scarce, although they may shed light on important was partitioned geographically and environmentally during the main factors. Using a comprehensive database and sampling stan- diversification phase. dardization, we dissect global diversity patterns. The trajectories We use sampling-standardized analyses of fossil occurrence of within-community, between-community, and global diversity data from the Paleobiology Database to derive accurate time during the main phase of the Cambrian radiation revealed a low- series of alpha, beta, and gamma diversity from the Ediacaran competition model, which was probably governed by niche into the earliest Ordovician. Gamma diversity is understood as contraction and the increase of predation at local scales. At global genus richness, whereas beta diversity is used to characterize continental scales, the increase of beta diversity was controlled turnover between individual assemblages as well as depositional Materials and Methods by the high rate of community turnover among adjacent con- environments or geographic areas ( ). We test tinents. This finding supports the general importance of plate whether the Cambrian increase in gamma diversity was preferen- tectonics in large-scale diversifications. tially governed by beta or alpha diversity. We also separated environmental and geographic beta to identify the main driver of beta Author contributions: L.N. and W.K. designed research, performed research, analyzed diversity. Environmental beta measures faunal dissimilarity between data, and wrote the paper. different habitats, whereas geographic beta (also termed geodis- The authors declare no conflict of interest. parity; ref. 14) measures faunal dissimilarity between different This article is a PNAS Direct Submission. D.H.E. is a Guest Editor invited by the Editorial geographic regions. The relationship of alpha and beta diversity Board. during the main diversification interval in the early Cambrian is 1To whom correspondence should be addressed. Email: [email protected]. assessed as a function of global diversity, which can elucidate This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. underlying processes (15). 1073/pnas.1424985112/-/DCSupplemental.

4702–4706 | PNAS | April 14, 2015 | vol. 112 | no. 15 www.pnas.org/cgi/doi/10.1073/pnas.1424985112 Downloaded by guest on September 27, 2021 geographic distance (Table S1), and this spatial interval is the distance typically measured between adjacent paleo-continents in the early Cambrian (Fig. S4). Plate-tectonic configuration in the early Cambrian is poorly constrained (20), but the Neoproterozoic formation of Gondwana is well established (21, 22). Beta diversity within Gondwana shows more muted fluctuations than global beta diversity. Subtracting the global beta from Gondwana beta reveals a major increase in Stage 3 (Fig. S5). Because this increase is con- current with the main increase of gamma diversity, geodisparity appears to be the main driver of the Cambrian diversity peak. Finally, although we binned all fossil collections into the cur- rently recognized Ediacaran assemblages and Cambrian stages (Materials and Methods), the Cambrian timescale remains in flux (e.g., ref. 23). This problem raises the question whether our results might change with further revisions of the timescale. We therefore tested how the changes in international correlations and calibrations over the last 20 y have affected the basic results. Binning our data to the traditional Siberian subdivision of the Early Cambrian and lumping all Ediacaran assemblages, as well as Middle and Late Cambrian stages (24), shows some differ- ences such as an extended peak in gamma diversity in the Atdabanian and Botomian, but the basic patterns are robust Fig. 1. Global genus-level diversity of marine animals from the Ediacaran to (Fig. S6): Gamma diversity peaked in the late Early Cambrian, the earliest Ordovician. (A) Raw counts of the number of genera (sampled- alpha diversity exhibits a profound increase until the Atdabanian, in-bin). Note log scale of y axis. (B) Sampling-standardized genus-level di- and beta diversity lagged behind alpha diversity in the earliest versity (sampled-in-bin) based on shareholder quorum subsampling with 70% frequency coverage per stage. The brown line refers to all marine Cambrianandthencaughtup. genera, and the blue line excludes archaeocyaths. Ma, million years ago. Discussion Ava, Avalon assemblage; Dru, Drumian; For, Fortunian; Guz, Guzhangian; Jia, Jiangshanian; Nam, Nama assemblage; Pai, Paibian; St2, Stage 2; St3, Although a surprising diversity of benthic organisms is now known Stage 3; St4, Stage 4; St5, Stage 5; St10, Stage 10; Tre, Tremadocian (Ordo- from the Ediacaran (7), diversity was substantially lower at the vician) Whs, White Sea assemblage. gamma and alpha level than in the Cambrian (Figs. 1 and 2). The high taxonomic turnover recognized at the Ediacaran-Cambrian transition (Fig. 3) that marks the disappearance of Ediacaran We find a strong correlation between global genus richness soft-bodied organisms may be tempered by secular variation in and beta diversity (ρ = 0.93, P < 0.001), whereas there is no global taphonomic regimes (25), but can also be attributed to significant correlation between global genus richness and alpha ecosystem engineering and predation (26). Environmental per- diversity (ρ = 0.42, P = 0.137). The same relationship is evident turbations were invoked to explain the extinction of the few with a moving-window approach of five successive stages (Fig. skeletal organisms (27). S2). Here the beta-gamma link is significant over the interval That the main pulse of the Cambrian radiation was in the early from Stage 2 to the Drumian. The strong correlation between Cambrian has long been known (28, 29), but defining the time of beta diversity and gamma diversity could be biased by the mul- peak diversity has been hampered by problems with stratigraphic tiplicative approach we are using to derive beta diversity from

correlations. Our improved data and updated stratigraphic as- EVOLUTION both alpha and gamma diversity, which are independently Materials and Methods signments demonstrate a pronounced origination and diver- assessed ( ). Although this method proba- sification pulse in the earliest Cambrian (Fig. 3). This pulse may bly has a better biological underpinning than the additive approach (15), a correlation between gamma and beta diversity is still evident when using an additive method (ρ = 0.84, P < 0.001). Therefore, gamma diversity in the Cambrian was largely governed by differentiation among communities or assemblages rather than by genus packing within assemblages. An alpha-beta-gamma plot during the time of unconstrained diversification, that is, in the first three Cambrian stages, reveals that alpha diversity initially increased faster than beta diversity, but subsequently, beta diversity increased more rapidly (Fig. 4). This pattern is predicted for a low-competition scenario (15). The pattern of beta diversity is similar for environmental and geographic beta, which both increased during the first three stages and then stabilized (Fig. S3). This finding suggests that taxonomic gradients among habitats and geographic regions were equally important. To disentangle geographic turnover, we assess geodisparity in three spatial intervals of paleogeographic distance among 5 × 5° paleogeographic grids. The result shows (Fig. 5) that turnover in assemblage composition increased gradually with paleogeographic distance in the intervals of less than 2,000 km and greater than 4,000 km, likely reflecting normal Fig. 2. Alpha diversity and beta diversity from the Ediacaran to the earliest Cambrian distance-decay patterns (19). However, turnover in Ordovician based on unweighted by-list subsampling of 45 collections per the 2,000- to 4,000-km interval increased dramatically with stage. Error bars are SDs of 100 subsampling trials.

Na and Kiessling PNAS | April 14, 2015 | vol. 112 | no. 15 | 4703 Downloaded by guest on September 27, 2021 sizes of sampling area and sampling units (51). In our case, local community differentiation was driven largely by niche contraction. However, at regional or continental scales, beta diversity or community differentiation between regions does not necessarily increase when niches contract, because environmental gradients can be strongly interrupted by dispersal limitation and topo- graphic isolation. Therefore, there must be other factors that drive beta diversity at continental scales in the Cambrian. The steep distance decay in the 2,000- to 4,000-km distance interval (connecting adjacent continents or distant parts of Gondwana; Fig. S4) suggests that the continents became biogeographically distinct in the first two Cambrian stages, and that deep oceans between continental shelf areas caused effective migration barriers, which likely enhanced allopatric speciation (52). In summary, the drivers of beta diversity varied with spatial scale: (i) at local scales, an increase of beta diversity was due to niche contraction, which, in turn, may have been fueled by predation; and (ii) at continental scales, beta diversity was governed by the strong increase of provincialism among paleo-continents. This Fig. 3. Sampling-standardized extinction and origination rates through the Ediacaran and Cambrian. Rates are per-capita rates of Foote (70) but not stan- increase was accompanied by profound continental reconfigurations dardized by stage durations (71). Error bars are SDs of 100 subsampling trials. often referred to as the breakup of the supercontinent Pannotia (20, 53). Pannotia assembled in the interval from 650 to 550 Ma (54). Its breakup was characterized by the opening of the Iapetus and Ægir be exaggerated by the closure of the Ediacaran taphonomic oceans (55), resulting in the separation of Laurentia, Baltica, window with widespread soft-body preservation and the opening Siberia, and Gondwana, but also orogenies leading to the amal- of a novel taphonomic window by the widespread acquisition of gamation of distinct cratonic blocks within Gondwana. The disas- skeletons (30). Cambrian diversity rose to a prominent peak in sembly of Pannotia (particularly the separation between Laurentia Stage 3, which is roughly equivalent to the Siberian Atdabanian and Gondwana) is suggested to have started close to the onset of and most of the Siberian Botomian (31). The subsequent decline the Cambrian radiation (Fortunian; ∼541 Ma) and ended before in global diversity may have been partly due to the Sinsk ex- Cambrian Stage 3 (∼521 Ma) (20). This rapid disassembly of tinction event in Stage 4 (32–34), but environmental factors are Pannotia corresponds well with the increase of geodisparity (Fig. 5). more plausible to explain the lack of further diversification in the Although the breakup of Pannotia is sometimes discussed as a later Cambrian. For example, prolonged tropical warming has potential trigger of the Cambrian radiation (54), the concept is been suggested to explain the scarcity of metazoan reefs in the not widely used. However, our results support the contention later Cambrian (35) and would also fit the gamma diversity that the disassembly of Pannotia increased geodisparity and, trajectories given that cooling is thought to have facilitated the thereby, beta and gamma diversity in the Cambrian. Disassembly subsequent Ordovician radiation (36). Alternatively, a late Cam- of supercontinents is rare and always seems to have profound i brian rise in oxygen levels has been proposed to explain the onset evolutionary consequences. Examples are ( ) the breakup of the of the Ordovician radiation (37). By inference, oxygen limitation supercontinent Rodinia some 750 Myr ago has been linked with global glaciations, which are often held responsible for the may have hindered further diversification after the early Cambrian. ii The relationship between alpha and beta diversity during the emergence of metazoans (56); ( ) further continental dispersal in the Ordovician is thought to have facilitated the Ordovician time of unbounded diversification (Fig. 4) suggests that a low- iii competition model (15) best explains the Cambrian radiation. diversification (57); and ( ), the link between the breakup of When competition is low, the addition of new species to a Pangea in the Early Jurassic and the Mesozoic-Cenozoic radiation has long been suggested (58) and is supported by sampling- community happens either by exploitation of previously unused standardized diversity curves (59). resources or by packing more species in marginal ecospace (38). This process will initially not shrink niches of preexisting taxa such that alpha diversity will increase steeply, whereas beta diversity will initially increase only moderately. As diversification continues, competition will increase, niches will contract, and consequently beta diversity will increase profoundly, whereas alpha diversity levels off. Niche contraction facilitates niche partitioning and, thus, changes of taxonomic composition among habitats. Predation is a potential factor for keeping the system in a low-competition mode (39). Predation is first recognized in the latest Ediacaran (40, 41) and well-documented in the early Cambrian (42, 43). Apex predators are first common in Cam- brian Stage 3 (44, 45). Therefore, escalation is a plausible trigger of the Cambrian radiation in terms of both biomineralization (46, 47) and community ecology (48). Predation universally defeats competition in benthic marine systems (49), suggesting that the Cambrian radiation was not exceptional in this aspect. We show that the increase in beta diversity was the principal driver of increasing gamma diversity during the Cambrian radiation. The pivotal role of beta diversity in structuring global diversity patterns has also been suggested for early Cambrian reef Fig. 4. Alpha-beta-gamma plot for the first three Cambrian stages, the time communities (50). Beta diversity strongly depends on both the of continuous diversification. Note log scale of all axes.

4704 | www.pnas.org/cgi/doi/10.1073/pnas.1424985112 Na and Kiessling Downloaded by guest on September 27, 2021 continental dispersal in the earliest Cambrian, they agree in that the Early Cambrian was a time of continental disassembly (SI Materials and Methods).

Diversity Estimation. To account for sampling heterogeneity (65), diversity has been estimated with sampling standardization. Sampling standardization can be achieved with random draws of the same number of fossil collections, taxonomic occurrences, or a fixed sum of frequency of genus abundance in each time interval (59, 66). We generally assessed diversity by counting taxa actually sampled in an interval (sampled-in-bin, SIB) and, thus, did not in- terpolate taxon occurrences between their first and last appearance in the fossil record. This counting method has the advantage that edge effects at the beginning and end of time series are avoided (59). We used shareholder quorum subsampling (66) with a quorum of 70% to estimate gamma diversity. Alpha and beta diversity as well as extinction and origination rates were assessed by drawing 45 taxonomic collections at random (by-list unweighted method; UW) (67) and averaging results across 100 subsampling trials. Alpha diversity was estimated as the number of genera found in a collection, where a collection can vary from a small sample taken from a single bed to a whole formation at a regional scale. To test whether this approach biases our estimate of alpha, we have also measured alpha diversity in the subset of collections for which specimen abundances are provided. We used Fig. 5. Distance-decay curves during the first three Cambrian stages plotted the Shannon–Wiener Index (68) for those collections that reported at least as taxonomic dissimilarity among 5 × 5° paleogeographic grids. Blue circles, 80 specimens. Stage 3; green circles, Stage 2; red circles, Fortunian. The black lines denote We use two commonly used measures of beta diversity: (i): β = γ=α , where separate regressions for three distance intervals. γ is total diversity at global scales, and α is the mean genus richness within assemblages. This metric is a global measure of beta diversity based on presence-absence data (1, 38); and (ii), a pairwise dissimilarity measure based Alternatively, the capacity of biological dispersal could have on the Bray–Curtis index (69), which assesses the pairwise dissimilarity among changed substantially in the early Cambrian. Our knowledge of sampling units with respect to environmental or geographic variables. dispersal in Ediacaran biota is limited but at least some Edia- Environmental beta was measured by pooling collections in the same basic caran taxa were able to cross oceanic basins and achieve a cosmo- environmental setting and comparing the faunas between environments politan distribution (26, 60). Cambrian animals probably dispersed that differed by one, two, or three environmental categories. Environmental beta is thus estimated by the mean dissimilarity in the context of habitat with nonplanktotrophic larval stages (61), which would limit their disparity. Environmental categories were tropical/nontropical (separated at geographic distribution relative to animals with planktotrophic lar- 30° absolute paleolatitude), carbonate/siliciclastic (distinguished by domi- vae (62). Therefore, the increase of geodisparity we observe during nant lithology, marls were ignored), and shallow-water/deep-water (sepa- the early Cambrian could be due to the widespread appearance rated by storm wave base). of animals with larval stages combined with continental disas- Geographic beta was estimated in the context of paleogeographic dis- sembly. In other words, biological innovation—the evolution of tance. To create a paleogeographic distance matrix, we applied the geo- larval stages (61)—in tandem with supercontinent breakup best disparity method introduced by Miller et al. (14). Occurrence data for a given explains the increase of geographic beta diversity. Our study pro- stratigraphic interval were pooled in 5 × 5° paleogeographic grids. A dis- vides evidence for niche partitioning, plate tectonics, and key in- similarity matrix of these pooled data was computed, and the data were then parsed into 2,000-km intervals of great circle distances between grid novations as strong and persistent evolutionary forces, and the centers. We focused on three geographic scales: within a continent (0–2,000 km), Cambrian radiation is no exception, although it was more sub- between adjacent continents or within a larger continent (2,000-4,000 km), stantial in quality than later radiations. Future work should ex- and between remote continents (greater than 4,000 km). The turnover, or plore the links between the ecological dynamics described here the rate of change in community composition, is represented by the slope of EVOLUTION and the astonishing increase of morphological disparity in the the relationship between dissimilarity and geographic distance. This dis- early Cambrian. tance–decay relationship was estimated by linear regression (Table S1).

Materials and Methods Statistical Tests. All statistical tests are nonparametric applying Spearman’s ρ Data. Fossil occurrence data of Ediacaran to Tremadocian age were entered rho ( ). Time-series data were tested for autocorrelations before performing into the Paleobiology Database (PaleobioDB; paleobiodb.org) and downloaded correlation tests. Because there are no significant autocorrelations in any of alongside all other occurrences on May 23, 2014. This dataset comprises 7,117 the relevant variables (alpha, beta, gamma, extinction rate), correlations are collections and 39,737 taxonomic occurrences. We assigned each collection to based on nondifferenced data. one of 14 stages based on the three widely recognized assemblages in the Ediacaran (63), the 10 stage subdivision of the Cambrian period according to the ACKNOWLEDGMENTS. We thank Uta Merkel, Mihaela-Cristina Krause, and 2012 International Commission on Stratigraphy time scale (31), and the Trem- all of the other contributors for Ediacaran-Cambrian data entry to Paleobi- adocian of the Ordovician (SI Materials and Methods, Fig. S7,andTable S2). ology Database. We also thank Qi-Jian Li (Friedrich-Alexander-Universität Erlangen-Nürnberg) for valuable suggestions. This work was supported by Plate tectonic configurations and paleopositions of fossil occurrences are ’ Deutsche Forschungsgemeinschaft KI 806/9-1, embedded in the Research based on Scotese s paleomap software (64). Paleopositions were automati- Unit “The Precambrian-Cambrian Biosphere (R)evolution: Insights from Chinese cally provided upon download of the occurrences from the PaleobioDB. Microcontinents” (FOR 736). We are grateful to two anonymous reviewers The concept of Pannotia is implemented in Scotese’s reconstructions, and for their constructive comments. This work is Paleobiology Database Publi- although newer reconstructions differ in some aspects such as the degree of cation No. 225.

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